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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, efficient and environment-

respecting materials requires a multidisciplinary approach.

CLÉMENT SANCHEZ1*, HERVÉ ARRIBART2* AND MARIE MADELEINEGIRAUD GUILLE1*1Laboratoire 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, 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 thatis of interest for complex macromolecular assembliessuch as molecular crystals, micelles and membranes;hybrid materials that combine organic and inorganiccomponents on a nanoscale with innovativecontrolled textures; polymeric materials of syntheticor natural origin, showing controlled length, selectedaffinities and rich structural combinations offeringa wide range of applications; bioinspired materialsreproducing principles or structures described inanimals 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 complexsystems, possibly in relation to external stimuli orfields and the use of genetically engineered proteinsfor inorganics are some promising challenges forbioinspired materials.

NATURE AS A SCHOOL FOR MATERIALS SCIENCE

Scientists are always amazed by the high degreeof sophistication and miniaturization found innatural materials. Nature is indeed a school formaterials science and its associated disciplines such

as chemistry, biology, physics or engineering1. Inall living organisms, whether very basic or highly complex, nature provides a multiplicity of materials,architectures, systems and functions2–6. For the pastfive hundred million years fully proven materialshave appeared resulting from stringent selectionprocesses. A most remarkable feature of naturally occurring materials is their finely carved appearancesuch as observed in radiolaria or diatoms (Fig. 1).Current examples of natural composites arecrustacean carapaces or mollusc shells and bone orteeth tissues in vertebrates.

A high degree of sophistication is the rule andthe various components of a structure are assembledfollowing a clearly defined pattern. Highly elaboratedperformances characterizing biological materialsresult from time-dependant processes. Selectingthe right material for the right function occurs at aprecise moment from sources available at that time.An advantage for chemists is to elaborate possiblenew constructions from all chemical componentswithout any time-restricted conditions. However, theresults of evolution converge on limited constituentsor principles. For example, a unique componentwill be found to obey different functions in thesame organism. A protein, such as type I collagen,

presents different morphologies in different tissuesto perform different functions (Fig. 2a,b). Associatedor not with hydroxyapatite crystals, it gives rigid(high Young modulus) and shock-resistant tissues inbone7, it behaves like an elastomer with low rigidity and high deformation to rupture in tendons8, orshows optical properties such as transparency incornea9. Another example is the arthropod cuticle,combining in different proportions chitin, proteinsand calcite crystals10 to give tissues that are rigid,flexible, opaque or translucent (Fig. 3a–c). Withinbiological organisms, identical organizationalprinciples to liquid-crystalline self-assemblieshave 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 (extracellularmatrix), and similar assemblies are now beingreproduced experimentally with purified biologicalmacromolecules11 (Figs 2c,d, 3d). In a non-selectivemanner, a recent approach of materials chemists has

been to organize mineral matter in vitro, by usingas templates more or less ordered phases of nucleicacids12, proteins13 and polysaccharides14.

The building of complex structures is promotedby specific links due to the three-dimensionalconformations of macromolecules, showingtopological variability and diversity. Efficientrecognition procedures occur in biology that imply stereospecific structures at the nanometre scale(antibodies, enzymes and so on). In fact, naturalmaterials are highly integrated systems having found acompromise between different properties or functions(such as mechanics, density, permeability, colourand hydrophobia, and so on), often being controlled

by a versatile system of sensor arrays15

. In many biosystems, such a high level of integration associatesthree aspects: miniaturization whose object is toaccommodate a maximum of elementary functionsin a small volume, hybridization between inorganicand organic components optimizing complementary possibilities and functions and hierarchy.

Indeed, hierarchical constructions on ascale ranging from nanometres, micrometres, tomillimetres are characteristic of biological structuresintroducing the capacity to answer the physicalor chemical demands occurring at these differentlevels16 (Figs 1–3). Such highly complex and aestheticstructures pass well beyond current accomplishmentsrealized in materials science, even if advances in

the field called ‘organized matter chemistry’17 showpromising man-made materials, as illustrated inmany publications of the past decade17–39. Key aspectsof these approaches are related to the controlledconstruction of textured organic–inorganicassemblies by direct or synergistic templating. Strikingexamples concern the synthesis of mesostructuredsilica in lipid helicoids40, the template-directed

synthesis of nanotubes using tobacco mosaic virusliquid crystals41, DNA-driven self-assembly of goldnanorods42, and the synthesis of linear chains of nanoparticles and nanofilament arrays in water andoil microemulsions43,44.

Should we then just be fascinated by whatnature proposes? Man has always made use of wood,cotton, silk, bone, horn or shells used as textiles,tools, weapons and ornaments. New and stricterrequirements are now being set up to achieve greaterharmony between the environment and humanactivities. New materials and systems producedby man must in future aim at higher levels of sophistication and miniaturization, be recyclable

and respect the environment, be reliable andconsume less energy. By elucidating the constructionrules of living organisms the possibility to createnew materials and systems will be offered. This fieldof research could obviously bring improved andeven higher-performing new materials. One strategy may be to ‘fish’ for interesting new materials incomplex mixtures and to understand the ‘languageof shape’ through the use of modern microscopy-based techniques. However, a real breakthroughrequires an understanding of the basic buildingprinciples of living organisms and a study of thechemical and physical properties at the interfaces, to control the form, size and compaction of objects.

This understanding is of paramount importance forthe efficient development of a ‘chemistry of form’in the laboratory 45. We believe that a biomimeticapproach to materials science cannot be limitedto the copy of objects proposed by nature, butrather a more global strategy, where the bestmultidisciplinary approaches must be efficiently expressed by the scientific commmunity throughthe creation of a new ‘Ecole de Pensée’ (think tank)1.The present review will summarize some of themain biomimetic or bionspired domains currently investigated in materials science. It will successively consider: supramolecular chemistry and hybridmaterials, polymeric materials, bioinspired materials

and biomaterials.

HIERARCHICAL ARCHITECTURES: FROM SUPRAMOLECULARCHEMISTRY TO HYBRID MATERIALS

Supramolecular chemistry, a fast-growing researchdomain, studies complex molecules and assemblies(molecular crystals, liposomes, micelles, bilayeredmembranes) resulting from the fine-tuning of intermolecular interactions46–51. Highly stereospecificprocesses exist in biology: substrate–receptorfixation, substrate–enzyme links, multiproteincomplexes, antigen–antibody immune responses,genetic code reading present in biologicalprocesses such as virus specific cell invasion,

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Figure 1 Silicic skeletons ofunicellular organisms. a,b,Radiolaria and c,d, diatomsshow complex and finelycarved morphologies inscanning electron microscopy

(SEM). a–c: Scale bar = 10 µm;d: Scale bar = 1 µm.Reproduced by permissionof 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 stimulateresearch, indeed synthetic catalytic systems already show properties close to natural ones such asrapidity and selectivity 50,51. Efficient catalysts havebeen created using cyclodextrines, cyclophanes orcalixarenes, chosen as subunits capable of specificmolecular recognition50,51. Studies on the principles

governing redox reactions will shed light on newartificial supramolecular devices, opening up ways of achieving more efficient and selective catalysts.

Molecular printing techniques offer newopportunities in affinity chromatography, catalysis,immunoanalysis and biosensors52. Antibodies andenzymes are the biomolecules currently used inanalytical chemistry or biochemistry to detect orquantify molecules specifically recognized by areceptor. Biomolecules are nevertheless expensive andtheir field of application often limited to restrictednatural conditions. A new approach is to create withina synthetic material, usually a polymer, prints of atarget molecule playing the role of a specific receptor.

