Gastropod nacre: Structure, properties and growth - Biological, chemical and physical basics

Biophysical Chemistry

Volumn 153, Issue 2-3, 2011, Pages 126-153

  Heinemann, Fabian ^a   Launspach, Malte ^a   Gries, Katharina ^a   Fritz, Monika ^a  

^a UNIVERSITY OF BREMEN   (Germany)

Author keywords

Biogenic composite; Biomineralisation; Biomineralising proteins; Columnar nacre; Mechanical properties; Organic matrix

Indexed keywords

MINERAL;

ABALONE; CERAMICS; CHEMICAL STRUCTURE; CORROSION; CRYSTALLIZATION; GROWTH; NONHUMAN; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN STRUCTURE; REVIEW;

ANIMALS; BIOMIMETIC MATERIALS; BIOPOLYMERS; ELECTRON MICROSCOPE TOMOGRAPHY; FORECASTING; GASTROPODA; MICROSCOPY, ATOMIC FORCE; MINERALS; SPECTROMETRY, X-RAY EMISSION; SPECTROSCOPY, ELECTRON ENERGY-LOSS;

BIVALVIA; GASTROPODA; HALIOTIS;

EID: 78651065369     PISSN: 03014622     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bpc.2010.11.003     Document Type: Review

References (188)

1. K. Wada Crystal growth of molluscan shells Bulletin of the National Pearl Research Laboratories 7 1961 703 828
2. H.K. Erben On the structure and growth of the nacreous tablets in gastropods Biomineralization 1 1974 14 27
3. H. Nakahara An electron microscope study of the growing surface of nacre in two gastropode species Turbo cornutus and Tegula pfeifferi Venus 38 1979 205 211
4. G. Bevelander Abalone: Gross and Fine Structure 1988 The Boxwood Press Pacific Grove
5. H. Nakahara, G. Bevelander, and M. Kakei Electron microscopic and amino acid studies on the outer and inner shell layers of Haliotis rufescens Venus 41 1982 33 46
6. A.P. Jackson, J.F.V. Vincent, and R.M. Turner The mechanical design of nacre Proceedings of the Royal Society of London. Series B. Biological Sciences 234 1988 415 440
7. H.A. Lowenstam Minerals formed by organisms Science 211 1981 1126 1131
8. M. Snow, A. Pring, P. Self, D. Losic, and J. Shapter The origin of the color of pearls in iridescence from nano-composite structures of the nacre American Mineralogist 89 2004 1353 1358
9. M. Meyers, P. Chen, A. Lin, and Y. Seki Biological materials: structure and mechanical properties Progress in Materials Science 53 2008 1 206
10. Y. Dauphin, J.P. Cuif, H. Mutvei, and A. Denis Mineralogy, chemistry and ultrasructure of the external shell-layer in ten species of Haliotis with reference to Haliotis tuberculata (Molusca: Archaeogastropoda) Bulletin of the Geological Institute, University of Uppsala 15 1989 7 36
11. H. Espinosa, J. Rim, F. Barthelat, and M. Buehler Merger of structure and material in nacre and bone-perspectives on de novo biomimetic materials Progress in Materials Science 54 2009 1059 1100
12. C.M. Zaremba, A.M. Belcher, M. Fritz, Y. Li, S. Mann, P.K. Hansma, D.E. Morse, J.S. Speck, and G.D. Stucky Critical transitions in the biofabrication of abalone shells and flat pearls Chemistry of Materials 8 1996 679 690
13. A. Lin, and M. Meyers Growth and structure in abalone shell Materials Science and Engineering A 390 2005 27 41
14. S. Wise Microarchitecture and mode of formation of nacre (mother-of-pearl) in pelecypods, gastropods, and cephalopods Eclogae Geologicae Helvetiae 63 1970 775 797
15. H. Nakahara Calcification of gastropode nacre P. Westbroeck, E.W. De Jong, Biomineralization and Biological Metal Accumulation 1983 D. Reidel Publishing Company Dordrecht, Netherlands 225 230
16. H. Mukai, K. Saruwatari, H. Nagasawa, and T. Kogure Aragonite twinning in gastropod nacre Journal of Crystal Growth 312 2010 3014 3019
17. M. Fritz, A.M. Belcher, M. Radmacher, D.A. Walters, P.K. Hansma, G.D. Stucky, D.E. Morse, and S. Mann Flat pearls from biofabrication of organized composites on inorganic substrates Nature 371 1994 49 51
18. S. Weiner, and L. Hood Soluble protein of the organic matrix of mollusk shells: a potential template for shell formation Science 190 1975 987 989
19. G. Falini, S. Albeck, S. Weiner, and L. Addadi Control of aragonite or calcite polymorphism by mollusk shell macromolecules Science 271 1996 67 69
20. S. Mann Biomineralization: Principles and Concepts in Bioinorganic Materials Chemistry 2001 Oxford University Press USA
