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Mineralized tissues

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1251: 105:. The remarkable structural organization and engineering properties makes these tissues desirable candidates for duplication by artificial means. Mineralized tissues inspire miniaturization, adaptability and multifunctionality. While natural materials are made up of a limited number of components, a larger variety of material chemistries can be used to simulate the same properties in engineering applications. However, the success of biomimetics lies in fully grasping the performance and mechanics of these biological hard tissues before swapping the natural components with artificial materials for engineering design. 161: 846: 743: 20: 1476:
unavailable. For nacre, the role of some nanograins and mineral bridges requires further studies to be fully defined. Successful biomimicking of mollusk shells will depend will on gaining further knowledge of all these factors, especially the selection of influential materials in the performance of mineralized tissues. Also the final technique used for artificial reproduction must be both cost effective and scalable industrially.
1363:, which expel the ceramic particles as they grow. After sublimation of the water, this results in a layered homogeneous ceramic scaffold that, architecturally, is a negative replica of the ice. The scaffold can then be filled with a second soft phase so as to create a hard–soft layered composite. This strategy is also widely applied to build other kinds of bioinspired materials, like extremely strong and tough 1130:, which then grow to occupy the maximum space available there. The mechanisms of mineral deposition within the organic portion of the bone are still under investigation. Three possible suggestions are that nucleation is either due to the precipitation of calcium phosphate solution, caused by the removal of biological inhibitors or occurs because of the interaction of calcium-binding proteins. 125:
the tissue. Due to this layering, loads and stresses are transferred throughout several length-scales, from macro to micro to nano, which results in the dissipation of energy within the arrangement. These scales or hierarchical structures are therefore able to distribute damage and resist cracking. Two types of biological tissues have been the target of extensive investigation, namely
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material that plays this role. Even though these tablets are usually illustrated as flat sheets, different microscopy techniques have shown that they are wavy in nature with amplitudes as large as half of the tablet's thickness. This waviness plays an important role in the fracture of nacre as it will progressively lock the tablets when they are pulled apart and induce hardening.
902:), and weaker strands inside nacre represent three hierarchical structures. On the microscale, the stacked tablet layers and the wavy interface between them are two other hierarchical structures. Lastly, on the nanoscale, the connecting organic material between the tablets as well as the grains from which they are made of is the final sixth hierarchical structure in nacre. 1367:, metal/ceramic, and polymer/ceramic hybrid biomimetic materials with fine lamellar or brick-and-mortar architectures. The "brick" layer is extremely strong but brittle and the soft "mortar" layer between the bricks generates limited deformation, thereby allowing for the relief of locally high stresses while also providing 865:, and it occupies 95% vol. Nacre is 3000 times tougher than aragonite and this has to do with the other component in nacre, the one that takes up 5% vol., which is the softer organic biopolymers. Furthermore, the nacreous layer also contains some strands of weaker material called growth lines that can deflect cracks. 133:
and atomic force microscopy are used to characterize these tissues. Although the degree of efficiency of biological hard tissues are yet unmatched by any man-made ceramic composites, some promising new techniques to synthesize them are currently under development. Not all mineralized tissues develop
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There are also two hierarchical structures on the nanoscale. The first being the structure inside the ultrastructure that are fibrils and extrafibrillar space, at a scale of several hundred nanometres. The second are the elementary components of mineralized tissues at a scale of tens of nanometres.
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and some other proteins. The hierarchical structural of bone spans across to a three tiered hierarchy of the collagen molecule itself. Different sources report different numbers of hierarchical level in bone, which is a complex biological material. The types of mechanisms that operate at different
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scales are used to imitate these week interfaces with layered composite ceramic tablets that are held together by weak interface “glue”. Hence, these large scale models can overcome the brittleness of ceramics. Since other mechanisms like tablet locking and damage spreading also play a role in the
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provides an additional toughening mechanism. Such a common strategy was perfected by nature itself over millions of years of evolution, giving us the inspiration for building the next generation of structural materials. There are several techniques used to mimic these tissues. Some of the current
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Understanding the formation of biological tissues is inevitable in order to properly reconstruct them artificially. Even if questions remain in some aspects and the mechanism of mineralization of many mineralized tissues need yet to be determined, there are some ideas about those of mollusc shell,
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The Microscale can be imagined by a three-dimensional brick and mortar wall. The bricks would be 0.5 μm thick layers of microscopic aragonite polygonal tablets approximately 5-8 μm in diameter. What holds the bricks together are the mortars and in the case of nacre, it is the 20-30 nm organic
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Hierarchical structures are distinct features seen throughout different length scales. To understand how the hierarchical structure of mineralized tissues contributes to their remarkable properties, those for nacre and bone are described below. Hierarchical structures are characteristic of biology
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present in teeth and bones. Although one might think that the mineral content of these tissues can make them fragile, studies have shown that mineralized tissues are 1,000 to 10,000 times tougher than the minerals they contain. The secret to this underlying strength is in the organized layering of
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occurs on a synthetic surface with some success. The technique occurs at low temperature and in an aqueous environment. Self-assembling films form templates that effect the nucleation of ceramic phases. The downside with this technique is its inability to form a segmented layered microstructure.
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Segmentation is an important property of nacre used for crack deflection of the ceramic phase without fracturing it. As a consequence, this technique does not mimic microstructural characteristics of nacre beyond the layered organic/inorganic layered structure and requires further investigation.