Complementary functions, combining optimalconfigurations and restricted space, can then beadded. 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 itsability to combine at the nanoscale (bio)organic andinorganic components. Advances made by the ‘softchemistry’ community during the past ten years haveproduced, by carefully controlled organic–inorganicinterfaces, original hybrid materials with controlledporosity and/or texture20,54–56 (Fig. 4). Abundantsol–gel-derived hybrid materials resulting from softchemistry give easy-to-process materials offering

many advantages as tuneable physical properties,high photochemical and thermal stability, chemicalinertness and negligible swelling, both in aqueousand organic solvents.

Original hybrid materials with tuneable opticalattributes offering modulated properties have beendesigned during this past decade57, the following aresome examples. Hybrid materials, pH sensitive over awide range form silica-indicator tensioactive-colouredcomposites56–59. Photochromic materials, designedfrom spyro-oxazines embedded in hybrid matricesgiving very fast responses; the performance dependingon the tuning of dye–matrix interactions implying aperfect adjustment of the hydrophilic–hydrophobic

balance, rheo-mechanical properties and accessibility of the matrix60,61. Organically modified silicas withgrafted azoic push–pull chromophores that exhibitvery high second-order optical nonlinearity 62.

All the synthesis approaches described in thevastly expanding literature will, without any doubt,allow hybrid materials to be designed with enhancedmechanical, optical and electric properties56,63,64.Such materials are thus expected to find applicationsin smart devices, sensors, catalysis, separation andvectorization domains and so on. Another developingdomain concerns the design of hybrid architecturesformed from inorganic nanoparticles or inorganicgels and biomolecules65–71. Specific biosensorscomposed of enzymes immobilized in silica xerogels

have recently been produced72–76. Good preservationof the enzyme activity can be tested by optical or

electro-chemical methods. Biotechnologies already use enzymes and bacteria as synthetic tools77–79; theirfurther encapsulation in solid matrices should bringmodulated and enhanced biosynthetic properties. Theexploitation of hybrid materials in domains includingimmunology tests, encapsulation and/or vectorizationis currently being tested. Biologically programmedassemblies built from inorganic building blocks withintelligent organic function make an interestinginterface for materials science80–85. For example, smartassemblies of gold nanoparticles coupled by surface-absorbed antibodies such as streptavidin-bovine havebeen recently designed82,83, and original biohybridscombining nucleic acids and oxide nanoparticleshave 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 polarizedlight microscopy (PLM) between crossed polars (a). Scale bar = 10 µm. Collagen fibrils drawseries of nested arcs (noted by thick bars on the figure) in ultrathin sections of decalcified material(b). Transmission electron microscopy (TEM), Scale bar = 1 µm. c,d, Liquid-crystalline collagenassemblies. Fingerprint texture in acid-soluble collagen solution (c). PLM, Scale bar = 10 µm. Arcedpatterns drawn by collagen fibrils in sections of pH induced gelated cholesteric phases (d). TEM, Scalebar = 0.5 µm. Parts a, b, d reprinted from ref. 142. Copyright (2003), with permission from Elsevier.





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therapy 84. The exploitation of DNA for materialpurposes77 and the use of genetically engineeredproteins and organisms for inorganic growth shapeand self-assembly opens up new avenues for thedesign of original nanostructures84–88. Indeed, the fieldof bio-related materials is a huge reservoir of originaland complex morphologies.

One smart feature of natural materials concerns

their beautiful organization in which structure andfunction are optimized at different length scales.Recent data on polymeric materials, textured hybridsand meso-organized structures20 have led to newunderstanding of organic–organic or organic–mineralinterfaces22–39,89, allowing the controlled design of newmaterials with complex or hierarchical structures.Synthetic pathways currently investigated concern(i) transcription17, using pre-organized or self-assembled molecular or supramolecular mouldsof an organic (possibly biological90,91) or inorganicnature, used as templates to construct the materialby nanocasting92 and nanolithographic processes91;(ii) synergetic assembly 17,93, co-assembling molecular

precursors and molecular moulds in situ; (iii)morphosynthesis17, using chemical transformationsin confined geometries (microemulsions, micellesand vesicles94) to produce complex structures; and(iv) integrative synthesis17,95, which combines allthe previous methods to produce materials havingcomplex 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 orhybrid phases through surfactant self-assembly allowsmaterials to be designed with original hierarchicalstructures26,96–98. Recent examples concern thesynthesis and self-assembly of barium sulphate or

chromate nanoparticles as linear superstructures by hydrophobic-driven surface interactions in complexfluids45, emergent self-organization of calciumphosphate block-copolymer nested colloids and theformation of microporous calcium carbonate colloidin foams and emulsion droplets99.

The possibility of generating complex shapeswith unique molecules or macromonomers has

been demonstrated in the past few years. Indeed,organogelators can be used to form inorganic or evenhybrid fibres and helicoids20,21. Moreover, surfactantsform liquid crystals with topological defects that canserve as moulds to form silica materials with complexand original morphologies19,26,96 (Fig. 5). Finally,controlled phase separation induced by couplingpolypeptides and inorganic CeO2 nanoparticles in asolvent can also yield crystalline materials having bi-modal and hierarchical porosity 98 (Fig. 4c).

Major advances in the field concerningbioinspired (inorganic, organic or hybrid) materialshaving complex hierarchical structures are beingmade due to synergistic collaborations occurring

between the organic polymer and inorganicchemistry communities.

POLYMER SCIENCE, THE RICHNESS OF ‘ALI-BABA’S CAVE’

Polymer chemists can engineer large sets of macromolecules with controlled lengths and selectedaffinities100–106 (Fig. 6). Many amphiphilic blockcopolymers, for example, allow copolymer ceramic-composites to be constructed with original Im3m morphologies such as the Plumber’s nightmaredescribed by the Wiesner group103,104.

Double hydrophilic block copolymers are also anew class of amphiphilic macromolecules of rapidly

increasing importance. They are water-solublepolymers in which amphiphilicity can be inducedthrough the presence of a substrate or by temperatureand pH changes. Their chemical structure can betuned for a wide range of applications coveringsuch differing aspects as colloid stabilization, crystalgrowth modification, induced micelle formation andpolyelectrolyte complexing towards novel drug-carrier systems. In particular, mineralization processescan be controlled by using double hydrophilic blockcopolymers inspired by biology, which contain amolecular head reacting with the metal and acentral non-reactive part similar to proteinscontaining hydrophilic and mineralophilic sites107.

Such polymers help control the size, form, structureand assemblies of inorganic crystals. Indeed, originalsuperstructures have been obtained, as well as alignedhydroxyapatite whiskers or mineral crystals havingcomplex morphologies107–110.

Natural systems are also characterized by mobility,and again the field of polymer research offers many opportunities for designing materials responding toexternal stimuli. The synthesis of adaptative systems,as electro-active gels or artificial muscles is in fullexpansion with studies of their physico-chemicalproperties. Such materials respond to externalstimuli such as solvent, pH, light, electric field ortemperature111,112. Positive results already concernphotoactive systems and hydrogels with possible future

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Figure 3 Ordered organic andmineral networks in the crabcuticle and self-assembledstructures. a, Decalcifiedchitin–protein organic matrixshowing periodic extinctionbands in PLM between crossedpolars. Scale bar = 20 µm.

b, Chitin–protein fibrils lyingsuccessively parallel, obliqueor normal to the section plan,analogous to a cholestericgeometry. TEM, Scalebar = 1 µm. c, Calcite skeletonformed around the regularlytwisting organic fibrils. SEM,Scale bar = 0.2 µm.d, Liquid-crystalline assemblyof aqueous colloidalchitin suspensions. PLM,Scale bar = 100 µm (Belamie,private communication).

