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Coordination Chemistry Reviews 386 (2019) 267–309

Contents lists available at ScienceDirect

Coordination Chemistry Reviews


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Review

Coordination chemistry of f-block metal ions with ligands bearing


bio-relevant functional groups
Linda Götzke a, Gerrit Schaper a, Juliane März b, Peter Kaden b, Nina Huittinen b, Thorsten Stumpf b,
Kaitlin K.K. Kammerlander c, Eike Brunner c, Peter Hahn d, Anne Mehnert d, Berthold Kersting d,
Thomas Henle e, Leonard F. Lindoy f, Giuseppe Zanoni g, Jan J. Weigand a,g,⇑
a
Chair of Inorganic Molecular Chemistry, Technische Universität Dresden, Mommsenstraße 4, 01069 Dresden, Germany
b
Institute of Resource Ecology, Helmholtz-Zentrum Dresden-Rossendorf (HZDR), Bautzner Landstraße 400, 01328 Dresden, Germany
c
Chair of Bioanalytical Chemistry, Technische Universität Dresden, Bergstraße 66, 01069 Dresden, Germany
d
Institut für Anorganische Chemie, Universität Leipzig, Johannisallee 29, 04103 Leipzig, Germany
e
Chair of Food Chemistry, Technische Universität Dresden, Bergstraße 66, 01069 Dresden, Germany
f
School of Chemistry, F11, The University of Sydney, Sydney, NSW 2006, Australia
g
Department of Chemistry, University of Pavia, Viale Taramelli 10, 27100 Pavia, Italy

a r t i c l e i n f o a b s t r a c t

Article history: Over recent decades there has been a great deal of interest and associated research into aspects of the
Received 1 November 2018 f-block (lanthanide and actinide) metal chemistry of naturally-occurring ligands, such as proteins,
Received in revised form 19 December 2018 peptides, porphyrins and related tetraaza derivatives as well as synthetically modified natural ligands
Accepted 9 January 2019
and solely synthetic ligand systems incorporating bio-relevant functional groups. In this review, we
Available online 27 February 2019
present a wide-ranging overview of published work spanning the above areas, with emphasis on selected
biological, medical and environmental aspects. Systems capable of discriminating between metal ions
Keywords:
from within, or between, the lanthanide and actinide groups are also discussed including the design
Lanthanides
Actinides
and synthesis of biomimetic radionuclide chelators and radionuclide decorporation agents as well as
Maillard products solid adsorbent materials for the uptake of radionuclides from the environment and elsewhere. Thus,
Siderophores the interaction of the f-group elements with a range of biopolymers, including systems based on
Calix[4]arenes cellulose, chitin, chitosan, humic substances as well as a range of synthetic model systems is also
Porphyrins presented. Other applications include the synthesis of new luminescent materials, including luminescent
Cellulose probes and luminescent metal coordination polymers exhibiting unusual photophysical properties as
Chitin well as systems showing potential for use in the development of new MRI imaging agents.
Chitosan
Ó 2019 Elsevier B.V. All rights reserved.
Humic substances
Peptides
Proteins

Abbreviations: AChE, acetylcholinesterase; Amy, a-amylase; An, actinide; Asn, asparagine; Asp, aspartic acid; bipy, 4,40 -bipyridin; BSA, bovine serum albumin; CaM,
calmodulin; CAM, catecholamide; CAM(C), carboxycatecholamide; CAM(S), sulfocatecholamide; CE, capillary electrophoresis; CMPO, carbamoylmethylphosphinoxide; cyt b5,
cytochrome b5; cyt c, cytochrome c; CYTAC, N,N0 ,N00 ,N000 -tetrakis(acetylacetonato)-1,4,8,11-tetraazacyclotetradecane; CYTROX, N,N0 ,N00 ,N000 -tetrakis(acetohydroxamato)-1,4,
8,11-tetraazacyclotetradecane; DFO, desferrioxamine; DFT, density functional theory; DGA, diglycolamid; DOTA, 1,4,7,10-tetraazacyclododecane-1,4,7,10-tetraacetic acid;
DTPA, diethylenetriaminepentaacetic acid; EB, enterobactin; EDTA, ethylenediaminetetraacetic acid; ESI-MS, electrospray ionisation mass spectrometry; EXAFS, extended X-
ray absorption fine structure; FA, fulvic acid; FRET, Förster resonance energy transfer; FUNMIG, fundamental processes of radionuclide migration; gfp, green fluorescent
protein; Glu, glutamic acid; Gly, glycine; GpA, glycophorin A; H2Pc, phthalocyanine; H2TPP, 5,10,15,20-tetraphenylporphyrin; HA, humic acid; Hb, hemoglobin; HOPO,
hydroxypyridinonate; HS, humic substance; HSA, human serum albumin; IAM, 2-hydroxisophthalamide; IL1b, interleukin-1b; Im, imidazole; LBT, lanthanide binding tag; LF,
lactoferrin; Ln, lanthanide; MAS, magic angle spinning; MDH, methanol dehydrogenase; MRP, Maillard reaction product; MT, metallothionein; NIR, near infrared; NTA,
nitrilotriacetic acid; OAc, acetate; OLED, organic light emitting diode; OPN, osteopontin; Pc, phthalocyanine (ligand class); PDB, protein data bank; PDE1, phosphodiesterase;
PDT, photodynamic therapy; pic, picrate; PmrA, polymyxin resistance A; PmrB, polymyxin resistance B; Por, porphyrin (ligand class); PQQ, pyrroloquinoline quinone; PRE,
paramagnetic relaxation enhancement; PUREX, plutonium and uranium refinement by extraction; PY, pyoverdine; REE, rare earth element; SC-XRD, single crystal X-ray
diffraction; SUP, super uranyl-binding protein; TAM, 2,3-dihydroxyterephthalamide; TEMPO, (2,2,6,6-tetramethylpiperidin-1-yl)oxyl; Tf, transferrin; TREN,
tris(2-aminoethyl)amine; TRLFS, time-resolved laser-induced fluorescence spectroscopy; Vtg, vitellogenin; WHAM, Windermere Humic Aqueous Model.
⇑ Corresponding author.
E-mail address: jan.weigand@tu-dresden.de (J.J. Weigand).

https://doi.org/10.1016/j.ccr.2019.01.006
0010-8545/Ó 2019 Elsevier B.V. All rights reserved.
268 L. Götzke et al. / Coordination Chemistry Reviews 386 (2019) 267–309

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 268
2. Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 269
2.1. NMR spectroscopy. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 269
2.1.1. NMR spectroscopy of lanthanide- or actinide-containing compounds in solution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 269
2.1.2. Solid-state NMR spectroscopy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 270
2.2. Vibrational spectroscopy. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 270
2.3. Laser-induced luminescence spectroscopy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 271
3. Small molecules . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 272
3.1. Maillard reaction products . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 272
3.2. Siderophores . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 275
3.2.1. Natural siderophores . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 275
3.2.2. Artificial siderophore analogues . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 278
3.3. Calix[4]arenes – effective ligands for f-elements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 280
3.3.1. Separation and extraction of lanthanides and actinides by lower-rim functionalized calix[4]arenes. . . . . . . . . . . . . . . . . . . . . . 281
3.3.2. Luminescent probes and materials incorporating lanthanides based on lower-rim functionalized calix[4]arenes . . . . . . . . . . . 284
3.3.3. Magnetic properties of lanthanide complexes supported by lower-rim functionalized calix[4]arenes . . . . . . . . . . . . . . . . . . . . 285
3.4. Porphyrins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 285
4. Biopolymers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 288
4.1. Glucans . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 288
4.1.1. Cellulose and its derivatives for f-element adsorption. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 288
4.1.2. Chitin and chitosan for f-element adsorption . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 289
4.2. Humic substances for f-element adsorption . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 290
4.2.1. Complex formation between f-elements and model substances . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 290
4.2.2. Ternary systems: f-element ions/humic substances/mineral phase . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 291
4.2.3. Studies of samples obtained from the natural environment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 291
4.3. Peptides . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 291
4.3.1. Amino acids and small model peptides . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 291
4.3.2. Natural proteins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 293
4.3.3. Artificial proteins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 295
5. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 297
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 297
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 297

1. Introduction radiobiological impact of the various radionuclides depends on


various factors such as the nature of their interaction with potential
With the discovery and utilisation of nuclear fission, actinides complexing agents, the effectiveness of their uptake into organisms
(An) have become of high socio-political relevance. This applies [10,11], their surface interactions with solids, and the transport and
especially to the elements Th, U, Np, Pu, Am, and Cm, of which only targeting that occurs within particular organisms [12]. For the An
Th and U can be found in significant amounts in nature. The elements, many of these complicated relationships have yet to be
remaining elements are products of nuclear fission applications. investigated or have only been studied to a limited extent. For exam-
Due to malfunction or damage occurring in nuclear plants, or leak- ple, detailed information concerning metal-ion speciation for differ-
age from disposal containers, these elements may contaminate the ent oxidation states, ligand exchange with bio-relevant ligands, and
environment [1]. The risk associated with these elements is two- details of transport behaviour are frequently not available. Further,
fold. On the one hand it is due to their nuclear radiation and, on crucial experimental data such as concentration, pH, temperature,
the other hand, a consequence of their heavy metal toxicity. An redox potential, carbon dioxide level, and ionic strength are also
appreciation of the means for preventing the environmental dis- often missing [3–6].
persion of radionuclides clearly depends on an understanding of While data, especially thermodynamic, speciation, and struc-
their environmental pathways and ultimate fate [2]. Consequently, tural data, for An complex formation with small inorganic ligands
an in-depth understanding of the chemistry of the An elements, is relatively abundant [13–15], in contrast this is generally less so
especially focused on their coordination chemistry is necessary for organic ligand systems [16,17] and especially for bio-relevant
for this to be achieved. organic ligand systems [18–20]. Notably, there is a lack of detailed
The effect of radioactive compounds on the environment as well investigations of complexes of multifunctional ligand systems pos-
as on the food chain has been an interdisciplinary area of investiga- sessing typical ‘natural’ functional groups such as carboxylate,
tion for decades. Many natural and anthropogenic processes causing phosphate, amine, imine, amide, ether, hydroxyl, phenol, and hete-
environmental contamination have been identified. The latter arise rocyclic groups. For that reason, in 2016 the joint research project
from nuclear tests, the use of depleted uranium in munitions and FENABIUM, which included several working groups from Dresden
accidental releases from nuclear power plants as well as from stor- and Leipzig, was established with its focus on the interaction of
age facilities. Other contributions have involved the recycling of used f-elements with organic ligands carrying binding sites related to
nuclear fuel rods and the disposal of radioactive waste. Pollution can those of natural products. This consortium aims to not only explore
also result from mining; for example, of uranium and the rare earth the interaction of f-block elements with organic ligands but also to
elements (REE), or from the use of natural resources contaminated ensure that the knowledge so obtained is made available to future
with U (i.e. fossil fuels, construction materials, fertilisers) [3–7]. workers in the area.
Metal complexation is often involved in such processes as well as An aspect of the coordination chemistry of 5f-elements is their
in the corresponding remediation procedures [8,9]. The overall often similarity to that of the 4f-analogues, the lanthanides (Ln).
L. Götzke et al. / Coordination Chemistry Reviews 386 (2019) 267–309 269

Although this similarity may not be observed for the early Ans, 2.1.1. NMR spectroscopy of lanthanide- or actinide-containing
there remains an opportunity for using the Ln ions as non- compounds in solution
radiative model species. Nevertheless, the An ions exhibit a stron- Paramagnetic effects – NMR spectroscopy of f-element-
ger tendency towards covalent bonding that leads to somewhat containing compounds has chiefly involved systems displaying
enhanced interaction with softer nitrogen, phosphorous, and/or paramagnetic interactions [56,57]. While for the (mostly) trivalent
sulfur donor atoms in contrast to the Ln, which are distinguished Ln series two diamagnetic metal ions, namely La(III) and Lu(III), are
by a distinct preference for hard oxygen donors [21,22]. Thus, var- available, there are no diamagnetic analogues existing in NMR-
ious heteroaromatic N-donor ligands have been reported for the relevant quantities for the trivalent An ions. For the tetravalent
separation of trivalent Ans and Lns [23–26]. and hexavalent Ans, Th(IV) and U(VI) are diamagnetic [58–60].
The investigation of f-block metal ion binding to ligand systems While the interpretation of diamagnetic spectra of An com-
carrying phenolic groups has attracted wide interest over many pounds is straight forward, the spectra of systems involving para-
years. The relatively hard aryl –OH or –O group in fact has a sub- magnetic interactions are more challenging to interpret. The
stantial affinity for both Ln and An ions [27]. This group is common presence of paramagnetic contributions, however, allow the inter-
to a range of biomolecules, such as particular peptides and proteins action of the metal ion with surrounding nuclei to be probed due to
(e.g. in the form of tyrosine) [28], siderophores [29,30], fulvic acids different effects that may include the generation of additional
(FA), and humic acids (HA) [31–34]. Various open-chain and chemical shifts, the broadening of particular signals or signal
macrocyclic polyphenol ligands have been investigated with bleaching by PRE (paramagnetic relaxation enhancement) [61–
respect to f-metal ion complexation. The motivations for undertak- 64]. Such effects are widely used to identify Ln binding sites in
ing these studies are diverse and include the investigation of bio- metallo-proteins or for following the binding to artificial binding
molecule f-element interactions [35], f-element separation by sites used to investigate the tertiary structure of proteins [57,65–
liquid–liquid extraction, nuclear fuel reprocessing [36–39], the 68]. Prior to the development of heteronuclear multidimensional
design and synthesis of biomimetic radionuclide chelators [40], spectroscopy, paramagnetically-induced shifts were employed to
radionuclide decorporation [29], the creation of sorbents for the overcome spectral crowding in 1D spectra by the use of NMR shift
removal of contrast agents [41] and the development of the next reagents [69–71]. Quantitative analysis of the observed chemical
generation of radiopharmaceuticals [42]. A further impetus for shifts [66,72–77] combined with the results from quantum chem-
studying f-metal phenolato systems is due to recent advances in ical calculations [78–80], has allowed more detailed information
the development of new Ln probes [43,44] for use in molecular about the nature of metal–ligand interactions to be obtained.
sensing and optical imaging [45–51]. Finally, it is noted that com- Paramagnetic chemical shifts – Paramagnetic shifts can be con-
plexation with polyphenols can drastically increase the solubility sidered as incorporating an additional chemical shift (hyperfine
of particular metal ions, which clearly has important implications contribution) to the shifts of a diamagnetic reference compound
for their mobilisation in the environment [52]. (orbital shift). The hyperfine contribution consists of two major
To deliver a short insight into the wide field of Ln and An com- contributions, the so-called FERMI contact shift and the pseudo con-
plexation, this review focusses on a few examples of naturally tact shift. All contributions can be derived theoretically [81]. His-
occurring ligands (such as Maillard reaction products, siderophors, torically, the temperature-dependent behaviour of a given
porphyrins, cellulose, chitin and chitosan, peptides, and proteins) paramagnetic shift and the resolution for the two major contribu-
and their synthetic derivatives. Because of structural analogy (in tions has led to good agreement with theoretical predictions for
terms of the presence of phenolic groups) a brief survey on the cur- systems containing light paramagnetic ions [82]; however Ln-
rent state of research of the f-block interaction with calix[4]arenes containing systems cannot be accurately described by these meth-
is also included. ods [68,83–86]. This is also especially true for An derivatives
[80,87,88] as spin-orbit effects, which are omitted in available
computational models, are expected to increase dramatically in
2. Methods such cases [80].
Practically, the influence of hyperfine effects on the chemical
Several experimental methods (such as UV-Vis and EXAFS spec- shift of a nucleus is usually observed for light nuclei (1H, 13C, 15N,
troscopy, ESI- or ICP-MS) allow the direct study of actinide-(bio) etc.) in direct proximity to the paramagnetic centre where electron
ligand interactions. Especially NMR, IR and TRLF spectroscopy are spin-polarization occurs [89,90]. Electron spin polarization, mainly
often used and these will be discussed briefly. involving the valence shell of heavy atoms, is introduced by spin-
orbit coupling near the nucleus of the heavy atom mixing triplet
2.1. NMR spectroscopy character into the ground state wave function in the presence of
an external magnetic field [91]. The major contributors to the para-
NMR spectroscopy is one of the few available methods for magnetic chemical shift can be identified by the magnitude and
studying the electronic interaction of Lns and Ans with complexing sign of the individual shift. While FERMI contact shifts may be
ligands in a non-destructive and non-invasive manner. However, shielding or deshielding, with a magnitude ranging from very small
there are only a limited number of An isotopes that can be readily to a multitude of the shielding range of the observed nucleus,
studied in normal NMR laboratories without appropriate radiation pseudo-contact shifts show a symmetrical vectorial dependence
protection. Differences in the coordination chemistry of the An(III) (distance and angle dependence from the general axis) becoming
series compared to the Ln series [53], such as the richer oxidation much smaller as the nucleus becomes more remote from the para-
state chemistry of the early An elements, provide a strong motiva- magnetic centre [90,92,93]. For organic ligands, this induced spin
tion for investigating such An compounds directly by NMR spec- polarization may then propagate along bonding orbitals in an anal-
troscopy [54]. However, unfortunately only a few institutions ogous manner to spin-spin coupling interactions and thus, for
worldwide are able to handle active An species and even fewer atoms further remote from the paramagnetic centre, follow a
institutions are equipped to perform such NMR experiments in KARPLUS-typedependence on dihedral angles or a damped oscilla-
their radiochemistry laboratories. With respect to this, a compre- tory behaviour in aromatic systems [90,91]. Following this transfer
hensive overview of the use of NMR spectroscopy in nuclear chem- of electron spin polarization, an additional contribution to the
istry in both the liquid and solid state has recently been published chemical shifts of the nucleus under investigation is caused by
[55]. hyperfine interactions, mainly via a FERMI contact. A FERMI contact
270 L. Götzke et al. / Coordination Chemistry Reviews 386 (2019) 267–309