21. T. Schäffer, C. Ionescu-Zanetti, R. Proksch, M. Fritz, D. Walters, N. Almqvist, C. Zaremba, A. Belcher, B. Smith, and G. Stucky Does abalone nacre form by heteroepitaxial nucleation or by growth through mineral bridges? Chemistry of Materials 9 1997 1731 1740
22. J. Bezares, R. Asaro, and M. Hawley Macromolecular structure of the organic framework of nacre in Haliotis rufescens: implications for growth and mechanical behavior Journal of Structural Biology 163 2008 61 75
23. F. Nudelman, B. Gotliv, L. Addadi, and S. Weiner Mollusk shell formation: mapping the distribution of organic matrix components underlying a single aragonitic tablet in nacre Journal of Structural Biology 153 2006 176 187
24. M. Rousseau, E. Lopez, P. Stempflé, M. Brendlé, L. Franke, A. Guette, R. Naslain, and X. Bourrat Multiscale structure of sheet nacre Biomaterials 26 2005 6254 6262
25. A. Jackson, J. Vincent, and R. Turner Comparison of nacre with other ceramic composites Journal of Materials Science 25 1990 3173 3178
26. H. Gao, B. Ji, I.L. Jäger, E. Arzt, and P. Fratzl Materials become insensitive to flaws at nanoscale: lessons from nature Proceedings of the National Academy of Sciences of the United States of America 100 2003 5597 5600
27. S. Rama Swamy X-ray analysis of the structure of iridescent shells Proceedings Mathematical Sciences 2 1935 345 351
28. H. Mutvei Ultrastructural characteristics of the nacre in some gastropods Zoologica Scripta 7 1978 287 296
29. B. Bruet, H. Qi, M. Boyce, R. Panas, K. Tai, L. Frick, and C. Ortiz Nanoscale morphology and indentation of individual nacre tablets from the gastropod mollusc Trochus niloticus Journal of Materials Research 20 2005 2400 2419
30. D. Chateigner, C. Hedegaard, and H. Wenk Mollusc shell microstructures and crystallographic textures Journal of Structural Geology 22 2000 1723 1735
31. X. Li, W. Chang, Y. Chao, R. Wang, and M. Chang Nanoscale structural and mechanical characterization of a natural nanocomposite material: the shell of red abalone Nano Letters 4 2004 613 617
32. K. Gries, R. Kröger, C. Kübel, M. Schowalter, M. Fritz, and A. Rosenauer Correlation of the orientation of stacked aragonite platelets in nacre and their connection via mineral bridges Ultramicroscopy 109 2009 230 236
33. R. Wang, Z. Suo, A. Evans, N. Yao, and I. Aksay Deformation mechanisms in nacre Journal of Materials Research 16 2001 2486
34. R. Ballarini, R. Kayacan, F.J. Ulm, T. Belytschko, and A.H. Heuer Biological structures mitigate catastrophic fracture through various strategies International Journal of Fracture 135 2005 187 197
35. K. Gries, R. Kröger, C. Kübel, M. Fritz, and A. Rosenauer Investigations of voids in the aragonite platelets of nacre Acta Biomaterialia 5 2009 3038 3044
36. R. Metzler, M. Abrecht, R. Olabisi, D. Ariosa, C. Johnson, B. Frazer, S. Coppersmith, and P. Gilbert Architecture of columnar nacre, and implications for its formation mechanism Physical Review Letters 98 2007 268102
37. P. Gilbert, R. Metzler, D. Zhou, A. Scholl, A. Doran, A. Young, M. Kunz, N. Tamura, and S. Coppersmith Gradual ordering in red abalone nacre Journal of the American Chemical Society 130 2008 17519 17527
38. R. Metzler, D. Zhou, M. Abrecht, J. Chiou, J. Guo, D. Ariosa, S. Coppersmith, and P. Gilbert Polarization-dependent imaging contrast in abalone shells Physical Review B 77 2008 64110 64118
39. S. Blank, M. Arnoldi, S. Khoshnavaz, L. Treccani, M. Kuntz, K. Mann, G. Grathwohl, and M. Fritz The nacre protein perlucin nucleates growth of calcium carbonate crystals Journal of Microscopy 212 2003 280 291
40. S. Weiner, Y. Talmon, and W. Traub Electron diffraction of mollusc shell organic matrices and their relationship to the mineral phase International Journal of Biological Macromolecules 5 1983 325 328
41. S. Weiner, and W. Traub Macromolecules in mollusc shells and their functions in biomineralization [and discussion] Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 304 1984 425 434
42. I.M. Weiss, C. Renner, M.G. Strigl, and M. Fritz A simple and reliable method for the determination and localization of chitin in abalone nacre Chemistry of Materials 14 2002 3252 3259
