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Collagen formation and calcification in teleost scales

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Summary

Electron microscopy of scales from the marine teleost Hippoglossoides elassodon (Pleuronectidae) indicates a morphological and functional similarity to bone and teeth in that a cellular layer apparently deposits collagen fibers which increase in diameter in extracellular locations. The collagen fibers form layers with fiber axes alternating at approximately 90° in the plane of the scale so that the overall structure resembles plywood. The evidence suggests that the matrix between the fibers becomes more concentrated, finally crystallizing by the deposition of material resembling hydroxyapatite located between and within the collagen fibers.

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References

  • Andrew, W.: A covering called skin. In: Textbook of comparative histology, p. 96–137. New York: Oxford University Press 1959.

    Google Scholar 

  • Armed Forces Institute of Pathology: Manual of histologic and special staining technics, 2nd ed., p. 63. New York: McGraw-Hill Book Co., Inc. 1960.

    Google Scholar 

  • Ascenzi, A., and E. C. Beneditti: An electron microscopic study of the foetal membranous ossification. Acta anat. (Basel) 37, 370–385 (1959).

    Google Scholar 

  • Avery, J.K., and S.S. Han: The formation of collagen fibrils in the dental pulp. J. dent. Res. 40, 1248–1261 (1961).

    Google Scholar 

  • Bennett, H.S., and J.H. Luft: S-collidine as a basis for buffering fixatives. J. biophys. biochem. Cytol. 6, 113–114 (1959).

    Google Scholar 

  • Bevelander, G., and H. Nakahara: The formation and mineralization of dentin. Anat. Rec. 156, 303–323 (1966).

    Google Scholar 

  • Bhatia, D.: On the production of annual zones in the scales of the rainbow trout (Salmo irideus) I. J. exp. Zool. 59, 45–60 (1931).

    Google Scholar 

  • Bradburg, S., and G.A. Meek: A study of fibrinogenesis in the leach, Hirudo medicinalis. Quart. J. micr. Sci. 99, 143–148 (1958).

    Google Scholar 

  • Cameron, D.A.: The fine structure of osteoblasts in the metaphysis of the tibia of the young rat. J. biophys. biochem. Cytol. 9, 583–595 (1961).

    Google Scholar 

  • Chapman, J.A.: Morphological and chemical studies of collagen formation. I. The fine structure of guinea pig granulomata. J. biophys. biochem. Cytol. 9, 639–651 (1961).

    Google Scholar 

  • Dudley, H.R., and D. Spiro: The fine structure of bone cells. J. biophys. biochem. Cytol. 11, 627–649 (1961).

    Google Scholar 

  • Farquhar, M.G., and G.E. Palade: Cell junctions in amphibian skin. J. Cell Biol. 26, 263–291 (1965).

    Google Scholar 

  • Fernandez-Madrid, F.: Biosynthesis of collagen. J. Cell Biol. 33, 27–42 (1967).

    Google Scholar 

  • Fitton-Jackson, S.: The fine structure of developing bone in the embryonic fowl. Proc. roy. Soc. B 146, 270–280 (1957).

    Google Scholar 

  • —: Connective tissue cells. In: The cell (J. Brachet and A.E. Mirsky, eds.), vol. VI, p. 387–520. New York: Academic Press 1964.

    Google Scholar 

  • —: The morphogenesis of collagen. In: Treatise on collagen (B. S. Gould, eds.), vol. 2, part B, p. 1–66. New York: Academic Press 1968.

    Google Scholar 

  • —, R.D. Harkness, S.M. Patridge, and G.R. Tristram: Structure and function of connective and skeletal tissue. London: Butterworths & Co. 1965.

    Google Scholar 

  • Frank, R.M.: Etude au microscope électronique de l'odontoblaste et du canalicule dentinaire humain. Arch. oral. Biol. 11, 179–200 (1966).

    Google Scholar 

  • Gallop, P.M.: Concerning some special structural features of the collagen molecule. Biophys. J. 4 (Suppl.), 79–92 (1964).

    Google Scholar 

  • Glimcher, M.J., E.P. Katz, and D.F. Travis: The solubilization and reconstitution of bone collagen. J. Ultrastruct. Res. 13, 163–171 (1965).

    Google Scholar 

  • —, and S.M. Krake: The organization and structure of bone, and the mechanism of calcification. In: Treatise on collagen (B.S. Gould, eds.), vol. 2, part B, p. 67–251. New York: Academic Press 1968.

    Google Scholar 

  • —, G. Mechanic, L.C. Bonar, and E. J. Daniel: The amino acid composition of the organic matrix of decalcified fetal bovine dental enamel. J. biol. Chem. 286, 3210–3213 (1961).