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in order to understand its alteration with aging. These alterations lead to “transparent” dentin, which is also called sclerotic. It was shown that a ‘‘dissolution and reprecipitation’’ mechanism reigns the formation of transparent dentin. The causes and cures of these conditions can possibly be
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process - dedicated cells deposit minerals to a soft polymeric (protein) matrix to strengthen, harden and/or stiffen it. Thus, biomimetic mineralization is an obvious and effective process for building synthetic materials with superior mechanical properties. The general strategy is started with
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The various studies have increased progress towards understanding mineralized tissues. However, it is still unclear which micro/nanostructural features are essential to the material performance of these tissues. Also constitutive laws along various loading paths of the materials are currently
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encompasses a family of technologies that draw on computer designs to build structures layer by layer. Recently, a lot of bioinspired materials with elegant hierarchical motifs have been built with features ranging in size from tens of micrometers to one submicrometer. Therefore, the
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Layer-by-layer deposition is a technique that as suggested by its name consists of a layer-by-layer assembly to make multilayered composites like nacre. Some examples of efforts in this direction include alternating layers of hard and soft components of TiN/Pt with an
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Fantner G.E.; Hassenkam T.; Kindt J.H.; Weaver J.C.; Birkedal H.; Pechenik L.; Cutroni J.A.; Cidade G.A.G.; Stucky G.D.; Morse D.E. & P.K. Hansma (2005). "Sacrificial bonds and hidden length dissipate energy as mineralized fibrils separate during bone fracture".
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These tissues have been finely tuned to enhance their mechanical capabilities over millions of years of evolution. Thus, mineralized tissues have been the subject of many studies since there is a lot to learn from nature as seen from the growing field of
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The organic part of mineralized tissues is made of proteins. In bone for example, the organic layer is the protein collagen. The degree of mineral in mineralized tissues varies and the organic component occupies a smaller volume as tissue
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The mineral-protein interface with its underlying adhesion forces is involved in the toughening properties of mineralized tissues. The interaction in the organic-inorganic interface is important to understand these toughening properties.
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of the whole structure. However, the time-consuming of manufacturing the hierarchical mechanical materials, especially on the nano- and micro-scale limited the further application of this technique in large-scale manufacturing.
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Density-Dependent Colour Scanning Electron Micrograph SEM (DDC-SEM) of cardiovascular calcification, showing in orange calcium phosphate spherical particles (denser material) and, in green, the extracellular matrix (less dense
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Porter, A.; Nalla, R.; Minor, A.; Jinschek, J.; Kisielowski, C.; Radmilovic, V.; Kinney, J.; Tomsia, A.; Ritchie, R. (2005). "A transmission electron microscopy study of mineralization in age-induced transparent dentin".
1450:. There are three films deposited consecutively. Although the MEMS technology is expensive and more time-consuming, there is a high degree of control over the morphology and large numbers of specimens can be made. 1288:) are lightweight, strong, flexible, tough, fracture-resistant, and self-repair. The general underlying mechanism behind such advanced materials is that the highly oriented stiff components give the materials great 992:, and monosodium urate are examples of minerals found in biological tissues. In mollusc shells, these minerals are carried to the site of mineralization in vesicles within specialized cells. Although they are in an 886:
grains detected by scanning electron microscopy from which the tablets themselves are made of together represent another structural level. The organic material “gluing” the tablets together is made of proteins and
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made by this sequential deposition technique do not have a segmented layered microstructure. Thus, sequential adsorption has been proposed to overcome this limitation and consists of repeatedly adsorbing
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The evolution of mineralized tissues has been puzzling for more than a century. It has been hypothesized that the first mechanism of animal tissue mineralization began either in the oral skeleton of
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organic scaffolds with ion-binding sites that promote heterogeneous nucleation. Then localized mineralization can be achieved by controlled ion supersaturation on these ion-binding sites. In such a
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are used to provide information on the type of mineral phase and changes in mineral and matrix composition involved in the disease. Also, clastic cells are cells that cause mineralized tissue
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or inhibition of hydroxyapatite formation. For example, the organic component in nacre is known to restrict the growth of aragonite. Some of the regulatory proteins in mineralized tissues are
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Belcherab A.M.; Hansmad P.K.; Stuckyac G.D. & D.E. Morsebe (1998). "First steps in harnessing the potential of biomineralization as a route to new high-performance composite materials".
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Some mollusc shells protect themselves from predators by using a two layered system, one of which is nacre. Nacre constitutes the inner layer while the other, outer, layer is made from
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through normal physiologic processes and are beneficial to the organism. For example, kidney stones contain mineralized tissues that are developed through pathologic processes. Hence,
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molecules, organic molecules such as lipids and proteins, and finally water. The hierarchical structure common to all mineralized tissues is the key to their mechanical performance.
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and basal bone, which is sometimes overlaid by enameloid. It is thought that the dermal skeleton eventually became scales, which are homologous to teeth. Teeth were first seen in
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and were made from all three components of the dermal skeleton, namely dentin, basal bone and enameloid. The mineralization mechanism of mammalian tissue was later elaborated in
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and small struts can be distinguished. The second hierarchical structure, the ultrastructure, at a scale of 5 to 10 μm, is the actual structure of the osteons and small struts.
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Fratzl, P.; Fratzl-Zelman, N.; Klaushofer, K.; Vogl, G.; Koller, K. (1991). "Nucleation and growth of mineral crystals in bone studied by small-angle X-ray scattering".
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Espinosa, H. D.; Rim, J. E.; Barthelat, F.; Buehler, M. J. (2009). "Merger of structure and material in nacre and bone – Perspectives on de novo biomimetic materials".
3043:"The degree of bone mineralization is maintained with single intravenous bisphosphonates in aged estrogen-deficient rats and is a strong predictor of bone strength" 2074:
Barthelat, F.; Tang, H.; Zavattieri, P.; Li, C.; Espinosa, H. (2007). "On the mechanics of mother-of-pearl: A key feature in the material hierarchical structure".
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Natural structural materials comprising hard and soft phases arranged in elegant hierarchical multiscale architectures, usually exhibit a combination of superior
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There are two hierarchical structures on the microscale. The first, at a scale of 100 μm to 1 mm, is inside the compact bone where cylindrical units called
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Addadi, L.; Joester, D.; Nudelman, F.; Weiner, S. (2006). "Mollusk shell formation: a source of new concepts for understanding biomineralization processes".
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Barthelat, F. O.; Li, C. M.; Comi, C.; Espinosa, H. D. (2006). "Mechanical properties of nacre constituents and their impact on mechanical performance".