43. Ch. Jeuniaux Chitine et Chitinolyse: un chapitre de la biologie moléculaire (Edited by Masson et Cie) 1963 127 135 Paris
44. G. Goffinet Etude au microscope electronique de structures organisees des constituants de la conchioline de nacre du Nautilus macromphalus sowerby Comparative Biochemistry and Physiology 29 1969 835 839
45. S. Weiner, and W. Traub X-ray diffraction study of the insoluble organic matrix of mollusk shells Federation of European Biochemical Societies Letters 111 1980 311 316
46. F. Lucas, J. Shaw, and S. Smith Comparative studies of fibroins: I. The amino acid composition of various fibroins and its significance in relation to their crystal structure and taxonomy Journal of Molecular Biology 2 1960 339 349
47. E. Degens Molecular mechanisms on carbonate, phosphate, and silica deposition in the living cell Topics in Current Chemistry 64 1976 1 112
48. J. Gosline, P. Guerette, C. Ortlepp, and K. Savage The mechanical design of spider silks: from fibroin sequence to mechanical function Journal of Experimental Biology 202 1999 3295
49. S. Sudo, T. Fujikawa, T. Nagakura, T. Ohkubo, K. Sakaguchi, M. Tanaka, K. Nakashima, and T. Takahashi Structures of mollusc shell framework proteins Nature 387 1997 563 564
50. B. Gotliv, L. Addadi, and S. Weiner Mollusk shell acidic proteins: in search of individual functions ChemBioChem 4 2003 522 529
51. J. Evans "Tuning in" to mollusk shell nacre- and prismatic-associated protein terminal sequences. Implications for biomineralization and the construction of high performance inorganic-organic composites Chemical Reviews 108 2008 4455 4462
52. F. Marin, and G. Luquet Molluscan shell proteins Comptes Rendus Palevol 3 2004 469 492
53. S. Weiner Aspartic acid-rich proteins: major components of the soluble organic matrix of mollusk shells Calcified Tissue International 29 1979 163 167
54. 3 biomineralization: acidic 8-kDa proteins isolated from aragonitic abalone shell nacre can specifically modify calcite crystal morphology Biomacromolecules 6 2005 1289 1298
55. F. Heinemann. Investigation of biopolymer-mineral interactions in the natural composite material nacre, PhD thesis Department of Physics, University of Bremen (2008).
56. K. Mann, I. Weiss, S. Andre, H. Gabius, and M. Fritz The amino-acid sequence of the abalone (Haliotis laevigata) nacre protein perlucin European Journal of Biochemistry 267 2000 5257 5264
57. I. Weiss, W. Göhring, M. Fritz, and K. Mann Perlustrin, a Haliotis laevigata (abalone) nacre protein, is homologous to the insulin-like growth factor binding protein N-terminal module of vertebrates Biochemical and Biophysical Research Communications 285 2001 244 249
58. L. Treccani, K. Mann, F. Heinemann, and M. Fritz Perlwapin, an abalone nacre protein with three four-disulfide core (whey acidic protein) domains, inhibits the growth of calcium carbonate crystals Biophysical Journal 91 2006 2601 2608
59. K. Mann, F. Siedler, L. Treccani, F. Heinemann, and M. Fritz Perlinhibin, a cysteine-, histidine-, and arginine-rich miniprotein from abalone (Haliotis laevigata) nacre, inhibits in vitro calcium carbonate crystallization Biophysical Journal 93 2007 1246 1254
60. X. Shen, B.A. M., P.K. Hansma, G.D. Sucky, and D.E. Morse Molecular cloning and characterisation of lustrin A, a matrix protein from shell and pearl nacre of Haliotis rufescens. Journal of Biological Chemistry 272 1997 32472 32481
61. B.L. Smith, T.E. Schäffer, M. Viani, J.B. Thompson, N.A. Frederick, J. Kindt, A. Belcher, G.D. Stucky, D.E. Morse, and P.K. Hansma Molecular mechanistic origin of toughness of natural adhesives, fibres and composites Nature 399 1999 761 763
62. M. Michenfelder, G. Fu, C. Lawrence, J. Weaver, B. Wustman, L. Taranto, J. Evans, and D. Morse Characterization of two molluscan crystal-modulating biomineralization proteins and identification of putative mineral binding domains Biopolymers 70 2003 522 533
63. G. Fu, S. Qiu, C. Orme, D. Morse, and J. De Yoreo Acceleration of calcite kinetics by abalone nacre proteins Advanced Materials 17 2005 2678 2683
64. 3 precipitation rates by water-soluble nacre proteins, Materials Science and Engineering C (2010) doi:10.1016/j.msec.2010.08.005.
