Biomimetism and Bioinspiration As Tools for the Design of Innovative

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REVIEW ARTICLE 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, efﬁ cient and environment- respecting materials requires a multidisciplinary approach.

CLÉMENT SANCHEZ1*, HERVÉ as chemistry, biology, physics or engineering1. In 2 all living organisms, whether very basic or highly ARRIBART * AND MARIE MADELEINE complex, nature provides a multiplicity of materials, GIRAUD GUILLE1* architectures, systems and functions2–6. For the past fi ve hundred million years fully proven materials 1Laboratoire de Chimie de la Matière Condensée, Université have appeared resulting from stringent selection Pierre & Marie Curie, Ecole Pratique des Hautes Etudes, processes. A most remarkable feature of naturally Centre National de la Recherche Scientifi que, 4 place Jussieu, occurring materials is their fi nely carved appearance Tour 54, 5ème étage, 75005 Paris, France such as observed in radiolaria or diatoms (Fig. 1). 2Saint-Gobain Recherche, 39 quai Lucien Lefranc, 93303 Current examples of natural composites are Aubervilliers, France crustacean carapaces or mollusc shells and bone or *e-mail: [email protected]; [email protected]; teeth tissues in vertebrates. [email protected] A high degree of sophistication is the rule and the various components of a structure are assembled This review considers the following currently following a clearly defi ned pattern. Highly elaborated investigated domains: supramolecular chemistry that performances characterizing biological materials is of interest for complex macromolecular assemblies result from time-dependant processes. Selecting such as molecular crystals, micelles and membranes; the right material for the right function occurs at a hybrid materials that combine organic and inorganic precise moment from sources available at that time. components on a nanoscale with innovative An advantage for chemists is to elaborate possible controlled textures; polymeric materials of synthetic new constructions from all chemical components or natural origin, showing controlled length, selected without any time-restricted conditions. However, the affi nities and rich structural combinations offering results of evolution converge on limited constituents a wide range of applications; bioinspired materials or principles. For example, a unique component reproducing principles or structures described in will be found to obey different functions in the animals or plants; biomaterials offering clinical same organism. A protein, such as type I collagen, applications in terms of compatibility, degradability presents different morphologies in different tissues and cell–matrix interactions. to perform different functions (Fig. 2a,b). Associated Efforts to understand and control self-assembly, or not with hydroxyapatite crystals, it gives rigid phase separation, confi nement, chirality in complex (high Young modulus) and shock-resistant tissues in systems, possibly in relation to external stimuli or bone7, it behaves like an elastomer with low rigidity fi elds and the use of genetically engineered proteins and high deformation to rupture in tendons8, or for inorganics are some promising challenges for shows optical properties such as transparency in bioinspired materials. cornea9. Another example is the arthropod cuticle, combining in different proportions chitin, proteins NATURE AS A SCHOOL FOR MATERIALS SCIENCE and calcite crystals10 to give tissues that are rigid, fl exible, opaque or translucent (Fig. 3a–c). Within Scientists are always amazed by the high degree biological organisms, identical organizational of sophistication and miniaturization found in principles to liquid-crystalline self-assemblies natural materials. Nature is indeed a school for have been demonstrated for a diversity of materials science and its associated disciplines such macromolecules. This has been shown for nucleic

