The Histology, Histochemistry, and Ultrastructure of Bone

  • Ermanno Bonucci
Part of the NATO ASI Series book series (NSSA, volume 184)


Bone is a composite tissue whose properties (mechanical and metabolic) closely depend on its structure and composition. Although its complexity is accentuated by the existence of different types and levels of tissue organization, knowledge of the histological, histochemical and ultrastructural characteristics of its individual components is fundamental for understanding its physiological activities (modality of formation and resorption, mechanism of calcification, metabolic turnover) and pathological changes. Because the bone tissue consists of cells and intercellular matrix, these constituents will be considered separately.


Bone Resorption Bone Cell Bone Matrix Collagen Fibril Acid Phosphatase Activity 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. 1.
    G. Vaes, Cellular biology and biochemical mechanism of bone resorption, Clin. Orthop. 231: 239–271 (1988).Google Scholar
  2. 2.
    W.A. Peck, and W.L. Woods, The cells of bone, in: “Osteoporosis: Etiology, Diagnosis, and management”, B.L. Riggs and L.J. Melton, eds., Raven Press, New York (1988).Google Scholar
  3. 3.
    D.A. Cameron, The fine structure of osteoblasts in the metaphysis of the tibia of the young rat, J. Biophys. Biochem. Cytol. 9: 583595 (1961).Google Scholar
  4. 4.
    R.H. Dudley, and D. Spiro, The fine structure of bone cells, J. Biophys. Biochem. Cytol. 11: 627–649 (1961).Google Scholar
  5. 5.
    G. Göthlin, and J.L.E. Ericsson, Electron microscopic studies of cytoplasmic filaments and fibers in different cell types of fracture callus in the rat. Virchows Arch. Abt. B Zellpath. 6: 24–37 (1970).Google Scholar
  6. 6.
    G.J. King, and M.E. Holtrop, Actine-like filaments in bone cells of cultured mouse calvaria as demonstrated by binding to heavy meromyosin, J. Cell Biol. 66: 445–451 (1975).PubMedCrossRefGoogle Scholar
  7. 7.
    S.B. Doty, Morphological evidence of gap junctions between bone cells, Calcif. Tiss. Int. 33: 509–512 (1981).Google Scholar
  8. 8.
    S.W. Whitson, Tight junction formation in osteon, Clin. Orthop. 86: 206–213 (1972).Google Scholar
  9. 9.
    R.L. Cabrini, Histochemistry of ossification, Int. Rev. Cytol. 11: 283–306 (1961).CrossRefGoogle Scholar
  10. 10.
    G.H. Bourne, Phosphatase and calcification, in: “The biochemistry and physiology of bone”, G.H. Bourne, ed., Academic Press, New York and London (1972).Google Scholar
  11. 11.
    M.S. Burstone, Histochemical observations on enzymatic processes in bone and teeth, Ann. N. Y. Acad. Sci. 85: 431–444 (1960).PubMedCrossRefGoogle Scholar
  12. 12.
    D.C. Morris, J.C. Randall, and H.C. Anderson, Light microscopic localization of alkaline phosphatase in fetal bovine bone using immunoperoxidase and immunogold-silver staining procedures, J. Histochem. Cytochem. 36: 323–327 (1988).Google Scholar
  13. 13.
    S.B. Doty, and B.H. Schofield, Enzyme histochemistry of bone and cartilage cells, Progr. Histochem. Cytochem. 8: 1–38 (1976).Google Scholar
  14. 14.
    G. Göthlin, and J.L.E. Ericsson, Studies on the ultrastructural localization of adenosine triphosphatase activity in fracture callus, Histochemie 35: 111–126 (1973).Google Scholar
  15. 15.
    Fukushima, and N. Goshi, Neutral ATP-hydrolyzing enzyme activity on the plasma membrane of osteoblasts, Acta Histochem. Cytochem. 16: 216–222 (1983).Google Scholar
  16. 16.
