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Biomimetism and bioinspiration as tools for the design of innovative

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Biomimetism and bioinspiration as
tools for the design of innovative
materials and systems
Materials found in nature combine many inspiring properties such as sophistication, miniaturization,
hierarchical organizations, hybridation, resistance and adaptability. Elucidating the basic components
and building principles selected by evolution to propose more reliable, efficient and environment-
respecting materials requires a multidisciplinary approach.
CLÉMENT SANCHEZ1*, HERVÉ
ARRIBART2* AND MARIE MADELEINE
GIRAUD GUILLE1*
1
Laboratoire de Chimie de la Matière Condensée, Université
Pierre & Marie Curie, Ecole Pratique des Hautes Etudes,
Centre National de la Recherche Scientifique, 4 place Jussieu,
Tour 54, 5ème étage, 75005 Paris, France
2
Saint-Gobain Recherche, 39 quai Lucien Lefranc, 93303
Aubervilliers, France
*e-mail: clems@ccr.jussieu.fr; mmgiraud@snv.jussieu.fr;
herve.arribart@saint-gobain.com
This review considers the following currently
investigated domains: supramolecular chemistry that
is of interest for complex macromolecular assemblies
such as molecular crystals, micelles and membranes;
hybrid materials that combine organic and inorganic
components on a nanoscale with innovative
controlled textures; polymeric materials of synthetic
or natural origin, showing controlled length, selected
affinities and rich structural combinations offering
a wide range of applications; bioinspired materials
reproducing principles or structures described in
animals or plants; biomaterials offering clinical
applications in terms of compatibility, degradability
and cell–matrix interactions.
Efforts to understand and control self-assembly,
phase separation, confinement, chirality in complex
systems, possibly in relation to external stimuli or
fields and the use of genetically engineered proteins
for inorganics are some promising challenges for
bioinspired materials.
NATURE AS A SCHOOL FOR MATERIALS SCIENCE
Scientists are always amazed by the high degree
of sophistication and miniaturization found in
natural materials. Nature is indeed a school for
materials science and its associated disciplines such
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©2005 Nature Publishing Group
nmat1339-print.indd 277
REVIEW ARTICLE
as chemistry, biology, physics or engineering1. In
all living organisms, whether very basic or highly
complex, nature provides a multiplicity of materials,
architectures, systems and functions2–6. For the past
five hundred million years fully proven materials
have appeared resulting from stringent selection
processes. A most remarkable feature of naturally
occurring materials is their finely carved appearance
such as observed in radiolaria or diatoms (Fig. 1).
Current examples of natural composites are
crustacean carapaces or mollusc shells and bone or
teeth tissues in vertebrates.
A high degree of sophistication is the rule and
the various components of a structure are assembled
following a clearly defined pattern. Highly elaborated
performances characterizing biological materials
result from time-dependant processes. Selecting
the right material for the right function occurs at a
precise moment from sources available at that time.
An advantage for chemists is to elaborate possible
new constructions from all chemical components
without any time-restricted conditions. However, the
results of evolution converge on limited constituents
or principles. For example, a unique component
will be found to obey different functions in the
same organism. A protein, such as type I collagen,
presents different morphologies in different tissues
to perform different functions (Fig. 2a,b). Associated
or not with hydroxyapatite crystals, it gives rigid
(high Young modulus) and shock-resistant tissues in
bone7, it behaves like an elastomer with low rigidity
and high deformation to rupture in tendons8, or
shows optical properties such as transparency in
cornea9. Another example is the arthropod cuticle,
combining in different proportions chitin, proteins
and calcite crystals10 to give tissues that are rigid,
flexible, opaque or translucent (Fig. 3a–c). Within
biological organisms, identical organizational
principles to liquid-crystalline self-assemblies
have been demonstrated for a diversity of
macromolecules. This has been shown for nucleic
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 REVIEW ARTICLE
a b
c
Figure 1 Silicic skeletons of
unicellular organisms. a,b,
Radiolaria and c,d, diatoms
show complex and finely
carved morphologies in
scanning electron microscopy
(SEM). a–c: Scale bar = 10 µm;
d: Scale bar = 1 µm.
Reproduced by permission
of CNRS editions, NATURE
×10.000, 1973. Copyright D.R.
(droits réservés).
278
nmat1339-print.indd 278
d nature proposes? Man has always made use of wood,
acids, proteins and polysaccharides, localized within
(nucleus, cytoplasm) or outside cells (extracellular
matrix), and similar assemblies are now being
reproduced experimentally with purified biological
macromolecules11 (Figs 2c,d, 3d). In a non-selective
manner, a recent approach of materials chemists has
been to organize mineral matter in vitro, by using
as templates more or less ordered phases of nucleic
acids12, proteins13 and polysaccharides14.