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a b 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. c Should we then just be fascinated by what d 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 Figure 1 Silicic skeletons of acids, proteins and polysaccharides, localized within of shape’ through the use of modern microscopy- unicellular organisms. a,b, (nucleus, cytoplasm) or outside cells (extracellular based techniques. However, a real breakthrough Radiolaria and c,d, diatoms matrix), and similar assemblies are now being requires an understanding of the basic building show complex and fi nely reproduced experimentally with purifi ed biological principles of living organisms and a study of the carved morphologies in macromolecules11 (Figs 2c,d, 3d). In a non-selective chemical and physical properties at the interfaces, scanning electron microscopy manner, a recent approach of materials chemists has to control the form, size and compaction of objects. (SEM). a–c: Scale bar = 10 µm; been to organize mineral matter in vitro, by using This understanding is of paramount importance for d: Scale bar = 1 µm. as templates more or less ordered phases of nucleic the effi cient development of a ‘chemistry of form’ Reproduced by permission acids12, proteins13 and polysaccharides14. in the laboratory45. We believe that a biomimetic of CNRS editions, NATURE The building of complex structures is promoted approach to materials science cannot be limited ×10.000, 1973. Copyright D.R. by specifi c links due to the three-dimensional to the copy of objects proposed by nature, but (droits réservés). conformations of macromolecules, showing rather a more global strategy, where the best topological variability and diversity. Effi cient multidisciplinary approaches must be effi ciently recognition procedures occur in biology that imply expressed by the scientifi c commmunity through stereospecifi c structures at the nanometre scale the creation of a new ‘Ecole de Pensée’ (think tank)1. (antibodies, enzymes and so on). In fact, natural The present review will summarize some of the materials are highly integrated systems having found a main biomimetic or bionspired domains currently compromise between different properties or functions investigated in materials science. It will successively (such as mechanics, density, permeability, colour consider: supramolecular chemistry and hybrid and hydrophobia, and so on), often being controlled materials, polymeric materials, bioinspired materials by a versatile system of sensor arrays15. In many and biomaterials. biosystems, such a high level of integration associates three aspects: miniaturization whose object is to HIERARCHICAL ARCHITECTURES: FROM SUPRAMOLECULAR accommodate a maximum of elementary functions CHEMISTRY TO HYBRID MATERIALS in a small volume, hybridization between inorganic and organic components optimizing complementary Supramolecular chemistry, a fast-growing research possibilities and functions and hierarchy. domain, studies complex molecules and assemblies Indeed, hierarchical constructions on a (molecular crystals, liposomes, micelles, bilayered scale ranging from nanometres, micrometres, to membranes) resulting from the fi ne-tuning of millimetres are characteristic of biological structures intermolecular interactions46–51. Highly stereospecifi c introducing the capacity to answer the physical processes exist in biology: substrate–receptor or chemical demands occurring at these different fi xation, substrate–enzyme links, multiprotein levels16 (Figs 1–3). Such highly complex and aesthetic complexes, antigen–antibody immune responses, structures pass well beyond current accomplishments genetic code reading present in biological realized in materials science, even if advances in processes such as virus specifi c cell invasion,

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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. 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 a 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 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 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 52,53 stability and lower cost . 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 fi brils draw Original hybrid materials with tuneable optical series of nested arcs (noted by thick bars on the fi gure) in ultrathin sections of decalcifi ed 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 fi brils 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 modifi ed 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 fi nd 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. Specifi c 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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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 a 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 c 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. b d POLYMER SCIENCE, THE RICHNESS OF ‘ALI-BABA’S CAVE’