    M. Takagi, R.T. Parmley, Y. Toda, and F.R. Denys, Ultrastructural cytochemistry of complex carbohydrates in osteoblasts, osteoid, and bone matrix, Calcif. Tiss. Int. 35: 309–319 (1983).Google Scholar
  17. 17.
    P. Bianco, P. Ballanti, and E. Bonucci E., Tartrate-resistant acid phosphatase activity in rat osteoblasts and osteocytes. Calcif. Tiss. Int. 43: 167–171 (1988).Google Scholar
  18. 18.
    M. Weinstock, Elaboration of precursor collagen by osteoblasts as visualized by radioautography after 3H-proline administration, in: “Extracellular matrix influence on gene expression”, H.C. Slavkin and R.C. Greulich, eds., Academic Press, New York (1975).Google Scholar
  19. 19.
    Von der Mark, H. Von der Mark, and S. Gay, Study of differential collagen synthesis during development of the chick embryo by immunofluorescence. II. Localization of type I and type II collagen during long bone development, Dev. Biol. 53: 153–170 (1976).Google Scholar
  20. 20.
    G.M. Wright, and C.P. Leblond, Immunohistochemical localization of procollagens. III. Type I procollagen antigenicity in osteoblasts and prebone (osteoid), J. Histochem. Cytochem. 29: 791–804 (1981).Google Scholar
  21. 21.
    S.C.Jr. Marks, and S.N. Popoff, Bone cell biology: the regulation of development, structure, and function in the skeleton, Am. J. Anat. 183: 1–44 (1988).PubMedCrossRefGoogle Scholar
  22. 22.
    M.P. Mark, C.W. Prince, S. Gay, R.L. Austin, M. Bhown, R.D. Finkelman, and W.T. Butler, A comparative immunocytochemical study on the subcellular distribution of 44kDa bone phosphoprotein and bone -carboxyglutamic acid (Gla)-containing protein in osteoblasts. J. Bone Min. Res. 2: 337–346 (1987).Google Scholar
  23. 23.
    A.L.J.J. Bronckers, S. Gay, M.T. Dimuzio, and W.T. Butler, Immunolocalization of -carboxyglutamic acid-containing proteins in developing molar tooth germs of the rat, Collag. Rel. Res. 5: 17–22 (1985).Google Scholar
  24. 24.
    A.J. Camarda, W.T. Butler, R.D. Finkelman, and A. Nanci Immunocytochemical localization of -carboxyglutamic acid-containing protein (Osteocalcin) in rat bone and dentin, Calcif. Tiss. Int. 40: 349–355 (1987).Google Scholar
  25. 25.
    G. Jundt, K.-H. Berghauser, J.D. Termine, and A. Schulz, Osteonectin–a differentiation marker of bone cells, Cell Tiss. Res. 248: 409–415 (1987).Google Scholar
  26. 26.
    P. Bianco, G. Silvestrini, J.D. Termine, and E. Bonucci, Immunohistochemical localization of osteonectin in developing human and calf bone using monoclonal antibodies, Calcif. Tiss. Int. 43: 155–161 (1988).Google Scholar
  27. 27.
    S. Sakamoto, and M. Sakamoto, Biochemical and immunohistochemical studies on collagenase in resorbing bone in tissue culture, J. Periodont. Res. 17: 523–526 (1982).PubMedCrossRefGoogle Scholar
  28. 28.
    S. Sakamoto, and M. Sakamoto, Bone collagenase, osteoblasts and cell-mediated bone resorption, in: “Bone and mineral research/4”, W.A. Peck, ed., Elsevier, Amsterdam, New York, Oxford (1986).Google Scholar
  29. 29.
    G. Marotti, Three dimensional study of the osteocyte lacunae, in: “Bone histomorphometry”, W.S.S. Jee, A.M. Parfitt, eds., Armour Montagu, Paris (1981).Google Scholar
  30. 30.
