biomimetism and bioinspiration as tools for the design … · biomimetism and bioinspiration as...

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Biomimetism and bioinspiration as tools for the design of innovative materials and systemsMaterials 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, effi cient and environment-

respecting materials requires a multidisciplinary approach.

CLÉMENT SANCHEZ1*, HERVÉ ARRIBART2* AND MARIE MADELEINE GIRAUD GUILLE1*1Laboratoire de Chimie de la Matière Condensée, Université Pierre & Marie Curie, Ecole Pratique des Hautes Etudes, Centre National de la Recherche Scientifi que, 4 place Jussieu, Tour 54, 5ème étage, 75005 Paris, France2Saint-Gobain Recherche, 39 quai Lucien Lefranc, 93303 Aubervilliers, France*e-mail: [email protected]; [email protected]; [email protected]

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 affi nities 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, confi nement, chirality in complex systems, possibly in relation to external stimuli or fi elds 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

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 fi ve hundred million years fully proven materials have appeared resulting from stringent selection processes. A most remarkable feature of naturally occurring materials is their fi nely 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 defi ned 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, fl exible, 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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acids, proteins and polysaccharides, localized within (nucleus, cytoplasm) or outside cells (extracellular matrix), and similar assemblies are now being reproduced experimentally with purifi ed 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 specifi c links due to the three-dimensional conformations of macromolecules, showing topological variability and diversity. Effi cient recognition procedures occur in biology that imply stereospecifi c 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

the fi eld 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 nanofi lament arrays in water and oil microemulsions43,44.

Should we then just be fascinated by what nature proposes? Man has always made use of wood, 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 fi eld of research could obviously bring improved and even higher-performing new materials. One strategy may be to ‘fi sh’ 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 effi cient 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 effi ciently expressed by the scientifi c 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 fi ne-tuning of intermolecular interactions46–51. Highly stereospecifi c processes exist in biology: substrate–receptor fi xation, substrate–enzyme links, multiprotein complexes, antigen–antibody immune responses, genetic code reading present in biological processes such as virus specifi c cell invasion,

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Figure 1 Silicic skeletons of unicellular organisms. a,b, Radiolaria and c,d, diatoms show complex and fi nely 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).

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neurotransmitting signals and cell recognition. 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. Effi cient catalysts have been created using cyclodextrines, cyclophanes or calixarenes, chosen as subunits capable of specifi c molecular recognition50,51. Studies on the principles governing redox reactions will shed light on new artifi cial supramolecular devices, opening up ways of achieving more effi cient and selective catalysts.

Molecular printing techniques offer new opportunities in affi nity chromatography, catalysis, immunoanalysis and biosensors52. Antibodies and enzymes are the biomolecules currently used in analytical chemistry or biochemistry to detect or quantify molecules specifi cally recognized by a receptor. Biomolecules are nevertheless expensive and their fi eld of application often limited to restricted 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 specifi c receptor. Complementary functions, combining optimal confi gurations 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.

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 inertness and negligible swelling, both in aqueous and organic solvents.

Original hybrid materials with tuneable optical attributes offering modulated properties have been designed during this past decade57, the following are some examples. Hybrid materials, pH sensitive over a wide range form silica-indicator tensioactive-coloured 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 perfect adjustment of the hydrophilic–hydrophobic balance, rheo-mechanical properties and accessibility of the matrix60,61. Organically modifi ed silicas with grafted azoic push–pull chromophores that exhibit very high second-order optical nonlinearity62.

All the synthesis approaches described in the vastly expanding literature will, without any doubt, allow hybrid materials to be designed with enhanced mechanical, optical and electric properties56,63,64. Such materials are thus expected to fi nd applications in smart devices, sensors, catalysis, separation and vectorization domains and so on. Another developing domain concerns the design of hybrid architectures formed from inorganic nanoparticles or inorganic gels and biomolecules65–71. Specifi c biosensors composed of enzymes immobilized in silica xerogels

have recently been produced72–76. Good preservation of the enzyme activity can be tested by optical or electro-chemical methods. Biotechnologies already use enzymes and bacteria as synthetic tools77–79; their further encapsulation in solid matrices should bring modulated and enhanced biosynthetic properties. The exploitation of hybrid materials in domains including immunology tests, encapsulation and/or vectorization is currently being tested. Biologically programmed assemblies built from inorganic building blocks with intelligent organic function make an interesting interface for materials science80–85. For example, smart assemblies of gold nanoparticles coupled by surface-absorbed antibodies such as streptavidin-bovine have been recently designed82,83, and original biohybrids combining nucleic acids and oxide nanoparticles have been obtained and are being tested in genetic

