Abstract
High-capacity calcium-binding macromolecules have been identified at mineralization fronts in heterodont bivalves, vertebrate tooth dentin and unicellular algae. They appear to be functionally similar to casein, the mineral ion carrier of milk. The bivalve phosphoprotein studied in this laboratory occurs as discrete high molecular weight (MW) particles in the hemolymph and extrapallial fluid and at the inner shell surface during mineral deposition. The phosphoprotein particles are characterized by a high content of aspartic acid, phosphoserine and histidine residues which comprise 80% or more of the peptide chain. The native particles contain a protected pool of calcium and phosphate ions and an exchangeable pool of calcium and magnesium ions. The phosphoprotein monomers are covalently cross-linked via histidinoalanine residues and ionically cross-linked via divalent cations into compact particles with a MW of about 50 million. High concentrations of phosphoprotein particles accumulate at the mineralization front during stimulated biomineralization, but neither inhibit mineral deposition nor influence the crystal habits. The particles are probably calcium ion transporters. However, the mechanism by which protein bound calcium is utilized to form calcium carbonate crystals is unknown.
The bivalve phosphoprotein particles share common characteristics with vertebrate tooth dentin and algal coccolithosomes which have been studied in other laboratories. All three are high-capacity calcium-binding macromolecules which have been localized at mineralization fronts. Both the bivalve phosphoprotein particles and dentin phosphophoryn are aspartic acid-rich, highly phosphosylated proteins which have a tendency to cross-link and fragment. Both coccolithosomes and the bivalve phosphoprotein occur as discrete high MW particles about 20–40 nm in diameter surrounding growing calcium carbonate crystals in vivo. It is postulated that intermediate calcium carriers in the form of high-capacity calcium-binding macromolecules may be a general phenomenon in the biological calcification of skeletal tissues.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
ADDADI, L., and WEINER, S., 1985. Interactions between acidic proteins and crystals: stereochemical requirements in biomineralization. Proc. Nat. Acad. Sci. U.S.A., 82:4110–4114.
BUTLER, W.T., BROWN, M., DIMUZIO, M.T., COTHRAN, W.C., and LINDE, A., 1983. Multiple Forms of rat dentin phosphorproteins. Arch. Biochem. Biophys., 225:178–186.
CRENSHAW, MA, 1972. The soluble matrix from Mercenaria mercenaria shell. Biomineralization, 6:6–11.
CRENSHAW, MA., and NEFF, J.M. 1969. Decalcification at the mantle-shell interface in mollusks. Amer. Zool., 9:881–885.
DIMUZIO, M.T., and VEIS, A., 1978. The biosynthesis of phosphophoryns and dentin collagen in the continuously erupting rat incisor. J. Biol. Chem., 253:6845–6852.
FUJISAWA, R., KUBOKI, Y., and SASAKI, S., 1985. In vivo cleavage of dentin phosphophoryn following ß-elimination of its phosphoserine residues. Arch. Biochem. Biophys., 243:619–623.
HOLT, C., 1982. Inorganic constituents of milk. III. The colloidial calcium phosphate of cow’s milk. J. Dairy Res., 49:29–38.
KUBOKI, Y., FUJISAWA, R., AOYAMA, K., and SASAKI, S., 1979. Calcium-specific precipitation of dentin phosphoprotein: a new method of purification and the significance for the mechanism of calcification. J. Den. Res., 58:1926–1932.
LEE, S.L., KOSSIVA, D., and GLIMCHER, M.J., 1983a. Phosphoproteins of bovine dentin: evidence for polydispersity during tooth maturation. Biochemistry 22:2596–2601.
LEE, S.L, GLONEK, T., and GLIMCHER, M.J., 1983b. Nuclear magnetic resonance spectroscopic evidence for ternary complex formation of fetal dentin phosphorprotein with calcium and inorganic orthophosphate ions. Calc. Tiss. Intern., 35:815–818.
LEE, S.L., VEIS, A., and GLONEK, T., 1977. Dentin phosphoprotein: an extracellular calcium-binding protein. Biochemistry, 16:2971–2979.
LYSTER, R.L.J., MANN, S., PARKER, S.B., and WILLIAMS, RT.P., 1984. Nature of micellar calcium phosphate in cows’ milk as studied by high-resolution electron microscopy. Biochim. Biophys. Acta, 801:315–317.
MARSH, M.E., 1986a. Histidinoalanine, a naturally occurring cross-link derived from phosphoserine and histidine residues in mineral-binding phosphoproteins. Biochemistry, 25:2392–2396.
MARSH, M.E., 1986b. Biomineralization in the presence of calcium-binding phosphoprotein particles. J. Exp. Zool., 239:207–220.
MARSH, M.E. and SASS, R.L., 1985. Distribution and characterization of mineral-binding phosphoprotein particles in Bivalvia. J. Exp. Zool., 234:237–242.
