Biomineralization proteins: from vertebrates to bacteria
Lijun WANG, Marit NILSEN-HAMILTON
Biomineralization proteins: from vertebrates to bacteria
Biomineralization processes are frequently found in nature. Living organisms use various strategies to create highly ordered and hierarchical mineral structures under physiologic conditions in which the temperatures and pressures are much lower than those required to form the same mineralized structures by chemical synthesis. Although the mechanism of biomineralization remains elusive, proteins have been found responsible for the formation of such mineral structures in many cases. These proteins are active components in the process of biomineralization. The mechanisms by which their function can vary from providing active organic matrices that control the formation of specific mineral structures to being catalysts that facilitate the crystallization of certain metal ions. This review summarizes the current understanding of the functions of several representative biomineralization proteins from vertebrates to bacteria in the hopes of providing useful insight and guidance for further elucidation of mechanisms of biomineralization processes in living organisms.
biomineralization proteins / structure-function relationships / self-assembly / nanoparticles
[1] |
Addadi L, Weiner S (1985). Interactions between acidic proteins and crystals: stereochemical requirements in biomineralization. Proc Natl Acad Sci USA, 82(12): 4110–4114
CrossRef
Pubmed
Google scholar
|
[2] |
Aichmayer B, Margolis H C, Sigel R, Yamakoshi Y, Simmer J P, Fratzl P (2005). The onset of amelogenin nanosphere aggregation studied by small-angle X-ray scattering and dynamic light scattering. J Struct Biol, 151(3): 239–249
CrossRef
Pubmed
Google scholar
|
[3] |
Amemiya Y, Arakaki A, Staniland S S, Tanaka T, Matsunaga T (2007). Controlled formation of magnetite crystal by partial oxidation of ferrous hydroxide in the presence of recombinant magnetotactic bacterial protein Mms6. Biomaterials, 28(35): 5381–5389
CrossRef
Pubmed
Google scholar
|
[4] |
Arakaki A, Webb J, Matsunaga T (2003). A novel protein tightly bound to bacterial magnetic particles in Magnetospirillum magneticum strain AMB-1. J Biol Chem, 278(10): 8745–8750
CrossRef
Pubmed
Google scholar
|
[5] |
Balkwill D L, Maratea D, Blakemore R P (1980). Ultrastructure of a magnetotactic spirillum. J Bacteriol, 141(3): 1399–1408
Pubmed
|
[6] |
Bazylinski D A, Frankel R B (2004). Magnetosome formation in prokaryotes. Nat Rev Microbiol, 2(3): 217–230
CrossRef
Pubmed
Google scholar
|
[7] |
Bell P E, Mills A L, Herman J S (1987). Biogeochemical donditions favoring magnetite formation during anaerobic iron reduction. Appl Environ Microbiol, 53(11): 2610–2616
Pubmed
|
[8] |
Berthet-Colominas C, Miller A, White S W (1979). Structural study of the calcifying collagen in turkey leg tendons. J Mol Biol, 134(3): 431–445
CrossRef
Pubmed
Google scholar
|
[9] |
Blakemore R (1975). Magnetotactic bacteria. Science, 190(4212): 377–379
CrossRef
Pubmed
Google scholar
|
[10] |
Blakemore R P, Maratea D, Wolfe R S (1979). Isolation and pure culture of a freshwater magnetic spirillum in chemically defined medium. J Bacteriol, 140(2): 720–729