1045:. In nacre, the organic component is porous, which allows the formation of mineral bridges responsible for the growth and order of the nacreous tablets. 774: 2699:
Hua, Mutian; Wu, Shuwang; Ma, Yanfei; Zhao, Yusen; Chen, Zilin; Frenkel, Imri; Strzalka, Joseph; Zhou, Hua; Zhu, Xinyuan; He, Ximin (February 2021).
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Thin film deposition focuses on reproducing the cross-lamellar microstructure of conch instead of mimicking the layered structure of nacre using
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Tang, H.; Barthelat, F.; Espinosa, H. (2007). "An elasto-viscoplastic interface model for investigating the constitutive behavior of nacre".
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toughness of nacre, other models assemblies inspired by the waviness of microstructure of nacre have also been devised on the large scale.
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analysis to investigate the behaviour of the interface. A model has shown that during tension, the back stress that is induced during the
2853:"Adhesion between biodegradable polymers and hydroxyapatite: Relevance to synthetic bone-like materials and tissue engineering scaffolds" 726: 1913:
Nalla, R.; Kruzic, J.; Ritchie, R. (2004). "On the origin of the toughness of mineralized tissue: microcracking or crack bridging?".
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Mohanty, B.; Katti, K.; Katti, D. (2008). "Experimental investigation of nanomechanics of the mineral-protein interface in nacre".
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solution having calcium and phosphate ions. The mineral nucleates, inside the hole area of the collagen fibrils, as thin layers of
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from mollusk shells and bone, which are both high performance natural composites. Many mechanical and imaging techniques such as
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The mineral is the inorganic component of mineralized tissues. This constituent is what makes the tissues harder and stiffer.
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Barthelat, F.; Espinosa, H. D. (2007). "An Experimental Investigation of Deformation and Fracture of Nacre–Mother of Pearl".
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that incorporate minerals into soft matrices. Typically these tissues form a protective shield or structural support. Bone,
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has a hierarchical structure that is also formed by the self-assembly of smaller components. The mineral in bone (known as
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nucleates within the hole area of the collagen fibrils and then grows in these zones until it occupies the maximum space.
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part). There are approximately 60 different minerals generated through biological processes, but the most common ones are
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Yao W.; Cheng Z.; Koester K.J.; Ager J.W.; Balooch M.; Pham A.; Chefo S.; Busse C.; Ritchie R.O. & N.E. Lane (2007).
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Meyers, M.; Lin, A.; Chen, P.; Muyco, J. (2008). "Mechanical strength of abalone nacre: role of the soft organic layer".
1984:"A new technique for imaging Mineralized Fibrils on Bovine Trabecular Bone Fracture Surfaces by Atomic Force Microscopy" 760: 1186:
that is on the tablet surfaces provide resistance to interlamellar sliding and so strengthen the material. A surface
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will provide more insight into the evolution of mineralized tissues and clarify evidence from early fossil records.
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structural length scales are yet to be properly defined. Five hierarchical structures of bone are presented below.
1983: 2502:"Nano-analytical electron microscopy reveals fundamental insights into human cardiovascular tissue calcification" 2191:
Hellmich, C.; Ulm, F. J. (2002). "Micromechanical Model for Ultrastructural Stiffness of Mineralized Tissues".
1423: 1314: 1296:, while the soft matrix “glues” the stiff components and transfer the stress to them. Moreover, the controlled 108:
Mineralized tissues combine stiffness, low weight, strength and toughness due to the presence of minerals (the
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At the interface, a very large force (>6-5 nN) is needed to pull the protein molecules away from the
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stretch of the material plays a big role in the hardening of the mineralized tissue. As well, the nanoscale
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is a new method that uses the physics of ice formation to develop a layered-hybrid material. Specifically,
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mineral in nacre, despite the fact that the molecular interactions are non-bonded. Some studies perform a
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pradhan, Shashindra (July 18, 2012). "Structural Hierarchy Controls Deformation Behavior of Collagen".
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Philosophical Transactions of the Royal Society of London. Series A, Mathematical and Physical Sciences
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T.G. Bromage (1991). "Issues related to mineralized tissue biology in human evolutionary research".
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Wegst, Ulrike G. K.; Bai, Hao; Saiz, Eduardo; Tomsia, Antoni P.; Ritchie, Robert O. (January 2015).
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suspensions are directionally frozen under conditions designed to promote the formation of lamellar
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study has shown that progressive tablet locking and hardening, which are needed for spreading large
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Glimcher, M. (1959). "Molecular Biology of Mineralized Tissues with Particular Reference to Bone".
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The method of self-assembly tries to reproduce not only the properties, but also the processing of
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embryo has been used extensively in developmental biology studies. The larvae form a sophisticated
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of materials only can happen and propagate on the microscopic scale, which wouldn't lead to the
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The large scale model of materials is based on the fact that crack deflection is an important
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Compact bone and spongy bone are on a scale of several millimetres to 1 or more centimetres.
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to a more stable form. Therefore, there are two mineral phases in larval spicule formation.
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is highly ordered and is the framework of the matrix. The main elements of the overall are:
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and are seen in all structural materials in biology such as bone and nacre from seashells
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processes. Some diseased areas that include the appearance of mineralized tissues include
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The 30 nm thick interface between the tablets that connects them together and the
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The silk gel fills the matrix to be mineralized before the mineralization takes place.
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and break easily. Hence, the organic component of mineralized tissues increases their
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The main structural elements involved in the mollusk shell formation process are: a
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increases. However, without this organic portion, the biological material would be
809: 674: 664: 644: 261: 181: 113: 58: 2357: 1701: 1569: 1442:. The MEMS technology repeatedly deposits a thin silicon film. The interfaces are 3295: 3224:"Ultrastructure and mineral composition of serpulid tubes (Polychaeta, Annelida)" 3147: 2871: 1239: 1219: 1211: 985: 813: 805: 540: 416: 330: 298: 130: 3134:
M.H. Shamos (1965). "The Origin of Bioelectric Effects in Mineralized Tissues".
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Proceedings of the National Academy of Sciences of the United States of America
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support. The silk gel is part of the protein portion and is mainly composed of
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Neuendorf R.E.; Saiz E.; Pearce E.I.; Tomsia A.P. & R.O. Ritchie (2008).
