Skip to main content

Advertisement

Log in

Calcification and silicification: a comparative survey of the early stages of biomineralization

  • Review Article
  • Published:
Journal of Bone and Mineral Metabolism Aims and scope Submit manuscript

Abstract

Most of the studies on biomineralization have focused on calcification and silicification, the two systems that predominate in nature in the construction of skeletal or integumental hard tissues. They have, however, been studied separately, as if they were completely distinct processes, in spite of their several points of contact, especially as far as the organic–inorganic relationships during the early mineralization stages are concerned. A very tight association of the inorganic substance with organic macromolecules, in fact, initially characterizes both systems. Although the mechanism of biomineralization remains elusive, a number of old and new findings, which have been taken into account in this review, support the view that, both in calcification and in silicification, genetically controlled organic macromolecules induce the formation of composite, organic–inorganic nanoparticles, behave as templates for the subsequent assemblage of the nanoparticles into micro- to macroarchitectures of complex pattern, and, eventually, are mostly reabsorbed. There are still many gaps left in our knowledge of this process. Comparative studies of the two biomineralization systems may help to fill them.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Barthelat F (2007) Biomimetics for next generation materials. Philos Trans A Math Phys Eng Sci 365:2907–2919

    CAS  Google Scholar 

  2. Mann S (2001) Biomineralization. Principles and concepts in bioinorganic materials chemistry. Oxford University Press, Oxford

    Google Scholar 

  3. Wilt FH (2005) Developmental biology meets materials science: morphogenesis of biomineralized structures. Dev Biol 280:15–25

    PubMed  CAS  Google Scholar 

  4. Glimcher MJ (1976) Composition, structure, and organization of bone and other mineralized tissues and the mechanism of calcification. In: Greep RO, Astwood EB (eds) Handbook of physiology: endocrinology. American Physiological Society, Washington, pp 26–116

    Google Scholar 

  5. Mann S (1988) Molecular recognition in biomineralization. Nature (Lond) 332:119–124

    CAS  Google Scholar 

  6. Bonucci E (2007) Biological calcification. Normal and pathological processes in the early stages. Springer-Verlag, Berlin-Heidelberg

    Google Scholar 

  7. Veis A (2003) Mineralization in organic matrix frameworks. Rev Miner Geochem 54:249–289

    CAS  Google Scholar 

  8. Perry CC, Keeling-Tucker T (2000) Biosilicification: the role of the organic matrix in structure control. J Biol Inorg Chem 5:537–550

    PubMed  CAS  Google Scholar 

  9. Pouget E, Dujardin E, Cavalier A, Moreac A, Valéry C, Marchi-Artzner V, Weiss T, Renault A, Paternostre M, Artzner F (2007) Hierarchical architectures by synergy between dynamical template self-assembly and biomineralization. Nat Mater 6:434–439

    PubMed  CAS  Google Scholar 

  10. Gröger C, Lutz K, Brunner E (2008) Biomolecular self-assembly and its relevance in silica biomineralization. Cell Biochem Biophys 50:23–39

    PubMed  Google Scholar 

  11. Kröger N, Deutzmann R, Bergsdorf C, Sumper M (2000) Species-specific polyamines from diatoms control silica morphology. Proc Natl Acad Sci USA 97:14133–14138

    PubMed  Google Scholar 

  12. Poulsen N, Sumper M, Kröger N (2003) Biosilica formation in diatoms: characterization of native silaffin-2 and its role in silica morphogenesis. Proc Natl Acad Sci USA 100:12075–12080

    PubMed  CAS  Google Scholar 

  13. Frigeri LG, Radabaugh TR, Haynes PA, Hildebrand M (2006) Identification of proteins from a cell wall fraction of the diatom Thalassiosira pseudonana: insights into silica structure formation. Mol Cell Proteomics 5:182–193

    PubMed  CAS  Google Scholar 

  14. Patwardhan SV, Maheshwari R, Mukharjee N, Kiick KL, Clarson SJ (2006) Conformation and assembly of polypeptide scaffolds in templating the synthesis of silica: an example of a polylysine macromolecular “switch”. Biomacromolecules 7:491–497

    PubMed  CAS  Google Scholar 

  15. Wenzl S, Hett R, Richthammer P, Sumper M (2008) Silacidins: highly acidic phosphopeptides from diatom shells assist in silica precipitation in vitro. Angew Chem Int Ed Engl 47:1729–1732