    Google Scholar 

  • Godman, G.C., and K.R. Porter: Chondrogenesis, studied with the electron microscope. J. biophys. biochem. Cytol. 8, 719–760 (1960).

    Google Scholar 

  • Goldberg, B., and H. Green: An analysis of collagen secretion by established mouse fibroblast lines. J. Cell Biol. 22, 227–258 (1964).

    Google Scholar 

  • Gould, B.S. (ed.): Treatise on collagen, vol. 2, Biology of collagen, part A. New York: Academic Press 1968a.

    Google Scholar 

  • — (ed.): Treatise on collagen, vol. 2, Biology of collagen, part B,. New York: Academic Press 1968b.

    Google Scholar 

  • Gray, J., and S.B. Setna: The growth of fish. J. exp. Biol. 8, 55–62 (1931).

    Google Scholar 

  • Green, E.H., and R.W. Tower: The organic constituents of the scales of fish. Bull. U.S. Fish Comm. 21, 97 (1902).

    Google Scholar 

  • Greenlee, T.K., Jr., and R. Ross: The development of the rat flexor digital tendon, a fine structure study. J. Ultrastruct. Res. 18, 354–376 (1967).

    Google Scholar 

  • —, and J. L. Hartmann: The fine structure of elastic fibers. J. Cell Biol. 30, 59–71 (1966).

    Google Scholar 

  • Gross, J.: Collagen. Science 204, 121–130 (1961).

    Google Scholar 

  • Henrickson, R.C., and A.G. Matoltsy: The fine structure of teleost epidermis. 1. Introduction and filament-containing cells. J. Ultrastruct. Res. 21, 194–212 (1967).

    Google Scholar 

  • Hyman, L.H.: The comparative anatomy of the skin and the exoskeleton. In: Comparative vertebrate antomy, p. 79–98. Chicago: University of Chicago Press 1962.

    Google Scholar 

  • Jakus, M.A.: Studies on the cornea: I. The fine structure of the rat cornea. Amer. J. Ophthal. 38 (1, part II), 40–53 (1954).

    Google Scholar 

  • Lacroix, P.: Bone and cartilage. In: The cell (J. Brachet and A.E. Mirsky, eds.), vol. V, p. 219–266. New York: Academic Press 1964.

    Google Scholar 

  • Moss, M.L.: Development of cellular dentin and lepidosteal tubules in the bowfin, Amia calva. Acta anat. (Basel) 58, 333–354 (1964).

    Google Scholar 

  • —: Studies of the cellular bone of teleost fish. V. Histology and mineral homeostasis of freshwater species. Acta anat. (Basel) 60, 262–276 (1965).

    Google Scholar 

  • —, and E. Applebaum: The fibrillar matrix of marsupial enamel. Acta anat. (Basel) 53, 289–297 (1963).

    Google Scholar 

  • —, S.J. Jones, and K.A. Piez: Calcified ectodermal collagen of shark tooth enamel and teleost scale. Science 145, 940–942 (1964).

    Google Scholar 

  • Neave, F.: Origin of the teleost scale-pattern and the development of the teleost scale. Nature (Lond.) 137, 1034–1035 (1936a).

    Google Scholar 

  • —: The development of the scales of Salmo. Trans. roy. Soc. Can., Sect. V 30, 55–72 (1936b).

    Google Scholar 

  • —: On the histology and regeneration of the teleost scale. Quart. J. micr. Sci. 81, 541–568 (1940).

    Google Scholar 

  • Nelsen, O.E.: The integumentary system. In: Comparative embryology of the vertebrates, p. 555–595. New York: The Blakiston Co., Inc. 1953.

    Google Scholar 

  • Norris, W.P., W. Chavin, and L. S. Lombard: Studies of calification in marine teleost. Ann. N.Y. Acad. Sci. 109, 312–336 (1963).

    Google Scholar 

  • Oosten, J. van: Skin and scales. In: The physiology of fishes (M.E. Brown, ed.), vol. 1, p. 207–244. New York: Academic Press, Inc. 1957.

    Google Scholar 

  • Piez, K.A., and J. Gross: The amino acid composition of some fish collagens: The relation between composition and structure. J. biol. Chem. 235, 995–998 (1960).

    Google Scholar 

  • Porter, K.R., and G.D. Pappas: Collagen formation by fibroblasts of the chick embryo dermis. J. biophys. biochem. Cytol. 5, 153–166 (1959).

    Google Scholar 

  • —, and P. Vanamee: Observations on the formation of connective tissue fibers. Proc. Soc. exp. Biol. (N.Y.) 71, 513–516 (1949).