Parts a and c reprinted withpermission from ref. 143.





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medical applications in robotics. Materials mimickingthe 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 bemore versatile than the current robots combiningcomplex electric and metallic elements.

When producing complex hierarchical structures,the part played by templating (weak or strong linksbetween 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 processescould be coupled with the response of the material(mechanical deformation) that could spontaneously generate a propagating structure. Such systems offerspecific chemical sensibility applied to humid automats(intelligent ‘valves’, autonomous movement actuation)and controlled drug-delivery systems3.

There has also been new inputs frombiopolymers. These are currently being usedin the medical field but they can also provide

1 µm10 µm 100 nm

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Figure 4 Multiscale porousmaterials in vivo and in vitro.a, Cubic mesotextured TiO2 film obtained by evaporationinduced self-assembly usingblock copolymer (polyethyleneoxide–polypropyleneoxide–polyethylene oxide;

PEO-PPO-PEO) templates.TEM, Scale bar = 100 µm.Reprinted with permissionfrom ref. 144. Copyright (2003)

American Chemical Society.b, Porous silica exoskeletonobserved in diatoms.SEM, Scale bar = 10 µm.Reproduced by permissionof CNRS editions, NATURE×10.000, 1973. Copyright D.R(droits réservés). c, Imageof hybrid template-directedassembly by PBLG of CeO2

nanoparticles, the compositeshows macroporous CeO2 withmicroporous nanocrystallineinorganic walls. SEM, Scalebar = 10 µm. Reproduced bypermission of the Royal Societyof Chemistry from ref. 98. d–f, Micrographs at differentscales of hierarchically orderedporous silica. MEB (d,e), TEM(f). Images d–f reprintedwith permission from ref. 97.Copyright 1998 AAAS.





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original construction elements for designing newmaterials115–117. Amorphous domains in syntheticpolymers originate from chain intertwining whenrestricted mobility or structural defects preventthe emergence of ordered crystallized domains.The three-dimensional structure of proteinscombines both regular and random domains,

showing crystalline and amorphous regions inthe same material. The possibility of controlling,by alternating or mixing such sequences couldpossibly bring interesting properties to newly synthesized polymers. Polymer science is closely concerned with biomimetic approaches as it offersa wide range of materials with various behavioursthat can possibly mimic that of animals or plants.Materials proposed include homopolymers,copolymers, mixed polymers, charged or fibre-reinforced polymers, small platelets or multilayersand so on. In the near future, materials showinghigher elasticity, improved plastic deformationand fracture resistance should be obtained in the

near future by coupling synthetic methods andprocessing 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 applicationsin agriculture, medicine and the environment. Thisthermoplastic is indeed degradable in soils or seawaterby an enzyme, a PHB depolymerase, present inbacteria and fungi. A protein, bacteriorhodopsin, by combining three interesting effects (proton pump–charge separator and photochromic properties)offers many potentially interesting applicationssuch as seawater desalination, converting solarenergy into electricity or developing new DNA

chips. The protein acts as a molecular commutatoror sensor, stocking optical information andimproving imaging or holographic techniques78.Other polymers such as spider threads are strongly anisotropic with remarkable mechanical properties.Biotechnology companies are already trying toproduce one of its components, fibroin, by meansof cloned bacteria or transgenic goats. However,

even if the genetically synthesized fibroins fit theexpected chemical composition, a great deal of effortis still needed to shape them as fibres that reachthe targeted mechanical properties. This exampleillustrates a classical rule in materials science that ‘theperformance of a material depends not only on itsformulation but also on an optimized process’.

New polymers using nucleic acids, amino acidsor 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) havestarted118–120. A link was established between the global

morphology and hierarchy of the echinoderm skeletonand self-assembled liquid-crystalline structures formedby surfactants; this initiated studies of calcium carbonategrowth in the presence of proteins extracted from sea-urchin spines115. Microporous silica has been synthesizedin the presence of gelatine a low-cost biopolymer116,121.Biopolymers such as block polypeptides can be usedto produce silica with different shapes117. The chemicalprocesses involved must be related in some way tothose found in natural biosilicas where proteins such assilafins (proteins involved in silica formation in diatoms)and silicateines (proteins involved in silica formationin sponge spicules) serve as structuring agents andcatalysts122,123. On the other hand, silafins were recently

used as structuring agents to produce holographicnanopatterning of silica spheres124. Only a few studiesactually concern the control of the chemical constitutionof biomaterials by regulated programming prior totheir formation. Molecular cloning and characterizationof lustrin A, a matrix protein from the nacreous layerof mollusc shell, is obtained with multiple functionsassociated with the protein125.

Genetically modified organisms will thusproduce molecular assemblies of possible interestin the search for materials with interestingstructure-directing or catalytic properties79,86,88.Moreover, the influence of confinement onthe dynamics of macromolecules (natural and

synthetic) trapped in aggregates or inorganic orhybrid lattices (mesoporous or lamellar hosts,and so on) and on the mechanical properties of nanocomposites has not been sufficiently studied.The biomimetic aspects previously describedconcern mainly new materials resulting fromchemical or biochemical designs. However, if the final goal of biomimesis is to try and mimicbiological materials in the sense of producingindistinguishable copies, it can also reproducesome essential aspects of a natural materialwithout duplicating it all. Indeed at present,human knowledge in materials and associatedsciences is not sufficiently advanced to engineersuch highly complex duplications.

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Figure 5 Original texturesof synthetic hybrid inorganicmaterials.a,b, Functionalizedfibrous organosilica obtained inthe presence of organogelators(a, SEM, Scale bar = 5 µm) ortemplate (b, TEM, Scale bar

= 0.2 µm). Reproduced bypermission of the Royal Societyof Chemistry from ref. 145.c,d, SEM images of organisedhexagonal mesoporous silicawith complex morphologies,spirals or helicoidal fibres arisingfrom topological liquid-crystallinedefects. Scale bar = 1 µm. Partc reprinted with permissionfrom ref. 26, and part d fromref. 96. e, Barium sulphate(BaSO4) mineralized at pH 5 inthe presence of the double-

hydrophilic block copolymerPEO-block-PEI-SO3H. SEM,Bar = 20 µm. Reprinted withpermission from ref. 107.





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BIO- AND BIOINSPIRED MATERIALS WITHCONTROLLED PROPERTIES

Natural materials offer remarkable hydrodynamic,aerodynamic, wetting and adhesive properties.Beautiful examples are butterfly wings andchameleons. Obvious applications concernsurface coatings with anti-fouling, hydrophobic,protective or adhesive characteristics and alsocosmetic products. One way to take advantage

of the emerging field of biomimetics is to selectideas and inventive principles from nature andapply them to engineering products. Materialsreproducing structures described in animals andplants already exist. The study of the microstructureof lily leaves has inspired rugose super hydrophobicor hydrophillic coatings126 (Fig. 7). The structuralanalysis of shark or dolphin skin has produced‘riblets’, which are plastic films covered by microscopic grooves. Experimentally placed on

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Figure 6 Complexmorphologies attainablein triblock copolymers. Forexample, lamella (a), cylinder(b, c), sphere (d), ring (e),gyroid (l), and so on. Differentultrastructures are illustrated insections of triblock copolymers.