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of nacre. This deflection happens because of the weak interfaces between the
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found from further studies on the role of the mineralized tissues involved.
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Nakamura H.K.; Chiou W.-A.; Saruwatari L.; Aita H. & T. Ogawa (2005).
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with a lot of carbonate ions, while the organic portion is made mostly of
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Miller, J. D. (2013). "Cardiovascular calcification: Orbicular origins".
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While crystals grow, some of the acidic proteins get trapped within them.
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shell has the highest degree of structural organization. The mineral
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over large volumes, occurred because of the waviness of the tablets.
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Oyen, M. (2006). "Nanoindentation hardness of mineralized tissues".
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during bony fish evolution. It is expected that genetic analysis of
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Barthelat, F. (2007). "Biomimetics for next generation materials".
1417: 1402: 1388: 1384: 1301: 1187: 1014: 961: 923: 845: 793: 580: 570: 305: 288: 2008:"Genetic basis for the evolution of vertebrate mineralized tissue" 1869: 1356: 1151: 1075: 1071: 1018: 944: 899: 854: 575: 500: 421: 310: 196: 74: 1686:"Infrared spectroscopic characterization of mineralized tissues" 1154:. The latter is a result of the transformation of amorphous CaCO 1110:
begins on the matrix, the calcium carbonate turns into crystals.
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is an important process to understand how these diseases occur.
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To summarize, on the macroscale, the shell, its two layers (
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Beniash, E.; Aizenberg, J.; Addadi, L.; Weiner, S. (1997).
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The components of the matrix are spatially distinguishable.
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Journal of the Mechanical Behavior of Biomedical Materials
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Proceedings of the Royal Society B: Biological Sciences
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and rinsing the tablets, which results in multilayers.
1150:. Each of the spicules is a single crystal of mineral 2461: 2005: 1268:. For instance, many natural mechanical materials ( 1234:or one analogous to it. Imaging techniques such as 2635: 2321: 2269: 2069: 2067: 2065: 2063: 2061: 1912: 1334:All hard materials in animals are achieved by the 837:Nacre has several hierarchical structural levels. 2943: 2431: 1783: 3323: 3222:Vinn, O., ten Hove, H.A. and Mutvei, H. (2008). 2776:Journal of Materials Engineering and Performance 1817: 1815: 1683: 1619: 1617: 1615: 1613: 1611: 1609: 1607: 1605: 1603: 1601: 1599: 1418:Thin film deposition: microfabricated structures 1346: 849:Hierarchical structure: brick and mortar concept 112:part) in soft protein networks and tissues (the 2186: 2184: 2182: 2180: 2178: 2176: 2058: 1597: 1595: 1593: 1591: 1589: 1587: 1585: 1583: 1581: 1579: 1551: 1549: 1547: 1545: 1543: 1541: 1539: 1537: 1535: 1533: 1531: 1529: 1527: 1525: 1230:. All physiologic deposits contain the mineral 1197: 2464:Journal of the Mechanics and Physics of Solids 2427: 2425: 2076:Journal of the Mechanics and Physics of Solids 1731: 1729: 1523: 1521: 1519: 1517: 1515: 1513: 1511: 1509: 1507: 1505: 1308: 1161: 910:Like nacre and the other mineralized tissues, 2317: 2315: 2230: 2228: 2226: 2224: 2222: 2220: 2218: 2216: 2214: 2107: 2105: 1812: 1777: 1446:by reactive ion etching and then filled with 768: 3260:: CS1 maint: multiple names: authors list ( 3113: 2821: 2593: 2173: 2006:Kawasaki, K.; Suzuki, T.; Weiss, K. (2004). 1999: 1865: 1863: 1861: 1679: 1677: 1675: 1673: 1671: 1576: 1395: 1329: 1066:silk gel, aspartic acid rich protein, and a 3173:"Biomaterials: Sacrificial bonds heal bone" 3133: 2896:Mechanical Behavior of Biomedical Materials 2698: 2457: 2455: 2422: 2373: 2270:Currey, J.; Brear, K.; Zioupos, P. (2004). 2190: 1726: 1502: 1093:determines the orientation of the crystals. 956:The components are the mineral crystals of 2312: 2263: 2211: 2102: 775: 761: 97:are some examples of mineralized tissues. 