    G. Marotti, Osteocyte orientation in human lamellar bone and its relevance to the morphometry of periosteocytic lacunae, Metab. Bone Dis. Rel. Res. 1: 325–333 (1979).Google Scholar
  31. 31.
    A. Baud, Morphologie et structure inframicroscopique des ostéocytes, Acta anat. 51: 209–225 (1962).Google Scholar
  32. 32.
    S.S. Jande, Fine structural study of osteocytes and their surrounding bone matrix with respect to their age in young chicks, J. Ultrastruct. Res. 37: 279–300 (1971)Google Scholar
  33. 33.
    S.S. Jande, and L.F. Bélanger, Electron microscopy of osteocytes and the pericellular matrix in rat trabecular bone, Calcif. Tiss. Res. 6: 280–289 (1971).Google Scholar
  34. 34.
    S.C. Luk, C. Nopajaroonsri, and G.T. Simon, The ultrastructure of cortical bone in young adult rabbits, J. Ultrastruct. Res. 46: 184205 (1974).Google Scholar
  35. 35.
    E. Bonucci, The ultrastructure of the osteocyte, in: “Ultrastructure of skeletal tissues - Bone and cartilage in normalcy and pathology”, E. Bonucci and P.M. Motta, eds., CRC Press, Boca Raton (1989; in press).Google Scholar
  36. 36.
    J.M. Weinger, and M.E. Holtrop, An ultrastructural study of bone cells: the occurrence of microtubules, microfilaments and tight junctions. Calcif. Tiss. Res. 14: 15–29 (1973).Google Scholar
  37. 37.
    M. Federman, and G.Jr. Nichols, Bone cell cilia: vestigial or functional organelles? Calcif. Tiss. Res. 17: 81–85 (1974).Google Scholar
  38. 38.
    F. Wassermann, and J.A. Yaeger, Fine structure of the osteocyte capsule and of the wall of the lacunae in bone, Z. Zellforsch. 67: 636–652 (1965).CrossRefGoogle Scholar
  39. 39.
    E. Bonucci, and G. Gherardi, 1977, Osteocyte ultrastructure in renal osteodystrophy, Virchows Arch. A Path. Anat. Histol. 373, 213–231 (1977).Google Scholar
  40. 40.
    K. Donath, and G. Delling, Elektronenmikroskopische Darstellung der periosteocytaren Matrix durch Ultradunnschnitt-EDTA-entkalkung, Virchows Arch. 354 A: 305–311 (1971).Google Scholar
  41. 41.
    S.S. Jande, and L.F. Bélanger, The life cycle of the osteocyte, Clin. Orthop. 94: 281–305 (1973).Google Scholar
  42. 42.
    E.A. Tonna, Electron microscopic evidence of alternating osteocyticosteoclastic and osteoplastic activity in the perilacunar walls of aging mice, Connect. Tiss. Res. 1: 221–230 (1972).Google Scholar
  43. 43.
    V.L. Yeager, S. Chiemchanya, and P. Chaiseri, Changes in size of lacunae during the life of osteocytes in osteons of compact bone, J. Gerontol. 30: 9–14 (1975).PubMedCrossRefGoogle Scholar
  44. 44.
    A. Zambonin Zallone, A. Teti, B. Nico, M.V. Primavera, Osteoplastic activity of mature osteocytes evaluated by 3H-proline incorporation, Basic Appl, Histochem. 26: 65–67 (1982).Google Scholar
  45. 45.
    C. Palumbo, A three-dimensional ultrastructural study of osteoidosteocytes in the tibia of chick embryos, Cell Tiss. Res. 246: 125131 (1986).Google Scholar
  46. 46.
    G. Marotti, Decrement in volume of osteoblasts during osteon formation and its effect on the size of the corresponding osteocytes, in: “Bone histomorphometry”, P.J. Meunier, ed., Armour Montagu, Paris (1977).Google Scholar
  47. 47.
    L.F. Bélanger, Osteocytic osteolysis, Calcif. Tiss. Int. 4: 1–12 (1969).Google Scholar
  48. 48.