occurs directly at the nucleus, thus a sizeable s-character in the


bond from the observed NMR-active nucleus to its neighbours is
essential [90,91] as only these possess a non-vanishing probability
of an electron being located at the nucleus. An in-depth discussion
of all components and their theoretical derivation can be found in a
review by Piguet and Geraldes [66]. However, in general, this
model is not sufficient for a full description of such observed chem-
ical shift behaviour [68,78,83,85,87,88,94]. Reviews of recent pro-
gress in calculating these effects by quantum chemical methods
are available [78,79,89,90].
Spin labels for structure determination – The determination of the
structure of a molecule by NMR spectroscopy has been classically
achieved by measuring a large number of ‘‘geometrical” parame-
ters such as coupling constants or NOEs to finally allow reconstruc-
tion of the relative positions of nuclei and thus yield the
corresponding nuclear coordinates. In the presence of a paramag-
net PRE and hyperfine shifts (mostly PCS), both being related to
the relative position of nuclei to the paramagnetic centre (r3
dependence), allow the determination of additional structural
restraints. Additionally, dynamic information such as dynamic
changes of conformation or the relative orientation of domains in
a (bio)molecule are able to be derived from such medium range Fig. 1. 13C CP MAS NMR spectra of hydrated sponge chitin from A. aerophoba (A),
interactions. Paramagnetic centres can be introduced by attaching hydrated sponge chitin loaded with 188 mg/g uranium at pH 6 (B), sponge chitin
paramagnetic probes to a structure or by substituting a diamag- after uranyl desorption in 0.1 M HCl (C). There are only subtle differences present in
the spectra suggesting no significant changes in the chitin structure upon uranyl
netic metal in the structure with a paramagnetic one [57,65,95–
adsorption and subsequent desorption. Reproduced from [115] with permission
97]. from Elsevier.
Solvent accessible surfaces – Soluble paramagnetic species may
interact with the solvent leading to a transfer of relaxation
enhancement by solvent molecules to the solvent-exposed surface
of the solute molecules and, for example, can be used to estimate dependent interactions such as magnetic dipole-dipole interac-
the solvent accessible surface of biomolecules, especially where tions, solid-state NMR spectroscopy has allowed the selective char-
classical methods such as H/D exchange fail due to the absence acterisation of interfaces in hybrid materials, e.g. between
of acidic protons [57,98–100]. inorganic phases and attached organic material in biominerals
Residual dipolar couplings – Of course, fast isotropic reorienta- [109–113]. Solid-state NMR spectroscopy has also been applied
tion of molecules leads to a simplification of NMR spectra in solu- to study various other composite and hybrid materials [114].
tion compared to solid state spectra by averaging out the Solid-state NMR spectroscopy offers different approaches for
contributions of nuclear positions relative to the external field. probing the interaction between f-elements and various complex-
Thus, the chemical shift of these nuclei in diamagnetic systems is ing agents. On one hand, it allows the study of NMR-active
centred at an average value that results from the respective shield- f-element isotopes. Examples are 139La, 141Pr, 151/153Eu, 231Pa, or
235
ing interactions and is split by scalar coupling with covalently U. These isotopes are, however, usually quadrupolar nuclei
bound spins according to their nJ coupling constant. Magnetic and only occur at low natural abundance. The direct observation
moments arising from magnetic anisotropy in paramagnetic sys- of f-element systems by solid-state NMR spectroscopy is, therefore,
tems, however, may prevent the averaging by reorientation gener- limited. On the other hand, solid-state NMR measurements are
ating a partial self-alignment of the molecules relative to the capable of characterising the structure of the complexing agents
strong external field. This effect can be observed in a perturbation (such as biopolymers) as well as documenting structural changes
of the J-splitting of coupled spins. The difference between the J induced by the binding of f-elements. As an example, the solid-
coupling in a diamagnetic system with isotropic reorientation state 13C NMR spectra of chitin from the marine sponge Aplysina
and the partially aligned paramagnetic sample has a distance aerophoba before and after uranyl sorption and subsequent desorp-
(r3) and angular dependence of the vector between the coupled tion are shown in Fig. 1 [115]. Solid-state NMR spectroscopy even
nuclei and the external magnetic field direction. Exploiting these allows for the distinction of different structural variants of chitin
residual dipolar couplings introduced at metal binding sites in pro- [116]. It should be noted that the study of solids usually requires
teins or by introducing artificial spin labels, structural information the application of the magic angle spinning (MAS) technique
in whole molecules like proteins, or even subdomains relative to [117] if highly resolved spectra are to be obtained. Moreover, the
each other, can be observed and, for example, folding processes detection of nuclei such as 13C is usually performed using the cross
can be analysed [57,95,97,101]. polarization (CP) technique [118] that results in the transfer of
nuclear spin polarization from sensitive, abundant nuclei such as
1
H to less sensitive and less abundant spins like 13C. While this
2.1.2. Solid-state NMR spectroscopy technique provides a very significant gain in sensitivity, it does
Solid-state NMR spectroscopy delivers structural information complicate the quantification of signal intensities.
that is based on the exploitation of short-range interactions and
hence does not require long-range (crystalline) order and has
found numerous applications involving the characterisation of var- 2.2. Vibrational spectroscopy
ious materials [102–104]. It is also widely used for the investiga-
tion of the structure and dynamics of biomolecules such as Vibrational spectroscopy in terms of Raman and Fourier-
membrane proteins, insoluble protein aggregates and others transform infrared (FTIR) and attenuated total reflectance (ATR)
[105–108]. Based on the exploitation of strongly distance- FTIR spectroscopy are techniques capable of providing structural
L. Götzke et al. / Coordination Chemistry Reviews 386 (2019) 267–309 271

Fig. 2. Left: ATR FTIR spectra of hydrated sponge chitin from A. aerophoba (A), hydrated sponge chitin loaded with 188 mg/g uranium at pH 6 (B). Right: Corresponding Raman
spectra of the same samples. Reproduced from [115] with permission from Elsevier.

information about biopolymers as well as their interaction with able laser light is used for the excitation of luminescent probes fol-
adsorbed species. Characteristic vibrational bands/band patterns lowed by detection of the emitted fluorescent or phosphorescent
often allow direct identification of biopolymers (such as chitin, light upon relaxation. Most f-elements from the Ln series and some
cellulose, and lignin) and their functional groups. By recording of the An elements show intense luminescence emission originat-
absorption changes caused by the direct interaction of f-elements ing from electronic f–f transitions. These are sensitive to changes in
with various functionalities in the bioligand, preferred binding the ligand field, thus making TRLFS an extremely useful tool for
sites and details of the coordination can often be identified, provid- investigating the speciation of 4f and 5f elements in solution, at
ing a more detailed understanding of the molecular interactions interfaces, or within solid matrices. Depending on the electronic
between Lns or Ans and the biomolecules of interest [119–121]. configuration of the luminescent ion, the number of non-
A specific use of vibrational spectroscopy in f-element complexa- equivalent species in a given system, binding-site symmetries,
tion studies, involves the probing of the (anti)symmetric stretch and potential quenching entities in the proximity of the lumines-
vibrations (m1 and m3) and the bending vibration (m2) of actinyl cent ion can be obtained from recorded excitation spectra, emis-
cations, i.e. of Ans stable in the oxidation states +V (such as sion spectra, and luminescence lifetimes. In the following
NpO+2) or +VI (such as UO2+ 2+
2 or PuO2 ) [122–124]. The stretch vibra- discussion, the luminescence characteristics of Eu(III) from the
tions of the actinyl bond (An@O) are influenced by the number and Ln series and the An, Cm(III), are focused upon, due to their favour-
type of coordinating ligands in the equatorial plane. Strongly able optical properties and corresponding wide range of applica-
donating ligands will withdraw electron density from the axial tions as luminescent probes for the characterisation of bio-
oxygens, resulting in a weakening of the An@O bond which in turn related systems.
reduces the total symmetric stretch vibration frequency [125]. By The luminescence emission signals for Eu(III) and Cm(III) are
combining the information obtained from the vibrational spectra each sensitive to changes occurring in their coordination spheres;
of the coordinating ligand with the shifts observed in the An@O including as a result of complex formation with organic (bio)-
stretch vibrational frequencies, a comprehensive picture of the molecules. For Cm(III) such complexation will typically induce a
formed f-element bioligand complex can be obtained. This has red-shift to longer wavelength of the emission peak position of
been demonstrated for uranyl complexation with the protein phos- the free aquo ion at 593.8 nm [126]. In the case of Eu(III), changes
vitin, where the collected ATR-FTIR spectra of the protein revealed are especially evident in the intensity of the hypersensitive emis-
U(VI) coordination to both carboxyl and phosphate groups of the sion transition, 5D0 ? 7F2 [127]. Such spectral changes can be used
amino acid side chains with a predominance of U-phosphate bind- to monitor Cm(III) and Eu(III) complexation reactions with biomo-
ing at high P/U ratios. The accompanying strong shift of the U@O lecules [20,128–136] as well as to derive the number of non-
antisymmetric stretch vibration with increasing P/U ratio was equivalent species present and their distribution as a function of
taken as an indication for bonding involving a larger number of metal-ion concentration [136–139], ligand concentration
coordinating ligands, suggesting a transition from monodentate [128,131,135], or solution pH [20,133,140]. In addition, the
to bidentate coordination of uranyl to two phosphate groups Eu(III) emission spectrum allows the assignment of the coordina-
[121]. Similarly, the absence of a strong shift of the m3 vibration tion symmetry of the complexes formed by making use of the
of U@O in amino acid complexes, could rule out an interaction of splitting patterns of (especially) the 5D0 ? 7F1 and 5D0 ? 7F2 tran-
UO2+2 with the amino group in the molecule, while bidentate bind- sitions. This is useful when investigating molecules with several
ing of the carboxylate group to the actinide ion was indicated by binding sites with known symmetries [141,142], as crystal-field
the characteristic shifts of the carboxylate modes [119]. For the perturbation splits the 7FJ terms in a number of crystal field levels
bioligand chitin, no significant changes in the FTIR spectra of chitin depending on the symmetry class [127].
material extracted from the marine sponge A. aerophoba before and By using non-selective excitation of Eu(III) and Cm(III) with
after the sorption of uranyl occur. This indicates an intact chitin laser light in the UV range to a strongly absorbing electronic level,
scaffold. The Raman spectra show distinct UO2+ 2 bands suggesting simultaneous excitation followed by luminescence emission of all
weak interactions between the adsorbed uranyl ions and the sor- species present in the system under investigation will take place.
bent (see Fig. 2 [115]). This results in an intense luminescence signal, which can be easily
detected, allowing for the use of nM-mM concentrations of the
2.3. Laser-induced luminescence spectroscopy trivalent elements in the complexation studies. Alternatively, the
excitation wavelength can be tuned to match the band gap
Time-resolved laser-induced luminescence spectroscopy between the ground state and the emitting state of single species,
(TRLFS) is a technique with outstanding sensitivity in which tune- allowing luminescence data to be collected for one species at a
272 L. Götzke et al. / Coordination Chemistry Reviews 386 (2019) 267–309

Fig. 3. Structures of hippuryl derivatives of Ne-fructoselysine (left) and Ne-carboxymethyllysine B (right).

time. For Eu(III), this selective excitation takes place between the resulting from Maillard reactions was studied by Seifert et al.
7
F0 ground state and the 5D0 excited state, which are both non- [159]. It was shown that the hippuryl derivatives of
degenerate. Thus, by measuring this transition as a function of Ne-fructoselysine and Ne-carboxymethyllysine (Fig. 3), quantita-
the excitation wavelength (excitation spectra) single peaks will tively important peptide-bound MRPs present in heated food, both
be observed for each individual species, enabling the determina- form moderately strong Cu(II) complexes. This is thus in agreement
tion of the number of Eu(III) species present or the Eu(III)- with the hypothesis that post-translational modification of proteins
associated metal binding sites in a given macromolecule [137– by carbohydrates leads to the formation of new coordination
139,143,144]. centres for metal ions within a protein chain.
Finally, by making use of luminescence resonance energy trans- Considerable research has been carried out on the coordination
fer (FRET) between two luminescent ions or a luminescence ion chemistry of Maillard products; this is mainly focused on the a-
and a ligand, distances between two metal-ion sites in a biomole- hydroxy ketones maltol (H1) and deferiprone (H2), the latter being
cule or metal-to-ligand distances can be determined [138,145– a hydroxypyridinone (HOPO), or more precisely a 3,4-HOPO
148]. FRET occurs between a donor fluorophore excited by incident derivative. Reflecting their a-positioned O,O-donor atoms, H1 and
light and an acceptor atom, when the emission transition of the H2 show high affinities towards hard metal ions such as Fe(III) to
donor and absorption transition of the acceptor overlap form octahedral, neutral complexes incorporating three deproto-
[149,150]. The efficiency of the energy transfer process is related nated ligand molecules [160] (Scheme 1).
to the luminescence lifetime of the donor in the absence and pres- The development of deferiprone (H2) as an iron chelating drug
ence of the acceptor and it is inversely proportional to the sixth for the treatment of iron deficiency anaemia via administering an
power of the distance between the donor and acceptor atoms appropriate Fe(III) complex, [161] or for its use in treating iron over-
[151–153]. Thus, by measuring changes in the luminescence life- load diseases, [162] has led to an increase in interest regarding
time of the 4f or 5f element in the absence and presence of acceptor employing its f-metal complexes in further medical applications.
atoms/ligands, the metal-to-metal or metal-to-ligand distance can Because of the relatively high H2 dosages (up to 75–100 mg/kg)
be calculated. during chelate therapy, there was a need to develop a reliable
method for monitoring H2 excretion. Owing to HOPOs being
3. Small molecules excellent photosensitizers [45,163], this was achieved via a sensitive
fluorometric procedure in which the H2 concentration in urine and
3.1. Maillard reaction products serum was detected by a procedure involving complex formation
with Tb(III) ions [164,165]. Furthermore, by means of silver-
The Maillard reaction, named after the French chemist Louis nanoparticle enhanced Tb(III) fluorescence, the general method
Camille Maillard, has become one of the most important chemical can also be applied to the analysis of exhaled breath condensate,
reactions in food chemistry [154]. Generally referred to as non- which considerably simplified the analytical procedure [166].
enzymatic browning or ‘‘glycation”, it describes various stages of Ln ions can be used for the treatment of osteoporosis and other
the reaction of amino compounds such as amino acids, peptides bone density diseases. Ln(III) is able to replace Ca(II) in
or proteins, respectively, with reducing sugars. This complex reac- hydroxylapatite resulting in a positive effect on bone formation
tion is responsible for the formation of colour, aroma and flavour [167,168]. Investigations with a series of Ln(III) complexes
during the preparation of many foods. The heterogenous group of (Ln = La, Eu, Gd, Tb, Yb) of H1, H2, as well as of two derivative com-
Maillard reaction products (MRPs) includes low molecular weight pounds show low ligand-independent cytotoxicity for La(III),
organic compounds with characteristic aromas, amino acid deriva- Gd(III), and Yb(III) complexes. Except for [LaIII(2)3] which yielded a
tives formed at peptides or proteins, as well as high molecular value of 9.07(233)%, the cell uptake was found to be less than 1%,
weight polymers, the so-called melanoidines. MRPs often contain being comparable with the value for inorganic carbonate species.
functional groups that make them suitable ligands for metal com- The different behaviour of [LaIII(2)3] is probably due to H2’s higher
plex formation [155]. With respect to the nutritional consequences lipophilicity leading to the increased transport into the cell [169].
of the Maillard reaction in food, it was found that the consumption However, substitution of the N-bound methyl group with more lipo-
of a MRP-rich food may result in a urinary loss of zinc, iron, and cop- philic groups does not increase cell uptake, nor does the introduc-
per ions, probably due to complex formation in the intestine [156]. tion of carboxylate or hydroxyl groups connected via aliphatic
Feeding studies with rats have shown that a diet rich in MRPs leads chains of varying length [170]. In subsequent follow-up studies,
to an increased urinary loss of zinc [157]. The Ca(II), Cu(II), and Orvig and co-workers have observed similar results [171,172].
Zn(II) binding ability of proteins was found to be related to their Because of the sometimes acute and chronic toxicity of Gd(III)
carboxymethyllysine content, which may be connected to MRI contrast agents [173,174] research towards obtaining new
increased oxidative stress under physiological conditions, as chelating agents for Gd(III) continues. Recent toxicological studies
metal-catalysed oxidations were found in some carboxymethyl- by Bose et al. have shown that injections of H2 into mice can sig-
rich tissues [158]. The binding of selected amino acid derivatives nificantly decrease the symptoms of nephrogenic systemic fibrosis,
L. Götzke et al. / Coordination Chemistry Reviews 386 (2019) 267–309 273

Scheme 1.

an ailment associated with Gd(III) contrast exposure [175]. While physiological conditions is comparable to other contrast agents,
Bose attributed the decrease in symptoms mainly to chelation of also exhibited good water solubility. The two aqua ligands also
iron which is mobilised by the Gd(III) contrast agent, he also noted present in the coordination sphere showed exchange rates compa-
that the chelation of free Gd(III) by H2 would contribute to the rable to the Gd(III) aqua complex and also high relaxivity, making
observed benefits. Indeed, similar HOPOs have long been discussed [GdIII(3)(H2O)2] a suitable contrast agent [181].
as binding motifs for Gd(III) complexation, most often in terms of The ether-bridged dipodal matol ligand H24 forms stable 1:2
tris(2-aminoethyl)amine (TREN) derivatives [173,176–185]. In complexes with Ln(III) ions (where Ln = Nd, Eu, Yb) that emit light
2006 Puerta et al. published a maltol-based TREN derivative in the red or NIR region upon excitation at 330 nm due to energy
(H33) for Gd(III) complexation. The resulting Gd(III) complex, transfer from the ligand to Ln(III). In contrast to the Nd(III) and
[GdIII(3)(H2O)2] (Fig. 4), whose stability (pGd(3) = 19.27(8)) under Yb(III) complexes, the Eu(III) complex gives a very poor
metal-centred quantum yield. This is attributed to efficient
thermal back energy transfer because of very close ligand donor
and metal acceptor energy levels [186]. Further maltol derivatives
utilized for metal complexation are the ethylendiamine- and
cyclen-bridged ligands H25 and H26. Both ligands readily form
mononuclear, neutral complexes [CuII(5)] and [CoII(6)],
respectively. Such complexation induces a preorganisation of the
two maltol functions that facilitate the subsequent binding of
additional Ln(III) ions to afford the hetero-trinuclear cationic
compounds {LnIII[CuII(5)(H2O)x]2(H2O)} (Ln = Gd, Dy, Eu) and
{LnIII[CoII(6)]2} (Ln = Gd, Eu). In all these complexes the softer
transition metals are coordinated by the N donor atoms of the
ethylendiamine and cyclen moieties, respectively, as well as by
Fig. 4. Maltol derived Gd(III) complex, [GdIII(3)(H2O)2] [181]. the deprotonated hydroxyl oxygen atoms of the maltol moieties

Fig. 5. Molecular structures of {GdIII[CuII(5)(H2O)]2(H2O)}3+ (left; showing only one arrangement for the disordered 52 ligand) and {GdIII[CoII(6)]2}3+ (right) [188].
274 L. Götzke et al. / Coordination Chemistry Reviews 386 (2019) 267–309

Fig. 6. Molecular structure of [(UVIO2)(2)2(H2O)] [189].