3304: 3294: 3239: 3228:Zoological Journal of the Linnean Society 3196: 3170: 3104: 3069: 2977: 2795: 2533: 2413: 2295: 2164: 2041: 2031: 1858: 1709: 1668: 1623: 1374: 823: 16:Biological tissues incorporating minerals 3268: 2772:"Metal Additive Manufacturing: A Review" 2499: 2452: 1941: 1906: 1735: 1259: 1249: 1048: 844: 18: 2887:Kruzic J.J. & R.O. Ritchie (2007). 2769: 2205:10.1061/(ASCE)0733-9399(2002)128:8(898) 2111: 1424:micro-electro mechanical systems (MEMS) 3324: 2556: 1122:In bone, mineralization starts from a 800:. The dermal skeleton is just surface 2495: 2493: 2146: 1947: 1133: 1007: 967: 2153:Materials Science and Engineering C 2149:"Why is Nacre so strong and tough?" 1772:The Biomimetic Materials Laboratory 1684:Boskey, A.; Mendelsohn, R. (2005). 1434:and organic matrix are replaced by 1371:without too much loss in strength. 938: 930: 13: 2770:Frazier, William E. (2014-06-01). 2763: 2692: 2638:"Bioinspired structural materials" 2629: 2615:10.1016/j.biomaterials.2005.05.059 2500:Bertazzo, S.; et al. (2013). 2490: 2147:Katti, Kalpana (October 5, 2005). 950: 14: 3358: 2944:Jäger I. & P. Fratzl (2000). 2434:Mechanics Research Communications 1103:is the first form of the mineral. 868: 840: 3241:10.1111/j.1096-3642.2008.00421.x 2446:10.1016/j.mechrescom.2007.09.006 2276:Proceedings: Biological Sciences 2193:Journal of Engineering Mechanics 1453: 1057: 877: 796:or the dermal skeleton of early 742: 741: 159: 2815: 2550: 2350: 2140: 1976: 1305:techniques are described here. 996:mineral phase while inside the 506:microbial calcite precipitation 3123:European Cells & Materials 1962:10.1016/j.jbiomech.2005.09.011 1872:Calcified Tissue International 1764: 1: 2970:10.1016/S0006-3495(00)76426-5 2937:10.1016/S1359-6454(97)00253-X 2237:Chemistry: A European Journal 1824:Journal of Materials Research 1702:10.1016/j.vibspec.2005.02.015 1570:10.1016/j.pmatsci.2009.05.001 1558:Progress in Materials Science 1496: 1470: 1347:Ice templation/Freeze casting 466:marine biogenic calcification 3296:10.1371/journal.pone.0075330 3148:10.1177/00220345650440060901 3093:Microscopy and Microanalysis 2872:10.1016/j.actbio.2008.04.006 1426:. Among mollusk shells, the 1198:Diseased mineralized tissues 787: 120:found in mollusk shells and 7: 2908:10.1016/j.jmbbm.2007.04.002 2336:10.1016/j.jmbbm.2007.03.001 1479: 1309:Large scale model materials 1162:Organic-inorganic interface 695:Biomineralising polychaetes 461:amorphous calcium carbonate 147:Part of a series related to 10: 3363: 3062:10.1016/j.bone.2007.06.021 2725:10.1038/s41586-021-03212-z 2484:10.1016/j.jmps.2006.12.009 2166:10.1016/j.msec.2005.08.013 2096:10.1016/j.jmps.2006.07.007 1927:10.1016/j.bone.2004.02.001 1300:of the soft matrix during 727:Burgess Shale preservation 3106:10.1017/S143192760550833X 2797:10.1007/s11665-014-0958-z 1798:10.1007/s11340-007-9040-1 1758:10.1103/RevModPhys.31.359 1738:Reviews of Modern Physics 1486:Shell growth in estuaries 1396:Layer-by-layer deposition 1330:Biomimetic mineralization 1117: 689:Cupriavidus metallidurans 1690:Vibrational Spectroscopy 1041:, bone sialoprotein and 832: 410:Teeth, scales, tusks etc 2033:10.1073/pnas.0404279101 1950:Journal of Biomechanics 905: 471:calcareous nannofossils 267:Choanoflagellate lorica 2406:10.1098/rspb.1997.0066 2288:10.1098/rspb.2003.2634 2249:10.1002/chem.200500980 1786:Experimental Mechanics 1646:10.1098/rsta.2007.0006 1380:Additive manufacturing 1375:Additive manufacturing 1321:tiles. Systems on the 1256: 850: 824:Hierarchical structure 660:Magnetotactic bacteria 485:oolitic aragonite sand 343:scaly-foot snail shell 51: 3114:U. Ripamonti (2003). 1844:10.1557/JMR.2006.0239 1266:mechanical properties 1260:Bioinspired materials 1253: 1236:infrared spectroscopy 1054:bone and sea urchin. 1049:Formation of minerals 848: 23:Mineralized tissues: 22: 1315:toughening mechanism 1176:finite element model 1146:that is made of two 1043:dentin phosphophoryn 3287:2013PLoSO...875330V 3189:2001Natur.414..699C 3010:2005NatMa...4..612F 2962:2000BpJ....79.1737J 2788:2014JMEP...23.1917F 2717:2021Natur.590..594H 2654:2015NatMa..14...23W 2571:2013NatMa..12..476M 2518:2013NatMa..12..576B 2476:2007JMPSo..55.1410T 2398:1997RSPSB.264..461B 2088:2007JMPSo..55..306B 2024:2004PNAS..10111356K 2018:(31): 11356–11361. 1836:2006JMatR..21.1977B 1750:1959RvMP...31..359G 1638:2007RSPTA.365.2907B 1632:(1861): 2907–2919. 1298:plastic deformation 1290:mechanical strength 1089:The highly ordered 387:Vertebrate skeleton 177:Mineralized tissues 55:Mineralized tissues 3171:J. Currey (2001). 