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 nature materials | VOL 4 | APRIL 2005 | www.nature.com/naturematerials 277 © 2005 Nature Publishing Group nnmat1339-print.inddmat1339-print.indd 227777 111/3/051/3/05 110:08:010:08:01 aamm REVIEW ARTICLE 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, 278 nature materials | VOL 4 | APRIL 2005 | www.nature.com/naturematerials © 2005 Nature Publishing