(Fig. 5); whereas the Ln(III) is coordinated by four bidentate maltol


moieties of two M(II) complexes. In the case of the H25 complexes
an additional aqua ligand completes the coordination of the Ln(III),
resulting in a distorted monocapped square antiprismatic coordina-
tion polyhedron. Investigation of the magnetic properties of the two
Gd(III) complexes revealed a ferromagnetic CuAGd and an antifer-
romagnetic CuACu interaction for {GdIII[CuII(5)(H2O)]2(H2O)}3+ and
overall ferromagnetic interactions for {GdIII[CoII(6)]2}3+ [187,188].
Recently Wang et al. showed that native H2 is a promising
decorporation agent for uranyl, giving rise to a metal decorporation
of 78.0(45)% in renal proximal tubular epithelial cells compared to
the control [189]. Their experiments further revealed the forma- Fig. 8. 3,4-HOPO modified silica (top); proposed binding mechanism to uranyl
tion of [(UO2)(2)2] as the most dominant species in solution at (bottom) [195].
physiological pH values. Single crystal X-ray analysis of the uranyl
complex showed a distorted pentagonal bipyramidal coordination
geometry for the uranyl centre with the two deprotonated 2 HOPO-derivative showed universal high adsorption rates with par-
ligands and an additional aqua ligand in the equatorial plane (see ticular high affinity for Th (log KD = 4.40(7)), U (log KD = 5.20(4))
Fig. 6). The 2 ligands provide a total of four UAO bonds with bond and Np (log KD = 5.00(9)) (values determined for the river water)
lengths of 2.339(3)–2.466(2) Å and are twisted 7.7(2)° with respect [194].
to each other. Pyrazine and its derivatives are other Maillard products that
In addition to uranyl, the decorportaion of Pu(IV), which is also often occur in wine and other fermented foods [199] and have been
widely used in nuclear technology, is also of considerable interest investigated as ligands in metal coordination chemistry. These
[190]. Raymond and co-workers have investigated the coordina- derivatives with their two obverse arranged nitrogen atoms, resem-
tion behaviour of Pu(IV) with different HOPOs and hydroxypyra- ble 4,40 -bipyridine (bipy) and share its coordination behaviour in
nones, including H1 [191–193]. Single crystal X-ray analysis forming bridged dinuclear metal complexes [200] (Scheme 2).
showed a 1:4 metal complex with a triangular dodecahedral (or In 2010 Irfanullah and Iftikhar investigated the formation of b-
snub disphenoid) coordination of the Pu(IV) (Fig. 7); the corre- diketonato complexes of the early Lns in the presence of pyrazine
sponding Ce(IV) complex, [CeIV(1)4], was found to be isostructural. [201]. While no crystals suitable for X-ray analysis were obtained,
1
The use of HOPOs for surface modification of solid-state metal H NMR and 4f-4f absorption spectroscopy as well as elemental
adsorbents has been the focus of many research groups in recent analysis indicated the formation of dinuclear metal species of the
years. The use of modified silica makes possible the extraction of type shown in Fig. 9. Investigation of the luminescence properties
uranyl from river and sea water (Fig. 8) [194–198]. The high affin- of the dinuclear Sm(III) complex gave a strong excitation band at
ity of HOPOs for f-block metals combined with their relative 345 nm attributed to the S0 ? S1 transition of the b-diketone. The
robustness towards organic compounds makes them favoured sur- emission spectrum showed three intense emission bands at
face modifiers. Johnson et al. determined distribution coefficients 562 nm, 599 nm and 645 nm that were attributed to the Sm-
(KD) for several f-block metals (i.e. Ce, Eu, Th, Pa, U, Np) from river centred transitions 4G5/2 ? 6H5/2, 4G5/2 ? 6H7/2 and 4G5/2 ? 6H9/2,
water and sea water for different adsorption materials. The respectively, resulting in intense pink luminescence.

Fig. 7. Molecular structure of [PuIV(1)4] [192].


L. Götzke et al. / Coordination Chemistry Reviews 386 (2019) 267–309 275

main volatile products resulting from caramelization but can also


form during the late phase of the Maillard reaction [154]. A range
of furfural-based Schiff base ligands have been reported. For exam-
ple, in 2003 Fan et al. reported the formation of a Dy(III) complex
with furfurylidenealanine (H8) [204] (Scheme 3). From spectro-
scopic and thermal decomposition data, it was proposed to be a
1:1 complex of the deprotonated tridentate ligand 8, with a
bidentate nitrate and an additional water molecule also coordinat-
ing the Dy(III).
More recent ligand examples include 4-[N-(furfural)amino]
Scheme 2. antipyrine semicarbazone (H9) and the difurfuryliden ligands of
type 10 incorporating different aromatic spacers [205,206]. Prasad
et al. synthesised several complexes of H9 with different Ln(III)
cations (namely, Ln = La, Pr, Nd, Sm, Gd, Tb, Dy, or Ho) and various
anions in order to investigate the antibacterial and antifungal
activities of the respective complexes. Spectroscopic data sug-
gested that no direct coordination of the furan moieties occurs in
these complexes [206]. In contrast, Pui et al. reported opposite
behaviour for their group of dipodal ligands of type 10. They pre-
pared several different Ln(III) complexes (Ln = La, Sm, Gd, Er),
and their spectroscopic data suggested that metal binding occurs
via the oxygen donors of these ligands without participation of
Fig. 9. Dinuclear Ln(III) complexes of the type [LnIII
2 (m-pyrazine)(C10H13F7O2)6] the nitrogen atoms [205].
incorporating a bridging pyrazine ligand.

3.2. Siderophores
In contrast to pyrazine, 2-carboxypyrazine (H7) shows signifi-
cantly different coordination behaviour. Reflecting its ortho- 3.2.1. Natural siderophores
substitution, H7 acts as a bidentate ligand and in 2004 Eliseeva Natural siderophores are low molecular-weight compounds
et al. were the first to investigate the luminescence properties of (typically 200–2000 Da) produced by bacteria, fungi and gramina-
its Tb(III) and Eu(III) complexes [202]. The Eu(III) complex showed ceous plants [207]. Most prominent examples are enterobactin
four well-resolved emission bands between 575 and 725 nm, (EB), rhizobactin, pyoverdine (PY), desferrioxamine B (H311) and
attributed to the 5D0 ? 7Fj (j = 1–4, kexc = 337 nm) transitions of the cyclic desferrioxamine E (H312) (see Fig. 11) [2,208,209]. Side-
Eu(III). The Tb(III) complex displayed five emission bands between rophores are well-known bio-control agents, biosensors, remedita-
475 and 700 nm attributed to 5D4 ? 7Fj (j = 2–6, kexc = 337 nm) tors and chelators [208] with an extremely high affinity for Fe(III)
respectively. However, the relative photoluminescence quantum (Kf >1030) [207]. Thus, their main and essential function is to mobi-
efficiencies of both [EuIII(7)3] and [TbIII(7)3] are only about 10% of lise iron sources from the environment and to scavenge and bind
the corresponding benzoate complexes. The Eu(III) complex crys- the concentration of soluble iron which is widely present in the
tallised as [EuIII(7)3(H2O)2]6H2O in which each Eu(III) is coordi- environment (but otherwise not readily bioavailable) [207,208].
nated by three bidentate 7 and two aqua ligands as well as by a However, in competition with Fe(III), protons as well as other di-
bridging carboxyl oxygen from a neighbouring 7, resulting in a and trivalent metal ions can bind to the siderophores. These
three dimensional network (Fig. 10). In 2013 Kai et al. expanded include Ln(III) ions as well as An ions in different oxidation states
this study by synthesising ten different Tb(III) complexes incorpo- [2,29,208,210,211]. Under environmentally relevant conditions,
rating H7 and butanedioic acid, nine of which were doped with the Ans can possess a variety of oxidation states, which typically
other REEs [203]. While the Tb(III) complex itself showed good range from +III to +VI for the early Ans (Th to Cm) [43]. The strong
luminescent properties, on doping with rare earth metals was tendency of siderophores to bind these highly charged metal ions
found to result in significantly increased luminescence lifetimes reflects the hard oxygen donor atoms present in their respective
and quantum yields. structures [212] which include i) catecholates (CAM) including sul-
Another group of important Maillard products are the deriva- focatechol, carboxycatechol, and catecholamide, ii) hydroxamates,
tives of the aromatic aldehyde furfural. These compounds are the iii) carboxylates and iv) amides [2,208,209,213]. In keeping with

Fig. 10. Molecular structure of [EuIII(7)3(H2O)2]6H2O [202].


276 L. Götzke et al. / Coordination Chemistry Reviews 386 (2019) 267–309

potential for therapeutic use of f-element siderophore complexes


[210,219–224].
Catecholates (CAM) – Most of the siderophores produced by bac-
teria are catecholates, with these being excellent chelators for hard
metal ions. An example is EB, secreted by Escherichia coli, and is
known to be the strongest Fe(III) binding siderophore [208,213].
It possesses three catecholate binding groups [213] and shows an
extraordinary tendency to bind Fe(III), in part reflecting its hard
Lewis basicity [225]. Apart from the enormous affinity for Fe(III),
with a binding constant of 1050, EB is also highly selective for
Pu(IV) (with a binding constant predicted to be comparable to that
for Fe(III)) [29,216].
Scheme 3.
Hydroxamates – Hydroxamate siderophores of the ferrichrome
family, namely, the desferrioxamines (DFO), further divide into
subgroups according to the nature of the side-chains associated
Fe(III) having a preferred coordination number of six, siderophores with the hydroxamate functional groups [208,226,227]. In both
are mostly hexadentate ligands, typically binding Fe(III) via three the linear H311 and cyclic H312, which are naturally produced by
bidentate functional groups [29]. As the An ions generally prefer Pseudomonas bacteria, three hydroxamate groups are responsible
higher coordination numbers (up to 12) binding to naturally occur- for the binding to Fe(III) as well as to trivalent Lns and to particular
ring siderophores often results in complexes of 2:1 (siderophore: Ans (i.e. Th(IV), U(VI), Pu(IV), Am(III) and Cm(III))
An) composition [214]. The physico-chemical similarity of Fe(III) [2,29,208,210,214,216,228–233]. Except for Ce(III) and Pm(III),
to the tetravalent Ans, and most notably Pu(IV), is mainly due to the stability constants for the entire series of Ln-11 complexes,
their comparable charge to ionic radius ratio which, for example, [LnIII(H11)]+ (with the remaining proton located on the terminal
is 4.6 e Å1 for Pu(IV) vs. 4.2 e Å1 for Fe(III). Additionally, the ten- amine group), were determined at seawater ionic strength [219].
dency to form highly insoluble hydroxides or colloidal species as The log b values for the preferred hexadentate binding mode
well as displaying similar binding constants for organic ligands increase with decreasing ionic radius of the Ln(III) and range
effectively makes Pu(IV) a close analogue of Fe(III) [213,215–217]. between 10 and 16 (Fig. 12).
In addition to siderophores produced by bacteria or fungi, The DFO complexes of the tetravalent Ans, Th(IV), U(IV), and
graminaceous plants (for example, barley and wheat) also secrete Pu(IV), all show remarkably high complex stabilities that are
Fe(III)-chelating compounds. These so-called phytosiderophores comparable with the corresponding EDTA complexes. Furthermore
containing amino and carboxyl groups [218] are significantly smal- they show high kinetic stabilities in contrast to the An(IV) com-
ler than siderophores produced by microorganisms [208,218]. plexes of DTPA, EDTA and DOTA [2,29,210,215,217,228]. The affin-
However, to the best of our knowledge, no f-element complexes ity of Pu(IV) for DFOs is high enough for its use in medical chelation
with this class of siderophores have been published to date. therapy [215]. The complex stability for the Pu(IV)-11 complex is
Over recent years, the investigation of f-element interaction higher than the Th(IV)-11 complex with log b values of 30.8(1)
with siderophores has mainly focused on the analysis of binding [234] and 26.6(1) [235], respectively. The trend of the distribution
modes and the determination of thermodynamic and kinetic com- coefficients Kd, however, is found to be in the reverse order, addi-
plex stabilities. This has resulted in further insight into fundamen- tionally showing a pH dependency, which underlines the potential
tal aspects of f-element complexation and has led to an increased influence of organic acids on the adsorption of Ans by microorgan-
awareness of possible biological implications as well as to the isms [210]. ESI-MS spectra confirm the formation of 1:1 Th(IV)-11

Fig. 11. Selection of naturally occurring siderophores. Potential chelating binding sites are shown in bold.
L. Götzke et al. / Coordination Chemistry Reviews 386 (2019) 267–309 277

carbonate, nitrate, oxalate or sulfonate that show coordination


numbers of 8, 10 or 12 and result in square antiprismatic, dodeca-
hedral or icosahedral coordination geometries [239]. With H311,
the coordination mode is expected to be similar to that for H312
and to have similar hydrolysis products [237].
Mixed catecholate-hydroxamate siderophores – Pyoverdines (PYs)
form a group of about 60 fluorescent species naturally produced by
the bacteria Pseudomonas aeruginosa and Pseudomonas fluorescens.
In general, they consist of three parts; the tricyclic chromophore
and the two side chains attached (see Fig. 11; R1 and R2). While
the chromophore bears a catecholate group to bind a metal centre,
Fig. 12. Stability constants (log b) of the hexadentate H311 complexes with Ln(III) the peptide chain (R2) carries two additional binding sites (hydrox-
(except for Ce and Pm) (the error bars are partly superposed on the data points) amate and/or a-hydroxy acid moieties); thus four protons can be
[219].
attached to the metal binding sites (H413; although the total num-
ber of acidic protons depends on the peptide sequence). The inter-
action of these siderophores with Ln and An ions in the oxidation
states +III, +IV and +VI has been investigated by UV-Vis, TRLFS (for
U(VI) and Cm(III)) and NIR spectroscopy for NpO+2 [134,240–242].
The determination of stability constants (log bMLH) by means of
UV-Vis spectroscopy with U(VI) and the PY mixture excreted by
Pseudomonas fluorescens, displayed high values of 30.5(4) (log b112)
and 26.6(4) (log b111), for two different PY complex species. The
values for the analogous determinations using TRLFS are only
slightly different at 29.60(43) (log b112) and 25.40(76) (log b111)
[134].
The formation of PY neptunyl complexes was identified by fol-
lowing changes in the characteristic absorption band of NpO+2 at
980 nm. The presence of three 1:1 complexes was indicated, corre-
sponding to species showing stepwise loss of protons on the bound
ligand, with values of log b112 = 26.9(7), log b111 = 20.9(6) and
log b110 = 13.40(17), respectively. Again, these high values indicate
a strong affinity of Np(V) for the catecholate-containing groups in
the PY siderophores [240]. Similar to uranyl and neptunyl, Cm(III)
also forms 1:1 complexes with PYs. Three complex species [Cm
Fig. 13. X-ray structure of the Pu(VI)-12 complex, [PuIV(12)(H2O)3]+ [237]. (H213)]+, [Cm(H13)] and [Cm(13)] were identified using TRLFS
by employing the distinct red-shifted emission band of the Cm
(III) aquo ion; formation constants (log b) of 32.50(6), 27.40(11)
complexes in which the binding mode is expected to be analogous and 19.30(17), respectively, were obtained for the above complex
to that of acetohydroxamic acid [236]. H311 is ideally suited for the species [242]. The consistently high constants for all reported
complexation of uranyl as it is a hexadentate ligand bearing three An-PY complexes of hard metal ions clearly reflect the presence
hydroxamate groups. Such 1:1 complexes were detected by ESI-MS of the hard oxygen binding sites in these PY-type siderophore
as well as by spectrophotometric titrations [230,231]. For example, ligands. PYs clearly bind An ions via their catechol groups, with
three species were identified by spectrophotometric titration, slightly more stable complexes being formed with Cm(III) relative
namely [UO2H211]+, [UO2(H11)] and [UO2(OH)(H11)], with stabil- to tetravalent Th(IV) or U(IV) and the uranyl ion [240,243]. UV-Vis
ity constants of 22.9(1), 17.1(4) and 22.8(3), respectively. The com- spectroscopic/pH titration studies have also confirmed that com-
plexes are stable over a wide pH range, with no reduction of uranyl plex formation occurs with Th(IV), U(IV) and U(VI), indicating coor-
arising from the presence of H311; further underlining the stability dination of the doubly deprotonated ligand H2132, with highest
of these complexes [231]. affinity for Th(IV) followed by U(IV) and U(VI) [244]. For PY-
The first structurally characterised siderophore complex with uranyl binding, pH values of up to 6.5 are optimal, most probably
Pu(IV) was published in 2000 by Neu et al. [237]. This complex due to uranyl hydrolysis interfering at higher pH values.
of H312 shows a Pu(IV) coordination number of nine. The PYs has been reported to result in high extraction of U(IV) from
Pu(IV)-12 complex is formed regardless of the plutonium oxidation monazite as well as from a Th-U-concentrate [245,246]. PYs bind
state employed for the synthesis, underlining the remarkable sta- to Fe(III) and Pu(IV) strongly via all three chelating groups (the cat-
bility of the complex. SC-XRD analysis of the Pu(IV)-12 complex, echolate, hydroxamate and the a-hydroxycarboxylic acid function-
[PuIV(12)(H2O)3]+, shows the nine-coordinated Pu(IV) in a tri- alities) and thus lead to the accumulation of both these metal ions
capped trigonal prismatic coordination sphere, with each of the in Pseudomonas putida [214,247].
three hydroxamate groups binding in a bidentate fashion, while Siderophore-actinides interaction in the environment – Natural
three water molecules complete the coordination shell (see siderophores are ubiquitous in nature. They have been found to
Fig. 13). The PuAO bond lengths range between 2.303 and affect, inter alia, the chemical speciation [212], complexation
2.375 Å, and are significantly longer than the FeAO bond lengths [214], and redox chemistry [1,214] of radionuclides in the environ-
in the corresponding Fe(III) complex (1.938–2.089 Å). This differ- ment and, as a consequence, also the migration behaviour of the
ence, as well as the change in the hydroxamate bite angle, from Ans in soils [212,215,222,231,237,248–250]. They are excellent
79.1° in Fe(III)-12 to 65.6° in Pu(IV)-12, indicates the flexibility of ligands for stabilising Ans in the oxidation states +III for late An
the H312 ligand [237,238]. This nine-coordinated Pu(IV) structure ions (for example, Am(III) and Cm(III)), +IV for early An ions (for
contrasts with the few structurally characterised Pu(IV) complexes example, Th(IV), U(IV) and Pu(IV)) as well as +VI for the uranyl
in the literature incorporating mono- or bidentate ligands such as ion (UO2+ 2 ) [2]. Complex stabilities directly follow the An ion’s
278 L. Götzke et al. / Coordination Chemistry Reviews 386 (2019) 267–309