2860:Acta Biomaterialia 2836:10.1007/BF02435617 1884:10.1007/BF02556454 1341:composite material 1257: 1216:tumoral calcinosis 851: 551:diatomaceous earth 517:Great Calcite Belt 434:Scale microfossils 427:otolithic membrane 338:small shelly fauna 311:echinoderm stereom 187:Biocrystallization 65:, deep sea sponge 52: 3347:Biomineralization 3269:Vinn, O. (2013). 2711:(7847): 594–599. 2609:(36): 7650–7660. 2392:(1380): 461–465. 2282:(1538): 517–522. 2126:10.1021/bm300801a 2114:Biomacromolecules 1956:(14): 2699–2702. 1491:Biomineralization 1336:biomineralization 1134:Sea urchin embryo 1128:calcium phosphate 1101:calcium carbonate 1008:Organic component 1002:calcium phosphate 978:calcium carbonate 968:Mineral component 785: 784: 715:permineralization 700:Mineral nutrients 625:Mineral evolution 294:foraminifera test 153:Biomineralization 136:biomineralization 118:calcium carbonate 3354: 3318: 3308: 3298: 3265: 3259: 3251: 3249: 3248: 3243: 3218: 3200: 3167: 3142:(6): 1114–1115. 3130: 3120: 3110: 3108: 3083: 3073: 3047: 3037: 3018:10.1038/nmat1428 2998:Nature Materials 2991: 2981: 2956:(4): 1737–1746. 2940: 2919: 2893: 2883: 2866:(5): 1288–1296. 2857: 2847: 2810: 2809: 2799: 2782:(6): 1917–1928. 2767: 2761: 2760: 2696: 2690: 2689: 2662:10.1038/nmat4089 2642:Nature Materials 2633: 2627: 2626: 2597: 2591: 2590: 2579:10.1038/nmat3663 2559:Nature Materials 2554: 2548: 2547: 2537: 2526:10.1038/nmat3627 2506:Nature Materials 2497: 2488: 2487: 2459: 2450: 2449: 2429: 2420: 2419: 2417: 2377: 2371: 2370: 2368: 2367: 2362: 2354: 2348: 2347: 2319: 2310: 2309: 2299: 2267: 2261: 2260: 2232: 2209: 2208: 2188: 2171: 2170: 2168: 2159:(8): 1317–1324. 2144: 2138: 2137: 2120:(8): 2562–2569. 2109: 2100: 2099: 2071: 2056: 2055: 2045: 2035: 2003: 1997: 1996: 1994: 1993: 1988: 1980: 1974: 1973: 1945: 1939: 1938: 1910: 1904: 1903: 1867: 1856: 1855: 1819: 1810: 1809: 1781: 1775: 1768: 1762: 1761: 1733: 1724: 1723: 1713: 1696:(1–2): 107–114. 1681: 1666: 1665: 1621: 1574: 1573: 1564:(8): 1059–1100. 1553: 810:actinopterygians 777: 770: 763: 750: 745: 744: 665:Magnetoreception 645:Ballast minerals 240:Cephalopod shell 235:Brachiopod shell 182:Remineralisation 163: 144: 143: 3362: 3361: 3357: 3356: 3355: 3353: 3352: 3351: 3322: 3321: 3253: 3252: 3246: 3244: 3198:10.1038/414699a 3136:Dental Research 3118: 3045: 2925:Acta Materialia 2891: 2855: 2830:(12): 165–174. 2824:Human Evolution 2818: 2813: 2768: 2764: 2697: 2693: 2634: 2630: 2598: 2594: 2555: 2551: 2498: 2491: 2460: 2453: 2430: 2423: 2378: 2374: 2365: 2363: 2360: 2356: 2355: 2351: 2320: 2313: 2268: 2264: 2233: 2212: 2189: 2174: 2145: 2141: 2110: 2103: 2072: 2059: 2004: 2000: 1991: 1989: 1986: 1982: 1981: 1977: 1946: 1942: 1911: 1907: 1868: 1859: 1820: 1813: 1782: 1778: 1769: 1765: 1734: 1727: 1682: 1669: 1622: 1577: 1554: 1503: 1499: 1482: 1473: 1456: 1420: 1398: 1377: 1351:Ice temptation/ 1349: 1332: 1311: 1262: 1228:salivary stones 1220:dermatomyositis 1212:atherosclerotic 1200: 1164: 1157: 1136: 1120: 1060: 1051: 1010: 986:calcium oxalate 970: 953: 941: 933: 908: 880: 871: 864: 843: 835: 826: 814:sarcopterygians 806:chondrichthyans 790: 781: 740: 733: 732: 731: 619: 611: 610: 609: 565: 557: 556: 555: 541:biogenic silica 535: 525: 524: 523: 508: 496: 475: 455: 445: 444: 443: 411: 403: 402: 401: 381: 366: 365: 364: 331:gastropod shell 299:testate amoebae 289:diatom frustule 214: 203: 202: 201: 171: 141: 131:nanoindentation 57:are biological 17: 12: 11: 5: 3360: 3350: 3349: 3344: 3339: 3334: 3320: 3319: 3281:(10): e75330. 3266: 3234:(4): 633–650. 3219: 3168: 3131: 3111: 3084: 3056:(5): 804–812. 3038: 3004:(8): 612–616. 2992: 2941: 2931:(3): 733–736. 2920: 2884: 2848: 2817: 2814: 2812: 2811: 2762: 2691: 2628: 2592: 2565:(6): 476–478. 2549: 2512:(6): 576–583. 2489: 2451: 2440:(1–2): 17–23. 2421: 2372: 2349: 2311: 2262: 2243:(4): 980–987. 2210: 2172: 2139: 2101: 2057: 1998: 1975: 1940: 1921:(5): 790–798. 1905: 1857: 1811: 1776: 1763: 1744:(2): 359–393. 