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Figure 2 Collagen supramolecular arrangements in biological tissues and self-assembled structures. a,b, Human compact bone osteon. Periodic extinctions concentric to the osteon canal in polarized light microscopy (PLM) between crossed polars (a). Scale bar = 10 µm. Collagen fi brils draw series of nested arcs (noted by thick bars on the fi gure) in ultrathin sections of decalcifi ed material (b). Transmission electron microscopy (TEM), Scale bar = 1 µm. c,d, Liquid-crystalline collagen assemblies. Fingerprint texture in acid-soluble collagen solution (c). PLM, Scale bar = 10 µm. Arced patterns drawn by collagen fi brils in sections of pH induced gelated cholesteric phases (d). TEM, Scale bar = 0.5 µm. Parts a, b, d reprinted from ref. 142. Copyright (2003), with permission from Elsevier.




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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 fi eld 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 confi ned 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

chromate nanoparticles as linear superstructures by hydrophobic-driven surface interactions in complex fl uids45, 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 been demonstrated in the past few years. Indeed, organogelators can be used to form inorganic or even hybrid fi bres 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 fi eld 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 affi nities100–106 (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 modifi cation, 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 fi eld of polymer research offers many opportunities for designing materials responding to external stimuli. The synthesis of adaptative systems, as electro-active gels or artifi cial muscles is in full expansion with studies of their physico-chemical properties. Such materials respond to external stimuli such as solvent, pH, light, electric fi eld or temperature111,112. Positive results already concern photoactive systems and hydrogels with possible future

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Figure 3 Ordered organic and mineral networks in the crab cuticle and self-assembled structures. a, Decalcifi ed chitin–protein organic matrix showing periodic extinction bands in PLM between crossed polars. Scale bar = 20 µm. b, Chitin–protein fi brils 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 fi brils. 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.




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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 fl exible 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 specifi c 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 fi eld but they can also provide

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Figure 4 Multiscale porous materials in vivo and in vitro. a, Cubic mesotextured TiO2 fi lm 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 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.




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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 fi bre-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 fi nd 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

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, fi broin, by means of cloned bacteria or transgenic goats. However, even if the genetically synthesized fi broins fi t the expected chemical composition, a great deal of effort is still needed to shape them as fi bres 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 or sugars are being synthesized by biochemists. 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 silafi ns (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, silafi ns 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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Figure 5 Original textures of synthetic hybrid inorganic materials. a,b, Functionalized fi brous 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 fi bres 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.




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BIO- AND BIOINSPIRED MATERIALS WITH CONTROLLED PROPERTIES

Natural materials offer remarkable hydrodynamic, aerodynamic, wetting and adhesive properties. Beautiful examples are butterfl y 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 fi eld 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 fi lms covered by microscopic grooves. Experimentally placed on

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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 sections of triblock copolymers. Reprinted with permission from ref. 146. Copyright 1999, American Institute of Physics. A, (corresponding to illustration c) Cylinders appear 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 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) 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.




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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

requires interdisciplinary approaches including strong biological knowledge, because designing implants for tissue repair requires a thorough 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 cells interact with the surrounding matrix and 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 soft tissues such as dermis, tendons and blood 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 fi lms 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 diversifi ed 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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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.




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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 fi eld 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 fi rst 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

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 confi nement 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 fi elds. These external stimuli can be produced during fi lm formation by reagent evaporation, or obtained by continuous or semi-continuous reactor synthesis with controlled fl ows, composition and temperature gradients, magnetic or electric fi elds, 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 scientifi c 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,




REVIEW ARTICLE

chemistry and physics together with biotechnology and information techniques; it represents a major international competitive sector of research for this new century. Even if these bio-inspired materials cannot be named ‘smart materials’ they will certainly be designed with intelligence.

DOI: 10.1038/nmat1339

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AcknowledgementsEmmanuel 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 fi nancial interestsThe authors declare that they have no competing fi nancial interests.




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