Deposition of apatite in mineralizing vertebrate extracellular matrices: A model of possible nucleation sites on type I collagen

REFERENCES

• Hodge, A.J., and Petruska, J.A. (1963). Recent studies with the electron microscope on ordered aggregates of the tropocollagen macromolecule. In Aspects of Protein Structure, G.N. Ramachandran (ed.) pp. 289–300. New York: Academic Press.
   Google Scholar
• Orgel, J.P.R.O., Irving, T.C., Miller, A., and Wess, T.J. (2006). Microfibrillar structure of type I collagen in situ. Proc. Natl. Acad. Sci. U.S.A. 103:9001–9005.
   PubMed Web of Science ®Google Scholar
• Landis, W.J., Song, M.J., Leith, A., McEwen, L., and McEwen, B. (1993). Mineral and organic matrix interaction in normally calcifying tendon visualized in three dimensions by high voltage electron microscopic tomography and graphic image reconstruction. J. Struct. Biol. 110:39–54.
   PubMed Web of Science ®Google Scholar
• Robinson, R.A. (1952). An electron-microscope study of the crystalline inorganic component of bone and its relationship to the organic matrix. J. Bone Joint Surg. 34:389–434.
   PubMed Web of Science ®Google Scholar
• Robinson, R.A., and Watson, M.L. (1952). Collagen-crystal relationships in bone as seen in the electron microscope. Anat. Rec. 114:383–410.
   PubMedGoogle Scholar
• Johnson, L.C. (1960). Mineralization of turkey leg tendon. I. Histology and histochemistry of mineralization. In Calcification in Biological Systems, R.F. Sognnaes (ed.) pp. 117–128. Washington, DC: American Association for the Advancement of Science.
   Google Scholar
• Nylen, M.J., Scott, D.B., and Mosley, V.M. (1960). Mineralization of turkey leg tendon. II. Collagen-mineral relations as revealed by electron and x-ray microscopy. In Calcification in Biological Systems, R.F. Sognnaes (ed.) pp. 129–142. Washington, DC: American Association for the Advancement of Science.
   Google Scholar
• Likens, R.C., Piez, K.A., and Kunde, M.L. (1960). Mineralization of turkey leg tendon. III. Chemical nature of the protein and mineral phases. In Calcification in Biological Systems, R.F. Sognnaes (ed.) pp. 143–149. Washington, DC: American Association for the Advancement of Science.
   Google Scholar
• Weiner, S., and Traub, W. (1986). Organization of hydroxyapatite crystals within collagen fibrils. FEBS Lett. 206:262–266.
   PubMed Web of Science ®Google Scholar
• Arsenault, A.L. (1989). A comparative electron microscopic study of apatite crystals in collagen fibrils of rat bone, dentin and calcified turkey leg tendon. Bone Miner. 6:165–177.
   PubMedGoogle Scholar
• Landis, W.J., and Arsenault, A.L. (1989). Vesicle- and collagen-mediated calcification in the turkey leg tendon. Connect. Tissue Res. 22:35–42.
   PubMed Web of Science ®Google Scholar
• Veis, A. (1993). Mineral-matrix interactions in bone and dentin. J. Bone Miner. Res. 8:S493–S497.
   PubMed Web of Science ®Google Scholar
• Lees, S., Prostak, K.S., Ingle, V.K., and Kjoller, K. (1994). The loci of mineral in turkey leg tendon as seen by atomic force microscope and electron microscopy. Calcif. Tissue Int. 55:180–189.
   PubMed Web of Science ®Google Scholar
• Landis, W.J., and Silver, F.H. (2002). The structure and function of normally mineralizing avian tendons. Comp. Biochem. Physiol. A 133:1135–1157.
   PubMed Web of Science ®Google Scholar
• Glimcher, M.J., and Krane, S.M. (1968). The organization and structure of bone, and the mechanism of calcification. In Biology of Collagen. Treatise on Collagen, Vol. IIB, G.N. Ramachandran and B.S. Gould (eds.) pp. 68–251. New York: Academic Press.