1725: 1667: 1575: 1500: 1498: 1495: 1494: 1493: 1488: 1481: 1478: 1472: 1469: 1455: 1452: 1419: 1416: 1397: 1394: 1376: 1373: 1353:Freeze casting 1348: 1345: 1331: 1328: 1310: 1307: 1261: 1258: 1232:hydroxyapatite 1199: 1196: 1163: 1160: 1155: 1135: 1132: 1119: 1116: 1115: 1114: 1111: 1104: 1097: 1094: 1087: 1059: 1056: 1050: 1047: 1009: 1006: 974:Hydroxyapatite 969: 966: 960:, cylindrical 958:hydroxyapatite 952: 949: 940: 939:The microscale 937: 932: 931:The macroscale 929: 920:hydroxyapatite 907: 904: 879: 876: 870: 869:The microscale 867: 862: 842: 841:The macroscale 839: 834: 831: 825: 822: 789: 786: 783: 782: 780: 779: 772: 765: 757: 754: 753: 752: 751: 735: 734: 730: 729: 724: 723: 722: 717: 707: 702: 697: 692: 685: 680: 672: 667: 662: 657: 652: 647: 642: 641: 640: 638:immobilization 635: 633:mineralization 627: 621: 620: 617: 616: 613: 612: 608: 607: 602: 601: 600: 590: 589: 588: 583: 573: 567: 566: 563: 562: 559: 558: 554: 553: 548: 546:siliceous ooze 543: 537: 536: 533:Silicification 531: 530: 527: 526: 522: 521: 520: 519: 514: 509: 497: 495: 494: 493: 492: 487: 476: 474: 473: 468: 463: 457: 456: 451: 450: 447: 446: 442: 441: 436: 431: 430: 429: 419: 413: 412: 409: 408: 405: 404: 400: 399: 394: 389: 383: 382: 372: 371: 368: 367: 363: 362: 357: 355:Sponge spicule 352: 351: 350: 348:estuary shells 345: 340: 335: 334: 333: 328: 323: 313: 303: 302: 301: 296: 291: 286: 281: 271: 270: 269: 259: 258: 257: 252: 247: 237: 232: 231: 230: 225: 216: 215: 209: 208: 205: 204: 200: 199: 194: 189: 184: 179: 173: 172: 169: 168: 165: 164: 156: 155: 149: 148: 122:hydroxyapatite 63:mollusc shells 15: 9: 6: 4: 3: 2: 3359: 3348: 3345: 3343: 3340: 3338: 3335: 3333: 3332:Bone products 3330: 3329: 3327: 3316: 3312: 3307: 3302: 3297: 3292: 3288: 3284: 3280: 3276: 3272: 3267: 3263: 3257: 3242: 3237: 3233: 3229: 3225: 3220: 3216: 3212: 3208: 3204: 3199: 3194: 3190: 3186: 3183:(6865): 699. 3182: 3178: 3174: 3169: 3165: 3161: 3157: 3153: 3149: 3145: 3141: 3137: 3132: 3128: 3124: 3117: 3112: 3107: 3102: 3098: 3094: 3090: 3085: 3081: 3077: 3072: 3067: 3063: 3059: 3055: 3051: 3044: 3039: 3035: 3031: 3027: 3023: 3019: 3015: 3011: 3007: 3003: 2999: 2993: 2989: 2985: 2980: 2975: 2971: 2967: 2963: 2959: 2955: 2951: 2947: 2942: 2938: 2934: 2930: 2926: 2921: 2917: 2913: 2909: 2905: 2901: 2897: 2890: 2885: 2881: 2877: 2873: 2869: 2865: 2861: 2854: 2849: 2845: 2841: 2837: 2833: 2829: 2825: 2820: 2819: 2807: 2803: 2798: 2793: 2789: 2785: 2781: 2777: 2773: 2766: 2758: 2754: 2750: 2746: 2742: 2738: 2734: 2730: 2726: 2722: 2718: 2714: 2710: 2706: 2702: 2695: 2687: 2683: 2679: 2675: 2671: 2667: 2663: 2659: 2655: 2651: 2647: 2643: 2639: 2632: 2624: 2620: 2616: 2612: 2608: 2604: 2596: 2588: 2584: 2580: 2576: 2572: 2568: 2564: 2560: 2553: 2545: 2541: 2536: 2531: 2527: 2523: 2519: 2515: 2511: 2507: 2503: 2496: 2494: 2485: 2481: 2477: 2473: 2469: 2465: 2458: 2456: 2447: 2443: 2439: 2435: 2428: 2426: 2416: 2411: 2407: 2403: 2399: 2395: 2391: 2387: 2383: 2376: 2359: 2353: 2345: 2341: 2337: 2333: 2329: 2325: 2318: 2316: 2307: 2303: 2298: 2293: 2289: 2285: 2281: 2277: 2273: 2266: 2258: 2254: 2250: 2246: 2242: 2238: 2231: 2229: 2227: 2225: 2223: 2221: 2219: 2217: 2215: 2206: 2202: 2198: 2194: 2187: 2185: 2183: 2181: 2179: 2177: 2167: 2162: 2158: 2154: 2150: 2143: 2135: 2131: 2127: 2123: 2119: 2115: 2108: 2106: 2097: 2093: 2089: 2085: 2081: 2077: 2070: 2068: 2066: 2064: 2062: 2053: 2049: 2044: 2039: 2034: 2029: 2025: 2021: 2017: 2013: 2009: 2002: 1985: 1979: 1971: 1967: 1963: 1959: 1955: 1951: 1944: 1936: 1932: 1928: 1924: 1920: 1916: 1909: 1901: 1897: 1893: 1889: 1885: 1881: 1878:(6): 407–13. 1877: 1873: 1866: 1864: 1862: 1853: 1849: 1845: 1841: 1837: 1833: 1829: 1825: 1818: 1816: 1807: 1803: 1799: 1795: 1791: 1787: 1780: 1774: 1773: 1767: 1759: 1755: 1751: 1747: 1743: 1739: 1732: 1730: 1721: 1717: 1712: 1707: 1703: 1699: 1695: 1691: 1687: 1680: 1678: 1676: 1674: 1672: 1663: 1659: 1655: 1651: 1647: 1643: 1639: 1635: 1631: 1627: 1620: 1618: 1616: 1614: 1612: 1610: 1608: 1606: 1604: 1602: 1600: 1598: 1596: 1594: 1592: 1590: 1588: 1586: 1584: 1582: 1580: 1571: 1567: 1563: 1559: 1552: 1550: 1548: 1546: 1544: 1542: 1540: 1538: 1536: 1534: 1532: 1530: 1528: 1526: 1524: 1522: 1520: 1518: 1516: 1514: 1512: 1510: 1508: 1506: 1501: 1492: 1489: 1487: 1484: 1483: 1477: 1468: 1465: 1461: 1454:Self-assembly 1451: 1449: 1445: 1441: 1437: 1433: 1429: 1425: 1415: 1413: 1408: 1404: 1393: 1390: 1386: 1381: 1372: 1370: 1366: 1362: 1358: 1354: 1344: 1342: 1337: 1327: 1324: 1320: 1316: 1306: 1303: 1299: 1295: 1291: 1287: 1283: 1279: 1275: 1271: 1267: 1252: 1248: 1245: 1241: 1237: 1233: 1229: 1225: 1221: 1217: 1213: 1209: 1205: 1195: 1193: 1189: 1185: 1181: 1177: 1173: 1168: 1159: 1153: 1149: 1145: 1141: 1131: 1129: 1125: 1124:heterogeneous 1112: 1109: 1105: 1102: 1098: 1095: 1092: 1088: 1085: 1084: 1083: 1081: 1077: 1073: 1069: 1065: 1058:Mollusk shell 1055: 1046: 1044: 1040: 1036: 1032: 1028: 1024: 1020: 1016: 1005: 1003: 999: 995: 991: 987: 983: 979: 975: 965: 963: 959: 951:The nanoscale 948: 946: 936: 928: 925: 921: 917: 913: 903: 901: 