Summary
Osteoclasts in metaphyses from young rats were systematically sectioned at different levels. Two types of osteoclasts were recognized. One type had no ruffled border while the other, and predominant type contained a ruffled border in a part of its length; some of the latter contained two ruffled borders. The closest contact between osteoclast and bone occurred at the level of the ruffled border and this bone under the border showed characteristic changes indicative of resorption. In some osteoclasts the ruffled border consisted of numerous slender cytoplasmic projections separated by very narrow spaces or channels while in other osteoclasts it was more open. The ruffled border was commonly surrounded by a transitional zone containing numerous thin filaments. The osteoclast usually had its greatest dimension at the level of the ruffled border and the cytoplasm here contained many bodies and vacuoles but a sparse endoplasmic reticulum. Away from the level of the ruffled border the cytoplasmic vacuoles and bodies were fewer while the endoplasmic reticulum was often more pronounced. Parts of the osteoclasts were usually situated close to a vessel. It is suggested that there is a correlation between the development of the ruffled border and the degree of bone resorption and that osteoclasts without a ruffled border are, at least temporarily, inactive with respect to bone resorption. The numerous cytoplasmic bodies, interpreted as lysosomes, are presumed to be important in the resorption process. The closely adjacent positioning of osteoclasts and vessels may facilitate the transport of resorption products to the blood.
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References
Arey, L.B.: The origin, growth and fate of osteoclasts and their relation to bone resorption. Amer. J. Anat. 26, 315–345 (1920).
Bencosme, S.A., Stone, R.S., Latta, H., Madden, S.C.: A rapid method for localization of tissue structures or lesions for electron microscopy. J. biophys. biochem. Cytol. 5, 508–509 (1959).
Biedermann, W.: Physiologie der Stütz- und Skelettsubstanzen. In: Handbuch der vergleichenden Physiologie, S. 319–1188 (Winterstein, H., ed.). Jena: Gustav Fischer 1914.
Boothroyd, B.: The problem of demineralisation in thin sections of fully calcified bone. J. Cell Biol. 20, 165–173 (1964).
Brody, I.: Keratinization of epidermal cells of normal guinea pig skin as revealed by electron microscopy. J. Ultrastruct. Res. 2, 482–511 (1959).
Cameron, D.A.: The fine structure of bone and calcified cartilage. Clin. Orthop. 26, 199–228 (1963).
Cameron, D.A.: The fine structure and function of bone cells. In: The biological basis of medicine, p. 391–423 (Bittar, E.E., Bittar, N., eds.). London and New York: Academic Press 1969.
Cooper, R.R., Milgram, J.W., Robinson, R.A.: Morphology of the osteon. J. Bone Jt Surg. A 48, 1239–1271 (1966).
Cretin, A.: Contribution histochimique a l'étude de la construction et de la destruction osseuse. Presse méd. 59, 1240–1242 (1951).
Dodds, G.S.: Osteoclasts and cartilage removal in enchondral ossification of certain mammals. Amer. J. Anat. 50, 97–127 (1932).
Doty, S.B., Schofield, H., Robinson, R.A.: The electron microscopic identification of acid phosphatase and adenosintriphosphatase in bone cells following parathyroid extract or thyrocalcitonin administration. In: Parathyroid hormone and thyrocalcitonin (calcitonin), p. 169–181 (Talmage, R.V., Bélanger, L.F., eds.). Amsterdam: Excerpta Medica Foundation 1968.
Dudley, H.R., Spiro, D.: The fine structure of bone cells. J. biophys. biochem. Cytol. 11, 627–649 (1961).
Fell, H.B.: The histiogenesis of cartilage and bone in the long bones of the embryonic fowl. J. Morph. and Physiol. 40, 417–459 (1925).
Fernández-Morán, H.: Applications of a diamond knife for ultrathin sectioning to the study of the fine structure of the biological tissues and metals. J. biophys. biochem. Cytol. 2, 29–30 (1956).