Pubmed
|
[11] |
Bonucci E (2009). Calcification and silicification: a comparative survey of the early stages of biomineralization. J Bone Miner Metab, 27(3): 255–264
CrossRef
Pubmed
Google scholar
|
[12] |
Brinker C J, Scherrer G W (1990). Sol-gel science: the chemistry of sol-gel processing. New York: Academic Press
|
[13] |
Brunner E, Gröger C, Lutz K, Richthammer P, Spinde K, Sumper M (2009). Analytical studies of silica biomineralization: towards an understanding of silica processing by diatoms. Appl Microbiol Biotechnol, 84(4): 607–616
CrossRef
Pubmed
Google scholar
|
[14] |
Brutchey R L, Cheng G, Gu Q, Morse D E (2008). Positive temperature coefficient of resistivity in donor-doped BaTiO3 ceramics derived from nanocrystals synthesized at low temperature. Adv Mater, 20(5): 1029–1033
CrossRef
Google scholar
|
[15] |
Brutchey R L, Morse D E (2006). Template-free, low-temperature synthesis of crystalline barium titanate nanoparticles under bio-inspired conditions. Angew Chem Int Ed Engl, 45(39): 6564–6566
CrossRef
Pubmed
Google scholar
|
[16] |
Brutchey R L, Morse D E (2008). Silicatein and the translation of its molecular mechanism of biosilicification into low temperature nanomaterial synthesis. Chem Rev, 108(11): 4915–4934
CrossRef
Pubmed
Google scholar
|
[17] |
Cha J N, Shimizu K, Zhou Y, Christiansen S C, Chmelka B F, Stucky G D, Morse D E (1999). Silicatein filaments and subunits from a marine sponge direct the polymerization of silica and silicones in vitro. Proc Natl Acad Sci USA, 96(2): 361–365
CrossRef
Pubmed
Google scholar
|
[18] |
Chen C L, Bromley K M, Moradian-Oldak J, DeYoreo J J (2011). In situ AFM study of amelogenin assembly and disassembly dynamics on charged surfaces provides insights on matrix protein self-assembly. J Am Chem Soc, 133(43): 17406–17413
CrossRef
Pubmed
Google scholar
|
[19] |
Cölfen H (2010). Biomineralization: A crystal-clear view. Nat Mater, 9(12): 960–961
CrossRef
Pubmed
Google scholar
|
[20] |
Cowan P M, McGavin S, North A C T (1955). The polypeptide chain configuration of collagen. Nature, 176(4492): 1062–1064
CrossRef
Pubmed
Google scholar
|
[21] |
Crookes-Goodson W J, Slocik J M, Naik R R (2008). Bio-directed synthesis and assembly of nanomaterials. Chem Soc Rev, 37(11): 2403–2412
CrossRef
Pubmed
Google scholar
|
[22] |
Daculsi G, Kerebel B (1978). High-resolution electron microscope study of human enamel crystallites: size, shape, and growth. J Ultrastruct Res, 65(2): 163–172
CrossRef
Pubmed
Google scholar
|
[23] |
Dey A, Bomans P H H, Müller F A, Will J, Frederik P M, de With G, Sommerdijk N A J M (2010). The role of prenucleation clusters in surface-induced calcium phosphate crystallization. Nat Mater, 9(12): 1010–1014
CrossRef
Pubmed
Google scholar
|
[24] |
Diekwisch T G H, Berman B J, Gentner S, Slavkin H C (1995). Initial enamel crystals are not spatially associated with mineralized dentine. Cell Tissue Res, 279(1): 149–167
CrossRef
Pubmed
Google scholar
|
[25] |
Du C, Falini G, Fermani S, Abbott C, Moradian-Oldak J (2005a). Corrections and clarifications. Science, 309(5744): 2166
CrossRef
Pubmed
Google scholar
|
[26] |