   Google Scholar
• Glimcher, M.J. (1984). Recent studies of the mineral phase in bone and its possible linkage to the organic matrix by protein-bound phosphate bonds. Phil. Trans. Roy. Soc. Lond. B 304:479–508.
   PubMed Web of Science ®Google Scholar
• Shadwick, R.E. (1990). Elastic energy storage in tendons: Mechanical differences related to function and age. J. Appl. Physiol. 68:1033–1040.
   PubMed Web of Science ®Google Scholar
• Freeman, J.W., and Silver, F.H. (2004). Elastic energy storage in unmineralized and mineralized extracellular matrices: A comparison between molecular modeling and experimental measurements. J. Theor. Biol. 229:371–381.
   PubMed Web of Science ®Google Scholar
• Freeman, J.W., and Silver, F.H. (2004). Analysis of mineral deposition in turkey tendons and self-assembled collagen fibers using mechanical techniques. Connect. Tissue Res. 45:131–141.
   PubMed Web of Science ®Google Scholar
• Anderson, H.C. (1969). Vesicles associated with calcification in the matrix of epiphyseal cartilage. J. Cell Biol. 41:59–72.
   PubMed Web of Science ®Google Scholar
• Anderson, H.C. (1984). Mineralization by matrix vesicles. Scan. Electron Microsc. 2:953–964.
   Google Scholar
• Bonucci, E. (1970). Fine structure and histochemistry of calcifying globules in epiphyseal cartilage. Z. Zellforsch. Mikroskop. Anat. 103:192–217.
   PubMedGoogle Scholar
• Landis, W.J., and Song, M.J. (1991). Early mineral deposition in calcifying tendon characterized by high voltage electron microscopy and three-dimensional graphic imaging. J. Struct. Biol. 107:116–127.
   PubMed Web of Science ®Google Scholar
• Traub, W., Jodaikin, A., Arad, T., Veis, A., and Sabsay, B. (1992). Dentin phosphophoryn binding to collagen fibrils. Matrix 12:97–201.
   Google Scholar
• Fisher, L.W., Torchia, D.A., Fohr, B., Young, M.F., and Fedarko, N. (2001). Flexible structures of SIBLING proteins, bone sialoprotein and osteopontin. Biochem. Biophys. Res. Commun. 280:460–465.
   PubMed Web of Science ®Google Scholar
• Qin, C., Brunn, J.C., Baba, O., Wygant, J.N., McIntyre, B.W., and Butler, W.T. (2003). Dentin sialoprotein isoforms: Detection and characterization of a high molecular weight dentin sialoprotein. Eur. J. Oral Sci. 111:235–242.
   PubMed Web of Science ®Google Scholar
• Tye, C.E., Rattray, K.R., Warner, K.J., Gordon, J.A.R., Sodek, J., Hunter, G.K., and Goldberg, H.A. (2003). Delineation of the hydroxyapatite-nucleating domains of bone sialoprotein. J. Biol. Chem. 278:7949–7955.
   PubMed Web of Science ®Google Scholar
• Tye, C.E., Hunter, G.K., and Goldberg, H.A. (2005). Identification of the type I collagen-binding domain of bone sialoprotein and characterization of the mechanism of interaction. J. Biol. Chem. 280:13487–13492.
   PubMed Web of Science ®Google Scholar
• George, A., and Veis, A. (2008). Phosphorylated proteins and control over apatite nucleation, crystal growth and inhibition. Chem. Rev. 108:4670–4693.
   PubMed Web of Science ®Google Scholar
• Schmitt, F.O. (1956). Macromolecular interaction patterns in biological systems. Proc. Am. Phil. Soc. 100:476–486.
   Web of Science ®Google Scholar
• Weiner, S., and Traub, W. (1989). Crystal size and organization in bone. Connect. Tissue Res. 21:259–265.
   PubMed Web of Science ®Google Scholar
• McEwen, B.F., Song, M.J., and Landis, W.J. (1992). Quantitative determination of the mineral distribution in different collagen zones of calcifying tendon using high voltage electron microscopic tomography. J. Computer Assist. Micros. 3:201–210.