net effective charge [1,212]. Thus, for uranium: U(IV) > uranyl > the surfaces of goethite and boehmite is drastically reduced to less
U(III), with the net effective charge on the uranyl ion being +3.2 than 20% on adding 240 mM H311 [218]. Yoshida et al. [254] inves-
(1) [1,231]. Another aspect is the high steric demand of the highly tigated the sorption of Ln ions onto Al2O3 in the presence of H311
stable actinyl ions (AnOn+ 2 ) compared to the simple An(III) or and found that the degree of sorption decreased as the atomic
An(IV) ions. Thus large, polydentate ligands (including sidero- number of the Ln increased; this was attributed to the increasing
phores) are normally restricted to occupying the equatorial plane Ln(III)-11 stability constants along the Ln series (see Fig. 12).
of actinyl ions whereas An(III) or An(IV) ions are able to be com- A further consequence of the strong An binding by siderophores
pletely enclosed on binding to siderophores [212]. In this context, is that the iron uptake in bacteria, fungi or plants strongly com-
it is noted that (similar to the behaviour of H312 [237]) the use of petes with An uptake and this has a significant impact on the
plutonium in oxidation states ranging from +III to +VI for H311 bioavailability of the latter [1,217,238,255]. Microbacterium flaves-
complex synthesis, produces only Pu(IV)-11. That is, Pu(III) is oxi- cens cells (JG-9) are reported to take up Pu(IV) and U(VI) by H311 in
dised by H311 to Pu(IV), whereas Pu(V) and Pu(VI) are reduced to a similar way to Fe(III), even though the uptake is slower [217,238].
Pu(IV), illustrating the extraordinary redox versatility of the DFOs In other studies it was shown that the Pu(IV)-11 complex tends to
[214,238]. remain on cell walls via binding to carboxylate, phosphonate, sul-
A study of the redox behaviour of Pu(IV) complexes, including fonate or hydroxyl groups (rather than being transported into the
those of the DFOs, H311 and H312, and PY, using cyclic voltamme- cells) [3,245]. This has been suggested to reflect the difference in
try showed a greatly decreased stability for the Pu(III) complexes the coordination numbers occurring for Fe(III) and Pu(IV). That is,
relative to those of Pu(IV), being 20 orders of magnitude lower in Fe(III) is coordinated by 113 to yield an approximately coplanar
the case of H311 [251]. The redox kinetics were found to be depen- arrangement, whereas the preferred higher coordination numbers
dent on the pH value as well as on the DFO concentration. For pH of 8–12 for Pu(IV) are reached by the additional coordination of
>7, the reduction leads directly to Pu(IV), whereas under acidic water molecules. This difference in the respective coordination
conditions a stepwise reduction to Pu(V), then finally, at a signifi- spheres was proposed to account for the above differences in cell
cantly slower rate, to Pu(IV) occurs. Interestingly, 12 equivalents of uptake [217]. In any case, bacteria-secreting siderophores are able
plutonium were shown to be reduced by each single molecule of to incorporate Ans into cells via ion channels, leading to an accu-
DFO. In contrast, the uranyl complex of DFO was shown to be redox mulation of the Ans in the cells [3]. In Pseudomonas putida the
stable [238]. accumulation rate of Pu(IV) by PY is similar to that for iron
Due to the low concentration and complex speciation of An [214]. The analogous behaviour of Pu(IV) and Fe(III), including sim-
compounds in the environment, their detection is difficult. ilar transport properties in mammals, clearly accounts for much of
Nonetheless, ESI-MS offers a possible means for dealing with this the biological hazard posed by plutonium in biosystems [29].
problem. Indeed, Th(IV) and uranyl siderophore complexes have Applications of siderophore-actinide interactions – Alongside the
already been detected using this method [230,236]. A rapid test natural biological weathering of soil minerals and biogeochemical
to at least show the presence of uranyl-complexing siderophores cycling of iron in the ocean [208,256], biotechnological applica-
excreted by microorganisms involves the use of two dyed agar tions involving siderophore-An interactions range from enhancing
plates (one containing a Chrome Azurol S-Fe(III) dye and the other growth and pathogen biocontrol in plants, biocontrol of fish patho-
containing a Chrome Azurol S-U(VI) dye) [232]. The contact of the gens [208], along with roles in microbial ecology and taxonomy
dyed agar plates with strongly coordinating ligands, such as H311, [208]. They have also been employed for bioremediation of envi-
causes a discolouration which is due to the decomposition of the ronmental pollutants (metals, petroleum hydrocarbons)
highly-coloured Chrome Azurol S complexes and the formation of [208,212,226], for incorporation in optical biosensors [208], for
the appropriate siderophore complex. The extent of this dis- bio-leaching of pulps [208], for medicinal chelation therapy
colouration showed a regular and reproducible relationship to [2,29,226,257,258] as well as for nuclear fuel reprocessing
the amount of siderophore added. The ratio of the discolourations [208,226,249,259]. The previously discussed extremely high com-
of the two agar plates turned out to be independent of the amount plex formation constants and the associated selectivity of sidero-
of siderophore added. phores for Ans in specific oxidation states also makes them ideal
Reflecting the high stability of An siderophore complexes, side- reagents for selective An extraction; for example, of Pu(IV) from
rophores like DFO and EB are not only able to form complexes with radioactive waste [249] or neptunium form the solvent phase dur-
dissolved An ions, but are also able to solubilise metals/metal oxi- ing the PUREX process [208,226].
des on mineral surfaces through complexation [214,243,245]. Siderophores have been employed under physiological condi-
Thus, for example, they have been found to leach uranium tions [2,29] as radiopharmaceutical and decorporation agents for
occurring in slate mines, or dissolve An solid compounds such as Th, U, Np, Am and Cm. Once again, both their high selectivity
Pu(IV) oxide or hydroxide under anaerobic conditions to form dis- and stability makes them ideal candidates for such therapeutic use.
solved complex species. Nevertheless, as might be expected, the Studies show that DFOs could potentially replace An complex-
process of dissolving such solids is quite slow [214,229,231,238]. ing species in blood, soft tissues and bone leading to the applica-
Solubilisation rates have been determined for the hydroxamate tion of DFOs for medical decorporation (for example, H311 with
siderophores H311 and EB towards plutonium dioxide in water, the trade name ‘‘Desferal”) of Ans (such as Pu) with a considerable
with the faster dissolution occurring for EB (103 times faster than success for liver and bones of rats [260]. The drawback is the gen-
for H311). Kinetic studies further confirmed that PuO2 dissolves erally slow reaction, an inefficiency for the Pu-removal from the
more quickly in the presence of the Fe(III)-EB complex compared kidney caused by the low pH yielding a partly dissociation of the
to EB alone. A possible reason proposed for this is that it could H312-complex, as well as a low selectivity of the ligand against
reflect the preorganisation of the ligand in the Fe(III) complex. trivalent Lns and Ans [29].
Interestingly, the presence of the Fe(III)-11 complex also pro-
motes the dissolution of uraninite (UO2) by H311 [216]. On binding 3.2.2. Artificial siderophore analogues
to an An, H311 uses all available functional groups. This was pro- As discussed already, natural siderophores are excellent Fe(III)
posed to potentially hinder the adsorption of the An species onto binding ligands whose functional groups are ideally positioned
the anionic binding sites of mineral oxide surfaces and hence have for hexadentate binding to this ion [214]. A biomimetic approach
a strong impact on An mobility [230]. Similar behaviour has been was employed for the design of synthetic siderophore-like
shown for Lns [243,252,253]. For example, Eu(III) adsorption onto octadentate ligands containing hydroxamate and catecholate func-
L. Götzke et al. / Coordination Chemistry Reviews 386 (2019) 267–309 279

tions for binding An(IV) ions [221,261]. Upon complexation, these


ligands’ functional motifs form four five-membered chelate rings
[193,262], leading to eight-fold coordination to yield a dodecahe-
dral coordination geometry; such a geometry had previously been
observed for unconstrained complexes of Pu(IV) incorporating
bidentate catechol ligands. Such ligands are very often of the
CAM class (with catechol functions, including the sulfonated
CAM(S), carboxylated CAM(C), and amide derivatives (TAM,
IAM)) or of the HOPO class [29,30,259] (in 1,2- or 3,2-
constitution) being isoelectronic and isostructural with the cate-
cholate dianion in its imine resonance form. The options to com-
bine these chelating units with a variety of different core
structures (for example, LI. . . and CY. . ., with linear and cyclic
backbones, respectively) to di-, tri-, and tetrapodant ligands are
manifold (see Fig. 14) [29,255,257].
Catecholates – Promising linear catechol ligands have been
developed for use in therapeutic decorporation therapy in vivo;
Fig. 15. Protein structure of siderocalin-bound complex, [ThIV(14)]4 (only one of
these include the 3,4,3-LICAM (H814, structure can be derived the pendant arms was found to be ordered in the structure; PDB ID 5KID) [221].
from Fig. 14) and its sulfonate and carboxylate derivatives, 3,4,3-
LICAM(S) and 3,4,3-LICAM(C), for use as Pu(IV)-specific chelators
[259]. These ligands are, just like their 1,2-HOPO derivatives (see
hydroxypyridinonates section), structurally enhanced synthetic towards more acidic catecholate analogues. An example is the
derivatives of EB and can serve as chelators for a-emitting 225Ac potentially octadentate 3,4,3-LI(1,2-HOPO) (H415, structure can
or 227Th in therapeutic cancer therapies. The Eu(III) and Th(IV) be derived from Fig. 14), containing four HOPO groups, which
complexes with H814 show extremely high thermodynamic stabil- was shown to form stable An complexes and have potential thera-
ity with log b values of 29.65(65) ([EuIII(14)]5) and 47.71(8) peutic application as an An decorporation agent [222]. H415 and
([ThIV(14)]4); the values for their protonated analogues are the HOPO derivative of H311 form very stable eight-coordinated
41.75(6) ([EuIII(H14)]4), 46.79(14) ([EuIII(H214)]3), and 55.36(9) complexes with Pu(IV) [29,259]. These high stabilities point to a
([ThIV(H14)]3). These values show that H814 is one of the most potential application as a Pu(IV) specific extraction agent [259].
powerful chelators for tri- and tetravalent metal ions at physiolog- The first structurally characterised Pu(IV) complex incorporating
ical pH. Despite only one pendant arm of the ligand was found to a synthetic HOPO was published in 2005 [193]. Two molecules of
be ordered in the X-ray structure, the binding of the metal com- the linear ether-bridged ligand, 5-LIO(Me-3,2-HOPO) (H216, struc-
plexes [MIV(14)]4 (M = Zr, Th) to the protein siderocalin was able ture can be derived from Fig. 14), coordinate to a Pu(IV) centre in
to be verified by SC-XRD (see Fig. 15) [221]. an octadentate fashion, with [PuIV(16)2] units stacking in a
Hydroxypyridinonates – Synthetic ligands inspired by multiden- sandwich-like arrangement in the lattice (see Fig. 16 right). An
tate HOPOs represent a further development of the CAM series analogous coordination arrangement occurs in the corresponding
Ce(IV) complex (see Fig. 16 left) [263]. Both, H216 and the poten-
tially hexadentate TREN(Me-3,2-HOPO), were designed to be
effective chelators for the removal of Pu(IV), Am(III), Np(V)/(VI)
and U(VI) for use in humans [193].
H415 is able to bind trivalent Ln ions such as Eu(III) and Gd(III)
as inactive analogues for corresponding An(III) species. A log b110
value of 20.2(2) was determined spectroscopically for formation
of the 1:1 complex, [EuIII(15)] [264] and corresponding complexes
of this ligand with Zr(IV) and Pu(IV) show even higher stability
constants: log b110 = 43.1(6) for [ZrIV(15)] and 43.5(7) for
[PuIV(15)]. Further, H415 was confirmed to be of low toxicity. For
these reasons, H415 was considered for use in 227Th-a-
immunotherapy (the log b for [ThIV(15)] is 40.1(5)) [228] as well
as for the therapeutic removal of Ln and An ions (including
Th(IV), Pu(IV) and U(VI)) from the human body. Further, even the
transuranium elements Cf(III) and Hf(III) are bound by H415 and
the resulting complexes interact with the protein siderocalin
(forming adducts via hydrogen bonds and weak interactions, such
as p-p and cation-p interactions). An adduct of this type was the
first reported structurally characterised macromolecular Cf(III)
assembly (see Fig. 17 right) [224]. In this, the Cf(III) is coordinated
by only two of the 1,2-HOPO groups of H415, whereas with Sm(III),
Am(III) and Cm(III), eight coordination occurs giving rise to snub
disphenoidal coordination geometries (see Fig. 17 left) [220].
Complex formation between Bk(IV) and H415 has been demon-
strated by UV-Vis spectroscopy, giving rise to absorption bands at
Fig. 14. Some synthetic siderophore-inspired ligands with their previously 305 and 400 nm for the characteristic p-p* transition for 1,2-HOPO
employed nomenclature. The backbones of the ligands are classified according to
the length of their bridging alkyl chains (indicated by numbers). The coordinating
and ligand-to-metal charge-transfer transition(s), respectively.
units are attached in the R positions. A comprehensive literature review of synthetic Interestingly, Bk(IV) is stable under mild aqueous conditions in
analogues is available [29]. the presence of this siderophore analogue [224]. Kelley et al.
280 L. Götzke et al. / Coordination Chemistry Reviews 386 (2019) 267–309

Fig. 16. Molecular structures of Ce(IV) (left [263]) and Pu(IV) (right [193]) complexes, each incorporating two 162 (5-LIO(Me-3,2-HOPO)) ligand molecules.

recently published a combination of theoretical calculations and ligand CYTAC (N,N0 ,N00 ,N000 -tetrakis(acetylacetonato)-1,4,8,11-tetraa
EXAFS studies undertaken to determine structural and thermody- zacyclotetradecane) exhibit selectivity for Fe(III), Th(IV), and
namic properties of the whole Ln(III) and An(III)/(IV) H415 com- Nd(III), with Th(IV) and Nd(III) acting as analogues for Pu(IV) and
plex series. The ligand binds via the oxygen atoms of the 1,2- Am(III).
HOPO units and shows a high redox activity and consequently A potentiometric titration study coupled with structure
serves as an electron density donor or acceptor, leading to excep- modelling indicated that the artificial hydroxamate siderophore
tionally high complex stabilities for the whole An series and stabil- analogue cyclohexane-1,2-diyl-dinitrilotetra(N-methylaceto-
ising the Ans in their preferred oxidation state. DFT calculations hydroxamic acid) (H417) forms 1:1 and/or dimeric 2:2 complexes,
confirm a higher An(IV) complex stability compared to corre- [ThIV(17)] and [ThIV
2 (17)2], in which the metal centres are eight coor-
sponding An(III) complexes; a result that is consistent with the dinated to yield a tetragonal antiprismatic geometry. The binding of
experimental findings [222]. 174 to the Th(IV) in the modelled structures occurs via the carbonyl
Hydroxamates – The hydroxamates are a further class of effec- and the a-hydroxy oxygen atoms [265].
tive synthetic Pu(IV)-binding siderophore analogues. In particular,
tetrahydroxamates (see Fig. 18) [259] have been developed for 3.3. Calix[4]arenes – effective ligands for f-elements
selective extraction of Pu(IV). Studies show that the hydroxamate
derivative CYTROX (N,N0 ,N00 ,N000 -tetrakis(acetohydroxamato)-1,4,8, Calix[4]arenes [266] (see Fig. 19) are cyclic polyphenols derived
11-tetraazacyclotetradecane) and the related (non-hydroxamate) from phenol-formaldehyde condensation reactions [267,268]. They

Fig. 17. Structures of siderocalin-bound complexes of Sm(III) (left; PDB ID: 4ZHH) [220] and Cf(III) (right; PDB ID: 5KIC) [224] with H415 (3,4,3-LI(1,2-HOPO)).

Fig. 18. Structures of CYTROX, CYTAC and H417 employed for An(IV) extraction.
L. Götzke et al. / Coordination Chemistry Reviews 386 (2019) 267–309 281

of co-extractants that lead to synergism, giving rise to both


enhanced extraction as well as (in some cases) also to higher
selectivity [297,298]. Synergistic solvent extraction of Lns and
Ans using a combination of a p-tert-butylcalix[4]arene and a
diketone, such as tetrakis(N,N-diethyl-acetamide)-calix[4]arene
(18) and 4-benzoyl-3-phenyl-5-isoxazolone (HBPI), was attributed
to co-complexation of the diketone. Based on spectroscopic data,
Fig. 19. Representation of the cone conformation. three deprotonated BPI units chelate to the respective Ln(III) ions
in concert with the pendant carbonyl oxygen donors of a
have a rich coordination chemistry with their ability to form com- calix[4]arene unit to yield the resulting overall coordination
plexes with main-group, d- and f-block elements now being well number of ten (Fig. 20) [299].
documented [269–276]. Since the first reported X-ray structure Similar 1:1:3 (Ln:calixarene:coligand) complex stoichiometries
of a binuclear Eu(III) complex with p-tert-butylcalix[8]arene by were determined for various other p-tert-butylcalix[4]arene/
Harrowfield and co-workers [277], the X-ray structures of a range diketone systems [300–302]. Compound 19 incorporating four
of Ln and An calix[4]arene complexes displaying different stoi- phosphinoyl pendant arms is a representive example [303,304]
chiometries have been reported [278–281]. (Scheme 4). Typically, the use of such calix[4]arene derivatives as
The parent calix[4]arene is unable to fully coordinately saturate co-extractants with a range of chelating extractants has been
a bound Ln or An ion. Thus, in order to accommodate the higher found to improve the extraction efficiency of Ln(III) ions very sig-
coordination numbers of these ions or to tune the properties of nificantly with synergistic effects of up to three-fold being
the resulting complexes, many lower-rim functionalized calix[4] observed [305]. The extraction efficiency of such ternary complex
arene-ligands bearing substituent ‘arms’ incorporating additional systems was found to improve further upon going from organic
donor functions have been synthesised. The rigid calixarene back- solvents to ionic liquids [306].
bone ensures that the pendent arms are somewhat preorganised The affinity of f-elements towards P@O groups is well docu-
[282,283], thus aiding control of subsequent complexation beha- mented, and several calixarenes bearing pendant phosphonate
viour towards the above ions [284]. The incorporation of hard oxy- (AP(@O)(OR)2) and phosphine oxides (AP(@O)R2) have been pre-
gen donors in the arms (such as carboxylate, ether, and pared [37]. A crystallographically characterised La(III) complex of
phosphonate groups) leads to increased affinity towards the Lns, 19, [LaIII(19)(H2O)5]3+ (see Fig. 20 right), shows that La(III) is coor-
whereas slightly stronger interactions are obtained for the Ans dinated to four phosphine oxide O atoms, but not to the lower-rim
when softer S- and N-containing donor groups are incorporated phenolether oxygen donors [307]. Instead, the coordination sphere
[21,22]. is completed by five water ligands. Notably, 19 and a more lipho-
The focus of the following discussion is on more recent develop- philic derivative with octyl in place of the tert-butyl substituents
ments in the coordination chemistry of lower-rim substituted calix were found to be more effective extractants for the Ans (U(VI),
[4]arenes towards f-elements, with emphasis on aspects which are Th(IV)) than for the Lns (La(III), Eu(III)) [308–310].
seen to have implications for the chemical and physical behaviour Despite the maturity of the field, the utilization of O-
of Ln and An ions towards naturally occurring phenol ligands. The functionalized calix[4]arenes as selective ionophors for Lns and
reader is referred to published excellent review articles covering Ans continues to be an active research field. Modification of the
earlier work in this area [39,285–290]. Where appropriate, some number and type of O-alkyl residues provides a means for tuning
chemistry involving upper-rim functionalized ligands has been structure–property relationships towards selective improvements
included here. However, the f-element chemistry on calix[n]arenes [274]. The complex structures [LnIII(20)(pic)]n+ (Ln = Sm, Gd, Ho,
with n > 4 [291,292], of calix-arene-based coordination polymers, Yb) of the mixed ligand, tris-amide-substitued calix[4]arene
as well as of thiacalixarenes is not discussed [293–295]. Where (H20), bearing one unsubstituted phenol group, together with
seemed appropriate, potential applications are also mentioned. picrate (pic) provide illustrative examples [311,312]. Upon moving
along the Ln series from the Sm(III) to the Yb(III) complex, subtle
3.3.1. Separation and extraction of lanthanides and actinides by lower- changes occur in the Ln(III) coordination environment. The pic
rim functionalized calix[4]arenes anion acts as a bidentate ligand with Sm(III) [311] and Gd(III)
Lower rim functionalized calix[4]arenes have attracted much [312] (see Fig. 21 left), is monodentate in the Ho(III) complex
attention as extractants for the separation of trivalent Lns from (see Fig. 21 middle), and in case of the smaller Yb(III) cation, it is
Ans [296]. A particular interest in these studies has been the use no longer found in the first coordination sphere [311].