Reprinted with permissionfrom ref. 146. Copyright1999, American Institute ofPhysics. A, (corresponding toillustration c) Cylinders appearas spherical microdomainsbetween two distinctlamellar domains. TEM, scalebar = 0.5 µm. Reprinted in partwith permission from ref. 147.Copyright (1993) AmericanChemical Society.B, (corresponding to illustrationd) Spheres appear as spherical

microdomains between twodistinct lamellar domains. TEM,scale bar = 0.5 µm. Reprintedin part with permission fromref. 148. Copyright (1995)

American Chemical Society.C, (corresponding to diagrame) Rings around the cylindersare recognized as smallspherical microdomains. TEM,scale bar = 0.5 µm. Reprintedin part with permission fromref. 147. Copyright (1993)

American Chemical Society.

D, ‘Knitting pattern’ in triblock copolymers. TEM, scalebar = 0.5 µm. Reprinted in partwith permission from ref. 149.Copyright (1998) AmericanChemical Society.





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airplane wings they reduce the hydrodynamic trailand economize fuel15. A number of notable successesthat have been exploited in engineering disciplineshave been described, such as Nylon or Kevlar

inspired from natural silk or Velcro inspired by thehooked seeds of goosegrass127–129.The present overview on the interfaces

between materials science and biology will notbe complete without mentioning the researchon materials for implants or prostheses3. Theterm biomaterial includes all materials orsystems proposed for clinical applications toreplace part of a living system or to function inintimate contact with living tissues. Traditionalmaterials science researchers and engineers arestill poorly exploring this complex domain, asit requires consideration of biocompatibility,that is, acceptance of the artificial implant by the surrounding tissues. Tissue engineering

requires interdisciplinary approaches includingstrong biological knowledge, because designingimplants for tissue repair requires a thoroughunderstanding of the structure and function of theorgan 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 theimplanted materials, whether for hard or softtissues, need to be accepted by the surroundingbiological environment, to elicit specific cellularresponses130. In a physiological process, specificcells interact with the surrounding matrix andexercise adhesion, migration, proliferationand remodelling. For example, fibroblasts inskin and tendon or osteoblasts in bone showproperties controlled by interactions between cellsurface receptors (integrins) and specific matrixmolecules (collagen, fibronectin). Consequently,for material recognition by cells, surface or bulkmodifications of biomimetic materials have been

processed by chemical or physical methods to addbioactive molecules either in the form of nativelong chains or of short peptide sequences131. Insoft tissues such as dermis, tendons and bloodvessels, the concept is to use a resorbable templatethat guides tissue regeneration and is progressively degraded. The role of living cells, either implantedwithin the biomaterial or originating from thepatient’s organ, will be to promote new tissueformation and degrade the implanted material by specific proteases. In hard tissue replacements theclassical ‘bioinert’ concepts have also progressedby means of physico-chemical studies of biomineral interfaces with interest for ‘bioactive’

materials that stimulate tissue mineralization. Anexample is the Bioglass process, a composite of silicium, calcium and sodium oxides favouringapatite hydroxyl-carbonate crystallization, butalso contributing to the cell cycle implied intissue formation. Coral, exploited from naturalresources, or synthetic coral (Interpore process)are also used as implant materials. As humanlongevity increases, this domain becomeseconomically significant and a major challenge of the biology/material interface.

In many biomineralization processes theprogression of mineral domains takes place on amigration front line moving through the organic

matrix. New ceramics and composites manufacturedby stereolithography, multilayering, three-dimensionalprinting or laser-sintering allow similar processesto be adapted to the formation of films or bulkcomposite132. Growth by successive layer depositsoffers better control of the material’s resultingproperties. It allows sensors to be incorporatedand the possibility of non-destructive tests duringfabrication steps as a function of size, volume oraging. Biological systems involve constant controlsby using sets of diversified sensors, and therefore thedesign of high-technology materials should followthis path. In the long term even more possibilitiesexist: metal sintering, the moulding of thermoplasticmaterials, processing of multifunctional materials

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Figure 7 Natural andbioinspired superhydrophobiccoatings126. a, Lily leaf showinga rugose coating. SEM, scale

bar = 3 µm. b, Water dropleton the top of leaves fromthe South American plantSetcreasea. c, Industrial rugosesurface of silica. SEM, scalebar =1 µm. d, Water droplet onindustrial hydrophobic coatings.Parts c and d reprinted withpermission from ref. 126.





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and ceramic objects for domestic use or as evolvingimplants and biomaterials showing a betterbiocompatibility 132–134. These approaches would notonly allow three-dimensional innovative compositesto be created but also ‘smart’ materials such ascements or bio-cements controlled over time and withthe capacity for self-repair132–134.

PROMISING RESEARCH DEVELOPMENTS

An eclectic approach to designing andmanufacturing advanced materials necessarily includes biology, because a remarkable property of biological systems is their capacity to integratemolecular synthesis at very high levels of organization, structure and dynamics. Industrialtechnologies have already been inspired by dolphinskin, lily leaves and spider threads to producenew materials, but this research field is only at itsinfancy. Despite the efforts made this past decadeto elaborate bio-inspired materials, characterizetheir structural and physico-chemical properties,

understand their structure–function relationshipsand most of all their different formation steps,many unexplored mechanisms still remain to beinvestigated. In relation to the surfactant-templatedgrowth of nanostructured materials, the recentuse of microorganisms to control inorganic crystalformation has been promoted as genetically engineered polypeptides binding to selectedinorganics (GEPIs), such as silica135 or gold136.GEPIs are based on three fundamental principles:molecular recognition, self-assembly and DNAmanipulation, and they promise numerous successesin bio-directed technologies84,85.

Models describing the formation path of

mesostructured hybrid and inorganic materialshave been proposed during the past few years17,18,20. Even if they are still naive, theseapproaches, which favour understanding, seema priori more elegant than purely combinatory ones and must be encouraged. Indeed, morerational knowledge on the nature and structureof new materials obtained by various syntheticpathways will allow the construction of ‘tailor-made’ materials. These studies must also comparein vivo synthetic strategies of natural systems andin vitro realizations. Moreover, studies concerninga better knowledge of inorganic–organic interfacesare strongly needed including the identification

of molecular interaction types, evaluation of linkenergy and stability. The still poorly understoodrole of these hybrid interfaces on the modulationof optical, mechanical, catalytic and thermalproperties must be investigated in depth.

Several remarks arise from the currentproductions of bioinspired materials with hierarchicalstructures. Chemists usually consider that a perfectproduct is pure, homogeneous and exhibits constantparameters. The first synthesis of liquid crystals hasbeen a success of chemistry but in the search for puresubstances, these results have long been denied. Thismindset is still present nowadays and could hinderinteresting discoveries. Indeed, many interestingassemblies arise from complex mixtures and living

beings owe their existence to blind evolution resultingin complex associations.

The elaboration of materials using liquid-crystalline self-assemblies as templates requires preciseknowledge of their phase diagram in the presenceof the growing mineral components. Exploring theexistence of domains and subdomains of these hybridphases in situ during their formation and under

controlled chemical and processing parameters isessential for obtaining reproducible products137,138.

