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Polyanion-mediated mineralization — assembly and reorganization of acidic polysaccharides in the Golgi system of a coccolithophorid alga during mineral deposition

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Summary

Immunolocalization of two highly acidic polysaccharides (PS-1 and PS-2) in a calcifying algaPleurochrysis carterae is described throughout the mineralization process, from before crystal nucleation through the cessation of crystal growth. This unicellular coccolithophorid alga is a useful model for mineralization because it produces calcified scales known as coccoliths in homogeneous cell culture. PS-1 and PS-2 were localized in the crystal coats of mature coccoliths and in electron dense Golgi particles. The polyanions are synthesized in medial Golgi cisternae and co-aggregate with calcium ions into discrete 25 nm particles. Particle-laden vesicles bud from cisternal margins and fuse with a coccolith-forming saccule containing an organic oval-shaped scale which forms the base of the future coccolith. The particles are localized on the base before the onset of mineral deposition and are present in the coccolith saccule throughout the period of crystal (CaCO3) nucleation and growth. During the final phase of coccolith formation, the particles disappear, and the mature crystals acquire an amorphous coat containing PS-1 and PS-2 polysaccharides which remain with the mineral phase after the coccoliths are extruded from the cell. Postulated mechanisms of polyanion-mediated mineralization are reviewed and their relevance to the calcification of coccoliths is addressed.

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Abbreviations

PS-1:

polysaccharide one

PS-2:

polysaccharide two

BSA:

bovine serum albumin

SDS:

sodium dodecyl sulfate

MES:

2-(N-morpholino)-ethanesulfonic acid

EDTA:

ethylenediaminetetraacetic acid

DHA:

3-deoxy-lyxo-2-heptulosaric acid

TCA:

trichloroacetic acid

References

  • Addadi L, Weiner S (1985) Interactions between acidic proteins and crystals: stereochemical requirements in biomineralization. Proc Natl Acad Sci USA 82: 4110–4114

    PubMed  Google Scholar 

  • Blumenkrantz N, Asboe-Hansen G (1973) New method for quantitative determination of uronic acids. Anal Biochem 54: 484–489

    PubMed  Google Scholar 

  • Charak JHM, Pirraglia CA, Reithmeier RAF (1990) Interaction of ruthenium red with Ca2+-binding proteins. Anal Biochem 188: 123–131

    PubMed  Google Scholar 

  • Crenshaw MA (1972) The soluble matrix fromMercenaria mercenaria shell. Biomineralization 6: 6–11

    Google Scholar 

  • — (1982) Mechanisms of normal biological mineralization of calcium carbonate. In: Nancollas GH (ed) Biological mineralization and demineralization. Springer, Berlin Heidelberg New York, pp 243–357

    Google Scholar 

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

    Google Scholar 

  • Dimuzio MT, Veis A (1978 a) Phosphophoryns — major noncollagenous proteins of rat incisor dentin. Calcif Tissue Res 25: 169–178

    PubMed  Google Scholar 

  • — — (1978 b) The biosynthesis of phosphophoryns and dentin collagen in the continuously erupting rat incisor. J Biol Chem 253: 6845–6852

    PubMed  Google Scholar 

  • Domozych DS, Wells B, Shaw PJ (1991) Basket scales of the green alga,Mesostigma viride: chemistry and ultrastructure. J Cell Sci 100: 397–407

    Google Scholar 

  • — — — (1992) Scale biogenesis in the green alga,Mesostigma viride. Protoplasma 167: 19–32

    Google Scholar 

  • Glimcher MJ (1989) Mechanism of calcification: role of collagen fibrils and collagen-phosphoprotein complexes in vitro and in vivo. Anat Rec 224: 139–153

    PubMed  Google Scholar 

  • Green MR, Pastewka JV, Peacock AC (1973) Differential staining of phosphoproteins on polyacrylamide gels with a cationic carbocyanine dye. Anal Biochem 56: 43–51

    PubMed  Google Scholar 

  • Kyhse-Anderson J (1984) Electroblotting of multiple gels: a simple apparatus without buffer tank for rapid transfer of proteins from polyacrylamide to nitrocellulose. J Biochem Biophys Methods 10: 203–209

    PubMed  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of bacteriophage T 4. Nature 227: 680–685

    PubMed  Google Scholar 

  • Lee SL, Veis A, Glonek T (1977) Dentin phosphoprotein: an extracellular calcium-binding protein. Biochemistry 16: 2971–2979

    PubMed  Google Scholar 

  • Linde A, Lussi A, Crenshaw MA (1989) Mineral induction by immobilized polyanionic proteins. Calcif Tissue Int 44: 286–295

    PubMed  Google Scholar 

  • Lyman J, Fleming RH (1940) Composition of sea water. J Marine Sci 3: 134–146

    Google Scholar 

  • McKee MD, Glimcher MJ, Nanci A (1992) High-resolution immunolocalization of osteopontin and osteocalcin in bone and cartilage during endochondral ossification in the chicken tibia. Anat Rec 234: 479–492

    PubMed  Google Scholar 

  • Manton I, Leedale GF (1969) Observations on the microanatomy ofCoccolithus pelagicus andCricosphaera carterae, with special reference to their origin and nature. J Mar Biol Assoc UK 49: 1–16