65. L. Treccani, S. Khoshnavaz, S. Blank, K. vonRoden, U. Schulz, I. Weiss, K. Mann, M. Radmacher, and M. Fritz Biomineralizing proteins, with emphasis on invertebrate-mineralized structures Fahnestock Steinbüchl Biopolymers 2003 Wiley-VCH Verlag GmbH Weinheim 289 321
66. H. Ehrlich, P. Koutsoukos, K. Demadis, and O. Pokrovsky Principles of demineralization: modern strategies for the isolation of organic frameworks: part I. Common definitions and history Micron 39 2008 1062 1091
67. H. Ehrlich, P. Koutsoukos, K. Demadis, and O. Pokrovsky Principles of demineralization: modern strategies for the isolation of organic frameworks: part II. Decalcification Micron 40 2009 169 193
68. P. Gilbert, M. Abrecht, and B. Frazer The organic-mineral interface in biominerals Reviews in Mineralogy and Geochemistry 59 2005 157
69. R. Metzler, I. Kim, K. Delak, J. Evans, D. Zhou, E. Beniash, F. Wilt, M. Abrecht, J. Chiou, and J. Guo Probing the organic-mineral interface at the molecular level in model biominerals Langmuir 24 2008 2680 2687
70. A.H. Pfund The colors of mother-of-pearl Journal of Franklin Institute 183 1917 453 464
71. S. Kinoshita, S. Yoshioka, and J. Miyazaki Physics of structural colors Reports on Progress in Physics 71 2008 1 30
72. Y. Liu, J.E. Shigley, and K.N. Hurwitt Iridescence color of a shell of the mollusk Pinctada margaritifera caused by diffraction Optics Express 4 1999 177 182
73. T.L. Tan, D. Wong, and P. Lee Iridescence of a shell of mollusk Haliotis glabra Optics Express 12 2004 4847 4854
74. D.J. Brink, and N.G. van der Berg An investigation of green iridescence on the mollusc Patella granatina Journal of Physics D: Applied Physics 38 2005 338 343
75. S.M. Doucet, and M.G. Meadows Iridescence: a functional perspective Journal of the Royal Society Interface 6 2009 S115 S132
76. S.M. Porter Seawater chemistry and early carbonate biomineralization Science 316 2007 1302
77. A.Y. Zhuravlev, and R.A. Wood Eve of biomineralization: controls on skeletal mineralogy Geology 36 2008 923 926
78. P.A. Sandberg An oscillating trend in Phanerozoic non-skeletal carbonate mineralogy Nature 305 1983 19 22
79. T.K. Lowenstein, M.N. Timofeeff, S.T. Brennan, L.A. Hardie, and R.V. Demicco Oscillations in Phanerozoic seawater chemistry: evidence from fluid inclusions Science 294 2001 1086 1088
80. L.A. Hardie Secular variation in seawater chemistry: an explanation for the coupled secular variation in the mineralogies of marine limestones and potash evaporites over the past 600 m.y. Geology 24 1996 279 283
81. J.B. Ries Aragonite production in calcite seas: effect of seawater Mg/Ca ratio on the calcification and growth of the calcareous alga Penicillus capitatus Paleobiology 31 2005 445 458
82. R.A. Berner The role of magnesium in the crystal growth of calcite and aragonite from sea water Geochimica et Cosmochimica Acta 39 1975 489 504
83. 3 precipitates from seawater Geology 25 1997 85 87
84. 2O Geochimica et Cosmochimica Acta 46 1982 1011 1040
85. 3 polymorphs calcite and aragonite I. Growth and dissolution rates in water Journal of Crystal Growth 158 1996 296 309
86. J.W. Morse, and R.S. Arvidson The dissolution kinetics of major sedimentary carbonate minerals Earth-Science Reviews 58 2002 51 84
87. A.G. Checa, C. Jiménez-López, A. Rodríguez-Navarro, and J.P. Machado Precipitation of aragonite by calcitic bivalves in Mg-enriched marine waters Marine Biology 150 2007 819 827
88. J.G. Carter, E. Barrera, and M.J. Tevesz Thermal potentiation and mineralogical evolution in the Bivalvia (Mollusca) Journal of Paleontology 72 1998 991 1010
89. M.A. Crenshaw The inorganic composition of molluscan extrapallial fluid Biological Bulletin 143 1972 506 512
90. E.M. Harper Are calcitic layers an effective adaptation against shell dissolution in the Bivalvia? Journal of Zoology 251 2000 179 186
91. P. Cubillas, S. Köhler, M. Prieto, C. Chaïrat, and E.H. Oelkers Experimental determination of the dissolution rates of calcite, aragonite, and bivalves Chemical Geology 216 2005 59 77