    Google Scholar 

  • Ramachandran, G.N. (ed.): Aspects of protein structure. New York: Academic Press, Inc. 1963.

    Google Scholar 

  • — (ed.): Treatise on collagen, vol. I, Chemistry of collagen. New York: Academic Press 1967.

    Google Scholar 

  • Reith, E.J.: The early stage of amelogenesis as observed in molar teeth of young rats. J. Ultrastruct. Res. 17, 503–526 (1967).

    Google Scholar 

  • —: Collagen formation in developing molar teeth of rats. J. Ultrastruct. Res. 21, 383–414 (1968).

    Google Scholar 

  • Revel, J.P., and E.D. Hay: An autoradiographic and electron microscopic study of collagen synthesis in differentiating cartilage. Z. Zellforsch. 61, 110–144 (1963).

    Google Scholar 

  • Reynolds, E.S.: The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, 208–212 (1963).

    Google Scholar 

  • Rhodin, J.A.G.: An atlas of ultrastructure. Philadelphia: W.B. Saunders Co. 1963.

    Google Scholar 

  • Rich, A., and F.H.C. Crick: The molecular structure of collagen. J. molec. Biol. 3, 483–506 (1961).

    Google Scholar 

  • Richardson, K.G., L. Jarrett, and E.H. Finke: Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Technol. 35, 313–323 (1960).

    Google Scholar 

  • Romer, A.S.: The vertebrate body, 2nd ed. Philadelphia: W.B. Saunders Co. 1962.

    Google Scholar 

  • Ross, R., and E.P. Benditt: Wound healing and collagen formation. V. Quantitative electron microscope radioautographic observations of proline-H3 utilization by fibroblasts. J. Cell Biol. 27, 83–106 (1965).

    Google Scholar 

  • Sasso, W.D., and H.D. Santos: Electron microscopy of enamel and dentin of teeth of the odontaspis (Selachii). J. dent. Res. 40, 49–57 (1961).

    Google Scholar 

  • Seshnaiya, R.V., P. Ambujabai, and M. Kalyani: Amino acid composition of ichthylepidin from fish scales. In: Aspects of protein structure (G.N. Ramachandran, ed.), p. 343–356. New York: Academic Press 1963.

    Google Scholar 

  • Shetyakova, L. F.: Some biological and topographic characteristics of fish scales. Gidrobiolzh 2, 60–67 (1966).

    Google Scholar 

  • Sognnaes, R.F. (ed.): Calcification in biological systems. Washington, D.C.: Amer. Ass. Adv. Sci. Publ. No. 64. 1960.

  • Takuma, S.: Ultrastructure of dentinogenesis. In: Structural and chemical organization of teeth (A.E. Miles, ed.), vol. I, p. 325–370. New York: Academic Press 1967.

    Google Scholar 

  • Travis, D.F.: Matrix and mineral deposition in skeletal structures of the decapod Crustacea. In: Calcification in biological systems (R.F. Sognnaes, ed.), p. 57–116. Washington, D.C.: Amer. Ass. Adv. Sci. Publ. 64. 1960.

  • —: The deposition of skeletal structures in the Crustacea: 5. The histomorphological and histochemical changes associated with the development and calcification of the branchial exoskeleton in the crayfish, Orconectes virilis Hagen. Acta histochem. (Jena) 20, 193–222 (1965).

    Google Scholar 

  • Wallen, O.: On the growth structure and developmental physiology of the scale of fishes. Drottningholm Rep. 38, 385–447 (1957).

    Google Scholar 

  • Watson, M.L., and J.K. Avery: The development of the hamster lower incisor as observed by electron microscopy. Amer. J. Anat. 95, 109–162 (1954).

    Google Scholar 

  • Wellings, S.R., R.G. Chuinard, and R.A. Cooper: Ultrastructural studies of normal skin and epidermal papillomas of the flathead sole, Hippoglossoides elassodon. Z. Zellforsch. 78, 370–387 (1967).

    Google Scholar 

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Authors and Affiliations

  1. Department of Pathology, University of Oregon Medical School, 97201, Portland, Oregon

    G. A. Brown & S. R. Wellings

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  1. G. A. Brown
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  2. S. R. Wellings
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This investigation was supported by Public Health Service research grant CA 08158 from the National Cancer Institute.

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Brown, G.A., Wellings, S.R. Collagen formation and calcification in teleost scales. Z. Zellforsch. 93, 571–582 (1968). https://doi.org/10.1007/BF00338539

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  • DOI: https://doi.org/10.1007/BF00338539

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