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Engineering of monomeric FK506-binding protein 22 withpeptidyl prolyl
cis-trans 
isomerase
Importance of a V-shaped dimeric structure for binding to proteinsubstrate
Cahyo Budiman
1
, Keisuke Bando
1
, Clement Angkawidjaja
1
, Yuichi Koga
1
, Kazufumi Takano
1,2
andShigenori Kanaya
1
1 Department of Material and Life Science, Graduate School of Engineering, Osaka University, Yamadaoka, Suita, Osaka, Japan2 CRESTO, JST, Yamadaoka, Suita, Osaka, Japan
Keywords
FKBP22; homodimer; peptidyl-prolyl
cis-trans 
isomerase (PPIase); proteinengineering; substrate binding
Correspondence
S. Kanaya, Department of Material and LifeScience, Graduate School of Engineering,Osaka University, 2-1, Yamadaoka, Suita,Osaka 565-0871, JapanTel
  ⁄  
Fax: +81 6 6879 7938E-mail: kanaya@mls.eng.osaka-u.ac.jp(Received 1 May 2009, revised 24 May2009, accepted 28 May 2009)doi:10.1111/j.1742-4658.2009.07116.x
FK506-binding protein 22 (FKBP22) from the psychrotrophic bacterium
Shewanella
sp. SIB1 is a homodimeric protein with peptidyl prolyl
cis–trans
isomerase (PPIase) (EC 5.2.1.8) activity. Each monomer consists of 205amino acid residues. According to a tertiary model, SIB1 FKBP22 assumesa V-shaped structure, in which two monomers interact with each other attheir N-termini. Each monomer consists of an N-terminal domain with adimerization core and a C-terminal catalytic domain, which are separatedby a 40-residue-long
a
-helix. To clarify the role of this V-shaped structure,we constructed a mutant protein, in which the N-domain is tandemlyrepeated through a flexible linker. This protein, termed NNC-FKBP22, isdesigned such that two repetitive N-domains are folded into a structuresimilar to that of the
Shewanella
sp. SIB1 FKBP22 wild-type protein (WT).NNC-FKBP22 was overproduced in
Escherichia coli 
in a His-tagged form,purified and biochemically characterized. Gel-filtration chromatographyand ultracentrifugation analyses indicate that NNC-FKBP22 exists as amonomer. Analysis of thermal denaturation using differential scanning cal-orimetry indicates that NNC-FKBP22 unfolds with two transitions, as doesthe WT protein. NNC-FKBP22 exhibited PPIase activity for both peptideand protein substrates. However, in contrast to its activity for peptide sub-strate, which was comparable to that of the WT protein, its activity forprotein substrate was reduced by five- to six-fold, compared to that of theWT. Surface plasmon resonance analyses indicate that NNC-FKBP22binds to a reduced form of 
a
-lactalbumin with a six-fold weaker affinitythan that of WT. These results suggest that a V-shaped structure of SIB1FKBP22 is important for efficient binding to a protein substrate.
Structured digital abstract
l
FKBP22
(uniprotkb:Q765B0)
binds
(MI:0407) to
Alpha-lactalbumin
(uni-protkb:P00711) by
surface plasmon resonance
Abbreviations
DSC, differential scanning calorimetry; FKBP, FK506-binding protein; MIP, macrophage-infectivity potentiator; pNA,
-nitroanilide; PPIase,peptidyl prolyl
cis–trans 
isomerase; RCM, reduced and carboxymethylated; suc-ALPF-
NA,
N- 
succinyl-Ala-Leu-Pro-Phe-
p- 
nitroanilide; WT,
Shewanella 
sp. SIB1 FKBP22 wild-type protein.
FEBS Journal
276
(2009) 4091–4101
ª
2009 The Authors Journal compilation
ª
2009 FEBS
4091
 
Introduction
Peptidyl prolyl
cis-trans
isomerase (PPIase) (EC5.2.1.8) catalyzes
cis
 – 
trans
isomerization of the Xaa– Pro peptide bonds of proteins [1]. Because the peptidebond in the
cis
conformation is energetically unfavor-able compared with that in the
trans
conformation[2,3], and
cis
 – 
trans
isomerization of this peptide bondis intrinsically very slow [4], prolyl isomerization isregarded as a rate-limiting step of the folding reactionof proteins that contain
cis
prolines in a folded state[5]. PPIases are divided into four structurally unrelatedfamilies: FK506-binding proteins (FKBPs), cyclophi-lines, parvulins and the Ser
  ⁄  
Thr phosphatase 2Aactivator, PTPA [6].FKBP22 is a member of the FKBP family and pres-ent in various Gram-negative bacteria [7–9]. It is ahomodimer, in which each subunit consists of anN-terminal domain (N-domain) and a C-terminalPPIase domain (C-domain). Based on its similarities tothe macrophage-infectivity potentiator (MIP) proteinfrom
Legionella pneumophila
in amino acid sequence,FKBP22 has been classified as a member of the MIP-like FKBP subfamily [7].