Du C, Falini G, Fermani S, Abbott C, Moradian-Oldak J (2005b). Supramolecular assembly of amelogenin nanospheres into birefringent microribbons. Science, 307(5714): 1450–1454
CrossRef
Pubmed
Google scholar
|
[27] |
Dugdale R C, Wilkerson F P (1998). Silicate regulation of new production in the equatorial Pacific upwelling. Nature, 391(6664): 270–273
CrossRef
Google scholar
|
[28] |
Dunin-Borkowski R E, McCartney M R, Frankel R B, Bazylinski D A, Pósfai M, Buseck P R (1998). Magnetic microstructure of magnetotactic bacteria by electron holography. Science, 282(5395): 1868–1870
CrossRef
Pubmed
Google scholar
|
[29] |
Eastoe J E (1979). Enamel protein chemistry—past, present and future. J Dent Res, 58(Spec Issue B suppl): 753–764
CrossRef
Pubmed
Google scholar
|
[30] |
Evans J W, Thiel P A (2010). Chemistry. A little chemistry helps the big get bigger. Science, 330(6004): 599–600
CrossRef
Pubmed
Google scholar
|
[31] |
Faivre D, Böttger L H, Matzanke B F, Schüler D (2007). Intracellular magnetite biomineralization in bacteria proceeds by a distinct pathway involving membrane-bound ferritin and an iron(II) species. Angew Chem Int Ed Engl, 46(44): 8495–8499
CrossRef
Pubmed
Google scholar
|
[32] |
Faivre D, Schüler D (2008). Magnetotactic bacteria and magnetosomes. Chem Rev, 108(11): 4875–4898
CrossRef
Pubmed
Google scholar
|
[33] |
Falciatore A, Bowler C (2002). Revealing the molecular secrets of marine diatoms. Annu Rev Plant Biol, 53(1): 109–130
CrossRef
Pubmed
Google scholar
|
[34] |
Fincham A G, Leung W, Tan J and Moradian-Oldak J (1998). Does amelogenin nanosphere assembly proceed through intermediary-sized structures? Connect Tissue Res, 38(1–4): 237–240; discussion 241–236
|
[35] |
Fincham A G, Moradian-Oldak J, Diekwisch T G, Lyaruu D M, Wright J T, Bringas P Jr, Slavkin H C (1995). Evidence for amelogenin “nanospheres” as functional components of secretory-stage enamel matrix. J Struct Biol, 115(1): 50–59
CrossRef
Pubmed
Google scholar
|
[36] |
Fincham A G, Moradian-Oldak J, Simmer J P, Sarte P, Lau E C, Diekwisch T, Slavkin H C (1994). Self-assembly of a recombinant amelogenin protein generates supramolecular structures. J Struct Biol, 112(2): 103–109
CrossRef
Pubmed
Google scholar
|
[37] |
Frankel R B, Bazylinski D A, Johnson M S, Taylor B L (1997). Magneto-aerotaxis in marine coccoid bacteria. Biophys J, 73(2): 994–1000
CrossRef
Pubmed
Google scholar
|
[38] |
Frankel R B, Blakemore R P, Wolfe R S (1979). Magnetite in freshwater magnetotactic bacteria. Science, 203(4387): 1355–1356
CrossRef
Pubmed
Google scholar
|
[39] |
Friddle R W, Battle K, Trubetskoy V, Tao J, Salter E A, Moradian-Oldak J, De Yoreo J J, Wierzbicki A (2011). Single-molecule determination of the face-specific adsorption of Amelogenin’s C-terminus on hydroxyapatite. Angew Chem Int Ed Engl, 50(33): 7541–7545
CrossRef
Pubmed
Google scholar
|
[40] |
Glimcher M J (1959). Molecular biology of mineralized tissues with particular reference to bone. Rev Mod Phys, 31(2): 359–393
CrossRef
Google scholar
|
[41] |
Glimcher M J, Bonar L C, Grynpas M D, Landis W J, Roufosse A H (1981). Recent studies of bone mineral: Is the amorphous calcium phosphate theory valid? J Cryst Growth, 53(1): 100–119
CrossRef
Google scholar
