Summary
The comparative ultrastructure of fish bone osteogenesis and resorption induced by scale removal was described in the osteocytic (cellular-boned)Carassius auratus and the anosteocytic (acellular-boned)Tilapia macrocephala. Osteocytes, present in osteocytic bone, were lacking in anosteocytic bone. In osteocytic bone the osteoblast secreted a collagenous preosseous matrix in which it became enmeshed and then was termed a preosteocyte. When the preosseous matrix mineralized, the preosteocyte was termed an osteocyte and was completely surrounded by bone. In anosteocytic bone the osteoblasts receded from the mineralizing front and never became trapped as osteocytes. During resorption, types A and B resorptive cells, present in both bone types, invaded the matrix and demineralized the osseous zone. These cells were characterized by large amounts of granular endoplasmic reticulum and intracellular inclusions containing crystal-like material. Although functionally similar to mammalian osteoclasts, these cells lacked a characteristic ruffled border and were not multinucleated. The osteocytes of cellular bone did not appear to be involved during demineralization.
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References
Moss, M.L.: Osteogenesis of acellular teleost fish bone, Am. J. Anat.108:99–110, 1961
Moss, M.L.: The biology of acellular teleost bone, Ann. N.Y. Acad. Sci.109:337–350, 1963
Moss, M.L.: Studies of the acellular bone of teleost fish. V. Histology and mineral homeostasis of fresh water species, Acta Anat. (Basel)60:262–276, 1965
Moss, M.L.: Studies of the acellular bone of teleost fish. I. Morphological and systematic variations, Acta Anat. (Basel)46:343–362, 1961
Lopez, E., Peignoux-Deville, J., Lallier, F., Martelly, E., Millet, C.: Effects of calcitonin and ultimobrancialectomy (UBX) on calcium and bone metabolism in the eel,Anguilla anguilla L., Calcif. Tissue Res.20:173–186, 1976
Moss, M.L.: Studies of the acellular bone of teleost fish. II. Response to fracture under normal and acalcemic conditions, Acta Anat. (Basel)48:46–60, 1962
Simmons, D.J., Simmons, N.B., Marshall, J.H.: The uptake of calcium-45 in the acellular-bone toadfish, Calcif. Tissue Res.5:206–221, 1970
Mugiya, Y., Watabe, N.: Studies on fish scale formation and resorption. II. Effects of estradiol on calcium homeostasis and skeletal tissue resorption in the goldfish,Carassius auratus, and the killifish,Fundulus heterolitus, Comp. Biochem. Physiol.57A:197–202, 1977
Norris, W.P., Chavin, W., Lombard, L.S.: Studies on calcification in a marine teleost, Ann. N.Y. Acad. Sci.109:312–336, 1963
Brehe, J.E., Fleming, W.R.: Calcium mobilization from acellular bone and effects of hypophysectomy on calcium metabolism inFundulus kansae, J. Comp. Physiol.110:159–169, 1976
Fleming, W.R., Brehe, J., Hanson, R.: Some complicating factors in the study of calcium metabolism of teleosts, Am. Zool.13:793–797, 1973
Weiss, R.E.: The comparative biology of osteogenesis and resorption of fish bone. Ph.D. dissertation, University of S. Carolina, Columbia, 1978
Weiss, R.E., Watabe, N.: Studies on the biology of fish bone. I. Bone resorption after scale removal, Comp. Biochem. Physiol.60A:207–211, 1978
Weiss, R.E., Watabe, N.: Studies on the biology of fish bone. II. Bone matrix changes during resorption, Comp. Biochem. Physiol.61A:245–251, 1978
Spurr, A.R.: A low-viscosity epoxy resin embedding medium for electron microscopy, J. Ultrastruct. Res.26:31–43, 1969