    PubMed  CAS  Google Scholar 

  16. Cha JN, Shimizu K, Zhou Y, Christiansen SC, Chmelka BF, Stucky GD, Morse DE (1999) 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

    PubMed  CAS  Google Scholar 

  17. Weaver JC, Morse DE (2003) Molecular biology of demosponge axial filaments and their roles in biosilicification. Microsc Res Tech 62:356–367

    PubMed  CAS  Google Scholar 

  18. Schröder HC, Natalio F, Shukoor I, Tremel W, Schlossmacher U, Wang X, Müller WEG (2007) Apposition of silica lamellae during growth of spicules in the demosponge Suberites domuncula: biological/biochemical studies and chemical/biomimetical confirmation. J Struct Biol 159:325–334

    PubMed  Google Scholar 

  19. Shimizu K, Cha J, Stucky GD, Morse DE (1998) Silicatein α: cathepsin L-like protein in sponge biosilica. Proc Natl Acad Sci USA 95:6234–6238

    PubMed  CAS  Google Scholar 

  20. Eckert C, Schröder HC, Brandt D, Perovic-Ottstadt S, Müller WEG (2006) Histochemical and electron microscopic analysis of spiculogenesis in the demosponge Suberites domuncula. J Histochem Cytochem 54:1031–1040

    PubMed  CAS  Google Scholar 

  21. Matsunaga S, Sakai R, Jimbo M, Kamiya H (2007) Long-chain polyamines (LCPAs) from marine sponge: possible implication in spicule formation. Chembiochem 8:1729–1735

    PubMed  CAS  Google Scholar 

  22. Tomczak MM, Glawe DD, Drummy LF, Lawrence CG, Stone MO, Perry CC, Pochan DJ, Deming TJ, Naik RR (2005) Polypeptide-templated synthesis of hexagonal silica platelets. J Am Chem Soc 127:12577–12582

    PubMed  CAS  Google Scholar 

  23. Foo CWP, Huang J, Kaplan DL (2004) Lessons from seashells: silica mineralization via protein templating. Trends Biotechnol 22:577–585

    PubMed  CAS  Google Scholar 

  24. Shchipunov YA, Kojima A, Imae T (2005) Polysaccharides as a template for silicate generated by sol-gel processes. J Colloid Interface Sci 285:574–580

    PubMed  CAS  Google Scholar 

  25. Heredia A, van der Strate HJ, Delgadillo I, Basiuk VA, Vrieling EG (2008) Analysis of organo-silica interactions during valve formation in synchronously growing cells of the diatom Navicula pelliculosa. Chembiochem 9:573–584

    PubMed  CAS  Google Scholar 

  26. Bonucci E (1967) Fine structure of early cartilage calcification. J Ultrastruct Res 20:33–50

    PubMed  CAS  Google Scholar 

  27. Bonucci E, Reurink J (1978) The fine structure of decalcified cartilage and bone: a comparison between decalcification procedures performed before and after embedding. Calcif Tissue Res 25:179–190

    PubMed  CAS  Google Scholar 

  28. Bonucci E (1971) The locus of initial calcification in cartilage and bone. Clin Orthop 78:108–139

    PubMed  CAS  Google Scholar 

  29. Bonucci E (2002) Crystal ghosts and biological mineralization: fancy spectres in an old castle, or neglected structures worthy of belief? J Bone Miner Metab 20:249–265

    PubMed  Google Scholar 

  30. Bonucci E (1969) Further investigation on the organic/inorganic relationships in calcifying cartilage. Calcif Tissue Res 3:38–54

    PubMed  CAS  Google Scholar 

  31. Appleton J (1971) Ultrastructural observations on the inorganic/organic relationships in early cartilage calcification. Calcif Tissue Res 7:307–317

    PubMed  CAS  Google Scholar 

  32. Sundström B, Takuma S (1971) A further contribution on the ultrastructure of calcifying cartilage. J Ultrastruct Res 36:419–424

    PubMed  Google Scholar 

  33. Davis WL, Jones RG, Knight JP, Hagler HK (1982) Cartilage calcification: an ultrastructural, histochemical, and analytical X-ray microprobe study of the zone of calcification in normal avian epiphyseal growth plate. J Histochem Cytochem 30:221–234