Escherichia coli 
FkpA is alsoa member of this subfamily [10]. Of the members of this subfamily,
L. pneumophila
MIP [11] and
E. coli 
FkpA [12] are the only ones for which the crystalstructures have been determined. These structuresstrongly resemble each other, having an rmsd of 0.8 A ˚for all C
a
atoms. According to these structures, theseproteins assume a nonglobular V-shaped homodimericstructure, in which two monomers interact with eachother at their N-domains. Each monomer assumes adumbbell-like structure, in which the N-domain (con-sisting of 
a
1 and
a
2 helices) and the C-domain [con-sisting of six
b
strands (
b
1– 
b
6) and an
a
4 helix] arelinked by a 40-residue-long
a
3 helix. As a result, theC-domains, which are located at both ends of aV-shaped structure, face each other across the cleft of this structure. The interface of two monomers, whichis located at the bottom of the V-shaped structure, isstabilized by the hydrophobic interactions between the
a
1 helix of one monomer and the
a
2 helix of the other.However, the role of a V-shaped structure of MIP-likeFKBP subfamily proteins remains to be understood.We have previously shown that FKBP22 from thepsychrotrophic bacterium
Shewanella
sp. SIB1 existsas a homodimer and exhibits PPIase activity for bothpeptide and protein substrates [8]. SIB1 FKBP22shows amino acid sequence identities of 56% to
E. coli 
FKBP22 [7], of 43% to
E. coli 
FkpA [10] andof 41% to
L. pneumophila
MIP [13]. Construction of the mutant proteins N-domain
+
and C-domain
+
,which lack the C- and N-domains of SIB1 FKBP22,respectively, followed by biochemical characterizationof these proteins, suggest that the C-domain isrequired for PPIase activity, and the N-domain isrequired for dimerization and efficient binding to aprotein substrate of PPIase [14,15]. However, itremains to be determined whether a V-shaped struc-ture is required for efficient binding of SIB1 FKBP22to a protein substrate, because the N-domain
+
, whichretains the ability to bind to a protein substrate, con-tains the entire
a
3 helix and therefore may be able toassume a V-shaped homodimeric structure. Attemptsto construct the N-domain without the
a
3 helix haveso far been unsuccessful because of the instability of the protein.In this report, we constructed the mutant protein,NNC-FKBP22, in which the N-terminal region (Met8– Ala60) is repeated twice within a single polypeptidechain, and characterized it biochemically. This mutantprotein was designed such that the repetitive N-termi-nal region is folded into a structure similar to that of the
Shewanella
sp. SIB1 FKBP22 wild-type protein(WT), which has a homodimeric structure. Based onthese results, we discuss the role of a V-shaped struc-ture of FKBP22.
Results
Design of monomeric mutant protein
The monomeric mutant protein (NNC-FKBP22) wasdesigned based on a model of the 3D structure of WT(SIB1 FKBP22) (Fig. 1A), which has previously beenreported [14]. According to this model, WT assumes aV-shaped homodimeric structure, like those of 
L. pneu-mophila
MIP [11] and
E. coli 
FkpA [12]. In this struc-ture, the Ala60 of one monomer is located in closeproximity to the Met8 of the other monomer. Bothresidues are located close to the bottom of the cleft of the V-shaped structure. Therefore, it is stronglyexpected that the mutant protein, termed NNC-FKBP22, in which Met1–Ala60 of SIB1 FKBP22 isattached to Met8–Ile205 of SIB1 FKBP22 throughthree glycine residues, is monomeric and folded into astructure similar to that of WT without one arm of the‘V’. A model of the 3D structure of NNC-FKBP22 isshown in Fig. 1A. Its primary structure is also sche-matically shown in Fig. 1B in comparison with that of WT. NNC-FKBP22 and SIB1 FKBP22 (WT) in a His-tagged form will be designated as NNC-FKBP22 andSIB1 FKBP22 (WT), respectively, hereafter.
Engineering of monomeric FKBP22
C. Budiman
et al.