   Google Scholar
• Landis, W.J., Hodgens, K.J., Arena, J., Song, M.J., and McEwen, B.F. (1996). The structural relation between collagen and mineral in bone as determined by high voltage electron microscopic tomography. Microsc. Res. Tech. 33:192–202.
   PubMed Web of Science ®Google Scholar
• Landis, W.J., Hodgens, K.J., Song, M.J., Arena, J., Kiyonaga, S., Marko, M., Owen, C., and McEwen, B.F. (1996). Mineralization of collagen occurs on fibril surfaces: Evidence from conventional and high voltage electron microscopy and three-dimensional imaging. J. Struct. Biol. 117:24–35.
   PubMed Web of Science ®Google Scholar
• Landis, W.J. (1999). An overview of vertebrate mineralization with emphasis on collagen-mineral interaction. Gravitational Space Biol. Bull. 12:15–26.
   PubMedGoogle Scholar
• Maitland, M.E., and Arsenault, A.L. (1991). A correlation between the distribution of biological apatite and amino acid sequence of type I collagen. Calcif. Tissue Int. 48:341–352.
   PubMed Web of Science ®Google Scholar
• Landis, W.J., Silver, F.H., and Freeman, J.W. (2006). Collagen as a scaffold for biomimetic mineralization of vertebrate tissues. J. Mater. Chem. 16:1495–1503.
   Web of Science ®Google Scholar
• Weiner, S., and Price P.A. (1986). Disaggregation of bone into crystals. Calcif. Tissue Int. 39:365–375.
   PubMed Web of Science ®Google Scholar
• Orgel, J.P.R.O., Miller, A., Irving, T.C., Fischetti, R.F., Hammersley, A.P., and Wess, T.J. (2001). The in situ supermolecular structure of type I collagen. Structure 9:1061–1069.
   PubMed Web of Science ®Google Scholar
• Eyre, D. (1987). Collagen cross-linking amino acids. Methods Enzymol. 144:115–139.
   PubMed Web of Science ®Google Scholar
• Yamauchi, M., Katz, E.P., Otsubo, K., Teraoka, K., and Mechanic, G.L. (1989). Cross-linking and stereospecific structure of collagen in mineralized and nonmineralized skeletal tissues. Connect. Tissue Res. 21:159–169.
   PubMedGoogle Scholar
• Otsubo, K., Katz, E.P., Mechanic, G.L., and Yamauchi, M. (1992). Cross-linking connectivity in bone collagen fibrils: The COOH-terminal locus of free aldehyde. Biochemistry 31:396–402.
   PubMed Web of Science ®Google Scholar
• Landis, W.J., and Silver, F.H. (2009). Mineral deposition in the extracellular matrices of vertebrate tissues: Identification of possible apatite nucleation sites on type I collagen. In Chemistry and Biology of Mineralized Tissues. Proceedings of the Ninth International Conference, Austin, TX, November, 2007, L. Bonewald and P. Krebsbach (eds.), Cells, Tissues, Organs 189:20–24.
   PubMed Web of Science ®Google Scholar
• Hulmes, D.J.S., and Miller, A. (1979). Quasi-hexagonal packing in collagen fibrils. Nature 282:878–880.
   PubMed Web of Science ®Google Scholar
• Christiansen, D.L., Huang, E.K., and Silver, F.H. (2000). Assembly of type I collagen: Fusion of fibril subunits and the influence of fibril diameter on mechanical properties. Matrix Biol. 19:409–420.
   PubMed Web of Science ®Google Scholar
• Chapman, J.A. (1974). The staining pattern of collagen fibrils. I. An analysis of electron micrographs. Connect. Tissue Res. 2:137–150.
   PubMed Web of Science ®Google Scholar
• Chapman, J.A., and Hardcastle, R.A. (1974). The staining pattern of collagen fibrils. II. A comparison with patterns computer-generated from the amino acid sequence. Connect. Tissue Res. 2:151–159.
   PubMed Web of Science ®Google Scholar
• Hodge, A.J. (1989). Molecular models illustrating the possible distribution of “holes” in simple systematically staggered arrays of type I collagen molecules in native-type fibrils. Connect. Tissue Res. 21:137–147.