Cameron, D.A.: The ultrastructure of bone. In G.H. Bourne (ed.): The Biochemistry and Physiology of Bone, Vol. I, pp. 191–201. Academic Press, New York, 1972
Pritchard, J.J.: The osteoblast. In G.H. Bourne (ed.): The Biochemistry and Physiology of Bone, Vol. I, pp. 21–44. Academic Press, New York, 1972
Robinson, R.A., Doty, S.B., Cooper, R.R.: Electron microscopy of mammalian bone. In I. Zipkin (ed.): Biological Mineralization, pp. 257–298. John Wiley & Sons, New York, 1974
Lopez, E., Baud, C.A., Boivin, G., Lallier, F.: Etude ultrastructurale, chez un poisson teleosteen l'anguille (Anguilla anguilla L.) des processus de mineralization dans les cas d'une ossification perichondrale de l'arc branchial et d'une apposition secondaire dans l'os vertebral, Ann. Biol. Anim. Biochem. Biophys.18:105–117, 1978
Young, R.W.: Cell proliferation and specialization during endochondral osteogenesis in young rats, J. Cell Biol.14:352–370, 1962
Scott, B.L.: Thymidine-3H electron microscopic autoradiography of osteogenic cells in the fetal rat, J. Cell. Biol.35:115–126, 1967
Marks, S.C., Jr., Walker, D.G.: Mammalian osteopetrosis—a model for studying cellular and humoral factors. In G.H. Bourne (ed.): The Biochemistry and Physiology of Bone, Vol. IV, pp. 223–303. Academic Press, New York, 1976
Weinstock, M.: Elaboration of precursor collagen by osteoblasts as visualized by radioautography after3H-proline administration. In: H.C. Slavkin, R.C. Greulich (eds.): Extracellular Matrix Influences on Gene Expression, Academic Press, New York, 1975
Matthews, J.L., Martin, J.H., Kennedy, J.W., III, Colins, E.J.: An ultrastructural study of calcium and phosphate deposition and exchange in tissues. In: Hard Tissue Growth, Repair and Demineralization, pp. 18–211. Elsevier, Amsterdam, 1973
Bonucci, E.: Fine structure of early cartilage calcification, J. Ultrastruct. Res.20:33–50, 1967
Bonucci, E.: Further investigation on the organic/inorganic relationships in calcifying cartilage, Calcif. Tissue Res.3:38–54, 1969
Bonucci, E.: Fine structure and histochemistry of “calcifying globules” in epiphyseal cartilage, Z. Zellforsch.103:192–217, 1970
Bonucci, E.: The locus of initial calcification in cartilage and bone, Clin. Orthop.78:108–139, 1971
Anderson, H.C.: Vesicles associated with calcification in the matrix of epiphyseal cartilage, J. Cell Biol.41:59–72, 1969
Anderson, H.C.: Matrix vesicle calcification, Fed. Proc.35:103–104, 1976
Maekawa, K., Yamada, J.: Morphological identification and characterization of cells involved in the growth of goldfish scale, Jpn. J. Icthyol.19:1–9, 1972
Waterman, R.E.: Fine structure of scale development in the teleost,Brachydanio rerio, Anat. Rec.168:361–369, 1970
Yamada, J.: A fine structural aspect of the development of the scale in the chum salmon fry, Bull. Jpn. Soc. Sci. Fish.37:18–29, 1971
Kobayashi, S., Yamada, J., Maekawa, K., Ouchi, K.: Calcification and nucleation in fish scales, Biomineralization6:84–90, 1972
Yamada, J., Watabe, N.: Studies on fish scale formation and resorption. I. Fine structure and calcification of the scale inFundulus heteroclitus (Atheriniformes: Cyprinodontidae), J. Morphol.159:49–66, 1979
Olson, O.P.: Histochemical and developmental studies of the scale of the sheepshead minnow,Cyprinodon variegatus. M.S. thesis, University of South Carolina, Columbia, 1977
Martin, J.H., Matthews, J.L.: Mitochondrial granules in chondrocytes, osteoblasts, and osteocytes, Clin. Orthop.68:273–278, 1970
Matthews, J.L.: Ultrastructure of calcifying tissues, Am. J. Anat.129:451–458, 1970