|
[42] |
Gorby Y A, Beveridge T J, Blakemore R P (1988). Characterization of the bacterial magnetosome membrane. J Bacteriol, 170(2): 834–841
Pubmed
|
[43] |
Gorski J P (1992). Acidic phosphoproteins from bone matrix: a structural rationalization of their role in biomineralization. Calcif Tissue Int, 50(5): 391–396
CrossRef
Pubmed
Google scholar
|
[44] |
Gower L B (2008). Biomimetic model systems for investigating the amorphous precursor pathway and its role in biomineralization. Chem Rev, 108(11): 4551–4627
CrossRef
Pubmed
Google scholar
|
[45] |
Grynpas M D, Omelon S (2007). Transient precursor strategy or very small biological apatite crystals? Bone, 41(2): 162–164
CrossRef
Pubmed
Google scholar
|
[46] |
Hildebrand M (2003). Biological processing of nanostructured silica in diatoms. Prog Org Coat, 47(3–4): 256–266
CrossRef
Google scholar
|
[47] |
Hildebrand M (2008). Diatoms, biomineralization processes, and genomics. Chem Rev, 108(11): 4855–4874
CrossRef
Pubmed
Google scholar
|
[48] |
Hodge A, Petruska J (1963). Aspects of Protein Structure. New York: Academic Press
|
[49] |
Hulmes D J, Wess T J, Prockop D J, Fratzl P (1995). Radial packing, order, and disorder in collagen fibrils. Biophys J, 68(5): 1661–1670
CrossRef
Pubmed
Google scholar
|
[50] |
Kaluzhnaya O, Belikova A, Podolskaya E, Krasko A, Müller W, Belikov S (2007). Identification of silicateins in freshwater sponge Lubomirskia baicalensis. Mol Biol, 41(4): 554–561
CrossRef
Google scholar
|
[51] |
Katz E P, Li S T (1973). Structure and function of bone collagen fibrils. J Mol Biol, 80(1): 1–15
CrossRef
Pubmed
Google scholar
|
[52] |
Kisailus D, Truong Q, Amemiya Y, Weaver J C, Morse D E (2006). Self-assembled bifunctional surface mimics an enzymatic and templating protein for the synthesis of a metal oxide semiconductor. Proc Natl Acad Sci USA, 103(15): 5652–5657
CrossRef
Pubmed
Google scholar
|
[53] |
Komeili A (2007). Molecular mechanisms of magnetosome formation. Annu Rev Biochem, 76(1): 351–366
CrossRef
Pubmed
Google scholar
|
[54] |
Komeili A (2012). Molecular mechanisms of compartmentalization and biomineralization in magnetotactic bacteria. FEMS Microbiol Rev, 36(1): 232–255
CrossRef
Pubmed
Google scholar
|
[55] |
Krasko A, Lorenz B, Batel R, Schröder H C, Müller I M, Müller W E G (2000). Expression of silicatein and collagen genes in the marine sponge Suberites domuncula is controlled by silicate and myotrophin. Eur J Biochem, 267(15): 4878–4887
CrossRef
Pubmed
Google scholar
|
[56] |
Krasko A, Schröder H C, Batel R, Grebenjuk V A, Steffen R, Müller I M, Müller W E G (2002). Iron induces proliferation and morphogenesis in primmorphs from the marine sponge Suberites domuncula. DNA Cell Biol, 21(1): 67–80
CrossRef
Pubmed
Google scholar
|
[57] |
Kröger N, Poulsen N (2008). Diatoms-from cell wall biogenesis to nanotechnology. Annu Rev Genet, 42(1): 83–107
CrossRef
Pubmed
Google scholar
|
[58] |
Landis W J, Silver F H (2009). Mineral deposition in the extracellular matrices of vertebrate tissues: identification of possible apatite nucleation sites on type I collagen. Cells Tissues Organs, 189(1–4): 20–24
CrossRef
Pubmed
Google scholar
|
[59] |