Fetter, A.W., Capen, C.C.: The fine structure of bone in the nasal turbinates of young pigs. Anat. Rec. 171, 329–346 (1971).
Freilich, L.S.: Ultrastructure and acid phosphatase cytochemistry of odontoclasts: Effects of parathyroid extract. J. dent. Res. 50, 1047–1055 (1971).
Furseth, R.: The resorption processes of human deciduous teeth studied by light microscopy, microradiography and electron microscopy. Arch. oral Biol. 13, 417–432 (1968).
Gaillard, P.J.: Parathyroid gland and bone in vitro. VI. Develop. Biol. 1, 152–181 (1959).
Galey, F.R., Nilsson, S.E.G.: A new method for transferring sections from the liquid surface of the trough through staining solutions to the supporting film of a grid. J. Ultrastruct. Res. 14, 405–410 (1966).
Garner, G.E., Steever, R.G.E.: Treatment of diamond knives with Aerosol OT for uniform wetting of their edges in ultramicrotomy. Stain Technol. 45, 186–187 (1970).
Goldhaber, P.: Behavior of bone in tissue culture. In: Calcfication in biological systems, p. 349–372 (Sognnaes, R.F., ed.). Washington, D.C.: American Ass. f. the Advancement of Science 1960.
Gonzales, F., Karnovsky, M.J.: Electron microscopy of osteoclasts in healing fractures of rat bone. J. biophys. biochem. Cytol. 9, 299–316 (1961).
Ham, A.W.: Some histophysiological problems peculiar to calcified tissues. J. Bone Jt Surg. A 34, 701–728 (1952).
Ham, A.W., Gordon, S.D.: Nature of the so-called striated borders of osteoclasts. Anat. Rec. 112, 449 (1952).
Hancox, N.M.: On the occurrence in vitro of cells resembling osteoclasts. J. Physiol. (Lond.) 105, 66–71 (1946).
Hancox, N.: The osteoclast. In: The biochemistry and physiology of bone, p. 213–250 (Bourne, G., ed.). New York: Academic Press Inc. 1956.
Hancox, N.M., Boothroyd, B.: Motion picture and electron microscope studies on the embryonic avian osteoclast. J. biophys. biochem. Cytol. 11, 651–661 (1961).
Hancox, N.M., Boothroyd, B.: Structure-function relationships in the osteoclast. In: mechanisms of hard tissue destruction, p. 497–514 (Sognnaes, R.F., ed.). Washington, D.C.: American Association for the Advancement of Science 1963.
Jackson, C.M.: Zur Histologie und Histogenese des Knochenmarkes. Arch. Anat. u. Entwickl.-Gesch. 1, 33–70 (1904).
Jaffe, H.L.: The resorption of bone. Arch. Surg. 20, 355–385 (1930).
Jordan, H.E.: Further evidence concerning the function of osteoclasts. Anat. Rec. 20, 281–295 (1921).
Kallio, D.M, Garant, P.R., Minkin, C.: Evidence of coated membranes in the ruffled border of the osteoclast. J. Ultrastruct. Res. 37, 169–177 (1971).
Kallio, D.M., Garant, P.R., Minkin, C.: Ultrastructural effects of calcitonin on osteoclasts in tissue culture. J. Ultrastruct. Res. 39, 205–216 (1972).
Kölliker, A.: Die normale Resorption des Knochengewebes. Leipzig: Vogel 1873.
Kroon, D.B.: The bone-destroying function of the osteoclasts. Acta anat. (Basel) 21, 1–18 (1954).
Lucht, U.: Acid phosphatase of osteoclasts demonstrated by electron microscopic histochemistry. Histochemie 28, 103–117 (1971).
Lucht, U.: Absorption of peroxidase by osteoclasts as studied by electron microscope histochemistry. Histochemie 29, 274–286 (1972a).
Lucht, U.: Cytoplasmic vacuoles and bodies of the osteoclast: An electron microscope study. Z. Zellforsch. 135, 229–244 (1972b).