   PubMed Web of Science ®Google Scholar
• www.ncbi.nlm.nih.gov/entrez/viewer.fcgi, National Institutes of Health, Bethesda, MD.
   Google Scholar
• Silver, F.H., Freeman, J.W., Horvath, I., and Landis, W.J. (2001). Molecular basis for elastic energy storage in mineralized tendon. Biomacromolecules 2:750–756.
   PubMed Web of Science ®Google Scholar
• Knott, L., and Bailey, A.J. (1998). Collagen cross-links in mineralizing tissues: A review of their chemistry, function, and clinical relevance. Bone 22:181–187.
   PubMed Web of Science ®Google Scholar
• Lowenstam, H.A., and Weiner, S. (1989). On Biomineralization. New York: Oxford University Press.
   Google Scholar
• Stetler-Stevenson, W.G., and Veis, A. (1986). Type I collagen shows a specific binding affinity for bovine dentin phosphophoryn. Calcif. Tissue Int. 38:135–141.
   PubMed Web of Science ®Google Scholar
• Stetler-Stevenson, W.G., and Veis, A. (1987). Bovine dentin phosphophoryn: Calcium ion binding properties of a high molecular weight preparation. Calcif. Tissue Int. 40:97–102.
   PubMed Web of Science ®Google Scholar
• Curley-Joseph, J., and Veis, A. (1979). The nature of covalent complexes of phosphoproteins with collagen in the bovine dentin matrix. J. Dent. Res. 58:1625–1633.
   PubMed Web of Science ®Google Scholar
• Chen, Y., Bal, B.S., and Gorski, J.P. (1992). Calcium and collagen binding properties of osteopontin, bone sialoprotein, and bone acidic glycoprotein-75 from bone. J. Biol. Chem. 267:24871–24878.
   PubMed Web of Science ®Google Scholar
• George, A., Sabsay, B., Simonian, P.A., and Veis, A. (1993). Characterization of a novel dentin matrix acidic phosphoprotein. Implications for induction of biomineralization. J. Biol. Chem. 268:12624–12630.
   PubMed Web of Science ®Google Scholar
• MacDougall, M., Simmons, D., Luan, X., Nydegger, J., Feng, J., and Gu, T.T. (1997). Dentin phosphoprotein and dentin sialoprotein are cleavage products expressed from a single transcript coded by a gene on human chromosome 4: Dentin phosphoprotein DNA sequence determination. J. Biol. Chem. 272:835–842.
   PubMed Web of Science ®Google Scholar
• Dahl, T., Sabsay, B., and Veis, A. (1998). Type I collagen-phosphophoryn interactions: Specificity of the monomer-monomer binding. J. Struct. Biol. 123:162–168.
   PubMed Web of Science ®Google Scholar
• Ganss, B., Kim, R.H., and Sodek, J. (1999). Bone sialoprotein. Crit. Rev. Oral Biol. Med. 10:79–98.
   PubMedGoogle Scholar
• Christiansen, D., and Silver, F.H. (1992). The pH dependent mineralization of a reconstituted collagen fiber: Physical and ultrastructural characterization. Biomimetics 1:265–291.
   Google Scholar
• Christiansen, D., and Silver, F.H. (1993). Mineralization of an axially aligned collagenous matrix: A morphological and ultrastructural study. Cells and Materials 3:177–188.
   Google Scholar
• Mertz, E.L., and Leikin, S. (2004). Interactions of inorganic phosphate and sulfate anions with collagen. Biochemistry 43:14901–14912.
   PubMed Web of Science ®Google Scholar
• Sweeney, S.M., Orgel, J.P., Fertala, A., McAuliffe, J.D., Turner, K.R., Di Lullo, G.A., Chen, S., Antipova, O., Perumal, S., Ala-Kokko, L., Forline, A., Cabral, W.A., Barnes, A.M., Marini, J.C., and San Antonio, J.D. (2008). Candidate cell and matrix interaction domains on the collagen fibril, the predominant protein of vertebrates. J. Biol. Chem. 283:21187–21197.