Fig. 20. Structural formulas of [LnIII(18)(BPI)3] (left) [299], and [LnIII(19)(BPI)3] (middle) [303,304] and the molecular structure of [LaIII(19)(H2O)5]3+ (right) [307].
282 L. Götzke et al. / Coordination Chemistry Reviews 386 (2019) 267–309

Scheme 4.

Lower-rim substituted derivatives with two pendant arms in a proximally-substituted calix[4]arene bisamide (H221) towards
1,2-arrangement [270,313] or with two different substituents have La(III) has been reported recently [315]. The crystal structure of
rarely been investigated [314]. However, coordination of [LaIII(H21)(pic)2] reveals a ten-coordinated La(III) ion, with the
L. Götzke et al. / Coordination Chemistry Reviews 386 (2019) 267–309 283

Fig. 21. Molecular structures of [SmIII(20)(pic)]+ (left), [HoIII(20)(pic)]+ (middle) [311] and [LaIII(H21)(pic)2] (right) [315].

Fig. 22. Molecular structures of [LaIII(22)(NO3)2](NO3) (left) and [PrIII(22)(NO3)(MeOH)](BPh4)2 (right) [316].

latter bound to six calixarene and four pic oxygen atoms (see ation and extraction properties investigated [325–327]. Calix[4]
Fig. 21 right). arenes appended with four DGA units to give 24 were found to
The coordination behaviour of the neutral calix[4]arene-based show excellent An ion extraction [328–330] and transport proper-
ligand 22, incorporating pendant phosphonate esters in the 1,3- ties [331,332]. The complexation of Eu(III) (as a surrogate for
and picolinamide groups in the 2,4-distal positions, has also been Am(III)) with 24 was studied by UV-Vis spectrophotometric titra-
investigated. Complexes of type [LnIII(22)(m1,3-NO3)2]+ (Ln = La, tion, luminescence titration and microcalorimetry to reveal the
Pr, Eu, Gd) were isolated [316], of which the La(III) and the Pr(III) formation of a 1:1 metal/ligand species. Fluorescence lifetime mea-
complexes were characterised crystallographically. Both display surements and DFT calculations suggested that the metal ion is
ten coordination by binding phosphoryl and amide oxygens as well bound to nine oxygen atoms from three DGA arms without
as the pyridine nitrogens from 22 along with four oxygen atoms of inner-sphere water molecules being present [333]. Extraction
two chelating nitrato ligands (see Fig. 22 left). In the case of the studies with ligand 25, carrying four pendant DGA units with
Pr(III), Eu(III) and Gd(III) complexes, metathesis of the nitrate shortened aliphatic chains, show a five- to seven-fold higher
counterion was accompanied by the replacement of one nitrato extraction selectivity for Eu(III) over Am(III). Slope analysis
coligand by a methanol molecule to yield the dicationic [LnIII(22) revealed that both metal ions are extracted as neutral
(m1,3-NO3)(MeOH)]2+ species (see Fig. 22 right). Solvent extraction [MIII(NO3)3(25)] complexes [334].
experiments with Ln picrates reveal that 22 is able to extract both An investigation of the An(III)/Ln(III) separation by solvent
La(III) and Eu(III) from an aqueous medium into a chloroform extraction employing different calix[6]arenes bearing N-
organic phase. heterocylces of different basicity, showed that the less basic pyra-
Calixarenes also have potential application as selective com- zine derivative induces an increased efficiency compared to the
plexation reagents for nuclear waste water treatment [317–320]. related pyridine derivatives [335]. The complexation behaviour of
The upper rim carbamoylmethylphosphinoxide (CMPO) deriva- calixarenes of type 26, incorporating four pyrazine pendant arms
tized calix[4]arene 23 is an early example that remains an effective carrying additional subunits (carbamoyl dioctyl, diisopropyl phos-
reagent for the above application, with significantly increased phonate, or diphenyl phosphoryl) towards Am(III) and Eu(III) in
extraction ability and selectivity towards Ans when compared ionic liquids has been studied by solvent extraction and lumines-
with the acyclic (non-derivatised) CMPO [321–323]. The solution cence spectroscopy [336,337]. Also, results from optical absorp-
behaviour of the calixarene derivative, however, was not as simple tion, luminescence and 31P NMR spectroscopy studies suggest
as expected. Bis-ligand complexes and polymeric assemblies were that only two of the four extended arms coordinate with the Ln
observed to form rather than simple 1:1 species. ion, with each arm acting as a tridentate moiety; three additional
Diglycolamides (DGAs) are another versatile class of organic water molecules complete the coordination sphere.
ligands that have been employed for the selective extraction of The development of water-soluble sequestering agents for
Ans from high-level radioactive wastes [24,324]. Glycolamide in vivo chelation and decorporation of radionuclides is also of par-
units were attached to calix[4]arene backbones and their complex- ticular interest [29,338]. The proven ability of HOPO and CAM(S)
284 L. Götzke et al. / Coordination Chemistry Reviews 386 (2019) 267–309

Fig. 23. Molecular structures of the Eu(III) and Pr(III) complexes with the dipodal and tripodal tetrazole derviatised calix[4]arenes H429 and H430, respectively (left:
[EuIII(H29)(H2O)2] [341], right: [PrIII(H330)(OAc)(H2O)5(OEt)]EtOH [342]).

Fig. 24. Molecular structures of the Nd(III) complex of the tetrapodal ligand 31 ([NdIII(31)(H2O)]3+) (left) [346] and the Tb(III) complex with the tripodal ligand H20 ([TbIII(20)
(DMSO)]2+) (right) [351].

ligands (see Section 3.2.2) for in vivo complexation of U(VI) led to be controlled by addition of base, with emission occurring in the
the development of the calix[4]arene-based CAM(S) and HOPO visible and IR regions [341]. The tris(tetrazole) derivative H430
ligands H1227 and H428, respectively [339]. The dipodal HOPO cal- has also been synthesized, but was found to be a less effective
ixarenes are water-soluble and show a significant affinity towards ligand. Thus, in the Pr(III) complex the calix[4]arene acts only as
uranyl ions under acidic and neutral conditions. The dipodal a monodentate ligand (neglecting the H-bonds in the second
CAM(S) calix[4]arenes are also effective ligands for this ion but sphere) (see Fig. 23 right) [342]. The tetrakis(tetrazole) compound
are only so in alkaline media. does not form a Ln complex at all [343].
The p-tert-butylcalix[4]arene 18 with four appended amide
3.3.2. Luminescent probes and materials incorporating lanthanides groups represents one of the archetypal ionophores based on the
based on lower-rim functionalized calix[4]arenes calixarene framework [344], but surprisingly only one Ln(III) com-
The complexation of f-elements by calix[4]arene ligands has plex appears to have been structurally characterised so far [345].
also been pursued as part of the search for novel luminescent Replacement of the tert-butyl groups by allyl moieties provides
probes and materials [340]. The calix[4]arene backbone can serve the calix[4]arene tetraamide 31 for which Nd(III) and Dy(III) com-
different functions; for example, as the coordinating site for the plexes have been characterised by X-ray crystallography [346].
Ln ion(s), as a chromophore unit (enabling an ‘‘antenna” effect Both structure determinations show the presence of a tricationic
and energy transfer from excited phenol ligand states to those of [LnIII(31)(H2O)]3+ complex (Fig. 24) with the calixarene binding
the Ln(III) ions), or to serve as the anchor unit for the attachment in an octadentate fashion; a single bound water molecule occupy-
of polymerizable groups for integration of the system into devices ing the calixarene cavity completes the slightly distorted capped
and materials. The p-tert-butylcalix[4]arene H429 bearing two square-antiprismatic coordination geometry of the metal atom.
tetrazole moieties is a recent example. It forms luminescent 1:1 Corresponding Tb(III), Dy(III) and Sm(III) complexes are all lumi-
complexes of the type [LnIII(H29)(H2O)2] (Ln = Nd, Gd, Eu, Tb), nescent in acetonitrile at room temperature.
the metal-centres being coordinated by the four phenol oxygen, The synthesis and photophysical properties of a series of octa-
two tetrazole nitrogen (N1) atoms of H429 and two water mole- coordinate Tb(III) complexes of the piperidine substituted calix
cules (see Fig. 23 left). Notably, the luminescence properties can [4]arenes 32 and 33 have also been reported [347]. Successful
L. Götzke et al. / Coordination Chemistry Reviews 386 (2019) 267–309 285

Fig. 25. Schematic (left) and solid state structure (right) of [EuIII
2 (H335)2]2CH3CN [358].

sensitization of the Tb(III) emission occurred in each case upon has been reported [359]. The key to the synthesis of clusters rather
excitation of the calixarene’s aryl units, reflecting energy transfer than mononuclear complexes in this study was the use of an
occurring within the complex. Complexes of 32 with its shorter ammonium acetate buffer to adjust the protonation state of the
and less flexible arms gave rise to significantly higher quantum calix[4]arene moiety. The cluster cores are based on Ln5O6 trigonal
yields (/ = 19.0, 18.6 vs 0.5, 0.2). The stability constants of the bipyramids. The magnetic properties of these compounds were not
1:1 complexes in methanol determined by luminescence titration reported.
fall in the range log b11 = 5.3–8.2. A Gd(III) complex of a tetrapodal pyridine-N-oxide functional-
The preparation of transparent polymeric materials exhibiting ized DOTA calix[4]arene has also been characterized. This com-
luminescent properties continues to be an attractive research field pound aggregates in water to form spherical micelles with a
[348,349] due to the many potential applications that, for example, radius of 8.2 nm, the critical micelle concentration being 35 lM.
range from light emitting devices to sensors [48]. Thus, the allyl- The relaxivity of these aggregates is 31.2 s–1mM1 at 25 °C and
functionalized calix[4]arene trisamide ligand H34 was utilized as 20 MHz, which corresponds to a molecular relaxivity of
a cross-linking agent in the polymerization of methyl methacrylate 125 s–1mM1. These calix[4]arene ligand derivatives appear to
and subsequent swelling of the resulting polymer monolith with show promise for the preparation of new magnetic resonance
TbIII(NO3)3(DMSO)4 yielded a luminescent material. The two-step imaging agents [360].
approach avoids the presence of inorganic components in the poly-
merization medium, which would otherwise lead to phase segre-
gation and loss of transparency [346]. The resulting hybrid 3.4. Porphyrins
materials can be tuned to emit various colours, even white, by
impregnating them with an appropriate mixture of Ln salts Because of their appearance in biological systems (for example,
[350]. An X-ray crystal structure of the reference compound as hemes), porphyrins (Por) are common biorelated ligands,
[TbIII(20)(DMSO)](ClO4)2 (see Fig. 24 right) revealed the presence belonging to a more general class of cyclic tetrapyrrolic molecules
of an octa-coordinated Tb(III) centre bound to phenolate, ether, (Fig. 26). Native Pors, such as protoporphyrin IX, feature mainly ali-
carbonyl and DMSO oxygen donors – a structure which most likely phatic substituents in the b-positions and are distinguished by the
occurs in the polymer as well [351]. lack of any meso-substituent. In contrast, synthetic Pors often bear
aromatic residues in all four meso-positions, like the well-
established group of easily assessable tetraarylporphyrins, of
3.3.3. Magnetic properties of lanthanide complexes supported by which 5,10,15,20-tetraphenylporphyrin (H2TPP) is the simplest
lower-rim functionalized calix[4]arenes representative. An analogous class of synthetic ligands, which need
While the often unusual magnetic properties of Ln complexes to be mentioned here because of their similar coordination proper-
have been widely investigated [352–354], such studies involving ties, are the phthalocyanines (Pc). They differ from Pors by the
Ln calixarene complexes have been more limited [355–357]. The presence of bridging nitrogen atoms in the meso-positions and an
synthesis of the calixarene-based N4O4-donor ligand H635 bearing expanded p-system due to the presence of attached benzene rings.
two 8-hydroxyquinoline-2-carbaldehyde units and its ability to Both Por and Pc macrocycles have been widely used for coordina-
form the dinuclear complex, [EuIII 2 (H335)2]2CH3CN, has been tion to various metal ions via their four coplanar preorganised
reported (see Fig. 25) [358]. The Eu(III) centres in this complex donor atoms. Besides the bio-relevant d- or main group elements
are well-separated at >8 Å, being coordinated by two tetradentate (for example, Fe(II/III), Ni(II), Co(II), Mg(II)), REEs also readily coor-
hydroxyquinoline-2-carbaldehyde-hydrazone units to give each dinate to these ligands and reviews focusing on the coordination
metal a dodecahedral geometry; there are no magnetic exchange chemistry of Ln(III)-Por species [361], synthetic strategies for
interactions between the Eu(III) ions in this case. preparing REE-Pc and REE-Por complexes [362], as well as on the
More recently, the ability of the dipodal tetrazole derivatised emission properties of Ln(III)-Por species [363,364] have appeared.
calix[4]arene H429 to form polynuclear Dy9 and Dy12 complexes Systems, in which the Ln(III) ion is not directly coordinated to the
286 L. Götzke et al. / Coordination Chemistry Reviews 386 (2019) 267–309

Sandwich complexes of Tb(III), Dy(III), Ho(III), Er(III), Tm(III),


and Yb(III), as well as Y(III) have been reported recently for both
H2TPP [369] and H2Pc [370] with the tetradentate macrocyclic
ligand cyclen as the second ligand. The absorption spectra are
almost identical for both ligand series and correlate well with
the corresponding spectra of typical [LnIII(TPP)]+ and [LnIII(Pc)]+
complex species. For the H2TPP complexes there is a very intensive
Soret-band at 422 nm and two less intensive Q-bands in the
range between 548 and 586 nm. In the case of the H2Pc complexes
there is an intensive Q-band at 677 nm with a weaker Soret-band
at 349 nm. The nitrogen atoms of the tetrapyrrolic ligand and the
cyclen coordinate to the metal centres in a square-antiprism
arrangement (see Fig. 28) with (almost) parallel N4-planes from
both ligands. The distances of the metal centres to the N4-plane
of the tetrapyrrolic ligand are smaller than the distances to the
cyclen N4-plane; this was attributed to the ligand charge in the for-
mer case as well as to the presence of steric hindrance involving
the hydrogen atoms on the cyclen nitrogen atoms.
Due to an efficient energy transfer from the ligand to the metal
centre, tetrapyrrolic ligands can be employed as antennae for sen-
sitizing the bound Ln ions for inducing light emission in the NIR
region (see Fig. 29) [363]. Such luminescent behaviour can be
observed for Por complexes with Lns exhibiting low-lying f-states
(such as Yb, Er, Nd, Ho, and Pr) and is of particular interest because
Fig. 26. Structures of three Pors and H2Pc.
of its potential application in biological imaging and in telecommu-
nications. The f-f transitions involved are sensitive to non-radiative
tetrapyrrolic core, but to a coordinating subunit (such as DOTA) quenching by vibrations of high-energy oscillators (such as O–H,
covalently linked to the Por-core, are not included in the present N–H and to a lesser extent C–H bonds); thus an effective shielding
discussion. Aspects of the chemistry of such systems have been of the Ln(III) ion is essential for a high quantum yield to be
presented in other reviews [361,363,365]. achieved. Hu et al. [366] investigated Yb(III) complexes of
On coordination, the REEs lie displaced from the tetrapyrrolic H2TPP derivatives incorporating a Kläui ligand (for example
nitrogen plane of Pors and Pcs (as shown in Fig. 27 [366]), reflect- {YbIII(36)[Co(Cp)(OP(OMe)2)3]}) (Fig. 27, Scheme 5). They found
ing the large ionic radii of these ions. Further, the four nitrogen that the replacement of the hydrogen atoms in their porphyrinate
donor atoms are not sufficient to coordinately saturate a Ln ion; ligand and the Kläui ligand by fluorine and deuterium, respectively,
thus, additional ligands are needed to complete the coordination improved the intrinsic quantum yield by up to 75%. Compared to
shell. The vacant coordination sites are either occupied by (at least the impact of the b-pyrrolic C–H bonds of the porphyrin and the
three) monodentate ligands or (one or two) additional chelating phosphito C–H bonds of the Kläui ligand, the C–H bonds of the
ligands. The tridentate, cobaltocene-derived phosphonate metal- meso-phenyl groups only have a minor effect on the Yb(III) lumines-
loligand, [Co(Cp)(OP(OR)2)3] (with Cp being cyclopentadienyl cence. Similar Yb(III) complexes with such b-fluorinated Pors bear-
ligand and R being a short alkyl residue) introduced by Kläui ing water-soluble groups on their meso-phenyl moieties (such as
[366–368], is quite commonly used to stabilise Ln(III) complexes glycosyl, carboxyl, and triphenylphosphonium) and the deuterated
of Pors and Pcs. If a second tetrapyrrole ligand binds, a sandwich Kläui ligand have been used for NIR living-cell imaging [371]. The
or ‘‘double-decker” complex may be formed. In the case of Pcs, complexes showed a high NIR luminescence quantum yield (up to
the double-decker compounds are formed as stable neutral 13% in water) and only a low cytotoxicity in the dark for the
p-radicals of the kind [Pc2LnIIIPc] (where H2Pc is the parent employed HeLa cells (cell viability >80%); the phototoxicity of the
compound for the class of Pcs), which can be oxidised or reduced Yb(III)-Por complexes was negligible. Except for the glycosyl
to [LnIII(Pc)2]+ or [LnIII(Pc2)2], respectively [362]. derivatives, all complexes were taken up by the cells and emitted
a specific intracellular Yb(III) luminescence signal. Due to potential
photobleaching of biological samples, the shift of the excitation
wavelength from the UV or near-UV range to longer wavelengths
was seen to be an advantage. This was achieved by the
combination of an Yb(III)-TPP complex with another chromophore,
namely a boron dipyrromethene (BODIPY) functionalised
1,10-phenanthroline (BDP-Phen), as second ligand [372]. The NIR
emission of the [Yb(TPP)(OAc)(BDP-Phen)] complex could be sen-
sitised by excitation of both the Por as well as the BODIPY moieties.
As can be seen from the energy diagram presented in Fig. 29,
Por complexes can also exhibit fluorescence as well as phosphores-
cence due to S1 ? S0 and T1 ? S0 transitions, respectively. While
the intensity of the fluorescence is not affected in the presence of
oxygen, the phosphorescence is quenched. This phosphorescence
quenching is attributed to the excitation of oxygen molecules from
their triplet ground state (3O2) to singlet oxygen (1O2) and shows a
linear correlation over a wide range of oxygen concentration. Thus,
such systems are well-suited for oxygen sensing [373]. Moreover,
Fig. 27. Molecular structure of {YbIII(36)[Co(Cp)(OP(OMe)2)3]} [366]. an intra-ratiometric measurement is feasible using the oxygen-
L. Götzke et al. / Coordination Chemistry Reviews 386 (2019) 267–309 287

Fig. 28. Molecular structures of [TbIII(TPP)(cyclen)]Cl (top) [369] and [TbIII(Pc)(cyclen)]Cl (bottom) [370].