The building of complex structures is promoted
by specific links due to the three-dimensional
conformations of macromolecules, showing
topological variability and diversity. Efficient
recognition procedures occur in biology that imply
stereospecific structures at the nanometre scale
(antibodies, enzymes and so on). In fact, natural
materials are highly integrated systems having found a
compromise between different properties or functions
(such as mechanics, density, permeability, colour
and hydrophobia, and so on), often being controlled
by a versatile system of sensor arrays15. In many
biosystems, such a high level of integration associates
three aspects: miniaturization whose object is to
accommodate a maximum of elementary functions
in a small volume, hybridization between inorganic
and organic components optimizing complementary
possibilities and functions and hierarchy.
Indeed, hierarchical constructions on a
scale ranging from nanometres, micrometres, to
millimetres are characteristic of biological structures
introducing the capacity to answer the physical
or chemical demands occurring at these different
levels16 (Figs 1–3). Such highly complex and aesthetic
structures pass well beyond current accomplishments
realized in materials science, even if advances in
©2005 Nature Publishing Group
the field called ‘organized matter chemistry’17 show
promising man-made materials, as illustrated in
many publications of the past decade17–39. Key aspects
of these approaches are related to the controlled
construction of textured organic–inorganic
assemblies by direct or synergistic templating. Striking
examples concern the synthesis of mesostructured
silica in lipid helicoids40, the template-directed
synthesis of nanotubes using tobacco mosaic virus
liquid crystals41, DNA-driven self-assembly of gold
nanorods42, and the synthesis of linear chains of
nanoparticles and nanofilament arrays in water and
oil microemulsions43,44.
Should we then just be fascinated by what
cotton, silk, bone, horn or shells used as textiles,
tools, weapons and ornaments. New and stricter
requirements are now being set up to achieve greater
harmony between the environment and human
activities. New materials and systems produced
by man must in future aim at higher levels of
sophistication and miniaturization, be recyclable
and respect the environment, be reliable and
consume less energy. By elucidating the construction
rules of living organisms the possibility to create
new materials and systems will be offered. This field
of research could obviously bring improved and
even higher-performing new materials. One strategy
may be to ‘fish’ for interesting new materials in
complex mixtures and to understand the ‘language
of shape’ through the use of modern microscopy-
based techniques. However, a real breakthrough
requires an understanding of the basic building
principles of living organisms and a study of the
chemical and physical properties at the interfaces,
to control the form, size and compaction of objects.
This understanding is of paramount importance for
the efficient development of a ‘chemistry of form’
in the laboratory45. We believe that a biomimetic
approach to materials science cannot be limited
to the copy of objects proposed by nature, but
rather a more global strategy, where the best
multidisciplinary approaches must be efficiently
expressed by the scientific commmunity through
the creation of a new ‘Ecole de Pensée’ (think tank)1.
The present review will summarize some of the
main biomimetic or bionspired domains currently
investigated in materials science. It will successively
consider: supramolecular chemistry and hybrid
materials, polymeric materials, bioinspired materials
and biomaterials.
HIERARCHICAL ARCHITECTURES: FROM SUPRAMOLECULAR
CHEMISTRY TO HYBRID MATERIALS
Supramolecular chemistry, a fast-growing research
domain, studies complex molecules and assemblies
(molecular crystals, liposomes, micelles, bilayered
membranes) resulting from the fine-tuning of
intermolecular interactions46–51. Highly stereospecific
processes exist in biology: substrate–receptor
fixation, substrate–enzyme links, multiprotein
complexes, antigen–antibody immune responses,
genetic code reading present in biological
processes such as virus specific cell invasion,
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 REVIEW ARTICLE
neurotransmitting signals and cell recognition. b
These biological examples both inspire and stimulate
research, indeed synthetic catalytic systems already
show properties close to natural ones such as
rapidity and selectivity50,51. Efficient catalysts have
been created using cyclodextrines, cyclophanes or
calixarenes, chosen as subunits capable of specific
molecular recognition50,51. Studies on the principles
governing redox reactions will shed light on new a
artificial supramolecular devices, opening up ways of
achieving more efficient and selective catalysts.