Levi C, Barton J L, Guillemet C, Bras E, Lehuede P (1989). A remarkably strong natural glassy rod: the anchoring spicule of the Monorhaphis sponge. J Mater Sci Lett, 8(3): 337–339
CrossRef
Google scholar
|
[60] |
Mahamid J, Aichmayer B, Shimoni E, Ziblat R, Li C, Siegel S, Paris O, Fratzl P, Weiner S, Addadi L (2010). Mapping amorphous calcium phosphate transformation into crystalline mineral from the cell to the bone in zebrafish fin rays. Proc Natl Acad Sci USA, 107(14): 6316–6321
CrossRef
Pubmed
Google scholar
|
[61] |
Matsunaga S, Sakai R, Jimbo M, Kamiya H (2007). Long-chain polyamines (LCPAs) from marine sponge: possible implication in spicule formation. ChemBioChem, 8(14): 1729–1735
CrossRef
Pubmed
Google scholar
|
[62] |
Matsunaga T, Okamura Y, Fukuda Y, Wahyudi A T, Murase Y, Takeyama H (2005). Complete genome sequence of the facultative anaerobic magnetotactic bacterium Magnetospirillum sp. strain AMB-1. DNA Res, 12(3): 157–166
CrossRef
Pubmed
Google scholar
|
[63] |
Miller A and Parker S B (1984). Collagen: The organic matrix of bone. Philos Trans R Soc, B 304(1121): 455–477
|
[64] |
Moradian-Oldak J (2001). Amelogenins: assembly, processing and control of crystal morphology. Matrix Biol, 20(5-6): 293–305
CrossRef
Pubmed
Google scholar
|
[65] |
Moradian-Oldak J, Bouropoulos N, Wang L, Gharakhanian N (2002). Analysis of self-assembly and apatite binding properties of amelogenin proteins lacking the hydrophilic C-terminal. Matrix Biol, 21(2): 197–205
CrossRef
Pubmed
Google scholar
|
[66] |
Moradian-Oldak J, Du C, Falini G (2006). On the formation of amelogenin microribbons. Eur J Oral Sci, 114(s1 Suppl 1): 289–296, discussion 327–329, 382
CrossRef
Pubmed
Google scholar
|
[67] |
Moradian-Oldak J, Jimenez I, Maltby D, Fincham A G (2001). Controlled proteolysis of amelogenins reveals exposure of both carboxy- and amino-terminal regions. Biopolymers, 58(7): 606–616
CrossRef
Pubmed
Google scholar
|
[68] |
Moradian-Oldak J, Paine M L, Lei Y P, Fincham A G, Snead M L (2000). Self-assembly properties of recombinant engineered amelogenin proteins analyzed by dynamic light scattering and atomic force microscopy. J Struct Biol, 131(1): 27–37
CrossRef
Pubmed
Google scholar
|
[69] |
Müller W E G, Boreiko A, Schlossmacher U, Wang X, Tahir M N, Tremel W, Brandt D, Kaandorp J A, Schröder H C (2007). Fractal-related assembly of the axial filament in the demosponge Suberites domuncula: relevance to biomineralization and the formation of biogenic silica. Biomaterials, 28(30): 4501–4511
CrossRef
Pubmed
Google scholar
|
[70] |
Murat D, Byrne M, Komeili A (2010a). Cell biology of prokaryotic organelles. Cold Spring Harb Perspect Biol, 2(10): a000422
CrossRef
Pubmed
Google scholar
|
[71] |
Murat D, Quinlan A, Vali H, Komeili A (2010b). Comprehensive genetic dissection of the magnetosome gene island reveals the step-wise assembly of a prokaryotic organelle. Proc Natl Acad Sci USA, 107(12): 5593–5598
CrossRef
Pubmed
Google scholar
|
[72] |
Murr M M, Morse D E (2005). Fractal intermediates in the self-assembly of silicatein filaments. Proc Natl Acad Sci USA, 102(33): 11657–11662
CrossRef
Pubmed
Google scholar
|
[73] |
Nies D H (2011). How iron is transported into magnetosomes. Mol Microbiol, 82(4): 792–796