92. S.A. Wainwright Stress and design in bivalved mollusc shell Nature 224 1969 777 779
93. M. Rubner Synthetic sea shell Nature 423 2003 925 926
94. L.J. Bonderer, A.R. Studart, and L.J. Gauckler Bioinspired design and assembly of platelet reinforced polymer films Science 319 2008 1069 1073
95. E. Munch, M.E. Launey, D.H. Alsem, E. Saiz, A.P. Tomsia, and R.O. Ritchie Tough, bio-inspired hybrid materials Science 322 2008 1516 1520
96. F. Barthelat Nacre from mollusk shells: a model for high-performance structural materials Bioinspiration & Biomimetics 5 2010 1 8
97. M.F. Ashby Materials Selection in Mechanical Design 1992 Pergamon Press Ltd. Oxford
98. U.G.K. Wegst, and M.F. Ashby The mechanical efficiency of natural materials Philosophical Magazine 21 2004 2167 2181
99. M.H. Sadd Elasticity - Theory, Applications, and Numerics 2009 Academic Press Burlington, MA, USA
100. A.I. Lurie Theory of Elasticity 2005 Springer-Verlag Berlin
101. D. Gross, W. Hauger, and J. Schröder Technische Mechanik 2 - Elastostatik 2005 Springer Verlag Berlin
102. T.L. Anderson Fracture Mechanics 2005 Taylor & Francis Boca Raton
103. J.G. Williams Fracture mechanics of anisotropic materials K. Friedrich, Application of Fracture Mechanics to Composite Materials 1989 Elsevier Science Publishers B.V. Amsterdam 3 38
104. M.E. Launey On the Fracture Toughness of Advanced Materials 2009 Lawrence Berkeley National Laboratory Retrieved from http://www.escholarship.org/uc/ item/7256s0nq on 19th of May 2009.
105. J.D. Currey, and J.D. Taylor The mechanical behaviour of some molluscan hard tissues Journal of Zoology 173 1974 395 406
106. J.D. Currey Further studies on the mechanical properties of mollusc shell material Journal of Zoology 180 1976 445 453
107. A.Y. Lin, M.A. Meyers, and K.S. Vecchio Mechanical properties and structure of Strombus gigas, Tridacna gigas, and Haliotis rufescens sea shells: a comparative study Materials Science and Engineering C 26 2006 1380 1389
108. R. Rabiei, S. Bekah, and F. Barthelat Failure mode transition in nacre and bone-like materials Acta Biomaterialia 6 2010 4081 4089
109. L. Liu, C. Chen, C. Lin, and Y. Yang Elasticity of single-crystal aragonite by Brillouin spectroscopy Physics and Chemistry of Minerals 32 2005 97 102
110. C. Kearney, Z. Zhao, B.J.F. Bruet, R. Radovitzky, M.C. Boyce, and C. Ortiz Nanoscale anisotropic plastic deformation in single crystal aragonite Physical Review Letters 96 2006 1 4
111. N.H. de Leeuw, and S.C. Parker Surface structure and morphology of calcium carbonate polymorphs calcite, aragonite and vaterite: an atomistic approach Journal of Physical Chemistry B 102 1998 2914 2922
112. F. Barthelat, and H.D. Espinosa An experimental investigation of deformation and fracture of nacre - mother of pearl Experimental Mechanics 47 2007 311 324
113. M.E. Broz, R.F. Cook, and D.L. Whitney Microhardness, toughness, and modulus of Mohs scale minerals American Mineralogist 91 2006 135 142
114. M.A. Meyers, A.Y. Lin, P. Chen, and J. Muyco Mechanical strength of abalone nacre: role of the soft organic layer Journal of the Mechanical Behavior of Biomedical Materials 1 2008 76 85
115. K.S. Katti, B. Mohanty, and D.R. Katti Nanomechanical properties of nacre Journal of Materials Research 21 2006 1237 1242
116. H. Gao, B. Ji, M.J. Buehler, and H. Yao Flaw tolerant bulk and surface nanostructures of biological systems Molecular and Cellular Biomechanics 1 2004 37 52
117. J.D. Currey Mechanics of mother of pearl in tension Proceedings of the Royal Society of London. Series B. Biological Sciences 196 1977 443 463
118. J. Cook, J.E. Gordon, C.C. Evans, and D.M. Marsh A mechanism for the control of crack propagation in all-brittle systems Proceedings of the Royal Society of London. Series A. Mathematical and Physical Sciences 282 1964 508 520
119. G. Mayer Rigid biological systems as models for synthetic composites Science 310 2005 1144 1147
120. B. Ji, and H. Gao Mechanical properties of nanostructure of biological materials Journal of the Mechanics and Physics of Solids 52 2004 1963 1990