    Google Scholar 

  • —, Peterfi LS (1969) Observations on the fine structure of coccoliths, scales, and the protoplast of a freshwater coccolithophoridHymenomonas roseola Stein, with supplementary observations on the protoplast ofCricosphaera carterae. Proc R Soc Lond [Biol] 172: 1–15

    Google Scholar 

  • Marsh ME (1986) Biomineralization in the presence of calciumbinding phosphoprotein particles. J Exp Zool 239: 207–220

    PubMed  Google Scholar 

  • — (1989) Self-association of calcium and magnesium complexes of dentin phosphophoryn. Biochemistry 28: 339–345

    PubMed  Google Scholar 

  • —, Sass RL (1983) Calcium-binding phosphoprotein particles in the extrapallial fluid and innermost shell lamella of clams. J Exp Zool 226: 193–203

    Google Scholar 

  • — — (1984) Phosphoprotein particles: calcium and phosphate binding structures. Biochemistry 23: 1448–1456

    PubMed  Google Scholar 

  • —, Chang DK, King GC (1992) Isolation and characterization of a novel acidic polysaccharide containing tartrate and glyoxylate residues from the mineralized scales of a unicellular coccolithophorid algaPleurochrysis carterae. J Biol Chem 267: 20507–20512

    PubMed  Google Scholar 

  • Milner RE, Famulske KS, Michalak M (1992) Calcium binding proteins in the sarcoplasmic/endoplasmic reticulum of muscle and non-muscle cells. Mol Cell Biochem 112: 1–13

    PubMed  Google Scholar 

  • Outka DE, Williams DC (1971) Sequential coccolith morphogenesis inHymenomonas carterae. J Protozool 18: 285–297

    PubMed  Google Scholar 

  • Pienaar RN (1969) The fine structure ofCricosphaera carterae: I. External morphology. J Cell Sci 4: 561–567

    PubMed  Google Scholar 

  • — (1976) The rhythmic production of body covering components in the haptophycean fagellateHymenomonas carterae. In: Watabe N, Wilbur KM (eds) The mechanisms of mineralization in the invertebrates and plants. University of South Carolina Press, Columbia, SC, pp 203–229

    Google Scholar 

  • Stetler-Stevenson WG, Veis A (1987) Bovine dentin phosphophoryn: calcium ion binding properties of a high molecular weight preparation. Calcif Tissue Int 40: 97–102

    PubMed  Google Scholar 

  • Vreeland V (1972) Immunocytochemical localization of the extracellular polysaccharide alginic acid in the brown seaweed,Fucus distichus. J Histochem Cytochem 20: 358–367

    PubMed  Google Scholar 

  • de Vrind-de Jong EW, Borman AH, Thierry R, Westbroek P, Gruter M, Kamerling JP (1986) Calcification in the coccolithophoridsEmiliania huxleyi andPleurochrysis carterae: II. Biochemical aspects. In: Leadbeater SC, Riding R (eds) Biomineralization in lower plants and animals. Clarendon Press, Oxford, pp 205–217

    Google Scholar 

  • van der Wal P, de Jong EW, Westbroek P, de Bruijn WC, Mulder-Stapel AA (1983 a) Polysaccharide localization, coccolith formation and Golgi dynamics in the coccolithophoridHymenomonas carterae. J Ultrastruct Res 85: 139–158

    PubMed  Google Scholar 

  • — — — — (1983 b) Calcification in the coccolithophorid algaHymenomonas carterae. In: Hallberg R (ed) Environmental biogeochemistry. Swedish Research Council, Stockholm, pp 251–258 (Ecological bulletin vol 35)

    Google Scholar 

  • — — — (1983 c) Ultrastructural polysaccharide localization in calcifying and naked cells of the coccolithophoridEmiliania huxleyi. Protoplasma 118: 157–168

    Google Scholar 

  • Westbroek P, van der Wal P, van Emburg PR, de Vrind-de Jong EW, de Bruijn WC (1986) Calcification in the coccolithophoridsEmiliania huxleyi andPleurochrysis carterae: I. Ultrastructural aspects. In: Leadbeater SC, Riding R (eds) Biomineralization in lower plants and animals. Clarendon Press, Oxford, pp 189–203

    Google Scholar 

  • Wheeler AP, Sikes CS (1989) Crystal matrix interactions in CaCO3 biomineralization. In: Mann S, Webb J, Williams RJP (eds) Biomineralization — chemical and biochemical perspectives. VCH, New York, pp 95–131

    Google Scholar 

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  1. Department of Biological Chemistry, The University of Texas, Houston Health Science Center, Dental Branch, P.O. Box 20068, 77225, Houston, TX, USA

    Mary E. Marsh

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  1. Mary E. Marsh
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Marsh, M.E. Polyanion-mediated mineralization — assembly and reorganization of acidic polysaccharides in the Golgi system of a coccolithophorid alga during mineral deposition. Protoplasma 177, 108–122 (1994). https://doi.org/10.1007/BF01378985

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  • DOI: https://doi.org/10.1007/BF01378985

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