    L.F. Bélanger, Osteocytic resorption, In: “The biochemistry and physiology of bone”, 2nd ed., v. 3, G.H. Bourne, ed., Academic Press, New York (1971).Google Scholar
  49. 49.
    A. Boyde, Scanning electron microscope studies of bone, in: “The biochemistry and physiology of bone”, 2nd ed., v. 1, G.H. Bourne, ed., Academic Press, New York (1972).Google Scholar
  50. 50.
    A. Boyde, S.J. Jones, and J. Ashford, Scanning electron microscope observations and the question of possible osteocytic bone mini-(re)modelling, in: “Current advances in skeletogenesis”, M. Silbermann, H.C. Slavkin, eds., Excerpta Medica, Amsterdam (1982).Google Scholar
  51. 51.
    G. Marotti, The original contribution of the SEM to the knowledge of bone structure, in: “Ultrastructure of skeletal tissues - Bone and cartilage in normalcy and pathology”, E. Bonucci and P.M. Motta, eds., CRC Press, Boca Raton (1989, in press).Google Scholar
  52. 52.
    L.F. Bélanger, and J. Robichon, Parathormone-induced osteolysis in dogs, J. Bone Joint Surg. 46A: 1008–1012 (1964).PubMedGoogle Scholar
  53. 53.
    P. Meunier, J. Bernard, and G. Vignon, La mesure de l’élargissement périostéocytaire appliquée au diagnostic des hyperparathyroidies, Path. Biol. 19: 371–378 (1971).Google Scholar
  54. 54.
    B. Krempien, G. Geiger, E. Ritz, and S. Buttner, Osteocytes in chronic uremia. Differential count of osteocytes in human femoral bone, Virchows Arch. Abt. A Path. Anat. 360: 1–9 (1973).Google Scholar
  55. 55.
    J. Duriez, Les modifications calciques péri-ostéocytaires. Etude microradiographique à l’analyseur automatique d’images, Nouv. Presse Méd. 3: 2007–2010 (1974).Google Scholar
  56. 56.
    E, Bonucci, V. Lo Cascio, S. Adami, L. Cominacini, G. Galvanini, and A. Scuro, The ultrastructure of bone cells and bone matrix in human primary hyperparathyroidism, Virchows Arch. Abt. A Path. Anat. 379: 11–23 (1978).Google Scholar
  57. 57.
    L.F. Bélanger and B.B. Migicovsky, Histochemical avidence of proteolysis in bone: the influence of parathormone, J. Histochem. Cytochem. 11: 735–737 (1963).CrossRefGoogle Scholar
  58. 58.
    D.A. Cameron, H.A. Paschall, and R.A. Robinson, Changes in the fine structure of bone cells after the administration of parathyroid extract, J. Cell Biol. 33: 1–14 (1967).PubMedCrossRefGoogle Scholar
  59. 59.
    W. Remagen, H.J. Höhling, T.T. Hall, and R. Caesar, Electron microscopical and microprobe observations on the cell sheath of stimulated osteocytes, Calcif. Tiss. Res. 4: 60–68 (1969).Google Scholar
  60. 60.
    A. Schulz, K. Donat, and G. Delling, Ultrastruktur und Entwicklung des Corticalisosteocyten. Tiereexperimentelle Untersuchungen an der Rattentibia, Virchows Arch. A Path. Anat. Histol. 364: 347–356 (1974).Google Scholar
  61. 61.
    S.E. Weisbrode, C.C. Capen, and L.A. Nagode, Effects of parathyroid hormone on bone of thyroparathyroidectomized rats, Am. J. Path. 75: 529–542 (1974).PubMedGoogle Scholar
  62. 62.
    M.P. Anderson, and C.C. Capen, Fine structural changes of bone cells in experimental nutritional osteodystrophy of green iguanas, Virchows Arch. B Cell Path. 20, 169–184 (1976).Google Scholar
  63. 63.