121. R.M. McMeeking, and A.G. Evans Mechanics of transformation-toughening in brittle materials Journal of the American Ceramic Society 65 1982 242 246
122. A.G. Evans, Z. Suo, R.Z. Wang, I.A. Aksay, M.Y. He, and J.W. Hutchinson Model for the robust mechanical behavior of nacre Journal of Materials Research 16 2001 2475 2484
123. A.G. Evans, and F.W. Zok The physics and mechanics of fibre-reinforced brittle matrix composites Journal of Materials Science 29 1994 3857 3896
124. J.C. McNulty, F.W. Zok, G.M. Genin, and A.G. Evans Notch-sensitivity of fiber-reinforced ceramic-matrix composites: effects of inelastic straining and volume-dependent strength Journal of the American Ceramic Society 82 1999 1217 1228
125. F. Barthelat, C. Li, C. Comi, and H. Espinosa Mechanical properties of nacre constituents and their impact on mechanical performance Journal of Materials Research 21 2006 1977 1986
126. F. Barthelat, H. Tang, P.D. Zavattieri, C.-M. Li, and H.D. Espinosa On the mechanics of mother-of-pearl: a key feature in the material hierarchical structure Journal of the Mechanics and Physics of Solids 55 2007 306 337
127. K.S. Katti, D.R. Katti, S.M. Pradhan, and A. Bhosle Platelet interlocks are the key to toughness and strenght in nacre Journal of Materials Research 20 2005 1097 1100
128. R. Menig, M.H. Meyers, M.A. Meyers, and K.S. Vecchio Quasi-static and dynamic mechanical response of Haliotis rufescens (abalone) shells Acta Materialia 48 2000 2383 2398
129. J.H.E. Cartwright, and A.G. Checa The dynamics of nacre self-assembly Journal of The Royal Society Interface 4 2007 491 504
130. S. Wise Jr., and W. Hay Scanning electron microscopy of molluscan shell ultrastructures II. Observations of growth surfaces Transactions of the American Microscopical Society 87 1968 419 430
131. S. Wise Jr. Microarchitecture and deposition of gastropod nacre Science 167 1970 1486
132. G. Bevelander, and H. Nakahara An electron microscope study of the formation of the nacreous layer in the shell of certain bivalve molluscs Calcified Tissue International 3 1969 84 92
133. H. Nakahara Nacre formation in bivalve and gastropod molluscs Mechanisms and Phylogeny of Mineralization in Biological Systems 1991 343 350
134. W. Schmidt Studien über Pinnaperlen. I. Mitteilung: Über Prismenperlen von Pinna nobilis Zoomorphology 25 1932 235 277
135. C. Gregoire Topography of the organic components in mother-of-pearl Journal of Cell Biology 3 1957 797
136. K. Towe, and G. Hamilton Ultrastructure and inferred calcification of the mature and developing nacre in bivalve mollusks Calcified Tissue International 1 1967 306 318
137. H. Erben, and N. Watabe Crystal formation and growth in bivalve nacre Nature 248 1974 2
138. L. Addadi, and S. Weiner Interactions between acidic proteins and crystals: stereochemical requirements in biomineralization Proceedings of the National Academy of Sciences USA 82 1985 4110 4114
139. K. Wada Studies on the mineralization of the calcified tissue in molluscs-X. Histochemical determination of the nature of acid mucopolysaccharide in organic crystals Bulletin of the Japanese Society of Scientific Fisheries 30 1964 993 998
140. A. Lin, P. Chen, and M. Meyers The growth of nacre in the abalone shell Acta Biomaterialia 4 2008 131 138
141. K. Wada, and T. Fujinuki Biomineralization in bivalve molluscs with emphasis on the chemical composition of the extrapallial fluid The Mechanisms of Mineralization in the Invertebrates and Plants 1976 175 190
142. C. Little Ionic regulation in the queen conch, Strombus gigas (Gastropoda, Prosobranchia) Journal of Experimental Biology 46 1967 459
143. Y. Kitano, N. Kanamori, and S. Yoshioka Influence of chemical species on the crystal type of calcium carbonate The Mechanisms of Mineralization in the Invertebrates and Plants 1976
144. K. Wilbur, and A. Bernhardt Effects of amino acids, magnesium, and molluscan extrapallial fluid on crystallization of calcium carbonate: in vitro experiments The Biological Bulletin 166 1984 251