Molecular printing techniques offer new
opportunities in affinity chromatography, catalysis,
immunoanalysis and biosensors52. Antibodies and
enzymes are the biomolecules currently used in
analytical chemistry or biochemistry to detect or
quantify molecules specifically recognized by a
receptor. Biomolecules are nevertheless expensive and
their field of application often limited to restricted d
natural conditions. A new approach is to create within
a synthetic material, usually a polymer, prints of a
target molecule playing the role of a specific receptor.
Complementary functions, combining optimal
configurations and restricted space, can then be
added. The end product mimics biological selectivity
by molecular recognition but with the advantage of
stability and lower cost52,53. c
Another of nature’s remarkable features is its
ability to combine at the nanoscale (bio)organic and
inorganic components. Advances made by the ‘soft
chemistry’ community during the past ten years have
produced, by carefully controlled organic–inorganic
interfaces, original hybrid materials with controlled
porosity and/or texture20,54–56 (Fig. 4). Abundant
sol–gel-derived hybrid materials resulting from soft
chemistry give easy-to-process materials offering
many advantages as tuneable physical properties,
high photochemical and thermal stability, chemical Figure 2 Collagen supramolecular arrangements in biological tissues and self-assembled structures.
inertness and negligible swelling, both in aqueous a,b, Human compact bone osteon. Periodic extinctions concentric to the osteon canal in polarized
and organic solvents. light microscopy (PLM) between crossed polars (a). Scale bar = 10 µm. Collagen fibrils draw
Original hybrid materials with tuneable optical series of nested arcs (noted by thick bars on the figure) in ultrathin sections of decalcified material
attributes offering modulated properties have been (b). Transmission electron microscopy (TEM), Scale bar = 1 µm. c,d, Liquid-crystalline collagen
designed during this past decade57, the following are assemblies. Fingerprint texture in acid-soluble collagen solution (c). PLM, Scale bar = 10 µm. Arced
some examples. Hybrid materials, pH sensitive over a patterns drawn by collagen fibrils in sections of pH induced gelated cholesteric phases (d). TEM, Scale
wide range form silica-indicator tensioactive-coloured bar = 0.5 µm. Parts a, b, d reprinted from ref. 142. Copyright (2003), with permission from Elsevier.
composites56–59. Photochromic materials, designed
from spyro-oxazines embedded in hybrid matrices
giving very fast responses; the performance depending
on the tuning of dye–matrix interactions implying a have recently been produced72–76. Good preservation
perfect adjustment of the hydrophilic–hydrophobic of the enzyme activity can be tested by optical or
balance, rheo-mechanical properties and accessibility electro-chemical methods. Biotechnologies already
of the matrix60,61. Organically modified silicas with use enzymes and bacteria as synthetic tools77–79; their
grafted azoic push–pull chromophores that exhibit further encapsulation in solid matrices should bring
very high second-order optical nonlinearity62. modulated and enhanced biosynthetic properties. The
All the synthesis approaches described in the exploitation of hybrid materials in domains including
vastly expanding literature will, without any doubt, immunology tests, encapsulation and/or vectorization
allow hybrid materials to be designed with enhanced is currently being tested. Biologically programmed
mechanical, optical and electric properties56,63,64. assemblies built from inorganic building blocks with
Such materials are thus expected to find applications intelligent organic function make an interesting
in smart devices, sensors, catalysis, separation and interface for materials science80–85. For example, smart
vectorization domains and so on. Another developing assemblies of gold nanoparticles coupled by surface-
domain concerns the design of hybrid architectures absorbed antibodies such as streptavidin-bovine have
formed from inorganic nanoparticles or inorganic been recently designed82,83, and original biohybrids
gels and biomolecules65–71. Specific biosensors combining nucleic acids and oxide nanoparticles
composed of enzymes immobilized in silica xerogels have been obtained and are being tested in genetic

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 REVIEW ARTICLE
a been demonstrated in the past few years. Indeed,
b d
Figure 3 Ordered organic and
mineral networks in the crab
cuticle and self-assembled
structures. a, Decalcified
chitin–protein organic matrix
showing periodic extinction
bands in PLM between crossed
polars. Scale bar = 20 µm.
b, Chitin–protein fibrils lying
successively parallel, oblique
or normal to the section plan,
analogous to a cholesteric
geometry. TEM, Scale
bar = 1 µm. c, Calcite skeleton
formed around the regularly
twisting organic fibrils. SEM,
Scale bar = 0.2 µm.
d, Liquid-crystalline assembly
of aqueous colloidal
chitin suspensions. PLM,
Scale bar = 100 µm (Belamie,
private communication).
Parts a and c reprinted with
permission from ref. 143.