897: 892: 890: 885: 878:The nanoscale 875: 866: 860: 856: 847: 838: 830: 821: 819: 815: 811: 807: 803: 799: 795: 778: 773: 771: 766: 764: 759: 758: 756: 755: 749: 739: 738: 737: 736: 728: 725: 721: 718: 716: 713: 712: 711: 710:Fossilization 708: 706: 705:Microbial mat 703: 701: 698: 696: 693: 691: 690: 686: 684: 681: 679: 677: 673: 671: 668: 666: 663: 661: 658: 656: 653: 651: 650:Magnetofossil 648: 646: 643: 639: 636: 634: 631: 630: 628: 626: 623: 622: 615: 614: 606: 603: 599: 596: 595: 594: 591: 587: 584: 582: 579: 578: 577: 574: 572: 569: 568: 561: 560: 552: 549: 547: 544: 542: 539: 538: 534: 529: 528: 518: 515: 513: 510: 507: 504: 503: 502: 499: 498: 491: 490:aragonite sea 488: 486: 483: 482: 481: 478: 477: 472: 469: 467: 464: 462: 459: 458: 454: 453:Calcification 449: 448: 440: 437: 435: 432: 428: 425: 424: 423: 420: 418: 415: 414: 407: 406: 398: 395: 393: 390: 388: 385: 384: 379: 375: 374:Endoskeletons 370: 369: 361: 358: 356: 353: 349: 346: 344: 341: 339: 336: 332: 329: 327: 324: 322: 319: 318: 317: 316:mollusc shell 314: 312: 309: 308: 307: 304: 300: 297: 295: 292: 290: 287: 285: 282: 280: 277: 276: 275: 274:Protist shell 272: 268: 265: 264: 263: 260: 256: 253: 251: 248: 246: 245:cirrate shell 243: 242: 241: 238: 236: 233: 229: 226: 224: 221: 220: 218: 217: 212: 207: 206: 198: 195: 193: 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Retrieved 3231: 3227: 3180: 3176: 3139: 3135: 3126: 3122: 3096: 3092: 3053: 3049: 3001: 2997: 2953: 2949: 2928: 2927:(abstract). 2924: 2899: 2895: 2863: 2859: 2827: 2823: 2816:Bibliography 2779: 2775: 2765: 2708: 2704: 2694: 2648:(1): 23–36. 2645: 2641: 2631: 2606: 2603:Biomaterials 2602: 2595: 2562: 2558: 2552: 2509: 2505: 2467: 2463: 2437: 2433: 2389: 2385: 2375: 2364:. Retrieved 2352: 2330:(1): 76–85. 2327: 2323: 2279: 2275: 2265: 2240: 2236: 2196: 2192: 2156: 2152: 2142: 2117: 2113: 2079: 2075: 2015: 2011: 2001: 1990:. Retrieved 1978: 1953: 1949: 1943: 1918: 1914: 1908: 1875: 1871: 1827: 1823: 1789: 1785: 1779: 1770: 1766: 1741: 1737: 1693: 1689: 1629: 1625: 1561: 1557: 1474: 1457: 1421: 1412:electrolytes 1405:system. The 1399: 1378: 1361:ice crystals 1350: 1333: 1312: 1263: 1208:pathological 1201: 1192:deformations 1169: 1165: 1144:endoskeleton 1137: 1121: 1061: 1052: 1011: 971: 954: 942: 934: 916:bone mineral 909: 893: 881: 872: 852: 836: 827: 791: 720:petrifaction 687: 675: 670:Microfossils 417:Limpet teeth 397:Ossification 392:Bone mineral 326:chiton shell 211:Exoskeletons 192:Biointerface 176: 140: 107: 99: 91:tooth enamel 71:radiolarians 66: 54: 53: 3099:: 184–185. 2950:Biophysical 2902:(1): 3–17. 2470:(7): 1410. 1830:(8): 1977. 1460:bioceramics 1448:photoresist 1440:photoresist 1436:polysilicon 1323:macroscopic 1218:, juvenile 1204:vertebrates 1064:hydrophobic 1039:osteocalcin 1035:osteopontin 1031:osteonectin 990:whitlockite 655:Magnetosome 598:phosphorite 564:Other forms 512:calcite sea 279:coccosphere 223:exoskeleton 103:biomimetics 67:Euplectella 41:radiolarian 3342:Physiology 3326:Categories 3247:2014-01-09 2366:2010-08-14 2199:(8): 898. 2082:(2): 306. 1992:2010-08-14 1792:(3): 311. 1497:References 1471:The future 1464:nucleation 1407:composites 1255:material). 1240:resorption 1184:asperities 1140:sea urchin 1108:nucleation 1099:Amorphous 1027:nucleation 250:cuttlebone 219:Arthropod 29:sea shells 25:sea sponge 2806:1544-1024 2757:232048202 2733:1476-4687 2686:263363492 2670:1476-4660 1432:aragonite 1369:ductility 1365:hydrogels 1319:aragonite 1294:stiffness 1214:plaques, 1172:aragonite 1023:toughness 994:amorphous 884:aragonite 859:aragonite 818:agnathans 798:agnathans 788:Evolution 676:engrailed 593:Phosphate 586:oil shale 480:Aragonite 284:coccolith 110:inorganic 87:cartilage 69:species, 3337:Pedology 3315:24116035 3275:PLOS ONE 3207:11742376 3164:45177549 3129:: 29–30. 3080:17825637 3034:20835743 3026:16025123 2988:11023882 2916:19627767 2880:18485842 2844:83595216 2749:33627812 2678:25344782 2623:16005961 2587:23695741 2544:23603848 2344:19627773 2306:15129962 2257:16315200 2134:22808993 2052:15272073 1970:16253265 1935:15121010 1806:16707485 1720:16691288 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Index


sea sponge
sea shells
conch
dentin
radiolarian
antler
bone
tissues
mollusc shells
radiolarians
diatoms
antler
tendon
cartilage
tooth enamel
dentin
biomimetics
inorganic
organic
calcium carbonate
hydroxyapatite
nacre
nanoindentation
biomineralization
Biomineralization

Mineralized tissues
Remineralisation
Biocrystallization

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