CrossRef
Pubmed
Google scholar
|
[74] |
Nudelman F, Pieterse K, George A, Bomans P H, Friedrich H, Brylka L J, Hilbers P A, de With G, Sommerdijk N A (2010). The role of collagen in bone apatite formation in the presence of hydroxyapatite nucleation inhibitors. Nat Mater, 9(12): 1004–1009
CrossRef
Pubmed
Google scholar
|
[75] |
Ofer S, Nowik I, Bauminger E R, Papaefthymiou G C, Frankel R B, Blakemore R P (1984). Magnetosome dynamics in magnetotactic bacteria. Biophys J, 46(1): 57–64
CrossRef
Pubmed
Google scholar
|
[76] |
Olszta M J, Cheng X, Jee S S, Kumar R, Kim Y-Y, Kaufman M J, Douglas E P and Gower L B (2007). Bone structure and formation: A new perspective. Mater Sci Eng, R 58(3–5): 77–116
|
[77] |
Pascal J L, Clementine G, Jacques L, Thibaud C (2005). Mimicking biogenic silica nanostructures formation. Curr Nanosci, 1(1): 73–83
CrossRef
Google scholar
|
[78] |
Penninga I, de Waard H, Moskowitz B M, Bazylinski D A, Frankel R B (1995). Remanence measurements on individual magnetotactic bacteria using a pulsed magnetic field. J Magn Magn Mater, 149(3): 279–286
CrossRef
Google scholar
|
[79] |
Piez K A (1965). Characterization of a collagen from codfish skin containing three chromatographically different α chains. Biochemistry, 4(12): 2590–2596
CrossRef
Pubmed
Google scholar
|
[80] |
Piez K A, Lewis M S, Martin G R, Gross J (1961). Subunits of the collagen molecule. Biochim Biophys Acta, 53(3): 596–598
CrossRef
Pubmed
Google scholar
|
[81] |
Posner A S, Betts F (1975). Synthetic amorphous calcium phosphate and its relation to bone mineral structure. Acc Chem Res, 8(8): 273– 281
CrossRef
Google scholar
|
[82] |
Pozzolini M, Sturla L, Cerrano C, Bavestrello G, Camardella L, Parodi A M, Raheli F, Benatti U, Müller W E G, Giovine M (2004). Molecular cloning of silicatein gene from marine sponge Petrosia ficiformis (Porifera, Demospongiae) and development of primmorphs as a model for biosilicification studies. Mar Biotechnol (NY), 6(6): 594–603
CrossRef
Pubmed
Google scholar
|
[83] |
Prozorov T, Mallapragada S, Narasimhan B, Wang L, Palo P, Nilsen-Hamilton M, Williams T, Bazylinski D, Prozorov R, Canfield P (2007a). Protein-mediated synthesis of uniform superparamagnetic magnetite nanocrystals. Adv Funct Mater, 17(6): 951–957
CrossRef
Google scholar
|
[84] |
Prozorov T, Palo P, Wang L, Nilsen-Hamilton M, Jones D, Orr D, Mallapragada S K, Narasimhan B, Canfield P C, Prozorov R (2007b). Cobalt ferrite nanocrystals: out-performing magnetotactic bacteria. ACS Nano, 1(3): 228–233
CrossRef
Pubmed
Google scholar
|
[85] |
Rabuffetti F A, Lee J S, Brutchey R L (2012). Vapor diffusion sol-gel synthesis of fluorescent perovskite oxide nanocrystals. Adv Mater, 24(11): 1434–1438
CrossRef
Pubmed
Google scholar
|
[86] |
Ramachandran G N, Kartha G (1955). Structure of collagen. Nature, 176(4482): 593–595
CrossRef
Pubmed
Google scholar
|
[87] |
Rich A, Crick F H C (1955). The structure of collagen. Nature, 176(4489): 915–916
CrossRef
Pubmed
Google scholar
|
[88] |
Richter M, Kube M, Bazylinski D A, Lombardot T, Glöckner F O, Reinhardt R, Schüler D (2007). Comparative genome analysis of four magnetotactic bacteria reveals a complex set of group-specific genes implicated in magnetosome biomineralization and function. J Bacteriol, 189(13): 4899–4910