280
nmat1339-print.indd 280
c
therapy84. The exploitation of DNA for material
purposes77 and the use of genetically engineered
proteins and organisms for inorganic growth shape
and self-assembly opens up new avenues for the
design of original nanostructures84–88. Indeed, the field
of bio-related materials is a huge reservoir of original
and complex morphologies.
One smart feature of natural materials concerns
their beautiful organization in which structure and
function are optimized at different length scales.
Recent data on polymeric materials, textured hybrids
and meso-organized structures20 have led to new
understanding of organic–organic or organic–mineral
interfaces22–39,89, allowing the controlled design of new
materials with complex or hierarchical structures.
Synthetic pathways currently investigated concern
(i) transcription17, using pre-organized or self-
assembled molecular or supramolecular moulds
of an organic (possibly biological90,91) or inorganic
nature, used as templates to construct the material
by nanocasting92 and nanolithographic processes91;
(ii) synergetic assembly17,93, co-assembling molecular
precursors and molecular moulds in situ; (iii)
morphosynthesis17, using chemical transformations
in confined geometries (microemulsions, micelles
and vesicles94) to produce complex structures; and
(iv) integrative synthesis17,95, which combines all
the previous methods to produce materials having
complex morphologies18,19,34.
Moreover, the use of preformed templates
(latex beads, bacteria, polydimethylsiloxane stamps,
topological defects of liquid crystals, and so on)
combined with the templated growth of inorganic or
hybrid phases through surfactant self-assembly allows
materials to be designed with original hierarchical
structures26,96–98. Recent examples concern the
synthesis and self-assembly of barium sulphate or
©2005 Nature Publishing Group
chromate nanoparticles as linear superstructures by
hydrophobic-driven surface interactions in complex
fluids45, emergent self-organization of calcium
phosphate block-copolymer nested colloids and the
formation of microporous calcium carbonate colloid
in foams and emulsion droplets99.
The possibility of generating complex shapes
with unique molecules or macromonomers has
organogelators can be used to form inorganic or even
hybrid fibres and helicoids20,21. Moreover, surfactants
form liquid crystals with topological defects that can
serve as moulds to form silica materials with complex
and original morphologies19,26,96 (Fig. 5). Finally,
controlled phase separation induced by coupling
polypeptides and inorganic CeO2 nanoparticles in a
solvent can also yield crystalline materials having bi-
modal and hierarchical porosity98 (Fig. 4c).
Major advances in the field concerning
bioinspired (inorganic, organic or hybrid) materials
having complex hierarchical structures are being
made due to synergistic collaborations occurring
between the organic polymer and inorganic
chemistry communities.
POLYMER SCIENCE, THE RICHNESS OF ‘ALI-BABA’S CAVE’
Polymer chemists can engineer large sets of
macromolecules with controlled lengths and selected
affinities100–106 (Fig. 6). Many amphiphilic block
copolymers, for example, allow copolymer ceramic-
composites to be constructed with original Im3m
morphologies such as the Plumber’s nightmare
described by the Wiesner group103,104.
Double hydrophilic block copolymers are also a
new class of amphiphilic macromolecules of rapidly
increasing importance. They are water-soluble
polymers in which amphiphilicity can be induced
through the presence of a substrate or by temperature
and pH changes. Their chemical structure can be
tuned for a wide range of applications covering
such differing aspects as colloid stabilization, crystal
growth modification, induced micelle formation and
polyelectrolyte complexing towards novel drug-
carrier systems. In particular, mineralization processes
can be controlled by using double hydrophilic block
copolymers inspired by biology, which contain a
molecular head reacting with the metal and a
central non-reactive part similar to proteins
containing hydrophilic and mineralophilic sites107.
Such polymers help control the size, form, structure
and assemblies of inorganic crystals. Indeed, original
superstructures have been obtained, as well as aligned
hydroxyapatite whiskers or mineral crystals having
complex morphologies107–110.
Natural systems are also characterized by mobility,
and again the field of polymer research offers many
opportunities for designing materials responding to
external stimuli. The synthesis of adaptative systems,
as electro-active gels or artificial muscles is in full
expansion with studies of their physico-chemical
properties. Such materials respond to external
stimuli such as solvent, pH, light, electric field or
temperature111,112. Positive results already concern
photoactive systems and hydrogels with possible future
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 REVIEW ARTICLE
a Figure 4 Multiscale porous
materials in vivo and in vitro.
a, Cubic mesotextured TiO2
film obtained by evaporation
induced self-assembly using
block copolymer (polyethylene
oxide–polypropylene
oxide–polyethylene oxide;
PEO-PPO-PEO) templates.