    B. Krempien, and E. Ritz, Effects of parathyroid hormone on osteocytes. Ultrastructural evidence for anisotropic osteolysis and involvement of the cytoskeleton, Metab. Bone Dis. Rel. Res. 1: 55–65 (1978).Google Scholar
  64. 64.
    V. Cané, G. Marotti, G. Volpi, D. Zaffe, S. Palazzini, F. Remaggi, and M.A. Muglia, Size and density of osteocyte lacunae in different regions of long bones, Calcif. Tiss. Int. 34: 558–563 (1982).Google Scholar
  65. 65.
    R. Steendijk, and A. Boyde, Scanning electron microscopic observations on bone from patients with hypophosphatemic (vitamin D resistant) rickets, Calcif. Tiss. Res. 11: 242–250 (1973).Google Scholar
  66. 66.
    C. Minkin, Bone acid phosphatase: tartrate-resistant acid phosphatase as a marker of osteoclast function, Calcif. Tiss. Int. 34: 285290 (1982).Google Scholar
  67. 67.
    F.P. Van de Wijngaert, and E.H. Burger, Demonstration of tartrate-resistant acid phosphatase in undecalcified, glycolmetacrylateembedded mouse bone: a possible marker of (pre)osteoclast identification, J. Histochem. Cytochem 34: 1317–1323 (1986).Google Scholar
  68. 68.
    P.L. Sannes, B.H. Schofield, and D.F. McDonald, Histochemical evidence of cathepsin B, dipeptidyl peptidase I, and dipeptidyl peptidase II in rat bone, J. Histochem. Cytochem. 34: 983–988 (1986).Google Scholar
  69. 69.
    Recklinghausen, F.v., “Untersuchungen über Rachitis und Osteomalacia”, Gustav Fischer, Jena (1910).Google Scholar
  70. 70.
    Miller, S.C., and Jee, W.S.S., The bone lining cell: a distinct phenotype? Calcif. Tiss. Int. 41: 1–5 (1987).Google Scholar
  71. 71.
    C.J. Vander Wiel, S.A. Grubb, and R.V. Talmage, The presence of lining cells on surfaces of human trabecular bone, Clin. Orthop. 134: 350–355 (1978).Google Scholar
  72. 72.
    B.M. Bowman’, and S.C. Miller, The proliferation and differentiation of the bone-lining cell in estrogen-induced osteogenesis, Bone 7: 351–357 (1986).Google Scholar
  73. 73.
    F. Canas, A.R. Terepka, and W.F. Neuman, Potassium and milieu interior of bone, Am. J. Physiol. 217: 117–120 (1969).PubMedGoogle Scholar
  74. 74.
    H. Norimatsu, C.J. Vander Wiel, and R.V. Talmage, Morphological support of a role for cells lining bone surfaces in maintenance of plasma calcium concentration, Clin. Orthop. 138: 254–262 (1979).Google Scholar
  75. 75.
    D.A. Cameron, The ultrastructure of bone, in: “The biochemistry and physiology of bone”, G.H. Bourne, ed., 2nd ed., v. 1, Academic Press, New York, San Francisco, London (1972).Google Scholar
  76. 76.
    N.M. Hancox, “Biology of bone”, University Press, Cambridge (1972).Google Scholar
  77. 77.
    U. Lucht, The ultrastructure of osteoclasts under normal and experimental conditions, Thesis, University of Aarhus (1974).Google Scholar
  78. 78.
    B.K. Hall, The origin and fate of osteoclasts, Anat. Record 183: 112 (1975).Google Scholar
  79. 79.
    G. Göthlin, and J.L.E. Ericsson, The osteoclast. Review of ultra-structure, origin, and structure-function relationship, Clin. Orthop. 120: 201–231 (1976).Google Scholar
  80. 80.
    M.E. Holtrop, and G.J. King, The ultrastructure of the osteoclast and its functional implications, Clin. Orthop. 123: 177–196 (1977).Google Scholar
  81. 81.