Complex biomineral structures found in natureprobably result from tailored combinations of several processes such as: self-assembly, controlledphase-separation and confinement in membrane-bounded compartments (controlling diffusion inand out of reagents), the use of topological defectsor dissipative structures as micromoulds, associatedwith external stimuli or fields. These externalstimuli can be produced during film formation by reagent evaporation, or obtained by continuous orsemi-continuous reactor synthesis with controlledflows, composition and temperature gradients,

magnetic or electric fields, or even by mechanical orultrasonic constraints. Only a few research groupsare currently tackling the question of assembly process in such ‘open systems’.

The role of molecular chirality is also littleinvestigated in current materials science studies,although it corresponds to the recognition,selection and construction paths assumed innatural systems. Clever use of chirality could bringnew possibilities21,139,140. Indeed, chirality in hybridliquid crystals, in surfactant organo–mineralorganized assemblies, nanobuilding blocks madeof organofunctional disymmetric clusters ornanoparticles 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, repairand destruction (recycling) are research domains thatmaterials scientists should consider further.

CONCLUSION

A biomimetic and bioinspired approach tomaterials is one of the most promising scientificand technological challenges of the coming years.Bioinspired materials and systems, adaptive

materials, nanomaterials, hierarchically structuredmaterials, three-dimensional composites, materialscompatible with ecological requirements, andso on, should become a major preoccupationin advanced technologies. Bioinspired selectivemultifunctional materials with associatedproperties (such as separation, adsorption, catalysis,sensing, biosensing, imaging, multitherapy) willappear in the near future.

An expanding need for biomimetic andbioinspired materials already exists as solutionsalways become limited with regard to new technical,economic or ecological evolutions and demands.The subject of biomimetism and materials is at thefrontier between biological and material sciences,





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chemistry and physics together with biotechnology and information techniques; it represents a majorinternational competitive sector of research for thisnew century. Even if these bio-inspired materialscannot be named ‘smart materials’ they will certainly be designed with intelligence.

DOI: 10.1038/nmat1339

References1. Bensaude-Vincent, B., Arribart, H., Bouligand, Y. & Sanchez, C. Chemists and

the school of nature. New J. Chem. 1, 1–5 (2002).

2. Mann, S. in Biomimetic Materials Chemistry (ed. Mann, S) 1–40 (Wiley-VCH,

Weinheim, 1997).

3. Biomimétisme et Matériaux Arago 25 (coord. Sanchez, C.) (OFTA, Paris, 2001).

4. Calvert, P. in Biomimetic Materials Chemistry (ed. Mann, S.) 315–336 (Wiley-

VCH, Weinheim, 1997).

5. Biomimetics: Design and Processing of Materials (eds. Sarikaya, M. & Aksay, I).

(AIP, Woodbury, Connecticut, 1995).

6. Bäuerlein, E. Biomineralization of unicellular organisms: an unusual

membrane biochemistry for the production of inorganic nano- and

microstructures. Angew. Chem. Int. Edn 42, 614–641 (2003).

7. Weiner, S. & Wagner, H. D. The materia l bone: structure-mechanical function

relations. Annu. Rev. Mater. Sci. 28, 271–298 (1998).

8. Evans, J. H. & Barbenel, J. C. Structural and mechanical properties of tendon

related to function. Equine Vet. J. 7, 1–8 (1975).

9. Meek, K. M. & Fullwood, N. J. Corneal and scleral collagens - a microscopist’s

perspective. Micron 32, 261–272 (2001).

10. Neville, A. C. Biology of the Arthropod Cuticle (ed. Farner, D. S.) (Springer,

Berlin, 1975)

11. Giraud-Guille, M. M. Twisted liquid cr ystalline supramolecular arrangements

in morphogenesis. Int. Rev. Cytol. 166, 59–101 (1996).

12. Peytcheva, A. & Antonietti, M. Carving on the nanoscale: Polymers for the

site-specific dissolution of calcium phosphate. Angew. Chem. Int. Edn 17,

3380–3383 (2001).

13. Sleytr, U. B., Schuster, B. & Pum, D. Nanotechnology and biomimetics with

2-D protein crystals. IEEE Eng. Med. Biol. Mag. 22, 140–50 (2003).

14. Kenichi, K., Kazushi, F., Junzo, S. & Kazunari, A. Hierarchical self-assembly

of hydrophobically modified pullulan in water: gelation by networks of

nanoparticles. Langmuir 18, 3780–3786 (2002).

15. Dittmar, A. & Delhomme, G. in Microsystèmes Arago 21 (ed. Masson, A.)

123–160 (OFTA, Paris, 1999).

16. Hierarchical Structures in Biology as a Guide for New Materials Technology

(coord. Tirrell, D. A.) 1–130 (National Material Advisory Board, The National

Academic press, Washington DC, 1994).

17. Mann, S. et al. Sol-gel synthesis of organized matter. Chem. Mater. 9, 2300–

2310 (1997).

18. Ozin, G. A. Panoscopic materials : synthesis over ‘all’ length scales. Chem.

Commun. 6, 419–432 (2000).

19. Mann, S. & Ozin, G. A. Synthesis of inorganic materials with complex form.

Nature 382, 313–318 (1996).

20. Soler-Illia, G. J. A. A., Sanchez, C., Lebeau, B. & Patarin, J. Chemical strategies

to design textured materials: from microporous and mesoporous oxides to

nanonetworks and hierarchical structures. Chem. Rev. 102, 4093–4138 (2002).

21. Van Bommel, K. J. C., Friggeri, A. & Shinkai, S. Organic templates for the

generation of inorganic materials. Angew. Chem. Int. Edn 42, 980–999 (2003).

22. Kresge, C. T., Leonowicz, M. E., Roth, W. J., Vartuli, J. C. & Beck, J. S. Ordered

mesoporous molecular sieves synthesized by a liquid-crystal template

mechanism. Nature 359, 710–712 (1992).

23. Monnier, A. et al. Cooperative formation of inorganic-organic interfaces in the

synthesis of silicate mesostructures. Science 261, 1299–1303 (1993).

24. Qisheng Huo, D. I. et al. Generalized synthesis of periodic surfactant/inorganic

composite materials. Nature 368, 317–321 (1994).

25. Bagshaw, S. A., Prouzet, E. & Pinnavaia, T. J. Templating of mesoporous

molecular sieves by nonionic polyethylene oxide surfactants. Science 269,

1242–1244 (1995).

26. Yang, H., Ozin, G. A. & Kresge, C. T. The role of defects in the formation of

mesoporous silica fibers, films, and curved shapes. Adv. Mater. 10,883–887 (1998).

27. Stupp, S. I. & Braun, P. V. Molecular manipulation of microstructures:

biomaterials, ceramics and semiconductors. Science 277, 1242–1248 (1999).

28. Braun, P. V., Osenar, P., Tohver, V., Kennedy, S. B. & Stupp, S. I. Nanostructure

templating in inorganic solids with organic lyotropic liquid crystals. J. Am.

Chem. Soc. 121, 7302–7309 (1999).

29. Göltner, C. G. & Antonietti, M. Mesoporous materials by templating of liquid

crystalline phase. Adv. Mater. 9, 431–436 (1997).

30. Schüth, F. Non-siliceous mesostructured and mesoporous materials. Chem.

Mater. 13, 3184–3195 (2001).

31. Sayari, A. & Liu, P. Non-silica periodic mesostructured materials: recent

progress. Micropor. Mater. 12, 149–177 (1997).

32. Sanchez, C. et al. Designed hybrid organic-inorganic nanocomposites from

functional nanobuilding blocks. Chem. Mater. 13, 3061–3083 (2001).