Polymer chemists can engineer large sets of Figure 3 Ordered organic and therapy84. The exploitation of DNA for material macromolecules with controlled lengths and selected mineral networks in the crab purposes77 and the use of genetically engineered affi nities100–106 (Fig. 6). Many amphiphilic block cuticle and self-assembled proteins and organisms for inorganic growth shape copolymers, for example, allow copolymer ceramic- structures. a, Decalcifi ed and self-assembly opens up new avenues for the composites to be constructed with original Im3m chitin–protein organic matrix design of original nanostructures84–88. Indeed, the fi eld morphologies such as the Plumber’s nightmare showing periodic extinction of bio-related materials is a huge reservoir of original described by the Wiesner group103,104. bands in PLM between crossed and complex morphologies. Double hydrophilic block copolymers are also a polars. Scale bar = 20 µm. One smart feature of natural materials concerns new class of amphiphilic macromolecules of rapidly b, Chitin–protein fi brils lying their beautiful organization in which structure and increasing importance. They are water-soluble successively parallel, oblique function are optimized at different length scales. polymers in which amphiphilicity can be induced or normal to the section plan, Recent data on polymeric materials, textured hybrids through the presence of a substrate or by temperature analogous to a cholesteric and meso-organized structures20 have led to new and pH changes. Their chemical structure can be geometry. TEM, Scale understanding of organic–organic or organic–mineral tuned for a wide range of applications covering bar = 1 µm. c, Calcite skeleton interfaces22–39,89, allowing the controlled design of new such differing aspects as colloid stabilization, crystal formed around the regularly materials with complex or hierarchical structures. growth modifi cation, induced micelle formation and twisting organic fi brils. SEM, Synthetic pathways currently investigated concern polyelectrolyte complexing towards novel drug- Scale bar = 0.2 µm. (i) transcription17, using pre-organized or self- carrier systems. In particular, mineralization processes d, Liquid-crystalline assembly assembled molecular or supramolecular moulds can be controlled by using double hydrophilic block of aqueous colloidal of an organic (possibly biological90,91) or inorganic copolymers inspired by biology, which contain a chitin suspensions. PLM, nature, used as templates to construct the material molecular head reacting with the metal and a Scale bar = 100 µm (Belamie, by nanocasting92 and nanolithographic processes91; central non-reactive part similar to proteins private communication). (ii) synergetic assembly17,93, co-assembling molecular containing hydrophilic and mineralophilic sites107. Parts a and c reprinted with precursors and molecular moulds in situ; (iii) Such polymers help control the size, form, structure permission from ref. 143. morphosynthesis17, using chemical transformations and assemblies of inorganic crystals. Indeed, original in confi ned geometries (microemulsions, micelles superstructures have been obtained, as well as aligned and vesicles94) to produce complex structures; and hydroxyapatite whiskers or mineral crystals having (iv) integrative synthesis17,95, which combines all complex morphologies107–110. the previous methods to produce materials having Natural systems are also characterized by mobility, complex morphologies18,19,34. and again the fi eld of polymer research offers many Moreover, the use of preformed templates opportunities for designing materials responding to (latex beads, bacteria, polydimethylsiloxane stamps, external stimuli. The synthesis of adaptative systems, topological defects of liquid crystals, and so on) as electro-active gels or artifi cial muscles is in full combined with the templated growth of inorganic or expansion with studies of their physico-chemical hybrid phases through surfactant self-assembly allows properties. Such materials respond to external materials to be designed with original hierarchical stimuli such as solvent, pH, light, electric fi eld or structures26,96–98. Recent examples concern the temperature111,112. Positive results already concern synthesis and self-assembly of barium sulphate or photoactive systems and hydrogels with possible future

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

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a b 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 c d e 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 Figure 5 Original textures original construction elements for designing new to produce silica with different shapes117. The chemical of synthetic hybrid inorganic materials115–117. Amorphous domains in synthetic processes involved must be related in some way to materials. a,b, Functionalized polymers originate from chain intertwining when those found in natural biosilicas where proteins such as fi brous organosilica obtained in restricted mobility or structural defects prevent silafi ns (proteins involved in silica formation in diatoms) the presence of organogelators the emergence of ordered crystallized domains. and silicateines (proteins involved in silica formation (a, SEM, Scale bar = 5 µm) or The three-dimensional structure of proteins in sponge spicules) serve as structuring agents and template (b, TEM, Scale bar combines both regular and random domains, catalysts122,123. On the other hand, silafi ns were recently = 0.2 µm). Reproduced by showing crystalline and amorphous regions in used as structuring agents to produce holographic permission of the Royal Society the same material. The possibility of controlling, nanopatterning of silica spheres124. Only a few studies of Chemistry from ref. 145. by alternating or mixing such sequences could actually concern the control of the chemical constitution c,d, SEM images of organised possibly bring interesting properties to newly of biomaterials by regulated programming prior to hexagonal mesoporous silica synthesized polymers. Polymer science is closely their formation. Molecular cloning and characterization with complex morphologies, concerned with biomimetic approaches as it offers of lustrin A, a matrix protein from the nacreous layer spirals or helicoidal fi bres arising a wide range of materials with various behaviours of mollusc shell, is obtained with multiple functions from topological liquid-crystalline that can possibly mimic that of animals or plants. associated with the protein125. defects. Scale bar = 1 µm. Part Materials proposed include homopolymers, Genetically modified organisms will thus c reprinted with permission copolymers, mixed polymers, charged or fi bre- produce molecular assemblies of possible interest from ref. 26, and part d from reinforced polymers, small platelets or multilayers in the search for materials with interesting ref. 96. e, Barium sulphate and so on. In the near future, materials showing structure-directing or catalytic properties79,86,88.