insensitive fluorescence intensity as internal standard [374]. and hematoprphyrin monomethylether (H240) [375–379] have
Gd(III) and Lu(III) complexes of various Pors, such as tetratolylpor- been employed in the corresponding investigations. Furthermore,
phyrin (H237), etioporphyrin (H238), benzopophyrin (H239) [374], Zang et al. [380,381] observed an enhancement of the phosphores-
cence of the Gd(III)-40 complex in the presence of free Gd(III) as
well as in the presence of imidazole. They attributed these results
to decreased nonradiative transitions due to the presence of free
Gd(III) and the formation of a ‘‘protective medium” by imidazole
leading to inhibition of the energy transfer from the Gd(III)
complex to oxygen. If the accessibility of oxygen is restricted, for
example by embedding the Por complex in regenerated cellulose,
which provides an oxygen-impermeable microenvironment, the
phosphorescence can also be employed for temperature sensing.
This has been demonstrated for the Gd(III) and Lu(III) complexes
of H240 [382].
The tumour targeting capability of Pors, which is closely associ-
Fig. 29. Schematic representation of the mechanism for the sensitization of Ln NIR ated with their high lipophilicity, in combination with their low
emitters by a Por [363]. dark toxicity makes them potential radio-lanthanide chelating

Scheme 5.
288 L. Götzke et al. / Coordination Chemistry Reviews 386 (2019) 267–309

agents for medicinal imaging and therapy. Further advantages of readily functionalised, it is a sorbent raw material whose proper-
radiolabeled Ln-Pors are their fast clearance rate from the body ties can often be tailored to meet the requirements of a particular
and their photosensitizing properties enabling their use for dual application. For example, functionalisation can lead to enhanced
imaging and photodynamic therapy (PDT) [383,384]. adsorption capacities relative to raw cellulose. The study of the
Investigations involving the interaction of Pors or Pcs with Ans interaction of cellulose with radioactive cations and elucidating
are rare and structural characterisation is limited to complexes of the corresponding coordination behaviour forms a background
Th(IV) and U(IV) [385]. As is the case for Lns, Ans are too large against which the impact of such cations upon the aquatic and ter-
to fit in the tetrapyrrolic cavity and occupy a position above the restrial environment (and the organisms therein) can be assessed.
centre of the macrocycle, with additional ligands filling the Interestingly, one such study inferred an ambivalent effect of REEs
remaining coordination sites of the An. However, very stable com- on plant growth; namely, these ions appear beneficial at lower
plexes are often not obtained, with the isolated products being concentrations but detrimental at higher concentrations [393].
heat and air sensitive. Analogous to the Ln complexes discussed Cellulose-derived materials capable of scavenging f-block ions
above, double-/tripledecker complexes can be formed. For exam- from aqueous media have been increasingly studied. In particular,
ple, the reaction of UO2(OAc)2 with H2TPP yields the doubledecker composite materials with partial negative charges tend to take up
([UIV(TPP)2]) and tripledecker ([UIII
2 (TPP)3]) complexes [386,387]. trivalent Lns through electrostatic interaction. Examples are lay-
The reduction of U(VI) to U(IV) is necessary for the complexation ered double hydroxide intercalated cellulose nanocomposites, that
and this is promoted in the presence of phenol, which is oxidised includes a recyclable adsorbent material for REEs that exhibits
to quinone. The transformation of [UIV(TPP)2] to [UIII 2 (TPP)3] can maximum adsorption capacities of about 102, 93 and 96 mg/g for
take place in a subsequent reaction with another equivalent of Y(III), La(III), and Ce(III) ions, respectively [394]. A further example
UO2(OAc)2. is a cellulose based silica (CLx/SiO2) nanocomposite for the
Compared to the ‘‘normal” tetrapyrrolic macrocycles, expanded removal of Eu(III), La(III) and Sc(III) [395]. The same concept has
porphyrins offer an enlarged cavity for metal ion binding and, in also been applied to the use of other saccharides, such as the use
general, are capable of forming more stable complexes with Ans of sacrane in a bionanocomposite designed for the selective uptake
[385,388,389]. Thus, the focus on macrocyclic complexation of of Nd(III) ions [396]. Li et al. have also reported the use of sodium
Ans has somewhat shifted towards this class of ligand; however, carboxymethyl cellulose doped with Tb(III) ion and its application
a discussion of such systems is beyond the scope of this review. as a luminescence sensor whose efficiency depends on the pH and
sodium ion concentration in the surrounding media [397].
Modification of a cellulose surface with nickel and titanium
4. Biopolymers nanoparticles proved to be a successful strategy for scavenging
Eu(III) from radioactive waste water. In the same study, however,
4.1. Glucans chitin and chitosan modified under the same conditions provided
enhanced adsorption (see below). Nevertheless, separation of the
4.1.1. Cellulose and its derivatives for f-element adsorption sorbent material from the treated media can pose major challenges
Cellulose, a polymer consisting of b-(1,4)-D-glucopyranose for practical remediation processes. The use of magnetic nanocom-
monomer units (see Fig. 30, top), is the most abundant biopolymer posite materials consisting of iron oxide co-precipitated with car-
on earth. Naturally synthesized as a structural component in boxymethyl cellulose (Fe3O4@CMC) for the removal of Eu(III) (as
plants, fungi, bacteria, and algae, it has long been a subject of sci- a surrogate for all the trivalent Ans) was reported to outperform
entific interest. Combining mechanical durability, biodegradability, other structurally similar metal oxide-composite materials. At
sustainability, and hydrophilicity, cellulose continues to be a the same time, the material allows easy recovery by magnetic sep-
promising material for applications that include filtration, mem- aration and provides favourable recyclability and stability [398].
brane separation, pharmaceutical preparations, as well as numer- Moreover, spinning cellulose doped with a variety of rare earth
ous uses in food science [390–392]. As cellulose’s structure is ion nanocrystals into fibers enables the fabrication of new textiles
and paper products [399]. Fang et al. reported a novel application
for a Ln ion-doped functionalized cellulose-based material with a
flame retardant effect [400]
Functionalization with organic molecules – Raw cellulose has
been employed as a sorbent for transition metal ions [401,402]
but it commonly does not give rise to high sorption capacities.
However, as already mentioned, functionalisation of the hydroxyl
groups, modification of the polymer surface, or incorporation of
inorganic particles into the cellulose matrix can enhance the
uptake significantly.
Following such a strategy, Tolba et al. reported that the intro-
duction of either amino groups or carboxylic acid and amino
groups on a cellulose matrix increased the maximum sorption
capacity for La(III) ions from 38 mg/g up to 101 and 170 mg/g,
respectively. Only minimal losses in uptake capacity after five
sorption/desorption cycles were observed under acidic conditions
[403]. Cellulose functionalization with thiourea yielded maximum
adsorption capacities of 27 mg/g and 73 mg/g for Eu(III) and
Nd(III), respectively [404]. Cross-linking the nanocrystalline cellu-
lose polymer chains with polyethylenimine and using this material
to scavenge Ce(III) resulted in a loading capacity of  83 mg/g
[405]. In most studies, the uptake kinetics were investigated
Fig. 30. Structure of cellulose (top), chitin (middle) and its deacetylation product [404–406] and the effects of varying the experimental conditions
chitosan (bottom). were demonstrated.
L. Götzke et al. / Coordination Chemistry Reviews 386 (2019) 267–309 289

Lanthanide incorporation in cellulose for optical applications – The radionuclides. It is noted that two models have been proposed for
luminescence properties of f-block ions such as Ce(III), Tb(III), or the structures of chitosan complexes formed by its chelation to
Eu(III) in combination with the adsorption properties of metal ions: one is the ‘‘bridge model” that proposes that binding
cellulose-based sorbents have been employed to create fluorescent of a metal occurs via NH2 groups from different polymer chains,
materials for application as new sensors [407,408] that parallel the while the second is the ‘‘pendant model” in which the metal binds
previously established analogous embedding of CdSe/ZnS quantum to a single polymer chain [434–439].
dots into cellulose hydrogels [409]. Fungal chitin for metal complexation – The sorption of uranium
The loading of carboxymethyl cellulose nanoparticles with mix- by chitin-containing fungal biomass has been studied extensively.
tures of Ce(III), Eu(III), Tb(III) ions has been employed by Altam In part, this reflects the availability of large amounts of waste fun-
et al. to produce new optical materials. These nanoparticles were gal biomass from fermentation industries and the amenability of
subsequently hierarchically assembled using quaternised cellulose microorganisms such as Aspergillus, Rhizopus, and Penicillium to
to generate thin films with tuneable optical properties that depend genetic and morphological manipulation [440,441]. Tsezos et al.
on the concentrations of the three fluorescent ions present and the measured a maximum sorption capacity of 180 mg uranium per
pH [410]. As fluorescence decay is affected by temperature, a heat- gram of biomass, where there was an excess of U(VI) present rela-
sensor was successfully developed, reflecting that the Eu(III) fluo- tive to a biomass consisting of Rhizopus arrhizus [432], whereas
rescence lifetime exhibits excellent temperature-sensitivity of Guibal et al. reported sorption capacities up to 240 mg/g at pH 5
9 ls/K in the range of 25–75 °C [411]. for biomass consisting of Mucor mihei [442]. On the other hand, a
A synthesis procedure for preparing fluorescent nanopapers maximum sorption capacity of 280 mg/g was found by Bengtsson
incorporating Eu(III), Yb(III) [412], and Nd(III) [413] complexes et al. for sorption by Talaromyces emersonii [443]. Further, patents
grafted onto nanofibrillated cellulose has been reported. This by Gorovoj and Kosyakov describe a chitin-containing material
results in almost transparent optical filters for light in the visible derived from Basidiomycetes fungi that is suitable for the sorption
range while effectively blocking UV light. This makes them promis- of uranium and other radionuclides [444]. The use of industrial
ing materials for use in sun screens, for luminescing labels as well bio-waste, exhausted brewer’s yeast, Saccharomyces cerevisiae, for
as for OLEDs. A more facile reaction path involving TEMPO oxida- the removal of heavy metals, including uranium as well as copper,
tion to such materials was recently described by Miao et al. [414]. nickel, manganese, aluminium, and zinc from acid mine drainage,
Hydrogels – Cellulose-based hydrogels combine biocompatibil- has been described by Ramírez-Paredes et al. [445]. This material
ity with degradability with a malleable texture [415,416] render- also contains significant amounts of chitin as well.
ing them suitable for applications involving cell therapy [417], as Crab and sponge chitin for metal complexation – The main source
temperature [418] or pH sensors, for transition metal ion detection of chitin is crab shells from fishing waste [446]. Measurements by
[418], or for applications that involve severe UV light exposure Lenhart et al. determined a sorption capacity for U(VI) of approxi-
[419]. Cellulose hydrogels with tuneable luminescence properties mately 0.22 mg/g for this material [447]. The chitin isomorphs iso-
that depend on the mixture of Ln ion nanoparticles present were lated so far from fungi, arthropods, and molluscs (such as squids)
reported by Wang et al. [420]. Further materials include nanorods occur in the form of granules, sheets, or powders [448]. Relative
[421] and cellulose-based materials cross-linked by epichlorohy- to these materials, chitin of poriferan origin has some potential
drin doped with Tb(III) [422]. important advantages. Thus, the unique chitin-based scaffolds
found in marine sponges [116,449–451] are three-dimensional
networks composed of tube-like interconnected fibres with a
4.1.2. Chitin and chitosan for f-element adsorption
diameter of 100 mm and an estimated internal surface area of
After cellulose, chitin (poly-b-(1,4)-N-acetyl-D-glucosamine) is
10 m2/g in the case of A. aerophoba (Fig. 31). This material shows
the second most abundant natural biopolymer. It occurs as a basic
favourable adsorption properties, with a maximum uranium sorp-
structural component of fungi and yeast cell walls, as well as of
tion capacity of 280 mg/g [115].
numerous invertebrates like sponges, molluscs, crustaceans, arach-
Chitin functionalisation for tailored applications – The presence of
nids, and insects [423–425]. Deacetylation transforms the water
the aforementioned functional groups in chitin/chitosan provides a
insoluble chitin into the soluble chitosan (see Fig. 30, middle and
means for chemical modification, with the potential for tailoring
bottom). Both, chitin and chitosan are aminopolysaccharides that
the adsorption properties of the resultant materials. Because of
are associated with a large number of hydroxyl and amide or
its water solubility, chitosan is often cross-linked or grafted onto
amino groups. They are potent sorbents for various metal ions
insoluble support materials. Such immobilised chitosan derivatives
[426–433] including uranium, thorium, plutonium, and neptunium

Fig. 31. Left: Fluorescence microscopic image of sponge chitin from A. aerophoba. Right: Uranium adsorption isotherms for A. aerophoba chitin. Reproduced from [115] with
permission from Elsevier.
290 L. Götzke et al. / Coordination Chemistry Reviews 386 (2019) 267–309

can exhibit more favourable sorption properties than chitin itself. and preparation of relevant model compounds for investigation
Up to 800 mg/g uranium sorption was observed for N-[2-(1,2-dihy under defined conditions. The current state of synthesis, function-
droxyethyl)-tetrahydrofuryl)chitosan [452]. Maity et al. [453] syn- alisation, and characterisation of model substances relevant to An
thesized a chitosan-based hydrogel by crosslinking chitosan with complexation and transport has been summarized by Sachs and
glyoxal. This hydrogel selectively adsorbs Eu from mixtures of Eu Bernhard [464].
and Cs ions. In an another study Roosen and Binnemans [454] cova-
lently coupled chitosan to the ligands EDTA and DTPA to produce 4.2.1. Complex formation between f-elements and model substances
derivatives with adsorption capacities between 50 and 100 mg/g Jain et al. employed succinic, phthalic, and mandelic acids as
for Nd(III), Dy(III), and Pr(III). The selectivity of these derivatives ligands in an attempt to model the functional groups in HS [465].
makes them also suitable for chromatographic separations of REEs; Comparison of TRLFS data for the Eu(III) complexes of these
for example, of Nd(III)/Ho(III) mixtures. Mahfouz et al. [455] have ligands, however, indicated that they represent inner-sphere com-
reported magnetic, functionalised chitosan particles obtained by plexes, whereas the Eu(III)-HA complexes appeared to prefer
co-precipitation of chitosan with Fe(II) and Fe(III), cross-linking outer-sphere coordination, underlining the difficulty in identifying
with epichlorohydrin and subsequent functionalizing with realistic models for the natural systems. In another study by
diethylenetriamine. Maximum sorption capacities up to 200 mg/g Raditzky et al. [466], the nitrogen-containing carboxylic model
occur for uranium depending on the pH value. On the other hand, ligands, anthranilic and picolinic acid, were employed in a study
Elsalamouny et al. [456] prepared the a-aminomethylphosphonic of their Am(III) complexes, with phthalic acid also employed as a
acid derivative of chitosan and observed adsorption capacities of solely carboxylic acid reference.
up to ca. 50–60 mg/g for U(VI) and Nd(III). Ramasamy et al. [457] The use of capillary electrophoresis (CE) coupled with ICP-MS
reported the synthesis of different silica-chitosan hybrid beads was successful in providing information about the complexation
suitable for the efficient and sustainable recovery of REEs from acid behaviour of f-elements in various oxidation states (for example,
mine drainage. An investigation of the photoluminescence of Ln- Eu(III), Th(IV), U(VI)) [33,467,468] and, in particular, about their
containing chitosan-silica particles was reported by Liu et al. solution speciation, their strength of complexation as well as their
[458] who showed that Eu(III) forms two different complexes with mobility. Kautenberger et al. [33] derived information concerning
chitosan and silica in these composite materials. the functional groups involved in complex formation, especially
carboxyl and hydroxyl groups, by selectively blocking them in ref-
erence experiments. Carboxyl groups were identified as the princi-
4.2. Humic substances for f-element adsorption pal binding groups in a study by Yamamoto et al. These workers
estimated the relative stability constants for almost all REEs (with
Humic substances (HS) are biopolymers produced in sediments the exception of Pm) under simultaneous exposure to different
and soil. They are classified as HA, FA and humin, according to their ions with varying concentrations using CE-coupled ICP-MS [469].
solubility in aqueous media. While HAs only dissolve in acidic solu- The combination of experimental data with modelling has facil-
tions, FAs are soluble regardless of the pH. Humin on the other itated the identification of functional groups involved in complex-
hand is insoluble in water at all pH values [459,460]. Studying ation as well as details of the complex formed. This is especially the
the interactions of Ln and An ions with this biomaterial ubiqui- case for the so-called Humic Ion-Binding Model VI [470–472] devel-
tously occurring in soils and waters is an important prerequisite oped by Tipping [472] to describe complexes of HS, as well as for
for a better understanding of the transport and accumulation of the further developed and frequently employed so-called Winder-
f-elements in the environment [461] as well as of the long-term mere Humic Aqueous Model (WHAM) [473] and Donnan [474] mod-
geological impact [462] along with the bioavailability of these els that have been widely used to study details of such
metal ions for living organisms [463]. Heterogeneous in composi- coordination behaviour. Pourret et al. have also studied the com-
tion and rather undefined in molecular structure, HS offer a multi- plexation between Lns and HA employing a Langmuir-sorption-
tude of different functional groups as metal complexation sites isotherm metal-complexation model in combination with a linear
(see Fig. 32). However, development of a fundamental understand- programming method using different metal ion:HA ratios (from 5
ing of their interaction with f-elements requires the identification to 20), pH values (2–10). These workers were subsequently able
to distinguish between carboxylic and phenolic complexation
motifs based on the respective binding strengths of these donor
groups [34]. Further insight into the speciation of Lns at solid-
water interfaces is provided in a review by Tan et al. [475].
Under anoxic conditions at pH 7.2, HA was found to fully solu-
bilize colloidal Pu(IV) polymers. The Pu species were observed to
be partially reduced to Pu(III) in the presence of EDTA depending
on the HA concentration as well as on the density of the HA coating
formed on a sparingly soluble metal oxide surface [476]. Marine
sediments coated with HA were studied by Liatsou et al. [477]
who concluded that the formation of inner sphere complexes
was considerably more significant at pH values below 4 above
which the formation of outer-sphere-complexes is favoured.
The complexation of trivalent f-elements with HS is also rele-
vant for the assessment of Gd(III) in the environment. As discussed
earlier, Gd(III) is used as a contrast agent in MRI diagnostics; it is
ultimately released into the aquatic environment. Matsumiya
et al. proposed a separation method for Gd-HS-complexes (as well
as Gd-containing contrast agents) by chromatographically precon-
centrating the species to be analysed [478]. HS were also used as
Fig. 32. Selection of possible structural functionalities in HAs. Reproduced from column material for the chromatographic removal of Nd(III) and
[464] with permission from Springer Nature. Dy(III) ions [479]. In this case, the stationary phase consisted of
L. Götzke et al. / Coordination Chemistry Reviews 386 (2019) 267–309 291