33. Stupp, S. I. et al. Supramolecular materials : self-organized nanostructures.

Science 1276, 384–389 (1997).

34. Ozin, G. A., Yang, H. & Coombs, N. Morphogenesis of shapes and surface

patterns in mesoporous silica. Nature 386, 692–695 (1997).

35. Tolbert, S. H., Firouzi, A., Stucky, G. D. & Chmelka, B. F. Magnetic field

alignment of ordered silicate-surfactant composites and mesoporous silica.

Science 278, 264–268 (1997).

36. Schmidt-Winkel, P., Yang, P., Margolese, D. I., Chmelka, B. F. & Stucky, G. D.

Fluoride-induced hierarchical ordering of mesoporous silica in aqueous acid-

syntheses. Adv. Mater . 11, 303–307 (1999).

37. Whitesides, G. M. & Ismagilov, R. F. Complexity in chemistry. Science 284, 89–92 (1999).

38.. Sellinger, A. et al. Continuous self-assembly of organic-inorganic

nanocomposite coatings that mimic nacre. Nature 394, 256–260 (1998).

39. Sanchez, C., Soler-Illia, G. J. A. A., Ribot, F. & Grosso, D. Design of functional

nano-structured materials through the use of controlled hybrid organic-

inorganic interfaces. C. R. Chimie 6, 1131–1151(2003).

40. Sedon, A. M. Patel, H. M., Burkett, S. L. & Mann, S. Chiral templating of silica-

lipid lamellar mesophase with helical tubular architecture. Angew . Chem. Int.

Edn 41, 2988–2991 (2002).

41. Shenton, W., Douglas, T., Young, M., Stubbs, G. & Mann S. Inorganic-organic

nanotube composites from template mineralization of tobacco mosaic virus.

Adv. Mater. 11, 253–256 (1999).

42. Li, M. & Mann, S. DNA-directed assembly of multifunctional nanoparticle

networks using metallic and bioinorganic building blocks. J. Mater. Chem. 14,

2260–2263 (2004).

43. Li, M., Schnablegger, H., & Mann, S. Coupled synthesis and self-assembly of

nanoparticles to give structures with controlled organization Nature 402, 393–395 (1999).

44. Li, M., Lebeau, B. & Mann, S. Synthesis of aragonite nanofilament networks by

mesoscale self-assembly and transformation in reverse microemulsions.Adv.

Mater. 15, 2032–2035 (2003).

45. Mann, S. The chemistry of form. Angew. Chem. Int. Edn 39, 3392–3406 (2000).

46. Lehn, J. M. Cryptates: inclusion complexes of macropolyciclic receptor

molecules. Pure Appl. Chem. 50, 871–892 (1978).

47. Lehn, J. M. Supramolecular Chemistry: concepts and perspectives (Wiley-VCH,

Weinheim, 1995).

48. Lehn, J. M. in Biomimetic Chemistry (eds Yoshida, Z. I. & Kodansha, N. I.)

(Elsevier, Amsterdam, 1983).

49. Lehn, J. M. Supramolecular chemistry: from molecular information

towards self-organization and complex matter. Rep. Prog. Phys. 67,

249–265 (2004).

50. Breslow, R. & Dong, S. D. Biomimetic reactions catalyzed by cyclodextrins and

their derivatives. Chem. Rev. 98, 1997–2011 (1998).

51. Vigneron, J. P. in Biomimétisme et Matériaux Arago 25 (coord. Sanchez, C.)

343–361 (OFTA, Paris, 2001).

52. Haupt, K. & Mosbach, K. Molecularly imprinted polymers and their use inbiomimetic sensors. Chem. Rev . 100, 2495–2504 (2000).

53. Haupt, K. & Fradet, A. in Biomimétisme et Matériaux Arago 25 (coord.

Sanchez, C.) 363–377 (OFTA, Paris 2001).

54. Livage, L. Henry, M. & Sanchez, C. Sol-gel chemistry of transition metal

oxides. Prog. Solid State Chem. 18, 259–342 (1988).

55. Brinker, C. J. & Scherrer, G. W. The Physics and Chemistry of Sol-Gel Processing

(Academic, San Diego, 1990).

56. Functional Hybrid Materials (eds. Gómez-Romero, P. & Sanchez, C.) (Wiley-

VCH, Weinheim, 2003).

57. Sanchez, C., Lebeau,B., Boilot, J. P. & Chaput, F. Optical properties of

functional hybrid organic-inorganic nanocomposites. Adv. Mater. 15,

1969–1976 (2003).

58. Rottman, C. & Avnir, D. Getting a library of activities from a single compound:

tunability and very large shifts in Acidity constants induced by sol-gel

entrapped micelles. J. Am. Chem. Soc. 123, 5730–5734 (2001).

59. Rottman, C., Grader, G., De Hazan, Y., Melchior, S. & Avnir , D. Surfactant-

induced modifictaion of dopants reactivity in sol-gel matrixes. J. Am. Chem.

Soc. 121, 8533–8543 (1999).60. Schaudel, B., Guermeur, C., Sanchez, C. Nakatani, K. & Delaire, B.

Spirooxazine- and spiropyran-doped hybrid organic-inorganic matrices with

very fast photochromic responses. J. Mater. Chem. 7, 61–65 (1997).

61. Ribot, F., Lafuma, A., Eychenne-Baron, C. & Sanchez, C. New photochromic

hybrid organic-inorganic materials built from well-defined nano-building

blocks. Adv. Mater. 14, 1496–1499 (2002).

62. Lebeau, B., Brasselet, S., Zyss, J. & Sanchez, C. Des ign, characterization, and

processing of hybrid organic-inorganic coatings with very hig h second-order

optical nonlinearities. Chem. Mater. 9, 1012–1020 (1997).

63. Nanostructured and functional materials. Chem. Mater. 13, 3059–3809 (2001).

64. Hybrid organic-inorganic materials. Mater. Res. Soc. Bull. 26, (2001).

65. Niemeyer, C. F., Buelent Ceyhan, Noyong, M. & Simon, U. Bifunctional DNA-

gold nanoparticle conjugates as building blocks for the self-assembly of cross-

linked paricle layers. Biochem. Biophys. Res. Commun. 311, 995–999 (2003).

66. Seeman, N. C. DNA in a material world. Nature 421, 427–431 (2003).

67. Mei, Li & Mann, S. DNA-directed assembly of multifunctional nanoparticle

networks using metallic and bioorganic building blocks. J. Mater. Chem. 14,

2260–2263 (2004).





REVIEW ARTICLE

68. Jin, R., Wu, G., Li, Z., Mirkin, C. A. & Schatz, G. C. What controls the melting

properties of D NA-linked gold nanoparticle assemblies? J. Amer. Chem. Soc.

125, 1643–1654 (2003).

69. Nagle, L., Ryan, D., Cobbe, S. & Fitzmaurice, D. Templated nanoparticle

assembly on the surface of a patterned nanosphere.Nano Lett. 3, 51–53 (2003).

70. Iacopino, D., Ongaro, A., Nagle, L., Eritja, R. & Fitzmaurice, D. Imaging the

DNA and nanoparticle components of a self-assembled nanoscale architecture.

Nanotechnology 14, 447–452 (2003).

71. Hartgerink, J. D., Beniash, E. & Stupp, S. I. Self-assembly and mineralization of

peptide-amphiphile nanofibers. Science 294, 1684–1688 (2001).