MARSH, M.S., and SASS, R.L.; 1984. Phosphoprotein particles: calcium and inorganic phosphate binding structures. Biochemistry, 23:1448–1456.
MARSH, M.E., and SASS, R.L., 1983. Calcium-binding phosphoprotein particles in the extrapallial fluid and innermost shell lamella of clams. J. Exp. Zool., 266:193–203.
MASTERS, P.M., 1985. In vivo decomposition of phosphoserine and serine in noncollagenous protein from human dentin. Calc. Tiss. Intern., 37:236–241.
MCGANN, T.C.A., KEARNEY, RD., BUCHHEIM, W., POSNER, A.S., BETTS, F. and BLUMENTHAL, N.C., 1983. Amorphous calcium phosphate in casein micelles of bovine milk. Calc. Tiss. Intern., 35:821–823.
MEPHAM, T.B., GAYE, P., and MERCIER, J.C., 1982. Biosynthesis of milk proteins. In Developments in Dairy Chemistry-1 (ed. P. F. Fox), pp. 115–156. New York: Elsevier.
OUTKA, D.E., and WILLIAMS, D.C., 1971. Sequential coccolith morphogenesis in Hymenomonas carterae. J. Protozool., 18:285–297.
PITA, J.C., CUERVO, L.A., MADRUGA, J.E., MULLER, F.J., and HOWELL, D.S., 1970. Evidence for a role of protein polysaccharides in regulation of mineral phase separation in calcifing cartilage. J. Clin. Invest., 49:2188–2197.
PRINCE, C.W., OOSAWA, T., BUTLER, W.T., TOMANA, M., BROWN, A.S., BHOWN, M., and SCHROHENLOHER, RE., 1987. Isolation, characterization, and biosynthesis of a phosphorylated glycoprotein from rat bone. J. Biol. Chem., 262:2900–2907.
RUNNEGAR, B., 1989. This volume.
SASS, RL. and MARSH, M.E., 1983. N t-and Np Jr-Histidinoalanine: naturally occurring cross-linking amino acids in calcium-binding phosphoproteins. Biochem. Biophys. Res. Comm., 114:304–309.
SCHMIDT, D.G., 1982. Association of caseins and casein micelle structure. In Developments in Dairy Chemistry-1 (ed. P.F. Fox, pp. 61–86). New York, Elsevier.
SCHMIDT, D.G., 1980. Colloidial aspects of casein. Netherlands Milk Dairy J., 34:42–64.
SIKES, C.S., and WHEELER, A.P., 1983. A systematic approach to some fundamental questions of carbonate calcification. In Biomineralization and Biological Metal Ion Accumulation (ed. P. Westbroek and E.W. de Jong), pp. 285–289. Dordrecht: D. Reidel Publishing Co.
SILER-SIEVENSON, W.G., and VEIS, A., 1983. Bovine dentin phosphophryn: composition and molecular weight. Biochemistry, 22:4326–4335.
SWAISGOOD, H.E., 1982. Chemistry of milk protein. In Developments in Dairy Chemistry-1 (ed. P.F. Fox), pp. 1–59. New York: Elsevier.
VAN DER WAL, P., DE JONG, E.W., WESTBROEK, P., DE BRUIJN, W.C., and MULDERSTAPEL, A.A., 1983a. Polysaccharide localization, coccolith formation, and Golgi dynamics in the Coccolithiphorid Hymenomonas carterae. J. Ultrastr. Res., 85:139–158.
VAN DER WAL, P., DE JONG, E.W., WESTBROEK, P., and DE BRUIJN, W.C., 1983b. Calcification in the Coccolithophorid alga Hymenomonas carterae. In Environmental Biogeochemistry, Ecological Bulletin No. 35 (ed. R Hallberg), pp. 251–258. Stockholm: Publishing House/FRN.
VEIS, DJ., ALBINDER, T.M., CLOHISY, J., RANIMA, M., SABSAY, B., and VEIS, A., 1986. Matrix proteins of the teeth of the sea urchin Lytechinus variegatus. J. Exp. Zool., 240:35–46.
WILBUR, KM., and BERNHARDT, A.M., 1982. Mineralization of molluscan shell: effects of free and polyamino acids on crystal growth rate in vitro. Amer. Zool., 22:952.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 1989 Springer Science+Business Media New York
About this chapter
Cite this chapter
Marsh, M.E. (1989). High Capacity Calcium-Binding Proteins as Intermediate Calcium Carriers in Biological Mineralization. In: Crick, R.E. (eds) Origin, Evolution, and Modern Aspects of Biomineralization in Plants and Animals. Springer, Boston, MA. https://doi.org/10.1007/978-1-4757-6114-6_21
Download citation
DOI: https://doi.org/10.1007/978-1-4757-6114-6_21
Publisher Name: Springer, Boston, MA
Print ISBN: 978-1-4757-6116-0
Online ISBN: 978-1-4757-6114-6
eBook Packages: Springer Book Archive