    PubMed  CAS  Google Scholar 

  34. Scherft JP, Moskalewski S (1984) The amount of proteoglycans in cartilage matrix and the onset of mineralization. Metab Bone Dis Relat Res 5:195–203

    PubMed  CAS  Google Scholar 

  35. Shepard N (1992) Role of proteoglycans in calcification. In: Bonucci E (ed) Calcification in biological systems. CRC Press, Boca Raton, pp 41–58

    Google Scholar 

  36. Dong W, Warshawsky H (1995) Failure to demonstrate a protein coat on enamel crystallites by morphological means. Arch Oral Biol 40:321–330

    PubMed  CAS  Google Scholar 

  37. Sone ED, Weiner S, Addadi L (2007) Biomineralization of the limpet teeth: a cryo-TEM study of the organic matrix and the onset of mineral deposition. J Struct Biol 158:428–444

    PubMed  CAS  Google Scholar 

  38. Warshawsky H (1989) Organization of crystals in enamel. Anat Rec 224:242–262

    PubMed  CAS  Google Scholar 

  39. Landis WJ, Glimcher MJ (1978) Electron diffraction and electron probe microanalysis of the mineral phase of bone tissue prepared by anhydrous techniques. J Ultrastruct Res 63:188–223

    PubMed  CAS  Google Scholar 

  40. Lee DD, Landis WJ, Glimcher MJ (1986) The solid, calcium-phosphate mineral phases in embryonic chick bone characterized by high-voltage electron diffraction. J Bone Miner Res 1:425–432

    Article  PubMed  CAS  Google Scholar 

  41. Bonucci E, Lozupone E, Silvestrini G, Favia A, Mocetti P (1994) Morphological studies of hypomineralized enamel of rat pups on calcium-deficient diet, and of its changes after return to normal diet. Anat Rec 239:379–395

    PubMed  CAS  Google Scholar 

  42. Nanci A (2003) Ten Cate’s oral histology: development, structure, and function, 6th edn. Mosby, St. Louis

    Google Scholar 

  43. Pugliarello MC, Vittur F, De Bernard B, Bonucci E, Ascenzi A (1970) Chemical modifications in osteones during calcification. Calcif Tissue Res 5:108–114

    PubMed  CAS  Google Scholar 

  44. Huffman NT, Keightley JA, Chaoying C, Midura RJ, Lovitch D, Veno PA, Dallas SL, Gorski JP (2007) Association of specific proteolytic processing of bone sialoprotein and bone acidic glycoprotein-75 with mineralization within biomineralization foci. J Biol Chem 282:26002–26013

    PubMed  CAS  Google Scholar 

  45. Satoyoshi M, Kawata A, Koizumi T, Inoue K, Itohara S, Teranaka T, Mikuni-Takagaki Y (2001) Matrix metalloproteinase-2 in dentin matrix mineralization. J Endod 27:462–466

    PubMed  CAS  Google Scholar 

  46. Hazelaar S, van der Strate HJ, Gieskes WW, Vrieling EG (2003) Possible role of ubiquitin in silica biomineralization in diatoms: identification of a homologue with high silica affinity. Biomol Eng 20:163–169

    PubMed  CAS  Google Scholar 

  47. Müller WEG, Wang X, Kropf K, Ushijima H, Geurtsen W, Eckert C, Tahir MN, Tremel W, Boreiko A, Schlossmacher U, Li J, Schröder HC (2008) Bioorganic/inorganic hybrid composition of sponge spicules: matrix of the giant spicules and of the comitalia of the deep sea hexactinellid Monorhaphis. J Struct Biol 161:188–203

    PubMed  Google Scholar 

  48. Müller WE, Boreiko A, Wang X, Belikov SI, Wiens M, Grebenjuk VA, Schlossmacher U, Schröder HC (2007) Silicateins, the major biosilica forming enzymes present in demosponges: protein analysis and phylogenetic relationship. Gene (Amst) 395:62–71

    Google Scholar 

  49. Müller WE, Boreiko A, Schlossmacher U, Wang X, Eckert C, Kropf K, Li J, Schröder HC (2008) Identification of a silicatein(-related) protease in the giant spicules of the deep-sea hexactinellid Monorhaphis chuni. J Exp Biol 211:300–309

    PubMed  Google Scholar 

  50. Watabe N (1963) Decalcification of thin sections for electron microscope studies of crystal-matrix relationships in mollusc shells. J Cell Biol 18:701–703