(BaSO4) mineralized at pH 5 in higher elasticity, improved plastic deformation Moreover, the influence of confinement on the presence of the double- and fracture resistance should be obtained in the the dynamics of macromolecules (natural and hydrophilic block copolymer near future by coupling synthetic methods and synthetic) trapped in aggregates or inorganic or

PEO-block-PEI-SO3H. SEM, processing techniques. hybrid lattices (mesoporous or lamellar hosts, Bar = 20 µm. Reprinted with The use of biological organisms to produce and so on) and on the mechanical properties of permission from ref. 107. interesting polymers is also a promising approach77,78. nanocomposites has not been sufficiently studied. Polyesters, for example, poly acid(3-hydroxybutyrate) The biomimetic aspects previously described or APHB synthesized by bacteria ﬁ nd applications concern mainly new materials resulting from in agriculture, medicine and the environment. This chemical or biochemical designs. However, if thermoplastic is indeed degradable in soils or seawater the final goal of biomimesis is to try and mimic by an enzyme, a PHB depolymerase, present in biological materials in the sense of producing bacteria and fungi. A protein, bacteriorhodopsin, by indistinguishable copies, it can also reproduce combining three interesting effects (proton pump– some essential aspects of a natural material charge separator and photochromic properties) without duplicating it all. Indeed at present, offers many potentially interesting applications human knowledge in materials and associated such as seawater desalination, converting solar sciences is not sufficiently advanced to engineer energy into electricity or developing new DNA such highly complex duplications.

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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 a b 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 e f 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 i j k l Chemical Society. B, (corresponding to illustration d) Spheres appear as spherical microdomains between two A B 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 0.5 µm American Chemical Society. D, ‘Knitting pattern’ in triblock copolymers. TEM, scale bar = 0.5 µm. Reprinted in part C D with permission from ref. 149. Copyright (1998) American Chemical Society.

0.5 µm

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

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b requires interdisciplinary approaches including strong biological knowledge, because designing a 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 d 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 c 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 Figure 7 Natural and airplane wings they reduce the hydrodynamic trail the biology/material interface. bioinspired superhydrophobic and economize fuel15. A number of notable successes In many biomineralization processes the coatings126. a, Lily leaf showing that have been exploited in engineering disciplines progression of mineral domains takes place on a a rugose coating. SEM, scale have been described, such as Nylon or Kevlar migration front line moving through the organic bar = 3 µm. b, Water droplet inspired from natural silk or Velcro inspired by the matrix. New ceramics and composites manufactured on the top of leaves from hooked seeds of goosegrass127–129. by stereolithography, multilayering, three-dimensional the South American plant The present overview on the interfaces printing or laser-sintering allow similar processes Setcreasea. c, Industrial rugose between materials science and biology will not to be adapted to the formation of ﬁ lms or bulk surface of silica. SEM, scale be complete without mentioning the research composite132. Growth by successive layer deposits bar =1 µm. d, Water droplet on on materials for implants or prostheses3. The offers better control of the material’s resulting industrial hydrophobic coatings. term biomaterial includes all materials or properties. It allows sensors to be incorporated Parts c and d reprinted with systems proposed for clinical applications to and the possibility of non-destructive tests during permission from ref. 126. replace part of a living system or to function in fabrication steps as a function of size, volume or intimate contact with living tissues. Traditional aging. Biological systems involve constant controls materials science researchers and engineers are by using sets of diversiﬁ ed sensors, and therefore the still poorly exploring this complex domain, as design of high-technology materials should follow it requires consideration of biocompatibility, this path. In the long term even more possibilities that is, acceptance of the artificial implant by exist: metal sintering, the moulding of thermoplastic the surrounding tissues. Tissue engineering materials, processing of multifunctional materials