CrossRef
Pubmed
Google scholar
|
[89] |
Schröder H C, Perović-Ottstadt S, Rothenberger M, Wiens M, Schwertner H, Batel R, Korzhev M, Müller I M, Müller W E G (2004a). Silica transport in the demosponge Suberites domuncula: fluorescence emission analysis using the PDMPO probe and cloning of a potential transporter. Biochem J, 381(Pt 3): 665–673
CrossRef
Pubmed
Google scholar
|
[90] |
Schröder H C, Perović-Ottstadt S, Wiens M, Batel R, Müller I M, Müller W E (2004b). Differentiation capacity of epithelial cells in the sponge Suberites domuncula. Cell Tissue Res, 316(2): 271–280
CrossRef
Pubmed
Google scholar
|
[91] |
Schüler D (2008). Genetics and cell biology of magnetosome formation in magnetotactic bacteria. FEMS Microbiol Rev, 32(4): 654–672
CrossRef
Pubmed
Google scholar
|
[92] |
Shaw W J, Campbell A A, Paine M L, Snead M L (2004). The COOH terminus of the amelogenin, LRAP, is oriented next to the hydroxyapatite surface. J Biol Chem, 279(39): 40263–40266
CrossRef
Pubmed
Google scholar
|
[93] |
Shimizu K, Cha J, Stucky G D, Morse D E (1998). Silicatein α: cathepsin L-like protein in sponge biosilica. Proc Natl Acad Sci USA, 95(11): 6234–6238
CrossRef
Pubmed
Google scholar
|
[94] |
Simmer J P, Fincham A G (1995). Molecular mechanisms of dental enamel formation. Crit Rev Oral Biol Med, 6(2): 84–108
CrossRef
Pubmed
Google scholar
|
[95] |
Simpson T L (1984). The cell biology of sponges. New York: Springer Publishing
|
[96] |
Staniland S, Ward B, Harrison A, van der Laan G, Telling N (2007). Rapid magnetosome formation shown by real-time X-ray magnetic circular dichroism. Proc Natl Acad Sci USA, 104(49): 19524–19528
CrossRef
Pubmed
Google scholar
|
[97] |
Stöber W, Fink A, Bohn E (1968). Controlled growth of monodisperse silica spheres in the micron size range. J Colloid Interface Sci, 26(1): 62–69
CrossRef
Google scholar
|
[98] |
Sumper M, Brunner E (2006). Learning from diatoms: Nature's tools for the production of nanostructured silica. Adv Funct Mater, 16(1): 17–26
CrossRef
Google scholar
|
[99] |
Tacke R (1999). Milestones in the biochemistry of silicon: From basic research to biotechnological applications. Angew Chem Int Ed Engl, 38(20): 3015–3018
CrossRef
Pubmed
Google scholar
|
[100] |
Tanaka M, Mazuyama E, Arakaki A, Matsunaga T (2011). MMS6 protein regulates crystal morphology during nano-sized magnetite biomineralization in vivo. J Biol Chem, 286(8): 6386–6392
CrossRef
Pubmed
Google scholar
|
[101] |
Tarasevich B J, Lea S, Bernt W, Engelhard M, Shaw W J (2009). Adsorption of amelogenin onto self-assembled and fluoroapatite surfaces. J Phys Chem B, 113(7): 1833–1842
CrossRef
Pubmed
Google scholar
|
[102] |
Tarasevich B J, Lea S, Shaw W J (2010). The leucine rich amelogenin protein (LRAP) adsorbs as monomers or dimers onto surfaces. J Struct Biol, 169(3): 266–276
CrossRef
Pubmed
Google scholar
|
[103] |
Termine J D, Kleinman H K, Whitson S W, Conn K M, McGarvey M L, Martin G R (1981). Osteonectin, a bone-specific protein linking mineral to collagen. Cell, 26(1 Pt 1): 99–105
CrossRef
Pubmed
Google scholar
|
[104] |