4092
FEBS Journal
276
(2009) 4091–4101
ª
2009 The Authors Journal compilation
ª
2009 FEBS
 
NNC-FKBP22 was overproduced in
E. coli 
at10
°
C, as previously reported for WT [8]. The proteinaccumulated in the
E. coli 
cells in a soluble form andwas purified to give a single band on SDS–PAGE (see,Fig. S1). WT was also overproduced and purified asreported previously [8].
Determination of oligomeric state
The molecular mass values of NNC-FKBP22 and WTwere estimated to be 34 and 28 kDa, respectively, fromSDS–PAGE. These values are considerably higher thanthose calculated from their amino acid sequences(27 kDa for NNC-FKBP22 and 21 kDa for WT). Ithas been reported for WT that the molecular mass of the protein determined by ESI-MS (23 kDa) is compa-rable to the calculated molecular mass and thereforethe molecular mass of the protein estimated fromSDS–PAGE is considerably higher than the calculatedmolecular mass as a result of its unusual behavior onSDS–PAGE [8]. Because the difference in molecularmass values of NNC-FKBP22 and WT, estimatedfrom SDS–PAGE, is comparable to the difference intheir molecular mass values calculated from aminoacid sequences, the molecular mass of NNC-FKBP22is considerably higher than the calculated molecularmass, probably as a result of its unusual behavior onSDS–PAGE, like WT. The molecular mass values of native forms of NNC-FKBP22 and WT were estimatedto be 58 and 99 kDa, respectively, from gel-filtrationcolumn chromatography. These values are 4.5- and2.1-fold higher than those calculated from their aminoacid sequences. However, it has been reported for WTthat the molecular mass of the protein, as determinedby sedimentation equilibrium analytical ultracentrifu-gation (44 kDa), is two-fold higher than the calculatedmolecular mass, and the discrepancy between themolecular mass values estimated from gel filtrationand analytical ultracentrifugation is a result of theunusual behavior of WT on gel filtration. The unusualbehavior of the protein on gel filtration has also beenreported for
L. pneumophila
MIP. The molecular massof this protein, as estimated from gel filtration, ishigher than the calculated molecular mass by 2.7-fold,instead of by two-folds, because it is cylindrical ratherthan globular [16]. Therefore, the molecular mass
9 23 34 45 52 9395 99102 111121 130134 139146 150155 163167 174195 205
α
1
α
2
α
3
β
1
β
2
β
3
β
4a
β
4b
β
5
β
6
α
4
1
N-domain
B
C-domain
65 79 90 101 108 149151 155158 167177 186190 195202 206211 219223 230251 261
α
4
α
5
α
6
β
1
β
2
β
3
β
4a
β
4b
β
5
β
6
α
7
9 23 34 45 52
α
1
α
2
α
3
1
60
GGG
C-domainN-domain
SIB1 FKBP22NNC-FKBP22
C-domain
Ala60(Gly)
3
Met64
N-domainN-domainC-domainC-domainAla60Met8SIB1 FKBP22NNC-FKBP22
α
1
α
5
α
4
α
2
α
2
α
1
α
2
α
1
α
3
α
6
α
3
N-domain
A
Fig. 1.
(A) 3D structure models of SIB1FKBP22 and NNC-FKBP22. For the SIB1FKBP22 structure, one monomer is deeply-colored, while the other is lightly-colored.The N- and C-domains and the
a
1-3 helicesare indicated. The side chain of Met8 of onemonomer and that of Ala60 of the othermonomer are indicated by stick models. Forthe NNC-FKBP22 structure, the correspond-ing domains, helices and side chains of theamino acid residues are indicated. A loopconsisting of three glycine residues, whichconnects Ala60 and Met64 (correspondingto Met8 of SIB1 FKBP22), is schematicallyshown in cyan. (B) Schematic representa-tions of the primary structures of SIB1FKBP22 and NNC-FKBP22. A His-tagattached to the N-termini of the proteins isrepresented by a shaded box. The
a
-helicesand
b
-strands are represented by cylindersand arrows, respectively. These secondarystructures are arranged based on tertiarymodels of SIB1 FKBP22 and NNC-FKBP22.Numbers indicate the positions of the resi-dues relative to the initiator methionine resi-due of the proteins without a His-tag. Theranges of the N- and C-domains are alsoshown.C. Budiman
et al.
Engineering of monomeric FKBP22
FEBS Journal
276
(2009) 4091–4101
ª
2009 The Authors Journal compilation
ª
2009 FEBS
4093
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