TEM, Scale bar = 100 µm.
Reprinted with permission
from ref. 144. Copyright (2003)
American Chemical Society.
b, Porous silica exoskeleton
observed in diatoms.
SEM, Scale bar = 10 µm.
Reproduced by permission
of CNRS editions, NATURE
×10.000, 1973. Copyright D.R
(droits réservés). c, Image
of hybrid template-directed
assembly by PBLG of CeO2
nanoparticles, the composite
b c shows macroporous CeO2 with
microporous nanocrystalline
inorganic walls. SEM, Scale
bar = 10 µm. Reproduced by
permission of the Royal Society
of Chemistry from ref. 98.
d–f, Micrographs at different
scales of hierarchically ordered
porous silica. MEB (d,e), TEM
(f). Images d–f reprinted
with permission from ref. 97.
Copyright 1998 AAAS.

d e f

10 µm 1 µm 100 nm

medical applications in robotics. Materials mimicking
the properties of muscles must combine short time-
lapse responses and weak stimuli113,114. Hydrogels,
photosensitive gels or ionizable gels, when electrically
stimulated, can be adapted to produce original water-
rich and flexible materials having the role of detectors,
transductors and actuators. Such materials may be
more versatile than the current robots combining
complex electric and metallic elements.
When producing complex hierarchical structures,
the part played by templating (weak or strong links
between organo-mineral domains) or diffusion (space-
and time-dependent concentration) is still not clear. If
the medium is sensitive to the chemical environment,
as found with some polyelectrolytes, reaction processes
could be coupled with the response of the material
(mechanical deformation) that could spontaneously
generate a propagating structure. Such systems offer
specific chemical sensibility applied to humid automats
(intelligent ‘valves’, autonomous movement actuation)
and controlled drug-delivery systems3.
There has also been new inputs from
biopolymers. These are currently being used
in the medical field but they can also provide

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 REVIEW ARTICLE
a b
c d
Figure 5 Original textures
of synthetic hybrid inorganic
materials. a,b, Functionalized
fibrous organosilica obtained in
the presence of organogelators
(a, SEM, Scale bar = 5 µm) or
template (b, TEM, Scale bar
= 0.2 µm). Reproduced by
permission of the Royal Society
of Chemistry from ref. 145.
c,d, SEM images of organised
hexagonal mesoporous silica
with complex morphologies,
spirals or helicoidal fibres arising
from topological liquid-crystalline
defects. Scale bar = 1 µm. Part
c reprinted with permission
from ref. 26, and part d from
ref. 96. e, Barium sulphate
(BaSO4) mineralized at pH 5 in
the presence of the double-
hydrophilic block copolymer
PEO-block-PEI-SO3H. SEM,
Bar = 20 µm. Reprinted with
permission from ref. 107.
282
nmat1339-print.indd 282
e or sugars are being synthesized by biochemists.
original construction elements for designing new
materials115–117. Amorphous domains in synthetic
polymers originate from chain intertwining when
restricted mobility or structural defects prevent
the emergence of ordered crystallized domains.
The three-dimensional structure of proteins
combines both regular and random domains,
showing crystalline and amorphous regions in
the same material. The possibility of controlling,
by alternating or mixing such sequences could
possibly bring interesting properties to newly
synthesized polymers. Polymer science is closely
concerned with biomimetic approaches as it offers
a wide range of materials with various behaviours
that can possibly mimic that of animals or plants.
Materials proposed include homopolymers,
copolymers, mixed polymers, charged or fibre-
reinforced polymers, small platelets or multilayers
and so on. In the near future, materials showing
higher elasticity, improved plastic deformation
and fracture resistance should be obtained in the
near future by coupling synthetic methods and
processing techniques.
The use of biological organisms to produce
interesting polymers is also a promising approach77,78.
Polyesters, for example, poly acid(3-hydroxybutyrate)
or APHB synthesized by bacteria find applications
in agriculture, medicine and the environment. This
thermoplastic is indeed degradable in soils or seawater
by an enzyme, a PHB depolymerase, present in
bacteria and fungi. A protein, bacteriorhodopsin, by
combining three interesting effects (proton pump–
charge separator and photochromic properties)
offers many potentially interesting applications
such as seawater desalination, converting solar
energy into electricity or developing new DNA
©2005 Nature Publishing Group
chips. The protein acts as a molecular commutator
or sensor, stocking optical information and
improving imaging or holographic techniques78.
Other polymers such as spider threads are strongly
anisotropic with remarkable mechanical properties.