Sayegh, F.S., Abousy, A.: Mitochondria granule distribution in tooth germ cells, Anat. Rec.189:451–466, 1977
Becker, G.L., Chen, C.-H., Greenwalt, J.W., Lehninger, A.L.: Calcium phosphate granules in the hepatopancreas of blue crab,Callinectes sapidus, J. Cell Biol.61:316–326, 1974
Watabe, N., Meenakshi, V.R., Blackwelder, P.L., Kurtz, E.M., Dunkelberger, D.G.: Calcareous spherules in the gastropod,Pomacia paludosa. In N. Watabe, K.M. Wilbur (eds.): The Mechanisms of Mineralization in the Invertebrates and Plants, pp. 283–308. University of South Carolina Press, Columbia, 1976
Watabe, N., Blackwelder, P.L.: Ultrastructure and calcium localization in the mantle epithelium of the freshwater gastropodPomacea paludosa during shell regeneration. Proc. 3rd Int. Conf. Biomineralization. (in press)
Sapiro, I.M., Greenspan, J.S.: Are mitochondria directly involved in biological mineralization?, Calcif. Tissue Res.3:100–102, 1969
Lehninger, A.L.: Mitochondria and calcium ion transport, Biochem. J.119:129–138, 1970
Lehninger, A.L., Reynafarje, B., Vercesi, A., Teiv, W.P.: Transport and accumulation of calcium in mitochondria, Ann. N.Y. Acad. Sci.307:160–176, 1978
Carafoli, E., Crompton, M.: Calcium ions and mitochondria. In: Calcium in Biological Systems, Symposium of The Society for Experimental Biology, No. XXX, pp. 80–116. Cambridge University Press, Cambridge, 1976
Simkiss, K.: Cellular aspects of calcification. In N. Watabe, K.M. Wilbur (eds.): The Mechanisms of Mineralization in the Invertebrates and Plants, pp. 1–31. University of South Carolina Press, Columbia, 1976
Bornstein, P.: The biosynthesis of collagen, Annu. Rev. Biochem.43:567–603, 1974
Bélanger, L.F.: Osteocytic resorption. In G.H. Bourne (ed.): The Biochemistry and Physiology of bone, Vol. III, pp. 240–270. Academic Press, New York, 1971
Krempien, B., Maregold, C., Ritz, E., Bommer, J.: The influence of immobilization on osteocyte morphology, Virchows Arch [Pathol. Anat.]370:55–68, 1976
Fleming, W.R.: Calcium metabolism of teleosts, Am. Zool.7:835–842, 1967
Hancox, N.J.: The osteoclast. In G.H. Bourne (ed.): The Biochemistry and Physiology of Bone, Vol. I, pp. 45–69. Academic Press, New York, 1972
Kahn, A.J., Simmons, D.J.: Investigation of cell lineage in bone using a chimera of chick and quail embryonic tissue, Nature258:325–327, 1975
Jotereau, F.V., Le Dovarin, N.M.: The developmental relationship between osteocytes and osteoclasts: a study using the quail-chick nuclear marker in endochondrial ossification, Dev. Biol.63:253–265, 1978
Ouchi, K., Yamada, J., Kosaka, S.: On the resorption of scales and associated cells in precocious male parr of the Masu salmon (Oncorhynchus masou), Bull. Jpn. Soc. Sci. Fish.38:423–430, 1972
Neuman, W.F., Mulryan, B.J., Martin, G.R.: A chemical study of osteoclasis based on studies with yttrium, Clin. Orthop.17:124–134, 1960
Baud, C.A.: Submicroscopic structure and functional aspects of the osteocyte, Clin. Orthop.56:223–236, 1968
Jande, S.S., Belanger, L.F.: The life cycle of the osteocyte, Clin. Orthop.94:281–305, 1973
Bonucci, E.: The organic-inorganic relationships in bone matrix undergoing osteoclastic resorption, Calcif. Tissue Res.16:13–36, 1974
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Weiss, R.E., Watabe, N. Studies on the biology of fish bone. III. Ultrastructure of osteogenesis and resorption in osteocytic (cellular) and anosteocytic (acellular) bones. Calcif Tissue Int 28, 43–56 (1979). https://doi.org/10.1007/BF02441217
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DOI: https://doi.org/10.1007/BF02441217