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and ceramic objects for domestic use or as evolving beings owe their existence to blind evolution resulting implants and biomaterials showing a better in complex associations. biocompatibility132–134. These approaches would not The elaboration of materials using liquid- only allow three-dimensional innovative composites crystalline self-assemblies as templates requires precise to be created but also ‘smart’ materials such as knowledge of their phase diagram in the presence cements or bio-cements controlled over time and with of the growing mineral components. Exploring the the capacity for self-repair132–134. existence of domains and subdomains of these hybrid phases in situ during their formation and under PROMISING RESEARCH DEVELOPMENTS controlled chemical and processing parameters is essential for obtaining reproducible products137,138. An eclectic approach to designing and Complex biomineral structures found in nature manufacturing advanced materials necessarily probably result from tailored combinations of includes biology, because a remarkable property several processes such as: self-assembly, controlled of biological systems is their capacity to integrate phase-separation and confi nement in membrane- molecular synthesis at very high levels of bounded compartments (controlling diffusion in organization, structure and dynamics. Industrial and out of reagents), the use of topological defects technologies have already been inspired by dolphin or dissipative structures as micromoulds, associated skin, lily leaves and spider threads to produce with external stimuli or fi elds. These external new materials, but this research fi eld is only at its stimuli can be produced during fi lm formation by infancy. Despite the efforts made this past decade reagent evaporation, or obtained by continuous or to elaborate bio-inspired materials, characterize semi-continuous reactor synthesis with controlled their structural and physico-chemical properties, fl ows, composition and temperature gradients, understand their structure–function relationships magnetic or electric fi elds, or even by mechanical or and most of all their different formation steps, ultrasonic constraints. Only a few research groups many unexplored mechanisms still remain to be are currently tackling the question of assembly investigated. In relation to the surfactant-templated process in such ‘open systems’. growth of nanostructured materials, the recent The role of molecular chirality is also little use of microorganisms to control inorganic crystal investigated in current materials science studies, formation has been promoted as genetically although it corresponds to the recognition, engineered polypeptides binding to selected selection and construction paths assumed in inorganics (GEPIs), such as silica135 or gold136. natural systems. Clever use of chirality could bring GEPIs are based on three fundamental principles: new possibilities21,139,140. Indeed, chirality in hybrid molecular recognition, self-assembly and DNA liquid crystals, in surfactant organo–mineral manipulation, and they promise numerous successes organized assemblies, nanobuilding blocks made in bio-directed technologies84,85. of organofunctional disymmetric clusters or Models describing the formation path of nanoparticles appear to be very promising for the mesostructured hybrid and inorganic materials construction of original architectures21,140,141. have been proposed during the past few The long-term evolution of materials is an years17,18,20. Even if they are still naive, these important issue for optimizing their applications. approaches, which favour understanding, seem Living cells possess the ability for self-diagnostic, self- a priori more elegant than purely combinatory repair and self-destruction (apoptosis). Ageing, repair ones and must be encouraged. Indeed, more and destruction (recycling) are research domains that rational knowledge on the nature and structure materials scientists should consider further. of new materials obtained by various synthetic pathways will allow the construction of ‘tailor- CONCLUSION made’ materials. These studies must also compare in vivo synthetic strategies of natural systems and A biomimetic and bioinspired approach to in vitro realizations. Moreover, studies concerning materials is one of the most promising scientifi c a better knowledge of inorganic–organic interfaces and technological challenges of the coming years. are strongly needed including the identification Bioinspired materials and systems, adaptive of molecular interaction types, evaluation of link materials, nanomaterials, hierarchically structured energy and stability. The still poorly understood materials, three-dimensional composites, materials role of these hybrid interfaces on the modulation compatible with ecological requirements, and of optical, mechanical, catalytic and thermal so on, should become a major preoccupation properties must be investigated in depth. in advanced technologies. Bioinspired selective Several remarks arise from the current multifunctional materials with associated productions of bioinspired materials with hierarchical properties (such as separation, adsorption, catalysis, structures. Chemists usually consider that a perfect sensing, biosensing, imaging, multitherapy) will product is pure, homogeneous and exhibits constant appear in the near future. parameters. The fi rst synthesis of liquid crystals has An expanding need for biomimetic and been a success of chemistry but in the search for pure bioinspired materials already exists as solutions substances, these results have long been denied. This always become limited with regard to new technical, mindset is still present nowadays and could hinder economic or ecological evolutions and demands. interesting discoveries. Indeed, many interesting The subject of biomimetism and materials is at the assemblies arise from complex mixtures and living frontier between biological and material sciences,

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