Biotechnology companies are already trying to
produce one of its components, fibroin, by means
of cloned bacteria or transgenic goats. However,
even if the genetically synthesized fibroins fit the
expected chemical composition, a great deal of effort
is still needed to shape them as fibres that reach
the targeted mechanical properties. This example
illustrates a classical rule in materials science that ‘the
performance of a material depends not only on its
formulation but also on an optimized process’.
New polymers using nucleic acids, amino acids
The construction of minerals in the presence of
synthetic polymers or natural polymers (collagen,
chitin, polysaccharides, polypeptides and so on) or of
unicellular biological organisms (such as bacteria) have
started118–120. A link was established between the global
morphology and hierarchy of the echinoderm skeleton
and self-assembled liquid-crystalline structures formed
by surfactants; this initiated studies of calcium carbonate
growth in the presence of proteins extracted from sea-
urchin spines115. Microporous silica has been synthesized
in the presence of gelatine a low-cost biopolymer116,121.
Biopolymers such as block polypeptides can be used
to produce silica with different shapes117. The chemical
processes involved must be related in some way to
those found in natural biosilicas where proteins such as
silafins (proteins involved in silica formation in diatoms)
and silicateines (proteins involved in silica formation
in sponge spicules) serve as structuring agents and
catalysts122,123. On the other hand, silafins were recently
used as structuring agents to produce holographic
nanopatterning of silica spheres124. Only a few studies
actually concern the control of the chemical constitution
of biomaterials by regulated programming prior to
their formation. Molecular cloning and characterization
of lustrin A, a matrix protein from the nacreous layer
of mollusc shell, is obtained with multiple functions
associated with the protein125.
Genetically modified organisms will thus
produce molecular assemblies of possible interest
in the search for materials with interesting
structure-directing or catalytic properties79,86,88.
Moreover, the influence of confinement on
the dynamics of macromolecules (natural and
synthetic) trapped in aggregates or inorganic or
hybrid lattices (mesoporous or lamellar hosts,
and so on) and on the mechanical properties of
nanocomposites has not been sufficiently studied.
The biomimetic aspects previously described
concern mainly new materials resulting from
chemical or biochemical designs. However, if
the final goal of biomimesis is to try and mimic
biological materials in the sense of producing
indistinguishable copies, it can also reproduce
some essential aspects of a natural material
without duplicating it all. Indeed at present,
human knowledge in materials and associated
sciences is not sufficiently advanced to engineer
such highly complex duplications.
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a b
e f
i j
A B
0.5 µm
C D
REVIEW ARTICLE
Figure 6 Complex
morphologies attainable
in triblock copolymers. For
example, lamella (a), cylinder
(b, c), sphere (d), ring (e),
gyroid (l), and so on. Different
ultrastructures are illustrated in
c d sections of triblock copolymers.
Reprinted with permission
from ref. 146. Copyright
1999, American Institute of
Physics. A, (corresponding to
illustration c) Cylinders appear
g h as spherical microdomains
between two distinct
lamellar domains. TEM, scale
bar = 0.5 µm. Reprinted in part
with permission from ref. 147.
Copyright (1993) American
k l Chemical Society.
B, (corresponding to illustration
d) Spheres appear as spherical
microdomains between two
distinct lamellar domains. TEM,
scale bar = 0.5 µm. Reprinted
in part with permission from
ref. 148. Copyright (1995)
American Chemical Society.
C, (corresponding to diagram
e) Rings around the cylinders
are recognized as small
spherical microdomains. TEM,
scale bar = 0.5 µm. Reprinted
in part with permission from
ref. 147. Copyright (1993)
0.5 µm American Chemical Society.
D, ‘Knitting pattern’ in triblock
copolymers. TEM, scale
bar = 0.5 µm. Reprinted in part
with permission from ref. 149.
Copyright (1998) American
Chemical Society.

0.5 µm

0.5 µm

BIO- AND BIOINSPIRED MATERIALS WITH
CONTROLLED PROPERTIES
Natural materials offer remarkable hydrodynamic,
aerodynamic, wetting and adhesive properties.