Luft, J.H.: Improvements in epoxy embedding methods. J. biophys. biochem. Cytol. 9, 409–414 (1961).
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. Amer. J. Anat. 129, 451–458 (1970).
Matthews, J.L., Martin, J.H., Collins, E.J.: Intracellular calcium in epithelial, cartilage and bone cells. Calcif. Tiss. Res. Suppl. 4, 37–38 (1970).
Miller, E.J., Martin, G.R.: The collagen of bone. Clin. Orthop. 59, 195–232 (1968).
Neuman, W.F., Mulryan, B.J., Martin, G.R.: A chemical view of osteoclasis based on studies with yttrium. Clin. Orthop. 17, 124–134 (1960).
Pease, D.C.: Buffered formaldehyde as a killing agent and primary fixative for electron microscopy. Anat. Rec. 142, 342 (1962).
Pommer, G.: Ueber die Ostoklastentheorie. Virchows Arch. path. Anat. 92, 296–363 (1883).
Rasmussen, H., Pechet, M.: Calcitonin and thyrocalcitonin. In: Pharmacology of the endocrine system and related drugs: Parathyroid hormone, thyrocalcitonin and related drugs, p. 237–260 (Rasmussen, H., ed.). New York: Pergamon Press 1970.
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).
Robinson, R.A., Cameron, D.A.: Bone. In: Electron microscopic anatomy, p. 315–340 (Kurtz, S.M., ed.). New York: Academic Press 1964.
Sabatini, D.D., Bensch, K., Barrnett, R.J.: Cytochemistry and electron microscopy. The preservation of cellular ultrastructure and enzymatic activity by aldehyde fixation. J. Cell Biol. 17, 19–58 (1963).
Schenk, R.K., Spiro, D., Wiener, J.: Cartilage resorption in the tibial epiphyseal plate of growing rats. J. Cell Biol. 34, 275–291 (1967).
Scherft, J.P.: The lamina limitans of the organic matrix of calcified cartilage and bone. J. Ultrastruct. Res. 38, 318–331 (1972).
Scott, B.L.: The occurrence of specific cytoplasmic granules in the osteoclast. J. Ultrastruct. Res. 19, 417–431 (1967).
Scott, B.L., Pease, D.C.: Electron microscopy of the epiphyseal apparatus. Anat. Rec. 126, 465–495 (1956).
Sjöstrand, F.S.: Ultrastructure of retinal rod synapses of the guinea pig eye as revealed by three-dimensional reconstructions from serial sections. J. Ultrastruct. Res. 2, 122–170 (1958).
Sjöstrand, F.S.: Electron microscopy of cells and tissues. New York and London: Academic Press 1967.
Tonna, E.A.: Osteoclasts and the aging skeleton: A cytological, cytochemical and autoradiographic study. Anat. Rec. 137, 251–269 (1960).
Vaes, G.: On the mechanism of bone resorption. The action of parathyroid hormone on the excretion and synthesis of lysosomal enzymes and on the extracellular release of acid by bone cells. J. Cell Biol. 39, 676–697 (1968).
Vaes, G.: Lysosomes and the cellular physiology of bone resorption. In: Lysosomes in biology and pathology, p. 217–253 (Dingle, J.T., Fell, H.B., eds.). Amsterdam: North-Holland Publishing Company 1969.
Watson, M.L.: Staining of tissue sections for electron microscopy with heavy metals. J. biophys. biochem. Cytol. 4, 475–478 (1958).
Zichner, L.: The effect of calcitonin on bone cells in young rats. An electron microscopic study. Israel J. med. Sci. 7, 359–366 (1971).
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This research was supported by the Danish Research Council. Grant no. 512–727, 512–819 and 512–1545.
I wish to thank Professor Arvid B. Maunsbach for valuable discussions.
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Lucht, U. Osteoclasts and their relationship to bone as studied by electron microscopy. Z. Zellforsch. 135, 211–228 (1972). https://doi.org/10.1007/BF00315127
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DOI: https://doi.org/10.1007/BF00315127