145. F. Song, X. Zhang, and Y. Bai Microstructure and characteristics in the organic matrix layers of nacre Journal of Materials Research 17 2002 1567 1570
146. R.A. Metzler, M. Abrecht, R.M. Olabisi, D. Ariosa, C.J. Johnson, B.H. Frazer, S.N. Coppersmith, and P. Gilbert Architecture of columnar nacre, and implications for its formation mechanism Physical Review Letters 98 2007 268102 268105
147. K. Saruwatari, T. Matsui, H. Mukai, H. Nagasawa, and T. Kogure Nucleation and growth of aragonite crystals at the growth front of nacres in pearl oyster, Pinctada fucata Biomaterials 30 2009 3028 3034
148. I. Weiss, V. Schönitzer, N. Eichner, and M. Sumper The chitin synthase involved in marine bivalve mollusk shell formation contains a myosin domain FEBS Letters 580 2006 1846 1852
149. I. Weiss, S. Kaufmann, B. Heiland, and M. Tanaka Covalent modification of chitin with silk-derivatives acts as an amphiphilic self-organizing template in nacre biomineralisation Journal of Structural Biology 167 2009 68 75
150. Y. Levi-Kalisman, G. Falini, L. Addadi, and S. Weiner Structure of the nacreous organic matrix of a bivalve mollusk shell examined in the hydrated state using cryo-TEM Journal of Structural Biology 135 2001 8 17
151. L. Pereira-Mouries, M. Almeida, C. Ribeiro, J. Peduzzi, M. Barthelemy, C. Milet, and E. Lopez Soluble silk-like organic matrix in the nacreous layer of the bivalve Pinctada maxima European Journal of Biochemistry 269 2002 4994 5003
152. L. Addadi, D. Joester, F. Nudelman, and S. Weiner Mollusk shell formation: a source of new concepts for understanding biomineralization processes Chemistry - A European Journal 12 2006 980 987
153. F. Nudelman, E. Shimoni, E. Klein, M. Rousseau, X. Bourrat, E. Lopez, L. Addadi, and S. Weiner Forming nacreous layer of the shells of the bivalves Atrina rigida and Pinctada margaritifera: an environmental- and cryo-scanning electron microscopy study Journal of Structural Biology 162 2008 290 300
154. A. Checa, J. Cartwright, and M. Willinger The key role of the surface membrane in why gastropod nacre grows in towers Proceedings of the National Academy of Sciences 106 2009 38
155. M. Crenshaw The soluble matrix from Mercenaria mercenaria shell Biomineralization 6 1972 6 11
156. E. Greenfield, D. Wilson, and M. Crenshaw Ionotropic nucleation of calcium carbonate by molluscan matrix Integrative and American Zoology 24 1984 925 932
157. A. Wheeler, J. George, and C. Evans Control of calcium carbonate nucleation and crystal growth by soluble matrix of oyster shell Science (New York, NY) 212 1981 1397 1398
158. M. Crenshaw, and H. Ristedt The histochemical localization of reactive groups in septal nacre from Nautilus pompilius L The Mechanisms of Mineralization in the Invertebrates and Plants 1976 University of South Carolina Press Columbia, SC 355 367
159. H. Thiele, and A. Awad Nucleation and oriented crystallization apatite in ionotropic gels Journal of Biomedical Materials Research 3 1969 431 442
160. M.A. Crenshaw, and H. Ristedt Histochemical and structural study of nautiloid septa nacre Biomineralization 8 1975 1 8
161. A. Wheeler, K. Rusenko, J. George, and C. Sikes Evaluation of calcium binding by molluscan shell organic matrix and its relevance to biomineralization Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 87 1987 953 960
162. S. Albeck, S. Weiner, and L. Addadi Polysaccharides of intracrystalline glycoproteins modulate calcite crystal growth in vitro Chemistry - A European Journal 2 1996 278 284
163. L. Addadi, J. Moradian, N. Shay, and S. Weiner A chemical model for the cooperation of sulfates and carboxylates in calcite crystal nucleation: relevance to biomineralization Proceedings of the National Academy of Sciences USA 84 1987 2732 2736
164. S. Mann Molecular recognition in biomineralization Nature 332 1988 119 124
165. L. Addadi, S. Raz, and S. Weiner Taking advantage of disorder: amorphous calcium carbonate and its roles in biomineralization Advanced Materials 15 2003 959 970