    PubMed  CAS  Google Scholar 

  51. Meenakshi VR, Hare PE, Wilbur KM (1971) Amino acids of the organic matrix of neogastropod shells. Comp Biochem Physiol 40B:1037–1043

    Google Scholar 

  52. Crenshaw MA (1972) The soluble matrix from Mercenaria mercenaria shell. Biomineralization 6:6–11

    CAS  Google Scholar 

  53. Wong V, Saleuddin ASM (1972) Fine structure of normal and regenerated shell of Helisoma duryi duryi. Can J Zool 50:1563–1568

    Google Scholar 

  54. Crenshaw MA, Ristedt H (1976) The histochemical localization of reactive groups in septal nacre from Nautilus pompilius L. In: Watabe N, Wilbur KM (eds) The mechanisms of mineralization in the invertebrates and plants. University of South Carolina Press, Columbia, pp 355–367

    Google Scholar 

  55. Albeck S, Addadi L, Weiner S (1996) Regulation of calcite crystal morphology by intracrystalline acidic proteins and glycoproteins. Connect Tissue Res 35:365–370

    PubMed  CAS  Google Scholar 

  56. Shen X, Belcher AM, Hansma PK, Stucky GD, Morse DE (1997) Molecular cloning and characterization of Lustrin A, a matrix protein from shell and pearl nacre of Haliotis rufescens. J Biol Chem 272:32472–32481

    PubMed  CAS  Google Scholar 

  57. Miyashita T, Takagi R, Okushima M, Nakano S, Miyamoto H, Nishikawa E, Matsushiro A (2000) Complementary DNA cloning and characterization of Pearlin, a new class of matrix protein in the nacreous layer of oyster pearls. Mar Biotechnol 2:409–418

    PubMed  CAS  Google Scholar 

  58. Dauphin Y (2002) Comparison of the soluble matrices of the calcitic prismatic layer of Pinna nobilis (Mollusca, Bivalvia, Pteriomorpha). Comp Biochem Physiol A Mol Integr Physiol 132:577–590

    PubMed  CAS  Google Scholar 

  59. Tong H, Hu J, Ma W, Zhong G, Yao S, Cao N (2002) In situ analysis of the organic framework in the prismatic layer of mollusc shell. Biomaterials 23:2593–2598

    PubMed  CAS  Google Scholar 

  60. Pokroy B, Quintana JP, Caspi EN, Berner A, Zolotoyabko E (2004) Anisotropic lattice distortions in biogenic aragonite. Nat Mater 3:900–902

    PubMed  CAS  Google Scholar 

  61. Berman A, Addadi L, Kvick Å, Leiserowitz L, Nelson M, Weiner S (1990) Intercalation of sea urchin proteins in calcite: study of a crystalline composite material. Science 250:664–667

    PubMed  CAS  Google Scholar 

  62. Benson SC, Wilt FH (1992) Calcification of spicules in the sea urchin embryo. In: Bonucci E (ed) Calcification in biological systems. CRC Press, Boca Raton, pp 157–178

    Google Scholar 

  63. Cho JW, Partin JS, Lennarz WJ (1996) A technique for detecting matrix proteins in the crystalline spicule of the sea urchin embryo. Proc Natl Acad Sci USA 93:1282–1286

    PubMed  CAS  Google Scholar 

  64. Ameye L, Compère P, Dille J, Dubois P (1998) Ultrastructure and cytochemistry of the early calcification site and of its mineralization organic matrix in Paracentrotus lividus (Echinodermata: Echinoidea). Histochem Cell Biol 110:285–294

    PubMed  CAS  Google Scholar 

  65. Wilt FH (1999) Matrix and mineral in the sea urchin larval skeleton. J Struct Biol 126:216–226

    PubMed  CAS  Google Scholar 

  66. Wilt FH (2002) Biomineralization of the spicules of sea urchin embryos. Zool Sci 19:253–261

    PubMed  CAS  Google Scholar 

  67. Kitajima T, Urakami H (2000) Differential distribution of spicule matrix proteins in the sea urchin embryo skeleton. Dev Growth Differ 42:295–306

    PubMed  CAS  Google Scholar 

  68. Urry LA, Hamilton PC, Killian CE, Wilt FH (2000) Expression of spicule matrix proteins in the sea urchin embryo during normal and experimentally altered spiculogenesis. Dev Biol 225:201–213