   Web of Science ®Google Scholar
• Engle, J. (1997). Versatile collagens in invertebrates. Science 277:1785–1786.
   PubMed Web of Science ®Google Scholar
• Silver, F.H., Horvath, I., and Foran, D.J. (2002). Mechanical implications of the domain structure of fibril forming collagens: Comparison of the molecular and fibrillar flexibilities of the α-chains found in types I, II and III collagen. J. Theor. Biol. 216:243–254.
   PubMed Web of Science ®Google Scholar
• Hofmann, H., Voss, T., Juhn, K., and Engle, J. (1984). Localization of flexible sites in thread-like molecules from electron micrographs: Comparison of interstitial, basement membrane and intima collagens. J. Mol. Biol. 172:325–343.
   PubMed Web of Science ®Google Scholar
• Paterlini, M.G., Nemethy, G., and Scheraga, H.A. (1995). The energy of formation of internal loops in triple-helical collagen polypeptides. Biopolymers 35:607–619.
   PubMed Web of Science ®Google Scholar
• Piez, K.A., and Trus, B.I. (1978). Sequence regularities and packing of collagen molecules. J. Mol. Biol. 122:419–432.
   PubMed Web of Science ®Google Scholar
• Wess, T.J. (2008). Collagen fibrillar structure and hierarchies. In Collagen: Structure and Mechanics, P. Fratzl (ed.) pp. 49–80. New York: Springer Science+Business Media, LLC.
   Google Scholar
• Hodge, A.J., and Schmitt, F.O. (1960). The charge profile of the tropocollagen macromolecule and the packing arrangement in native-type collagen fibrils. Proc. Natl. Acad. Sci. U.S.A. 46:186–197.
   PubMed Web of Science ®Google Scholar
• Trus, B.L., and Piez, K.A. (1976). Molecular packing of collagen: Three-dimensional analysis of electrostatic interactions. J. Mol. Biol. 108:705–732.
   PubMed Web of Science ®Google Scholar
• Itoh, T., Kobayashi, M., and Hashimoto, M. (1998). The role of intermolecular electrostatic interaction on appearance of the periodic band structure in type I collagen fibril. Jpn. J. Appl. Phys. 37:L190–L192.
   Web of Science ®Google Scholar
• Scott, J.E. (1996). Proteodermatan and proteokeratan sulfate (decorin, lumican/fibromodulin) proteins are horseshoe shaped. Implications for their interactions with collagen. Biochemistry 35:8795–8799.
   PubMed Web of Science ®Google Scholar
• Tenni, R., Viola, M., Weiser, F., Sini, P., Giudici, C., Rossi, A., and Tira, M.E. (2002). Interaction of decorin with CNBr peptides from collagens I and II: Evidence for multiple binding sites and lysyl residues in collagen. Eur. J. Biochem. 269:1428–1437.
   PubMedGoogle Scholar
• McKee, M.D., Zalzal, S., and Nanci, A. (1996). Extracellular matrix in tooth cementum and mantle dentin: Localization of osteopontin and other noncollagenous proteins, plasma proteins, and glycoconjugates by electron microscopy. Anat. Rec. 245:293–312.
   PubMedGoogle Scholar
• Gower, L.B. (2008). Biomimetic model systems for investigating the amorphous precursor pathway and its role in biomineralization. Chem. Rev. 108:4551–4627.
   PubMed Web of Science ®Google Scholar
• Jee, S.S., Thula, T.T., and Gower, L.B. (2010). Development of bone-like composites via the polymer-induced liquid-precursor (PILP) process. Part 1: Influence of polymer molecular weight. Acta Biomater. 6:3676–3686.
   PubMed Web of Science ®Google Scholar
• Nudelman, F., Pierterse, K., George, A., Bomans, P.H.H., Friedrich, H., Brylka, L.J., Hilbers, P.A.J., de With, G., and Sommerdijk, N.A.J.M. (2010). The role of collagen in bone apatite formation in the presence of hydroxyapatite nucleation inhibitors. Nat. Mater. 9:1004–1009.
   PubMed Web of Science ®Google Scholar