HA extracted from Giza Zoo soil, yielding a column capacity of chromatography. Interestingly, the different fractions exhibit sim-
about 19 mg/g for Nd(III) and 18 to 39 mg/g for Dy(III) ions ions ilar spectra and fluorescence lifetimes. Further spectroscopic stud-
under varying initial metal ion concentrations that also depended ies of Eu(III)-HA and Eu(III)-FA complexes are described in
on the pH. references [471–473].
At this point, it is appropriate to mention the FUNMIG project
4.2.2. Ternary systems: f-element ions/humic substances/mineral (Fundamental processes of radionuclide migration, funded by the
phase European Atomic Energy Community Seventh Framework Pro-
Ternary systems consisting of f-element ions, HS, and a mineral gramme). Radionuclide migration and transport processes within
phase have been the subject of many studies. Understanding the the geosphere pertinent to the safety of nuclear waste repositories
mutual interactions in such ternary systems is necessary in the were examined by FUNMIG [491]. In this context, we note that a
geo-ecological context to assess the suitability of long-term waste review article stemming from the FUNMIG project and dealing
disposal repositories. TRLFS has proved a suitable technique for with the influence of HS on radionuclide transport processes has
probing the complexation behaviour under different conditions, been published [492]. It describes mathematical models for the
such as varying pH, ion concentration, metal ion:HS ratio, temper- prediction of speciation and transport mechanisms in ternary sys-
ature, and ionic strength. tems consisting of metal (radionuclide) ions, HS, and mineral sur-
Armstrong et al. have investigated the interaction between faces in considerable detail. Particular emphasis is given to
Nd(III), FA, and goethite. This ternary system, as well as three challenges for the experimental realization and prediction of equi-
separate binary systems for each combination of the three compo- librium and kinetic data related to interactions in complexes of f-
nents were studied [480]. Sorption experiments were conducted element ions and HS as well as in the aforementioned ternary
over the pH range 2–12. The results were in accord with the forma- systems.
tion of Nd-FA-species that proved to be soluble at pH values around Another study by Bryan et al. investigated the factors
9. For the ternary system (consisting of Nd, FA, and goethite), the influencing the dissociation over time of Eu(III) complexed to
adsorption of the Nd(III) by goethite was shown to be pH dependent. HA. They compared ‘‘natural” samples (i.e. obtained from the
The results of further investigations dealing with Eu(III) complexa- environment) with ‘‘synthetic” samples, which were prepared
tion involving related ternary systems are provided in references in the laboratory. Their results suggested that neither the contact
[34,475–478]. Kar et al. studied the influence of HA upon the Cm time, the metal ion to HA ratio nor the origin of the complexes
(III) sorption on colloidal silica [481]. Depending on pH, ion concen- affected the rate of dissociation as did the concentration of the
tration, and the metal charge, HA coagulation processes were also HS itself [493].
proposed to be involved [482]. In summary, the sorption of metal
ions by HS and mineral surfaces clearly depends on various factors,
and especially on the composition of the HS, its protonation/ 4.3. Peptides
deprotonation state and the charge of the mineral phase.
Iijima et al. and Reitzel et al. have also examined the interaction 4.3.1. Amino acids and small model peptides
of Nd(III) and La(III), respectively, within a ternary system contain- In general, complexes of Ln(III) with amino acids or small pep-
ing metal ion, HS and modified bentonite clay in aqueous media tides are distinguished by low thermodynamic stability and high
with regard to the migration of the metal [483] and its desorption sensitivity towards hydrolysis [28]. Due to the hard Lewis acid
behaviour [484]. An migration was also examined in detail in a character of the Lns, coordination is largely restricted to the
study by Zhao et al. who extensively investigated the sorption of a-carboxylic function of these ligands. Exceptions are amino acids
Am(III), Pu(IV), Np(V), and U(VI) onto dissolved organic matter that offer a second carboxylic or a hydroxylic group, namely
(DOM) collected from the Nevada Test Site [485]. glutamic acid (Glu), aspartic acid (Asp), threonine and serine.
Monodentate binding of the carboxylic group is quite uncommon
4.2.3. Studies of samples obtained from the natural environment as usually a chelating or bridging coordination mode is favoured
Brevet et al. have studied Eu(III) complexes of HS that originate by this donor group. Indeed, the formation of polymetallic
from different sources, including from various locations in the Uni- complexes in the solid state can often be observed and has been
ted States and Germany, and compared these results with those reviewed by Kremer [28] in 2005 and more recently by Canaj
obtained using commercially available, purified reference materi- et al. [494]. For example, Nd(III) and Sm(III) complexes obtained
als [486]. Luminescence decay data and emission spectra were from glycine (Gly) in the presence of imidazole (Im) were of the
recorded for Eu(III) complexes formed from seven different humic type [NdIII(Gly)4Im(ClO4)4]n and [SmIII(Gly)4Im(ClO4)4]n [495]. The
and fulvic extracts which could be categorized as being of either metal ions are bound to eight oxygen atoms from glycine, with
terrestrial or aquatic origin. Despite the natural heterogeneity glycine carboxylic groups acting as bridge between metal centres
(and inherent complexity) of these samples, the results for all to yield polynuclear chains.
humic and fulvic substances appeared rather similar, only showing Structure-binding relationships between proteins and metal
minor differences. Compared to the aquated Eu(III) ion used as a ions have been probed employing small peptides. On comparing
reference, an increase of the 5D0 ? 7F0 band intensity in the emis- the uranyl affinities of the phosphorylated and non-
sion spectra points to an overall loss of symmetry in the Eu(III)-HS- phosphorylated pentapeptides, 41 and 42 (sequences: WpTPpTW
complexes formed which is slightly exacerbated in the case of the and WTPTW), the effect of phosphorylation is easily seen
complex derived from HS of aquatic origin. In all cases, the lumi- (Scheme 6). The conditional stability constants (log K values)
nescence lifetime data show biexponential decay curves with life- determined at pH 4 are 6.6(2) and 3.4(1), respectively. That is,
times of 40–60 ms and 145–190 ms for the shorter-lived and the the peptide affinity for the uranyl ion increases by almost three
longer-lived components, respectively. The former species thus orders of magnitude after phosphorylation [496]. Retaining the
decays even faster than the aquated Eu(III) ion (110 ms) potential binding sites while varying the flexibility can also affect
[487,488]. Marang et al. reported an even faster decay of 10– the affinities of peptides towards metal ions. The three pentapep-
20 ms for the faster decaying component in their Eu(III)-HA studies tides 43–45 (sequences: DGDGD (43), ADPDA (44) and DPDPD
[489]. The spectral similarity of Eu(III)-HA complexes using HA (45)) with identical coordinating Asp residues, mainly differ in
samples of different origin was further confirmed by Reiller et al. the number of proline residues present. These prolines induce
[490]. HA was fractionated by high performance size exclusion angular strain, which increases the rigidity of the peptide back-
292 L. Götzke et al. / Coordination Chemistry Reviews 386 (2019) 267–309

Scheme 6.

Fig. 33. Left: principle structure of cyclodecapeptides; right: Optimized structure of the uranyl complex with a monophosphorylated cyclodecapeptide from DFT calculations.
Reproduced from [503] with permission from John Wiley and Sons.

bone. Within this series, the most flexible peptide, namely 43, spheres occurring for the native OPN. In the case of U(VI) the
shows the highest affinity towards uranyl as well as strong affinity coordination sphere is proposed to consist of one monodentate
for Eu(III). However, EXAFS measurements indicate that the coordi- phosphoryl group, one bidentate carboxylic group and two water
nation sphere generated for all three peptides stays more or less molecules [498]. On the other hand, for the Th(IV) complex the
the same, consisting of one monodentate and one bidentate results indicate that the sphere consists of both phosphoryl
carboxylic acid in combination with two water molecules for the groups, each bound in a monodentate fashion, and one bidentate
uranyl complexes. In the case of the Eu(III) complexes, five water carboxylic group, with an additional four water molecules pre-
molecules and an additional amide carbonyl group are required sent to complete the coordination shell [499].
to complete the coordination sphere [497] . Cyclic decapeptides have also been used to mimic the binding of
Selected amino acid sequences of various length have also U(VI) to proteins. Two prolylglycine sequences incorporated in the
been used to mimic proposed protein binding sites. Besides the structure induce two b-turns leading to an antiparallel b-sheet
obvious advantage of a simple synthesis compared to the exten- conformation for the cyclic structure [500–503]. Essentially, the
sive purification processes required for natural proteins, the tentative advantage of these cyclic decapeptides is the presence
above approach avoids effects arising from the tertiary structure of a preorganised arrangement of four parallel amino acid residues
of proteins. For example, the doubly serine-phosphorylated in positions 1, 3, 6, and 8 (Fig. 33 left). Compared to cyclopeptides
hexapeptide 46 (sequence: pSDEpSDE) represents a section of bearing histidine, glutamine and serine residues in these positions,
the intrinsically disordered protein osteopontin (OPN) which is the peptides with four acidic amino acid functions (i.e. Glu or Asp)
responsible for bone growth regulation. Peptide 46 forms a stable form the most stable complexes. The length of the carboxylate side
1:1 complex with U(VI) [498] as well as with Th(IV) [499] with chain also influences the uranyl affinity, with preference for this
comparable affinities (with log K of 5.2 and 4.2, respectively). ion occurring when the longer glutamic acid is present. The substi-
From EXAFS measurements, the coordination spheres of both tution of one of the prolylglycine sequences by a more flexible
these metal ions correlate very well with the coordination serylglycine loop causes a decline in uranyl affinity [500].
L. Götzke et al. / Coordination Chemistry Reviews 386 (2019) 267–309 293

The above cyclodecapeptides can be readily modified so as to of the Cm(III) forms carbonate species reflecting the competitive
sense uranyl with high selectivity by the insertion of two phospho- nature of the carbonate anion for metal complexation.
serine residues in positions 3 and 8 [501]. While the fluorescence An EXAFS study of Am(III) Tf complex formation also indicated
of the two tryptophan residues in positions 2 and 7 is not signifi- a pH dependence. While only the aquo species seems to be formed
cantly affected by addition of a range of metal ions (including at pH 7.2, at pH 8.5 Am(III) was seen to be located in a well-defined
main-group metals, transition metals, Lns and Ans), uranyl induces complex environment with a coordination number of nine in the
a strong fluorescent quenching with a quenching efficiency of 75%. first coordination sphere. Short Am(III)-donor atom distances of
The demonstrated ability of the above peptide to reliably detect 2.38 Å in combination with the existence of a second and third
uranyl ions in aqueous solutions makes it a suitable sensor for coordination shell suggest that the Am(III) is located most probably
monitoring contaminated environments. In general, the introduc- in the iron-binding site [133]. An extraordinary high affinity for Tf
tion of two phosphoserine groups yields uranyl affinities around with a conditional bicarbonate-free binding constant of
twice as high as occurs for the cyclopeptide with four Glu residues log K*1 = 22.50(19) was observed for Pu(IV) (for comparison: log K*1
[502]. Furthermore, a diametral arrangement in positions 1 and 6 for Fe(III) is 18.06) [505]. Even though uranyl is a relatively large
enables the binding of two chelated uranyl ions. Comparison of dif- cation with free coordination sites only in its equatorial plane
ferent isomers demonstrates that the stability is rather insensitive (due to the axial oxo-ligands), two UO2+ 2 ions are nevertheless able
to the relative arrangement of the phosphoserines to each other. to bind to Tf. Coordination occurs via several steps, starting with
For the resulting conformations of the complexes, on the other the very fast incorporation of a uranyl ion into the C-terminal bind-
hand the different phosphoserine arrangements play a decisive ing site. The further steps are slower and partially accompanied by
role. The two-fold phosphorylated peptides show a dependency conformational changes [506]. Although Tf is capable of binding
of the uranyl stability constants on the pH (log KC (pH 6) 8.2–8.8 two uranyl molecules, the involvement of U(VI)-Tf complexes in
vs. log KC (pH 7.4) 10.0–10.3). In contrast, the single phosphory- the transport mechanism in blood is unlikely, since a determina-
lated analogues display no significant alteration of the stability tion of the uranyl affinity of several serum proteins resulted in a
constants at different pH (log KC (pH 6) 9.5–9.8 vs. log KC (pH predicted percentage of U(VI)-Tf formation corresponding to
7.4) 9.2–9.8). Based on the results of EXAFS measurements and merely 2.4% of the protein-bound uranyl [507].
in agreement with DFT calculations, the uranyl ion is vertically ori- For a Tf mediated uptake of metal ions into cells, the Tf must be
ented above the centre of the decapeptide. The three carboxylic as able to bind to the appropriate receptor. This is only possible, if the
well as the phosphoryl function bind in a monodentate fashion metal binding induces an adequate conformational change within
(Fig. 33 right) [503]. both lobes towards a closed form. The receptor affinity of homonu-
clear M2-Tf complexes compared to iron decreases in the order
4.3.2. Natural proteins Fe(III) >> Th(IV)  U(VI)  Cm(III) > La(III) >>> Yb(III)  Pu(IV) [508].
Interaction with proteins occurring in the blood – Except for ura- However, not only does the type of metal ion play a crucial role
nium and thorium associating mainly with blood cells, other Ans in influencing the resulting Tf conformation, it is also influenced
(i.e. Pu(IV), Am(III), Cm(III), and Cf(III)) accumulate (>90%) in the by the occupation of the different binding sites. While the
plasma [10]. Transferrin (Tf), an iron-binding blood plasma glyco- PuCFeN-Tf shows a twofold closed conformation similar to Fe2-Tf,
protein, is often discussed as a potential carrier for Ans in blood as FeCPuN-Tf and Pu2-Tf exhibit a more open conformation.
well as being involved in cellular uptake. A review covering the Consequently, only PuCFeN-Tf can interact sufficiently with the
interaction of Tf with metal ions other than iron (including the Tf-receptor leading to an incorporation of the complex into cells
Ans) was published in 2012 by Vincent and Love [504]. (whereas FeCPuN-Tf and Pu2-Tf are not taken up) [509]. The fact
Tf consists of two lobes each with an iron-binding site, the N- that the uptake of Pu(IV) as well as its distribution within the cell
and C-terminal sites. Investigations of the interaction of Cm(III) seems to be independent of the kind of available Pu(IV) complex
with human serum Tf revealed two different affinities for these (i.e. Pu-NTA, Pu-citrate, PuCFeN-Tf) supports the proposed
C- and N-terminal binding sites with association constants of Tf-mediated uptake. In contrast to molecular Pu(IV) complexes,
log KC = 8.8(3) and log KN = 7.0(1) [136], respectively. In accor- aged Pu(IV) polymers that are representative of pre-existing aggre-
dance with this finding, Bauer et al. [140] found that the Cm(III) gates as found in the environment, are unable to be incorporated.
complex of the recombinant N-lobe of human transferrin (hTf/2N) As the most abundant protein in blood, serum albumin lends
(with only the N-terminal binding site available for coordination) itself to being a potential binding species for various metal ions
shows a significantly reduced stability compared to the Cm(III) [510]. Binding sites for uranyl in human serum albumin (HSA)
complex of natural Tf. Even though, their TRLFS results suggested and other metalloproteins can be classified into specific and unspe-
a similar coordination environment for Cm(III)-hTf/2N and cific. In general, the specific binding sites are distinguished by a
Cm(III)-Tf, consisting of four amino acid residues from the protein, low number of bound uranyl ions in combination with high bind-
two water molecules and three additional ligands (namely, syner- ing constants. Compared to Tf the binding constant with HSA is
gistic anions such as carbonate) [133]. Furthermore, TRLFS shows slightly lower with log K values of 6.1(4) (log KTf = 7.7(6)) [511].
the formation of two different Cm(III)-Tf species whose formation Ans, uranyl, Th(IV), as well as Ce(IV) provoke a partial unfolding
is pH dependent. The luminescence data collected for species I, of the protein’s a-helices. This is due to the interaction with the
show a broad emission peak and a lifetime corresponding to carbonyl and amide functions of the protein’s backbone. In con-
approximately four water molecules in the coordination sphere trast, La(III) and Ce(III) do not affect the secondary structure of
of the An cation. The second species yields a sharper emission peak HSA [512]. A comparable effect for the uranyl complexation on
with an unusually large bathochromic shift in combination with the secondary structure is also observed for bovine serum albumin
two hot bands. Finally, species I is assigned to contain an unspecif- (BSA). The structural change of this protein is mainly attributed to
ically bound Cm(III), whereas for species II the Cm(III) was the interaction of uranyl with carbonyl and hydroxyl groups which
assigned to be incorporated at the iron-binding site of Tf. Interest- makes a disruption in the natural protein function most likely
ingly, the formation of species I is completely suppressed in the [513,514].
presence of carbonate [132]. This is due to the latter’s function as The functional proteins acetylcholinesterase (AChE) and vitel-
a synergistic ligand for metal complexation at the iron-binding logenin (Vtg) occur widely in various organisms. Because AChE is
site, favouring the formation of species II. However, only 15% of an important membrane bound protein involved in nerve impulse
the Cm(III) is bound to Tf under physiological conditions; the bulk transmission, it also occurs on red blood cell membranes. However,
294 L. Götzke et al. / Coordination Chemistry Reviews 386 (2019) 267–309