    PubMed  CAS  Google Scholar 

  69. Ingersoll EP, McDonald KL, Wilt FH (2003) Ultrastructural localization of spicule matrix proteins in normal and metalloproteinase inhibitor-treated sea urchin primary mesenchymal cells. J Exp Zool Part A Comp Exp Biol 300:101–112

    Google Scholar 

  70. Seto J, Zhang Y, Hamilton P, Wilt F (2004) The localization of occluded matrix proteins in calcareous spicules of sea urchin larvae. J Struct Biol 148:123–130

    PubMed  CAS  Google Scholar 

  71. Allemand D, Bénazet-Tambutté S (1996) Dynamics of calcification in the Mediterranean red coral, Corallium rubrum (Linnaeus) (Cnidaria, Octocorallia). J Exp Zool 276:270–278

    Google Scholar 

  72. Rahman MA, Isa Y, Uehara T (2005) Proteins of calcified endoskeleton: II.Partial amino acid sequences of endoskeletal proteins and the characterization of proteinaceous organic matrix of spicules from the alcyonarian, Synularia polydactyla. Proteomics 5:885–893

    PubMed  CAS  Google Scholar 

  73. Kingsley RJ, Watabe N (1982) Ultrastructural investigation of spicule formation in the gorgonian Leptogorgia virgulata (Lamarck) (Coelenterata: Gorgonacea). Cell Tissue Res 223:325–334

    PubMed  CAS  Google Scholar 

  74. Lambert G, Lambert CC (1996) Spicule formation in the New Zealand ascidian Pyura pachydermatina (Chordata, Ascidiacea). Connect Tissue Res 34:263–269

    PubMed  CAS  Google Scholar 

  75. Lambert G (1998) Spicule formation in the solitary ascidian Bathypera feminalba (Ascidiacea, Pyuridae). Invertebr Biol 117:341–349

    Google Scholar 

  76. Aizenberg J, Ilan M, Weiner S, Addadi L (1996) Intracrystalline macromolecules are involved in the morphogenesis of calcitic sponge spicules. Connect Tissue Res 34:255–261

    PubMed  CAS  Google Scholar 

  77. Westbroek P, de Jong EW, Dam W, Bosch L (1973) Soluble intracrystalline polysaccharides from coccoliths of Coccolithus huxleyi (Lohmann) Kamptner (I). Calcif Tissue Res 12:227–238

    PubMed  CAS  Google Scholar 

  78. Marsh ME, Chang D-K, King GC (1992) Isolation and characterization of a novel acidic polysaccharide containing tartrate and glyoxylate residues from the mineralized scales of a unicellular coccolithophorid alga Pleurochrysis carterae. J Biol Chem 267:20507–20512

    PubMed  CAS  Google Scholar 

  79. Bonucci E, Derenzini M, Marinozzi V (1973) The organic-inorganic relationship in calcified mitochondria. J Cell Biol 59:185–211

    PubMed  CAS  Google Scholar 

  80. Doyle IR, Ryall RL, Marshall VR (1991) Inclusion of proteins into calcium oxalate crystals precipitated from human urine: a highly selective phenomenon. Clin Chem 37:1589–1594

    PubMed  CAS  Google Scholar 

  81. Ryall RL, Fleming DE, Grover PK, Chauvet M, Dean CJ, Marshall VR (2000) The hole truth: intracrystalline proteins and calcium oxalate kidney stones. Mol Urol 4:391–402

    PubMed  CAS  Google Scholar 

  82. Ryall RL, Fleming DE, Doyle IR, Evans NA, Dean CJ, Marshall VR (2001) Intracrystalline proteins and the hidden ultrastructure of calcium oxalate urinary crystals: implications for kidney stone formation. J Struct Biol 134:5–14

    Google Scholar 

  83. Khan SR, Glenton PA, Backov R, Talham DR (2002) Presence of lipids in urine, crystals and stones: implications for the formation of kidney stones. Kidney Int 62:2062–2072

    PubMed  CAS  Google Scholar 

  84. Walton RC, Kavanagh JP, Heywood BR (2003) The density and protein content of calcium oxalate crystals precipitated from human urine: a tool to investigate ultrastructure and the fractional volume occupied by organic matrix. J Struct Biol 143:14–23

    PubMed  CAS  Google Scholar 

  85. Berman A, Addadi L, Weiner S (1988) Interactions of sea-urchin skeleton macromolecules with growing calcite crystals: a study of intracrystalline proteins. Nature (Lond) 331:546–548