72. Avnir, D., Braun, S., Lev, O. & Ottolenghi, M. Enzymes and other proteinsentrapped in sol-gel materials. Chem. Mater. 6, 1605–1614 (1994).

73. Livage, J. Bioactivity in sol-gel glasses C. R. Acad. Sci. Paris 322, 417–427

(1996).

74. Livage, J., Coradin, T. & Roux, C. in Functional Hybrid Materials, Bioactive sol

gel hybrids (eds Gómez-Romero, P. & Sanchez, C.) Ch. 11, 387–401 (Wiley-

VCH. Weinheim, 2003).

75. Livage, J., Coradin, T. & Roux, C. Encapsulation of biomolecules in silica gels.

J. Phys. Condens. Matter 13, R673–R691 (2001).

76. Nassif, N. et al. Living bacteria in silica gels. Nature Mater. 1, 42–44 (2002).

77. Alper, M. Biology and materials. Synthesis part I. Mat. Res. Soc. Bull. 17, 24–25

(1992).

78. Alper, M. Biology and Materials. Synthesis part II Mater. Res. Soc. Bull. 17,

36–37 (1992).

79. Gill, I. Bio-doped nanocomposite polymers: sol-gel bioencapsulates. Chem.

Mater. 13, 3404–3421 (2001).

80. Mornet, S. et al. DNA-magnetite nanocomposite materials. Mater. Lett. 42,

183–188 (2000).

81. Mann, S., Shenton, W., Li, M., Connolly, S. & Fitzmaurice, D. Biologically programmed nanoparticle assembly. Adv. Mater. 12, 147–150 (2000).

82. Connolly, S. & Fitzmaurice, D. Programmed assembly of gold nanocrystals in

aqueous solution. Adv. Mater. 11, 1202–1205 (1999).

83. Shenton, W., Davis, S. A. & Mann, S. Directed self-assembly of nanoparticles

into macroscopic materials using antibody-antigen recognition. Adv. Mater.

11,449–452 (1999).

84. Mirkin, C. A. Programming the assembly of two- and three-dimensional

architectures with DNA and nanoscale inorganic building blocks. Inorg. Chem.

39, 2258–2272 (2000).

85. Sarikaya, M., Tamerler, C., Jen, A. K.-Y., Schulten, K. & Baneyx, F. Molecular

biomimetics: nanotechnology through biology. Nature Mater. 2, 577–585

(2003).

86. Gillitzer, E., Willits, D., Young, M. & Douglas, T. Chemical modification of a

viral cage for multivalent presentation. Chem. Comm. 2390–2391 (2002).

87. Flynn, C. E., Lee, S. W. Peele, B. R. & Belcher, A. M. Viruses as vehicles for

growth, organization and assembly of materials. Acta Mater. 51, 5867–5880

(2003).

88. Wang, O., Lin, T., Tang, L., Johnson, J. E. & Finn, M. G. Icosahedral virusparticles as addressable nanoscale building blocks. Angew. Chem. Int. Edn 41,

459–462 (2002).

89. Antoniettti, M. Self-organization of functional polymers. Nature Mater. 2,

9–10 (2002).

90. Ha Y. H. et al. Three-dimensional network photonic crystals via cyclic size

reduction/infiltration of sea urchin exoskeleton. Adv. Mater. 16, 1091–1094

(2004).

91. Sundar, V. C., Yablon, A. D., Grazul, J. L., Ilan, M. & Aizenberg, J. Fibre-optical

features of a glass sponge. Nature 424, 899–900 (2003).

92. Zhou, Y. & Antonietti, M. A series of highly ordered super-microporous,

lamellar silicas prepared by nanocasting with ionic liquids. Chem. Mater. 16,

544–550 (2004).

93. Volkmer, D., Tugulu, S., Fricke, M. & Nielsen, T. Morphosynthesis of star-

shaped titania-silica shells. Angew. Chem. Int. Edn 42, 58–61 (2003).

94. Richardi, J., Motte, L. & Pileni, M. P. Mesoscopic organisations of magnetic

nanocrystals: the influence of short-range interactions. Curr. Opin. Colloid

Interface Sci. 9, 185–191 (2004).

95. Busch, S., Schwarz, U. & Kniep, R. Morphogenesis and structure of humanteeth in relation to biomimetically grown fluorapatite-gelatine composites.

Chem. Mater. 13, 3260–3271 (2001).

96. Yang, S. M., Sokolov, I., Coombs, N., Kresge, C. T. & Ozin, G. A. Formation of

hollow helicoids in mesoporous silica: supramolecular origami. Adv. Mater .

11, 1427–1431 (1999).

97. Yang, P. et al. Hierarchically ordered oxides. Science 282, 2244–2246 (1998).

98. Bouchara, A., Soler Illia, G. J. A. A., Chane-Ching, J. Y. & Sanchez, C.

Nanotectonic approach of the texturation of Ce202 based nanomaterials. Chem.

Comm. 1234–1235 (2002).

99. Li, M. & Mann, S. Emergent nanostructures: water induced mesoscale

transformation of surfactant stabilized amorphous calcium carbonate

nanoparticles in reverse microemulsions. Adv. Funct. Mater. 12,773–779 (2002).

100. Förster, S. & Antonietti, M. Amphiphilic block copolymers in structure

controlled nanomaterial hybrids. Adv. Mater. 10, 195–217 (1998).

101. Förster S. & Plantenberg, T. From self-organizing polymers to nanohybrid

and biomaterials. Angew. Chem. Int. Edn 41, 689–714 (2002).

102. Hamley, I. W. Nanotechnology with soft materials. Angew. Chem. Int. Edn 42,

1692–1712 (2003).

103. Finnefrock, A. C., Ulrich, R., Toombes, G. E.S, Gruner, S. M. & Wiesner , U.

The Plumber’s nightmare: A new morphology in block copolymer-ceramic

nanocomposites and mesoporous aluminosilicates. J. Am. Chem. Soc. 125,

13084–13093 (2003).

104. Simon, P. F. W., Ulrich, R., Spiess, H. W. & Wiesner, U. Block copolymer-

ceramic hybrid materials from organically modified ceramic precursors Chem.

Mater. 13, 3464–3486 (2001).

105. Thomas, A., Schlaad, H. & Antonietti, M. Replication of lyotropic block

copolymer mesophases into porous silica by nanocasting: learning about finer

details of polymer self assembly.Langmuir 19, 4455–4459 (2003).

106. Faul, C. F., Antonietti, M., Hentze, H. P. & Smarsly, B. Solid statenanostructure of PAMAM dendrimer-fluorosurfactant complexes and

nanoparticles synthesis within the ionic subphase. Colloid. Surf. 212, 115–131

(2003).

107. Cölfen, H. Double hydrophilic block copolymers: Synthesis and application

as novel surfactants and crystal growth modifiers. Macromol. Rapid. Commun.

22, 219–252 (2001).

108. Yu, S. H. & Cölfen, H. Bio-inspired crystal morphogenesis by hydrophilic

polymers. J. Mater. Chem. 14 (special issue on new developments on biorelated

materials), 2124–2147 (2004).

109. Li, M., Cölfen, H. & Mann, S. Morphological control of BaSO4

microstructures by double hydrophilic block copolymer mixtures. J. Mater.

Chem. 14 (special issue on new developments on biorelated materials),

2269–2276 (2004).

110. Yunfeng Lu, A. et al. Self-assembly of mesoscopically ordered chromatic

polydiacetylene/silica composites. Nature 410, 913–917 (2001).