Vtg occurs in the bloodstream; it is a precursor for egg-yolk pro- Comparison of human (hOPN) and bovine (bOPN) reveal that they
teins produced in the liver and needs to be transported to its final are able to form stable complexes with nine and six equivalents of
destination. Similar to HSA, these proteins offer two kinds of bind- uranyl, respectively. Dephosphorylation of the proteins results in a
ing sites for uranyl – specific and unspecific. Taking the number of very large decrease in the uranyl affinity from KD = 3.1(12) to 185
binding sites and the appropriate binding constants for the uranyl (10) nM for bOPN. Moreover, the proteins are no longer able to
complexes into account, a preferred coordination to AChE and Vtg form complexes stable enough for isolation using size exclusion
compared to other metalloproteins, is expected chromatography. The values determined most probably represent
(AChE > Vtg > Tf > ferritin > HSA > metallothionein (MT)) [515]. the upper limit of uranyl binding, because the serine groups are
For hemoglobin (Hb), Ce(III), La(III), U(VI), and Th(IV) strongly usually not completely phosphorylated [523]. Although a confor-
interact with the protein backbone inducing a comparable mational change is observed for OPN after uranyl complexation
decrease in the percentage of a-helices [516]. As Hb is to be found [419], for both proteins, OPN and fetuin A, the ability to avoid or
inside the erythrocytes in higher organisms, a hemolysis is neces- slow down the process of precipitation of calcium phosphate is
sary prior to possible interference. This was found to occur for both not affected in the presence of uranyl [522]. Similar to this result,
Ce(IV) and Th(IV) [516,517]. In the case of Th(IV) an important fac- the interaction of OPN, or rather fOPN (a naturally occurring frag-
tor influencing the mechanism of hemolysis is the Th(IV) to cell ment), with its antagonist lactoferrin (LF) is also not impaired by
ratio. While low ratios mainly induce aggregation of the erythro- uranyl. The UO2-fOPN complex is able to bind four equivalents of
cytes and only partial hemolysis, high ratios cause hemolysis of LF as does the free fOPN. Furthermore, the determination of the
the majority of the cells. For both scenarios the proposed mecha- thermal stabilities showed that the UO2-fOPN-LF complex is even
nisms include the interaction of Th(IV) with the glycosyl chain of slightly more stable than the fOPN-LF complex without uranyl
the membrane protein glycophorin A (GpA) to effect a conforma- [524].
tional change in the protein. The inhibition of Th(IV)-induced Interaction with gastrointestinal tract proteins – Exposure of
hemolysis following removal of GpA supports this postulate [517]. humans to particular Lns and Ans due to their accidental release
The biodistribution of metal ions in blood can be determined by or associated with their medical treatments is a major concern.
employing the dissociation constants Kd for each potential protein Consequently, investigation of the interaction of these elements,
target along with its concentration. An investigation by Basset et al. or appropriate subrogates (i.e. U(VI), Cm(III), Eu(III)), with different
[507] of the affinities of 15 serum proteins for uranyl, identified body fluids is necessary for understanding the pathway of these
fetuin A as the dominant binder. More than 80% of the protein- ions through the body. Although the speciation of Lns and Ans is
bound uranyl is expected to be bound by fetuin A. On consideration often primarily dominated by inorganic species, e.g. by carbonate
of the only moderate concentration of fetuin A available, such a or phosphate species, depending on the conditions, and as dis-
preference is huge. The 40 times higher concentrated HSA follows cussed earlier, several proteins may also contribute to the coordi-
with a percentage of about 7%. Fetuin A features three binding sites nation of these metal ions [525–527]. For oral ingestion, one of
for uranyl, with two of them showing high affinity in the nanomo- the first proteins such a metal ion will encounter is a-amylase
lar range for this ion. However, the coordination of U(VI) is not (Amy) in saliva. Speciation modelling of U(VI) in combination with
accompanied by a structural change and the impact on the normal a TRLFS study suggested the formation of a complex of type [(UO2)
life cycle of the protein seems to be negligible. This is of particular ((COO)2-Amy)]2+ (as the dominant species until a pH of  6.6) in
interest since fetuin A is involved in the mineralization of bone, a which the uranyl ion is coordinated to two carboxyl groups of
target organ for the uranyl ion. Amy [525]. At higher pH values, inorganic species such as [Ca
In contrast to studies involving more or less simple model solu- (UO2)(PO4)]+ or [Ca2(UO2)(CO3)3] become dominant. According to
tions, in a living organism the metal ions can of course interact sorption experiments, the uptake of Eu(III) is accompanied by the
with more than one protein type. The addition of uranyl to bovine release of Ca(II) initially linked to Amy [135]. This selective
serum results in the formation of a high-molecular compound replacement takes place even in the presence of excess Ca(II), in
(650,000 kDa), which can be separated by ultracentrifugation. This keeping with a stronger interaction of Amy with Eu(III). Further-
compound contains about 95% of the added U(VI) and is built up of more, Amy exhibits three independent binding sites for Eu(III).
multiple proteins forming a kind of uranyl–protein network, with This is indicated by the luminescence data, which imply the forma-
74 of the involved proteins able to be identified [518]. In vivo tion of two different species (of 1:1 and 1:3 stoichiometry) for
experiments with zebrafish gills as highly vascular organs repre- Eu(III) as well as for Cm(III). The corresponding stability constants
sent one further step to gain better insight into the mechanisms do not differ significantly with log b11 = 4.7(2) and log b13 = 12.0(4)
of uranyl accumulation. Bucher et al. [519] compared acute and for Eu(III) and 4.8(1) and 12.1(1) for Cm(III). The binding of Eu(III),
chronic waterborne exposure; under chronic conditions uranyl or more precisely the replacement of the Ca(II), induces a massive
can be found mainly ( 80%) in the low molecular fraction reduction of the enzymatic activity of Amy. However, this can be
(<18 kDa). The acute intoxication on the other hand resulted in easily reversed by addition of excess Ca(II). Linear combination fit-
an equal distribution between low and high molecular fractions ting of various luminescence spectral data of natural human saliva
with percentages of about 40% in each case. This is contradictory yielded an Amy-bound average percentage of 12% for Eu(III)
to the results of a subsequent study, also by Bucher et al., reporting (range: 3–34%) and 65% for Cm(III) (range: 58–70%) [526]. In con-
congruent distribution patterns of the uranyl in the proteome of trast, a subsequent study dealing with simulated body fluids
the gills for chronic and acute intoxication. Despite a 10-fold reported an insignificant impact of Amy on the speciation of Eu(III),
higher accumulation level for acute exposure, in both cases the which is readily explained by the increase of inorganic components
major part of the uranyl can be found in the low molecular fraction (i.e. carbonate and phosphate) by a factor of more than three in this
[520]. study. Further proteins were included in this study in order to sim-
Interaction with proteins involved in bone growth – Proteins ulate different body fluids (gastric juice, pancreatic juice and bile
involved in bone growth are also of special interest because of fluid); these were mucin, pepsin, lipase, pancreatin and trypsin.
the bones’ role as a major target organ for many metals [521]. As Of these proteins only pepsin and mucin play a significant role in
already mentioned in Section 4.3.1 and also above, OPN and fetuin the speciation of Eu(III) and Cm(III) within the human gastroin-
A are two of these proteins. Due to its high percentage of phospho- testinal tract. Noteworthy, the percentage of Eu(III) speciation of
rylated amino acid residues OPN is particularly suited for uranyl mucin increases to 66% in the small intestine. Probably the strong
binding and shows a comparable affinity to fetuin A [522]. complexation of trivalent f-elements by mucin could restrain the
L. Götzke et al. / Coordination Chemistry Reviews 386 (2019) 267–309 295

incorporation of these metal ions and facilitate their excretion


[527].
Interaction with intracellular proteins – The small cytoplasmatic
protein MT, which is capable of binding heavy metals due to its
numerous cysteine residues, is involved in detoxification processes
and is able to bind up to five uranyl ions [511]. Competition for the
cysteine binding sites seems unlikely, because of the hard Lewis
acid character of uranyl. Consequently, even with four additional
bound Zn(II) ions used for protein purification, MT is still able to
complex uranyl with two Glu, one Asp and the C-terminal carboxy-
late group. At the same time, the conformation of the protein stays
unchanged. Moreover, in the absence of the Zn(II) ions the uranyl
addition provokes the oxidation of the cysteine residues [528].
Another intracellular type of protein, located in the mitochon-
dria and essential for all organisms, are the cytochromes. Investiga-
Fig. 34. Close-up of the active site of the Eu(III)-MDH (PDB ID: 6FKW) from SolV
tions of the interaction of cytochromes with uranyl yielded strain in combination with the protein structure [536].
different affinities that depended on the particular cytochrome
used. The KD values for cytochrome c (cyt c) and cytochrome b5
(cyt b5) were determined to be KD = 87 mM and 10 mM, respectively. contained Eu(III) in its active site, the addition of further Ln(III) ali-
A minor change of the protein conformation of cyt b5 on binding quots (Ln = La, Pr, Eu, Yb) was expected to further enhance the
uranyl, disturbs the interaction between the two proteins in the enzymatic activity of this ‘‘partial-apo” Eu(III)-MDH. Indeed, the
cyt b5-cyt c complex. In turn, this results in a decrease of the per- addition of La(III) or Pr(III) led in each case to increased activity
oxidase activity for both the cyt c itself and the cyt b5-cyt c com- by factors of 1.5 and 2, respectively. The effect of Eu(III) addition
plex [529]. was significantly lower and the addition of Yb(III) surprisingly
Calmodulin (CaM) is an intracellular protein which has various reduced the enzymatic activity. This is probably due to a dynamic
regulation functions in eukaryotic cells. Each molecule of CaM con- exchange of metal ions bound in the active site.
tains four so-called EF-hand motifs – two in the N-terminal domain
and two in the C-terminal domain, respectively. As these motifs are 4.3.3. Artificial proteins
designed to bind Ca(II) ions, CaM is also well suited to bind Lns and Lanthanide binding tags – The unique properties of Ln can aid
Ans. Using a modified CaM, Pardoux et al. demonstrated the effect characterisation of proteins using NMR, photophysical or X-ray
of phosphorylation on uranyl affinity. For this study, several mod- crystallographic techniques. However, for this purpose it is neces-
ifications of the protein were necessary, including the insertion of a sary to incorporate a specific Ln binding site(s) into the native pro-
tyrosine residue for fluorescence measurements and a recognition tein. In general, this may be accomplished by the introduction of a
sequence for the enzymatic phosphorylation of threonine. Phos- multidentate ligand binding site (such as DOTA or DTPA deriva-
phorylation results in an improved affinity of about a factor of five tives) or by incorporation of peptide sequences that are particu-
(from Kd = 25(6) nM to 5(1) nM at pH 6). Increasing the pH to 7 led larly suited for Ln(III) binding. In the case of the latter peptide
to a further stability increase, reaching the subnanomolar range lanthanide binding tags (LBT), stable Ln(III) complexes form
(Kd = 0.32(6) nM). In contrast, the affinity for Ca(II) is only slightly mainly by coordination with the acidic Asp and Glu residues. For
affected by phosphorylation [530]. From EXAFS measurements and fluorescence studies, the LBTs often incorporate Tb(III) which in
in agreement with FTIR and molecular modelling results, the ura- addition coordinates to the carbonyl oxygen atom of an introduced
nyl is five coordinated, being bound to a monodentate phosphoryl (sensitizing) tryptophan residue [537,538].
group as well as to two monodentate and one bidentate carboxylic For analytical applications such as the structure determination
group. In the unphosphorylated CaM, the coordination is most of native proteins, the effect of the introduction of the LBT on the
likely completed by an additional hydroxo ligand [531]. Although protein structure should be as small as possible. With respect to
CaM itself is not enzymaticly active, its regulating functions can this, it is noted that comparison of the native form of
be influenced by the presence of particular metal ions. The enzyme interleukin-1b (IL1b) [539] with nine different LBT-modified forms
phosphodiesterase (PDE1), for example, is activated by CaM in (with the LBT in three different loop positions and spacers of vari-
combination with Ca(II). Both uranyl and neptunyl induce a confor- ous lengths) revealed that the native structure is more or less unaf-
mational change in CaM which impairs its interaction with PDE1 fected. Consequently, the binding to the protein receptor was not
finally leading to its inhibition. This effect can be reversed by the impaired. A comparison of the structures of the native IL1b and
addition of a simple decorporation reagent such as H216 (5-LIO LBT-modified IL1b (incorporating an LBT consisting of a sequence
(Me-3,2-HOPO)) (see Fig. 14) [532]. of 17 amino acid residues) is given in Fig. 35. The Tb(III) in the
Biological role – Since the discovery that the Lns can be directly structure depicted (in Fig. 35, right) is coordinated by two biden-
associated with cell growth of some methylotrophic bacteria, it tate Glu, two monodentate Asp, one monodendate Asn and the
was postulated that Lns could also have a functional role in partic- backbone carbonyl function of a tryptophan residue [540].
ular biological systems. This was confirmed by the first crystal Besides their role for structure determination, LBTs can also be
structure of an alcohol dehydrogenase containing Ce(III) in its used to sense Ln ions. The exchange of a Fe(II)-binding motif for an
active site [533–535]. Replacing the Ce(III) with Eu(III) in the active LBT in the trans-membrane protein PmrB (polymyxin resistance B)
site of methanol dehydrogenase (MDH) does not induce a struc- enables the engineered E. coli to bind Ln. The Ln(III) binding to the
tural change [536]. The Eu(III) in the Eu(III)-MDH complex is anal- histidine kinase PmrB induces its autophosphorylation and this
ogously coordinated by two Asp, one Glu and one asparagine (Asn) serves as a signal for the partner protein PmrA which is subse-
residue in combination with a prosthetic pyrroloquinoline quinone quently phosphorylated. This triggers the expression of a green
(PQQ) ligand (see Fig. 34). However, the catalytic efficiency as well fluorescent protein (gfp) that can easily be visualised (see
as the observed rate of bacterial growth decreases significantly. Fig. 36). Finally, in contrast to other metal ions (i.e. Ca(II), Mn(II)
This reflects the very significant impact of the ionic radius of the Fe(III), Cu(II), Zn(II)) that do not lead to the expression of the gfp
particularly bound metal ion. Because only  70% of the protein (even if they are much higher concentrated), the E. coli respond
296 L. Götzke et al. / Coordination Chemistry Reviews 386 (2019) 267–309

Fig. 35. Comparison of the molecular structures of native IL1b (left; PDB ID: 9ILB [539]) and LBT-modified IL1b (right; PDB ID: 3LTQ [540]; the amino acid residues of the LBT
coordinated to Tb(III) are displayed as sticks).

selectively only in the presence of Tb(III) (by the expression of the De novo proteins – The build-up of proteins particularly
gfp) [541]. designed to complex a selected metal ion allow for highly special-
A similar approach has been adopted for the extraction of Ln(III) ized applications that include their use as contrast agent for MRI
using the bacterium Caulobacter crescentus [542]. The genetically [543] or for metal recovery from highly dilute solutions, like sea-
modified microorganism displays LBTs in high density on its cell water [544]. So-called coiled coils [545], a helical arrangement of
surface. This enables the selective extraction of Tb(III) even in a three synthetic protein a-helices, represents a tuneable class of
high excess of Ca(II). Among a group of d- and main group metal proteins. Leaving the structure determining amino acids
ions (i.e. Mg(II), Al(III), Mn(II), Fe(III), Co(II), Ni(II), Cu(II), and Zn(II)) unchanged, but introducing certain coordinating amino acids (i.e.
only Cu(II) turns out to be a potent competitor for LBT binding. Asp and Asn) in the structure, has been established to yield well-
That is, the other metal ions do not affect the Tb(III) binding signif- defined coordination sites for an appropriate metal ion. When
icantly (up to at least a tenfold higher concentration). Comparison bound to Gd(III), for example, the coiled coils show promising
with other REEs (i.e. Y(III), La(III), Ce(III), Nd(III), Eu(III), Dy(III), and MRI properties. From molecular dynamics simulations, a Ln(III)
Yb(III)) yielded the expected preference for the ions with smaller ion such as Tb(III) or Gd(III) will be bound by one Asp and one
atomic radii. The resulting preference order is Eu(III), Dy(III), Asn residue from each a-helix, respectively. Although, its position
Yb(III) > Y(III), Nd(III) > La(III), Ce(III). The bound Tb(III) can be in the hydrophobic core severely limits the accessibility of water to
removed from the cell surface by simple washing with a solution the Ln(III), an additional water ligand was proposed to complete
of a complexing agent such as citrate. This desorption procedure the coordination sphere in this modelled structure. In contrast,
does not reduce the REE adsorption capacity for further subsequent the luminescence lifetimes determined for the Tb(III) complex sug-
adsorptions, allowing the reuse of the engineered cells. gest the absence of any directly coordinated water molecule,
resulting in coordinately-saturated, [LnIII(Asp)3(Asn)3], coordina-
tion being present [546]. The exact location of the binding site
within the coiled coil (see Fig. 37) has a very large impact on the
coordination chemistry of the Ln(III) and also on its luminescence
and MRI properties. Due to the increased flexibility of the single
helix strands, binding sites close to a terminus are able to include
water. In the case of the N-terminal binding site, three additional
water ligands replace the Asn residues, which are no longer essen-
tial for Ln(III) complexation (i.e. giving [LnIII(Asp)3(H2O)3] coordi-
nation). Consequently, the transverse relaxivity for the Gd(III)
complex increases by about a factor of four; this result makes such
systems especially promising as potential imaging agents [547].
Zhou et al. [548] used a more empirical method to design a pro-
tein for the complexation of uranyl. Browsing PDB entries and
employing a computational screening algorithm, which specifically
looks for proteins with a suitable binding pocket, resulted in a
library of potential uranyl binding proteins. Of ten selected promis-
ing proteins, four showed an uranyl affinity with KD less than
100 nM. The mutant of a small protein from Methanobacterium
thermoautotrophicum with modifications in three amino acid resi-
dues appeared especially suitable for further tuning due to its high
stability and the small KD value of 37 nM for uranyl. Similar to the
coiled coils, it consists of three a-helices in a tight bundle. From the
computational model, the native amino acid Asp68 and the modi-
Fig. 36. Schematic representation of the Fe(III)-responsive (left) and Ln(III)-
responsive (right) systems based on the PmrA/PmrB two-component arrangement.
fied amino acid residues, Glu17, Asn13, and Gln64 coordinate to
The LBT (amino acids 34–49) is highlighted in green. The figure is reprinted with uranyl. The formation of an additional stabilising hydrogen bond
permission from reference [541]. Copyright 2013 American Chemical Society. from a uranyl oxo group towards an arginine was also expected.
L. Götzke et al. / Coordination Chemistry Reviews 386 (2019) 267–309 297

Molecular modelling of the binding motif in SUP, taking the


probable coordination of Glu64 and Asp13 under neutral pH con-
ditions and the hydrogen bond in the second coordination shell
into account, gave insight into the effect of the respective modifi-
cations on the selectivity of the protein and the stability of the ura-
nyl complex [549]. Computation of ten more mutations of SUP led
to the prediction that the replacement of Glu64 by Asp64 should
further improve the protein’s ability to bind uranyl. This prediction
was confirmed experimentally; a modest increase in affinity of
about 45% was found to occur.

5. Conclusion

An aim of the above discussion was to present an overview of a


selection of the very large number of diverse, but often related,
studies that involve the interaction of Ln and An ions with a wide
range of both naturally-occurring and synthetic ligands (the latter
bearing bio-relevant functional groups) and materials. Often these
investigations have been paralleled by model laboratory and/or
computation studies that, in combination, have enabled consider-
able insight into both the transport and accumulation of these
Fig. 37. Schematic representation of four isomeric coiled coils with differently
f-block ions in the natural environment as well as in biological sys-
positioned Ln(III) binding sites. The coordinating Asn and Asp residues as well as
the Tb(III) sensitizing Trp residue are shown as sticks, the Ln(III) ions as mauve tems, including humans. Moreover, the wide range of both single-
spheres. The figure is reproduced from [547] with permission from The Royal and two-phase studies reported have clearly contributed to a much
Society of Chemistry. fuller understanding of the metal coordination chemistry of the
f-block elements and especially of their behaviour towards the
wide range of ligand types mentioned above. In many instances
Based on this structure, further modifications, including the this has led to the design of new adsorbent ligand systems and
exchange of Gln64 and Asn13 to Glu and Asp, enhanced the uranyl materials capable of sequestering and accumulating the above
affinity even more. metal ions – and especially toxic radionuclides – with actual or
Finally, it is noted that the super uranyl-binding protein (SUP) potential application for removal of such ions from the environ-
falls in the femtomolar range with a KD value of 7.4(20) fM for this ment and/or from humans.
ion making it a potential reagent for sequestering uranyl from sea-
water. The crystal structure of the SUP-uranyl complex confirms
Acknowledgements
the expected coordination of uranyl in an appropriate binding
pocket. Surprisingly, only two amino acid residues (Asp68 and
The authors thank the German Federal Ministry of Education
Glu17) coordinate to U(VI) to form a pentagonal bipyramidal coor-
and Research (BMBF – project 02NUK046A, 02NUK046B and
dination geometry containing an equatorial water ligand and the
02NUK046C) for financial support and Dr. Kathleen Schnaars for
usual two axial oxo groups (see Fig. 38). A possible influence for
the design of the FENABIUM logo. We also like to acknowledge
the binding of only two amino acid residues is the low pH of 4 pre-
financial support of Fondazione Cariplo – Regione Lombardia grant
sent during crystallization. Besides its extremely large affinity for
(Sottomisura A - 2015).
uranyl, SUP is also distinguished by a high selectivity for this ion.
Within a series of seventeen metal ions found in sea water, only
Cu(II) and VO+ proved to be potential competitors. However, the References
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