Termine J D, Posner A S (1966). Infrared analysis of rat bone: age dependency of amorphous and crystalline mineral fractions. Science, 153(3743): 1523–1525
CrossRef
Pubmed
Google scholar
|
[105] |
Thiel P A, Shen M, Liu D J, Evans J W (2009). Coarsening of two-dimensional nanoclusters on metal surfaces. J Phys Chem C, 113(13): 5047–5067
CrossRef
Google scholar
|
[106] |
Traub W, Arad T, Weiner S (1989). Three-dimensional ordered distribution of crystals in turkey tendon collagen fibers. Proc Natl Acad Sci USA, 86(24): 9822–9826
CrossRef
Pubmed
Google scholar
|
[107] |
Uebe R, Junge K, Henn V, Poxleitner G, Katzmann E, Plitzko J M, Zarivach R, Kasama T, Wanner G, Pósfai M, Böttger L, Matzanke B, Schüler D (2011). The cation diffusion facilitator proteins MamB and MamM of Magnetospirillum gryphiswaldense have distinct and complex functions, and are involved in magnetite biomineralization and magnetosome membrane assembly. Mol Microbiol, 82(4): 818–835
CrossRef
Pubmed
Google scholar
|
[108] |
Wang L, Prozorov T, Palo P E, Liu X, Vaknin D, Prozorov R, Mallapragada S, Nilsen-Hamilton M (2012a). Self-assembly and biphasic iron-binding characteristics of Mms6, a bacterial protein that promotes the formation of superparamagnetic magnetite nanoparticles of uniform size and shape. Biomacromolecules, 13(1): 98– 105
CrossRef
Pubmed
Google scholar
|
[109] |
Wang W, Bu W, Wang L, Palo P E, Mallapragada S, Nilsen-Hamilton M, Vaknin D (2012b). Interfacial properties and iron binding to bacterial proteins that promote the growth of magnetite nanocrystals: X-ray reflectivity and surface spectroscopy studies. Langmuir, 28(9): 4274–4282
CrossRef
Pubmed
Google scholar
|
[110] |
Weaver J C, Morse D E (2003). Molecular biology of demosponge axial filaments and their roles in biosilicification. Microsc Res Tech, 62(4): 356–367
CrossRef
Pubmed
Google scholar
|
[111] |
Weiner S (2006). Transient precursor strategy in mineral formation of bone. Bone, 39(3): 431–433
CrossRef
Pubmed
Google scholar
|
[112] |
Weiner S (2008). Biomineralization: a structural perspective. J Struct Biol, 163(3): 229–234
CrossRef
Pubmed
Google scholar
|
[113] |
Weiner S, Addadi L (1991). Acidic macromolecules of mineralized tissues: the controllers of crystal formation. Trends Biochem Sci, 16(7): 252–256
CrossRef
Pubmed
Google scholar
|
[114] |
Wheeler E J, Lewis D (1977). An x-ray study of the paracrystalline nature of bone apatite. Calcif Tissue Res, 24(3): 243–248
CrossRef
Pubmed
Google scholar
|
[115] |
Yuk J M, Park J, Ercius P, Kim K, Hellebusch D J, Crommie M F, Lee J Y, Zettl A, Alivisatos A P (2012). High-resolution EM of colloidal nanocrystal growth using graphene liquid cells. Science, 336(6077): 61–64
CrossRef
Pubmed
Google scholar
|
[116] |
Zeichner-David M, Diekwisch T, Fincham A, Lau E, MacDougall M, Moradian-Oldak J, Simmer J, Snead M, Slavkin H C (1995). Control of ameloblast differentiation. Int J Dev Biol, 39(1): 69–92
Pubmed
|
[117] |
Zhou Y, Shimizu K, Cha J N, Stucky G D, Morse D E (1999). Efficient catalysis of polysiloxane synthesis by silicatein α requires specific hydroxy and imidazole functionalities. Angew Chem Int Ed Engl, 38(6): 779–782
CrossRef
Google scholar
|
/
〈 | 〉 |