Beautiful examples are butterfly wings and
chameleons. Obvious applications concern
surface coatings with anti-fouling, hydrophobic,
protective or adhesive characteristics and also
cosmetic products. One way to take advantage
of the emerging field of biomimetics is to select
ideas and inventive principles from nature and
apply them to engineering products. Materials
reproducing structures described in animals and
plants already exist. The study of the microstructure
of lily leaves has inspired rugose super hydrophobic
or hydrophillic coatings126 (Fig. 7). The structural
analysis of shark or dolphin skin has produced
‘riblets’, which are plastic films covered by
microscopic grooves. Experimentally placed on

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a implants for tissue repair requires a thorough
c soft tissues such as dermis, tendons and blood
Figure 7 Natural and
bioinspired superhydrophobic
coatings126. a, Lily leaf showing
a rugose coating. SEM, scale
bar = 3 µm. b, Water droplet
on the top of leaves from
the South American plant
Setcreasea. c, Industrial rugose
surface of silica. SEM, scale
bar =1 µm. d, Water droplet on
industrial hydrophobic coatings.
Parts c and d reprinted with
permission from ref. 126.
284
nmat1339-print.indd 284
b requires interdisciplinary approaches including
d cells interact with the surrounding matrix and
airplane wings they reduce the hydrodynamic trail
and economize fuel15. A number of notable successes
that have been exploited in engineering disciplines
have been described, such as Nylon or Kevlar
inspired from natural silk or Velcro inspired by the
hooked seeds of goosegrass127–129.
The present overview on the interfaces
between materials science and biology will not
be complete without mentioning the research
on materials for implants or prostheses3. The
term biomaterial includes all materials or
systems proposed for clinical applications to
replace part of a living system or to function in
intimate contact with living tissues. Traditional
materials science researchers and engineers are
still poorly exploring this complex domain, as
it requires consideration of biocompatibility,
that is, acceptance of the artificial implant by
the surrounding tissues. Tissue engineering
©2005 Nature Publishing Group
strong biological knowledge, because designing
understanding of the structure and function of the
organ to be replaced. Either permanent implants
(metallic, alloy, ceramic, composite) in the case of
weight-bearing or resorbable implants (polymeric,
biologic) for soft-tissue replacement have been
successively proposed. It further appears that the
implanted materials, whether for hard or soft
tissues, need to be accepted by the surrounding
biological environment, to elicit specific cellular
responses130. In a physiological process, specific
exercise adhesion, migration, proliferation
and remodelling. For example, fibroblasts in
skin and tendon or osteoblasts in bone show
properties controlled by interactions between cell
surface receptors (integrins) and specific matrix
molecules (collagen, fibronectin). Consequently,
for material recognition by cells, surface or bulk
modifications of biomimetic materials have been
processed by chemical or physical methods to add
bioactive molecules either in the form of native
long chains or of short peptide sequences131. In
vessels, the concept is to use a resorbable template
that guides tissue regeneration and is progressively
degraded. The role of living cells, either implanted
within the biomaterial or originating from the
patient’s organ, will be to promote new tissue
formation and degrade the implanted material by
specific proteases. In hard tissue replacements the
classical ‘bioinert’ concepts have also progressed
by means of physico-chemical studies of
biomineral interfaces with interest for ‘bioactive’
materials that stimulate tissue mineralization. An
example is the Bioglass process, a composite of
silicium, calcium and sodium oxides favouring
apatite hydroxyl-carbonate crystallization, but
also contributing to the cell cycle implied in
tissue formation. Coral, exploited from natural
resources, or synthetic coral (Interpore process)
are also used as implant materials. As human
longevity increases, this domain becomes
economically significant and a major challenge of
the biology/material interface.
In many biomineralization processes the
progression of mineral domains takes place on a
migration front line moving through the organic
matrix. New ceramics and composites manufactured
by stereolithography, multilayering, three-dimensional
printing or laser-sintering allow similar processes
to be adapted to the formation of films or bulk
composite132. Growth by successive layer deposits
offers better control of the material’s resulting
properties. It allows sensors to be incorporated
and the possibility of non-destructive tests during
fabrication steps as a function of size, volume or
aging. Biological systems involve constant controls
by using sets of diversified sensors, and therefore the
design of high-technology materials should follow
this path. In the long term even more possibilities
exist: metal sintering, the moulding of thermoplastic
materials, processing of multifunctional materials
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11/3/05 10:08:11 am

and ceramic objects for domestic use or as evolving
implants and biomaterials showing a better
biocompatibility132–134. These approaches would not
only allow three-dimensional innovative composites
to be created but also ‘smart’ materials such as
cements or bio-cements controlled over time and with
the capacity for self-repair132–134.