    CAS  Google Scholar 

  86. Gayathri S, Lakshminarayanan R, Weaver JC, Morse DE, Kini RM, Valiyaveettil S (2007) In vitro study of magnesium-calcite biomineralization in the skeletal materials of the seastar Pisaster giganteus. Chemistry 13:3262–3268

    PubMed  CAS  Google Scholar 

  87. Marin F, Pokroy B, Luquet G, Layrolle P, De Groot K (2007) Protein mapping of calcium carbonate biominerals by immunogold. Biomaterials 28:2368–2377

    PubMed  CAS  Google Scholar 

  88. Nudelman F, Gotliv BA, Addadi L, Weiner S (2006) Mollusk shell formation: mapping the distribution of organic matrix components underlying a single aragonite tablet in nacre. J Struct Biol 153:176–187

    PubMed  CAS  Google Scholar 

  89. Pokroy B, Fitch AN, Lee PL, Quintana JP, Caspi EN, Zolotoyabko E (2006) Anisotropic lattice distortions in the mollusk-made aragonite: a widespread phenomenon. J Struct Biol 153:145–150

    PubMed  CAS  Google Scholar 

  90. Pokroy B, Kapon M, Marin F, Adir N, Zolotoyabko E (2007) Protein-induced, previously unidentified twin form of calcite. Proc Natl Acad Sci USA 104:7337–7341

    PubMed  CAS  Google Scholar 

  91. Przenioslo R, Stolarski J, Mazur M, Brunelli M (2008) Hierarchically structured scleractinian coral biocrystals. J Struct Biol 161:74–82

    PubMed  CAS  Google Scholar 

  92. Cuif J-P, Dauphin Y (2005) The two-step mode of growth in the scleractinian coral skeletons from the micrometre to the overall scale. J Struct Biol 150:319–331

    PubMed  Google Scholar 

  93. Bigi A, Boanini E, Gazzano M, Rubini K, Torricelli P (2004) Nanocrystalline hydroxyapatite-polyaspartate composites. Biomed Mater Eng 14:573–579

    PubMed  CAS  Google Scholar 

  94. Boanini E, Torricelli P, Gazzano M, Giardino R, Bigi A (2006) Nanocomposites of hydroxyapatite with aspartic acid and glutamic acid and their interaction with osteoblast-like cells. Biomaterials 27:4428–4433

    PubMed  CAS  Google Scholar 

  95. Li H, Estroff LA (2007) Hydrogels coupled with self-assembled monolayers: an in vitro matrix to study calcite biomineralization. J Am Med Soc 129:5480–5483

    CAS  Google Scholar 

  96. Sethmann I, Wörheide G (2008) Structure and composition of calcareous sponge spicules: a review and comparison to structurally related biominerals. Micron 39:209–228

    PubMed  CAS  Google Scholar 

  97. Kröger N, Lehmann G, Rachel R, Sumper M (1997) Characterization of a 200-kDa protein that is specifically associated with a silica-based substructure of the cell wall. Eur J Biochem 250:99–105

    PubMed  Google Scholar 

  98. Kröger N (2007) Prescribing diatom morphology: toward genetic engineering of biological nanomaterials. Curr Opin Chem Biol 11:662–669

    PubMed  Google Scholar 

  99. Tesson B, Masse S, Laurenti G, Maquet J, Livage J, Martin-Jézéquel V, Coradin T (2008) Contribution of multi-nuclear solid state NMR to the characterization of the Thalassiosira pseudonana diatom cell wall. Anal Bioanal Chem 390:1889–1898

    PubMed  CAS  Google Scholar 

  100. Croce G, Viterbo D, Milanesio M, Amenitsch H (2007) A mesoporous pattern created by nature in spicules from Thetya aurantium sponge. Biophys J 92:288–292

    PubMed  CAS  Google Scholar 

  101. Shchipunov YA, Karpenko TY (2004) Hybrid polysaccharide-silica nanocomposites prepared by the sol-gel technique. Langmuir 20:3882–3887

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ermanno Bonucci.

About this article

Cite this article

Bonucci, E. Calcification and silicification: a comparative survey of the early stages of biomineralization. J Bone Miner Metab 27, 255–264 (2009). https://doi.org/10.1007/s00774-009-0061-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00774-009-0061-y

Keywords

Navigation