166. S. Weiner, Y. Levi-Kalisman, S. Raz, and L. Addadi Biologically formed amorphous calcium carbonate Connective Tissue Research 44 2003 214 218
167. A. Navrotsky Energetic clues to pathways to biomineralization: precursors, clusters, and nanoparticles Proceedings of the National Academy of Sciences of the United States of America 101 2004 12096
168. S. Weiner, I. Sagi, and L. Addadi Choosing the crystallization path less traveled Science (Washington) 309 2005 1027 1028
169. B. Hasse, H. Ehrenberg, J. Marxen, W. Becker, and M. Epple Calcium carbonate modifications in the mineralized shell of the freshwater snail Biomphalaria glabrata Chemistry European Journal, Weinheim 6 2000 3679 3685
170. J.C. Marxen, W. Becker, D. Finke, B. Hasse, and M. Epple Early mineralization in Biomphalaria glabrata: microscopic and structural results Journal of Molluscan Studies 69 2003 113
171. I. Weiss, N. Tuross, L. Addadi, and S. Weiner Mollusc larval shell formation: amorphous calcium carbonate is a precursor phase for aragonite Journal of Experimental Zoology 293 2002 478 491
172. R. Van Santen The Ostwald step rule The Journal of Physical Chemistry 88 1984 5768 5769
173. Y. Li, and S. Gregory Diffusion of ions in sea water and in deep-sea sediments Geochimica et Cosmochimica Acta 38 1974 703 714
174. M. Lauffer Theory of diffusion in gels Biophysical Journal 1 1961 205 213
175. E. Johnson, D. Berk, R. Jain, and W. Deen Hindered diffusion in agarose gels: test of effective medium model Biophysical Journal 70 1996 1017 1023
176. I. Weiss, S. Kaufmann, K. Mann, and M. Fritz Purification and characterization of perlucin and perlustrin, two new proteins from the shell of the mollusc Haliotis laevigata Biochemical and Biophysical Research Communications 267 2000 17 21
177. S. Elhadj, J. De Yoreo, J. Hoyer, and P. Dove Role of molecular charge and hydrophilicity in regulating the kinetics of crystal growth Proceedings of the National Academy of Sciences 103 2006 19237
178. A. Belcher, X. Wu, R. Christensen, P. Hansma, G. Stucky, and D. Morse Control of crystal phase switching and orientation by soluble mollusc-shell proteins Nature 391 1996 56 58
179. J. Thompson, G. Paloczi, J. Kindt, M. Michenfelder, B. Smith, G. Stucky, D. Morse, and P. Hansma Direct observation of the transition from calcite to aragonite growth as induced by abalone shell proteins Biophysical Journal 79 2000 3307 3312
180. G. Falini, S. Fermani, and A. Ripamonti Crystallization of calcium carbonate salts into beta-chitin scaffold Journal of inorganic biochemistry 91 2002 475 480
181. N. Gehrke, N. Nassif, N. Pinna, M. Antonietti, H. Gupta, and H. Cölfen Retrosynthesis of nacre via amorphous precursor particles Chemistry of Materials 17 2005 6514 6516
182. F. Heinemann, L. Treccani, and M. Fritz Abalone nacre insoluble matrix induces growth of flat and oriented aragonite crystals Biochemical and Biophysical Research Communications 344 2006 45 49
183. A. Becker, and M. Epple A High-throughput Crystallization Device to Study Biomineralization In Vitro 2005 Materials Research Society Warrendale, Pa 190
184. A.C. Maloof, D.P. Schrag, J.L. Crowley, and S.A. Bowring An expanded record of Early Cambrian carbon cycling from the Anti-Atlas Margin, Morocco, Canadian Journal of Earth Science 42 2005 2195 2216
185. B. Bjellqvist, G. Hughes, C. Pasquali, N. Paquet, F. Ravier, J. Sanchez, S. Frutiger, and D. Hochstrasser The focusing positions of polypeptides in immobilized pH gradients can be predicted from their amino acid sequences Electrophoresis 14 1993 1023 1031
186. M. Sarikaya, K.E. Gunnison, M. Yasrebi, and I.A. Aksay Mechanical property-microstructural relationships in abalone shell Materials Research Society Symposium Proceedings 174 1990 109 116
187. Y. Sugimura, J. Meyer, M.Y. He, H. Bart-Smith, J. Grenstedt, and A.G. Evans On the Mechanical Performance of Closed Al Alloy Foams Acta materialia 45 1997 5245 5259
188. W. Weibull A Statistical Distribution Function of Wide Applicability Journal of Applied Mechanics 18 1951 293 297