PROMISING RESEARCH DEVELOPMENTS
An eclectic approach to designing and
manufacturing advanced materials necessarily
includes biology, because a remarkable property
of biological systems is their capacity to integrate
molecular synthesis at very high levels of
organization, structure and dynamics. Industrial
technologies have already been inspired by dolphin
skin, lily leaves and spider threads to produce
new materials, but this research field is only at its
infancy. Despite the efforts made this past decade
to elaborate bio-inspired materials, characterize
their structural and physico-chemical properties,
understand their structure–function relationships
and most of all their different formation steps,
many unexplored mechanisms still remain to be
investigated. In relation to the surfactant-templated
growth of nanostructured materials, the recent
use of microorganisms to control inorganic crystal
formation has been promoted as genetically
engineered polypeptides binding to selected
inorganics (GEPIs), such as silica135 or gold136.
GEPIs are based on three fundamental principles:
molecular recognition, self-assembly and DNA
manipulation, and they promise numerous successes
in bio-directed technologies84,85.
Models describing the formation path of
mesostructured hybrid and inorganic materials
have been proposed during the past few
years17,18,20. Even if they are still naive, these
approaches, which favour understanding, seem
a priori more elegant than purely combinatory
ones and must be encouraged. Indeed, more
rational knowledge on the nature and structure
of new materials obtained by various synthetic
pathways will allow the construction of ‘tailor-
made’ materials. These studies must also compare
in vivo synthetic strategies of natural systems and
in vitro realizations. Moreover, studies concerning
a better knowledge of inorganic–organic interfaces
are strongly needed including the identification
of molecular interaction types, evaluation of link
energy and stability. The still poorly understood
role of these hybrid interfaces on the modulation
of optical, mechanical, catalytic and thermal
properties must be investigated in depth.
Several remarks arise from the current
productions of bioinspired materials with hierarchical
structures. Chemists usually consider that a perfect
product is pure, homogeneous and exhibits constant
parameters. The first synthesis of liquid crystals has
been a success of chemistry but in the search for pure
substances, these results have long been denied. This
mindset is still present nowadays and could hinder
interesting discoveries. Indeed, many interesting
assemblies arise from complex mixtures and living
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REVIEW ARTICLE
beings owe their existence to blind evolution resulting
in complex associations.
The elaboration of materials using liquid-
crystalline self-assemblies as templates requires precise
knowledge of their phase diagram in the presence
of the growing mineral components. Exploring the
existence of domains and subdomains of these hybrid
phases in situ during their formation and under
controlled chemical and processing parameters is
essential for obtaining reproducible products137,138.
Complex biomineral structures found in nature
probably result from tailored combinations of
several processes such as: self-assembly, controlled
phase-separation and confinement in membrane-
bounded compartments (controlling diffusion in
and out of reagents), the use of topological defects
or dissipative structures as micromoulds, associated
with external stimuli or fields. These external
stimuli can be produced during film formation by
reagent evaporation, or obtained by continuous or
semi-continuous reactor synthesis with controlled
flows, composition and temperature gradients,
magnetic or electric fields, or even by mechanical or
ultrasonic constraints. Only a few research groups
are currently tackling the question of assembly
process in such ‘open systems’.
The role of molecular chirality is also little
investigated in current materials science studies,
although it corresponds to the recognition,
selection and construction paths assumed in
natural systems. Clever use of chirality could bring
new possibilities21,139,140. Indeed, chirality in hybrid
liquid crystals, in surfactant organo–mineral
organized assemblies, nanobuilding blocks made
of organofunctional disymmetric clusters or
nanoparticles appear to be very promising for the
construction of original architectures21,140,141.
The long-term evolution of materials is an
important issue for optimizing their applications.
Living cells possess the ability for self-diagnostic, self-
repair and self-destruction (apoptosis). Ageing, repair
and destruction (recycling) are research domains that
materials scientists should consider further.
CONCLUSION
A biomimetic and bioinspired approach to
materials is one of the most promising scientific
and technological challenges of the coming years.
Bioinspired materials and systems, adaptive
materials, nanomaterials, hierarchically structured
materials, three-dimensional composites, materials
compatible with ecological requirements, and
so on, should become a major preoccupation
in advanced technologies. Bioinspired selective
multifunctional materials with associated
properties (such as separation, adsorption, catalysis,
sensing, biosensing, imaging, multitherapy) will
appear in the near future.
An expanding need for biomimetic and
bioinspired materials already exists as solutions
always become limited with regard to new technical,
economic or ecological evolutions and demands.
The subject of biomimetism and materials is at the
frontier between biological and material sciences,
285
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Acknowledgements
Emmanuel Belamie and Thibaud Coradin are gratefully acknowledged for their
critical reading of the manuscript and for interesting discussions.
Correspondence should be addressed to C. S., H. A. or M.M.G.G.
Competing financial interests
The authors declare that they have no competing financial interests.
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