    E. Bonucci, New knowledge on the origin, function and fate of osteoclasts, Clin. Orthop. 158: 252–269 (1981).Google Scholar
  82. 82.
    G.R. Mundy, and G.D. Roodman, Osteoclast ontogeny and function, in: “Bone and mineral research/V”, W.A. Peck, ed., Elsevier, Amsterdam, New York, Oxford (1987).Google Scholar
  83. 83.
    W.E. Huffer, Biology of disease. Morphology and biochemistry of bone remodeling: possible control by vitamin D, parathyroid hormone, and other substances, Lab. Invest. 59: 418–442 (1988).Google Scholar
  84. 84.
    S.C.Jr. Marks, and S.N. Popoff, Ultrastructural biology and pathology of the osteoclast, in: “Ultrastructure of skeletal tissues - Bone and cartilage in normalcy and pathology”, E. Bonucci and P.M. Motta, eds., CRC Press, Boca Raton (1989, in press).Google Scholar
  85. 85.
    E. Bonucci, The organic-inorganic relationships in bone matrix undergoing osteoclastic resorption, Calcif. Tiss. Res. 16: 13–36 (1974).Google Scholar
  86. 86.
    N.M. Hancox, and B. Boothroyd, Structure-function relationships in the osteoclast, in: “Mechanisms of hard tissue destruction”, R.F. Sognnaes, ed., Amer. Ass. for the Advancement of Science, Washington (1963).Google Scholar
  87. 87.
    G. Göthlin, and J.L.E. Ericsson, Fine structural localization of acid phosphomonoesterase in the brush border region of the osteoclasts, Histochemie 28: 337–344 (1971).Google Scholar
  88. 88.
    S.B. Doty, and B.H. Schofield, Electron microscopic localization of hydrolytic enzymes in osteoclasts, Histochem. J. 4: 245–258 (1972).Google Scholar
  89. 89.
    U. Lucht, Acid phosphatase of osteoclasts demonstrated by electron microscopic histochemistry, Histochemie 28: 103–117 (1971).Google Scholar
  90. 90.
    R.E. Anderson, D.M. Woodbury, and W.S.S. Jee, Humoral and ionic regulation of osteoclast acidity, Calcif. Tiss. Int. 39: 252–258 (1986).Google Scholar
  91. 91.
    C.V. Gay, and W.J. Mueller, Carbonic anhydrase and osteoclasts: localization by labelled inhibitor autoradiography, Science 183: 432–434 (1974).Google Scholar
  92. 92.
    R.E. Anderson, H. Schraer, and C.V. Gay, Ultrastructural immunocytochemical localization of carbonic anhydrase in normal and calcitonin-treated chick osteoclasts, Anat. Record 204: 9–20 (1982).CrossRefGoogle Scholar
  93. 93.
    H.K. Vaananen, and E.-K. Parvinen, High active isoenzyrne of carbonic anhydrase in rat calvaria osteoclasts. Immunohistochemical study, Histochemistry 78: 481–485 (1983).CrossRefGoogle Scholar
  94. 94.
    R. Baron, L. Neff, C. Roy, A. Boisvert, and M. Caplan, Cell-mediated extracellular acidification and bone resorption: evidence for a low pH in resorbing lacunae and localization of a 100-kD lysosomal membrane protein at the osteoclast ruffled border, J. Cell Biol. 101: 2210–2222 (1986).Google Scholar
  95. 95.
    H. Rasmussen, and P. Bordier, “The physiological and cellular basis of metabolic bone disease”, Williams and Wilkins, Baltimore (1974).Google Scholar
  96. 96.
    H.M. Frost, Dynamics of bone remodelling, in: “Bone biodynamics”, H.M. Frost, ed., Little, Brown, and Co., Boston (1964).Google Scholar
  97. 97.
    P. Tran Van, A. Vignery, and R. Baron, An electron-microscopic study of the bone-remodeling sequence in the rat, Cell Tiss. Res. 225: 283–292 (1982).Google Scholar
  98. 98.