111. Osada, Y. & Matsuda, A. Shape memory in hydrogels. Nature , 376, 219–220

(1995).

112. Ueoka, Y., Gong, J. & Osada, Y. Chemomechanical polymer gel with fish-likemotion. J. Intelligent Mater. Syst. and Struct . 8, 465–471 (1997).

111. Auroy, P. in Biomimétisme et Matériaux Arago 25 (coord. Sanchez, C.)

457–459 (OFTA, Paris, 2001).

114. Smela, E., Inganas, O. & Lundstrom, I. Conducting polymers as artificial muscles:

challenges and possibilities. J. Micromech. Microeng. 3, 203–205 (1993).

115. McGrath, K. M. Probing material formation in the presence of organic and

biological molecules. Adv. Mater. 13, 989–992 (2001).

116. Jia, J., Zhou, X., Caruso, R. A. & Antonietti, M. Synthesis of microporous

silica templated by gelatin. Chem. Lett. 33, 202–203 (2004).

117. Cha, J. N., Stucky, G. D., Morse, D. E. & Deming, T. J. Biomimetic synthesis

of ordered silica structures mediated by block copolypeptides. Nature 403,

289–292 (2000).

118. Vauthey, S., Santoso, S., Haiyan Gong, Watson, N. & Zhang, S. Molecular self-

assembly of surfactant-like peptides to form nanotubes and nanovesicles.Proc.

Natl Acad. Sci. 99, 5355–5360 (2002).

119. Fogleman, E. A., Yount, W. C., Xu, J. & Craig, S. L. Modular, well-behaved

reversible polymers from DNA based monomers. Angew. Chem. Int. Edn 41,

4026–4028 (2002).120. Hartgerink, J. D., Beniash, E. & Stupp, S. I. Self-assembly and mineralization

of peptide-amphiphile nanofibers. Science 294, 1684–1688 (2001).

121. Faul, C. F. J. & Antonietti, M. Ionic self-assembly: facile synthesis of

supramolecular materials. Adv. Mater. 15, 673–683 (2003).

122. Shimizu, K., Cha, J. N., Stucky, G. D. & Morse, D. E. Silicatein & alpha

Cathepsin L-like protein in sponge biosilica. Proc. Natl Acad. Sci. USA. 95,

6234–6238 (1998).

123. Cha, J. N. et al. Silicatein filaments and subunits from a marine sponge direct

the polymerization of silica and silicones in vitro. Proc. Natl Acad. Sci. USA 96,

361–365 (1999).

124. Brott, L. L. et al. Ultrafast holographic nanopatterning of biocatalytically

formed silica. Nature 413, 291–293 (2001).

125. Shen, X., Belcher, A., Hansma, P. K., Stucky, G. D. & Morse, D. E. Molecular

cloning and characterisation of Lustrin A, a matrix protein from shell and

pearl nacre of Haliotis rufescens. J. Biol. Chem. 272, 32472–32481 (1997).

126. Bico, J., Marzolin, C. & Quéré, D. Pearl drops. Europhysics Letters 47, 220–226

(1999).

127. Vincent, J. in Biomimétisme et Matériaux Arago 25 (coord. Sanchez, C.)313–324 (OFTA, Paris, 2001).

128. Vincent, J. Structural Biomaterials (Princeton Univ. Press, USA, 1990).

129. Simmons, A. H., Michal, C. A. & Jelinski, L. W. Molecular orientation and

two-component nature of the crystalline fraction of spider dragline silk.

Science 271, 84–87 (1996).

130. Shin, H., Jo, S. & Mikos, A. G. Biomimetic materials for tissue engineering.

Biomater, 24, 4353–4364 (2003).

131. Li, S. T. in Biomaterials Principles and Applications (eds Park, J. B. & Bronzino,

J. D.) Ch. 6, 117–139 (CRC press, New York, 2003).

132. Calvert, P. in Biomimétisme et Matériaux Arago 25 (coord. Sanchez, C.)

299–312 (OFTA, Paris, 2001).

133. Calvert, P. in Materials Science and Technology Vol. 17 (ed. Brook, R. J.) 51–82

(VCH,Wienheim, 1996).

134. Calvert, P. & Crockett, R. Chemical solid free-form fabrication : making

shapes without molds. Chem. Mater. 9, 650–663 (1997).

135. Naik, R. J., Brott, L. L., Clarson, S. J. & Stone, M. O. Silica-precipitating

peptides isolated from a combinatorial phage display peptide library.

J. Nanosci. Nanotechnol. 2, 95–100 (2002).





REVIEW ARTICLE

136. Braun, R., Sarikaya, M. & Schulten, K. Genetically engineered gold-binding

polypeptides: Structure prediction and molecular dynamics. J. Biomat. Sci. 13,

747–757 (2002).

137. Cagnol, F. et al. Humidity-controlled mesostructuration in CTAB-templated

silica thin film processing. The existence of a modulable steady state. J. Mater.

Chem. 13, 61–66 (2002).

138. Grosso, D. et al. Fundamentals of mesostructuring through evaporation-

induced self-assembly. Adv. Funct. Mater. 14, 309–322 (2004).

139. Orme, C. A. et al. Formation of chiral morphologies through selective

binding of amino acids to calcite surface steps. Nature 411, 775–779 (2001).

140. Petit, L., Sellière, E., Duguet, E., Ravaine, S. & Mingotaud, C. Diss ymmetricsilica nanospheres: a first step to difunctionalized nanomaterials J. Mater.

Chem. 10, 253–254 (2000).

141. Reculusa, S., Mingotaud, C., Duguet, E. & Ravaine, S. in The Dekker Encyclopedia

of Nanoscience and Nanotechnology (ed. Dekker, M.) 943–953 (in the press).

142. Giraud-Guille, M. M., Besseau, L. & Martin, R. Liquid crystalline assemblies

of collagen in bone and in vitro systems. J. Biomech. 36, 1571–1579 (2003).

143. Giraud-Guille, M. M. Liquid crystalline order of biopolymers in cuticles and

bones. Microsc. Res. Technol . 27, 420–428 (1994).

144. Crepaldi, E. L. et al. Controlled formation of highly organized mesoporous

titania thin films: From mesostructured hybrids to mesoporous nanoanatase

TiO2. J. Am. Chem. Soc. 125, 9770–9786 (2003).

145. Llusar, M., Monros, G., Roux, C., Pozzo, L. J. & Sanchez, C. One-pot

synthesis of phenyl- and amine-functionalized silica fibers through the use of

anthracenic and phenazinic organogelators. J. Mater. Chem. 13, 2505–2514

(2003).

146. Bates, F. S. & Fredrickson, G. H. Block copolymers-designer soft materials.

Phys. Today 52, 32–38 (1999).

147. Auschra, C. & Stadler, R. New ordered morphologies in ABC triblock

copolymers. Macromolecules 26, 2171–2174 (1993).

148. Stadler, R. et al. Morphology and thermodynamics of symmetric poly(A-

block-B-block-C) triblock copolymers. Macromolecules.28, 3080–3097 (1995).

149. Breiner, U., Krappe, U., Thomas, E. L. & Stadler, R. Structuralcharacterization of the „knitting pattern“ in polysty rene-block-poly(ethylene-

co-butylene)-block-poly(methyl methacrylate) triblock copolymers.

Macromolecules 31, 135–141 (1998).

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 financial interestsThe authors declare that they have no competing financial interests.

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