    R. Baron, A. Vignery, and M. Horowitz, Lymphocytes, macrophages and the regulation of bone remodeling, in: “Bone and Mineral Research Annual 2”, W.A. Peck, ed., Elsevier, Amsterdam, New York, Oxford (1984).Google Scholar
  99. 99.
    G.A. Rodan, and S.B. Rodan, Expression of the osteoblastic phenotype, in: “Bone and mineral research annual 2”, W.A. Peck, ed., Elsevier, Amsterdam, New York, Oxford (1984).Google Scholar
  100. 100.
    G.A. Rodan, T.J. Martin, Role of osteoblasts in hormonal control of bone resorption - a hypothesis. Calcif. Tiss. Int. 33: 349–351 (1981).Google Scholar
  101. 101.
    E.G. Burger, J.W.M. Van der Meer, and P.J. Nijweide, Osteoclast formation from mononuclear phagocytes: role of bone-forming cells, J. Cell Biol. 99: 1901–1906 (1984).PubMedCrossRefGoogle Scholar
  102. 102.
    J.K. Heath, S.J. Atkinson, M.C. Meikle, and J.J. Reynolds, Mouse osteoblasts synthesize collagenase in response to bone resorbing agents, Biochim. Biophys. Acta 802: 151–154 (1984).Google Scholar
  103. 103.
    G.L. Wong, Paracrine interactions in bone-secreted products of osteoblasts permit osteoclasts to respond to parathyroid hormone, J. Biol. Chem. 259: 4019–4022 (1984).Google Scholar
  104. 104.
    T.J. Chambers, and K. Fuller, Bone cells predispose bone surface to resorption by exposure of mineral to osteoclastic contact, J. Cell Sci. 76: 155–165 (1985).PubMedGoogle Scholar
  105. 105.
    R.L. Jilka, Are osteoblastic cells required for the control of osteoclast activity by parathyroid hormone?, Bone and Miner. 1: 261266 (1986).Google Scholar
  106. 106.
    P.M.J. McSheehy, and T.J. Chambers, 1,25-dihydroxyvitamin D stimulates rat osteoblastic cells to release a soluble factor that increases osteoclastic bone resorption, J. Clin. Invest. 80: 425–429 (1987).PubMedCrossRefGoogle Scholar
  107. 107.
    A. Ascenzi, and E. Bonucci, A quantitative investigation of the birefringence of the osteon, Acta anat. 44: 236–262 (1961).CrossRefGoogle Scholar
  108. 108.
    A. Ascenzi, The micromechanics versus the macromechanics of corti-cal bone — A comprehensive presentation, J. Biomechan. Engineer. 110: 357–363 (1988).CrossRefGoogle Scholar
  109. 109.
    J.D. Termine, Phenotypic proteins of calf lamellar bone, in: “Current advances in skeletogenesis”, M. Silbermann, and H.C. Slavkin, eds., Excerpta Medica, Amsterdam, Oxford, Princeton (1982).Google Scholar
  110. 110.
    J.D. Termine, Osteonectin and other newly described proteins of developing bone, in: “Bone and mineral research, annual 1”, W.A. Peck, ed., Excerpta Medica, Amsterdam, Oxford, Princeton (1983).Google Scholar
  111. 111.
    W.T. Butler, Matrix macromolecules of bone and dentin, Collagen Rel. Res. 4: 297–307 (1984).Google Scholar
  112. 112.
    J.D. Termine, A.B. Belcourt, K.M. Conn, and H.K. Kleinman, Mineral and collagen-binding proteins of fetal calf bone, J. Biol. Chem. 256: 10403–10408 (1981).Google Scholar
  113. 113.
    P. Bianco, Y. Hayashi, G. Silvestrini, J.D. Termine, and E. Bonucci, Osteonectin and GLA-protein in calf bone: ultrastructural immunohistochemical localization using the protein A-gold method, Calcif. Tiss. Int. 37: 684–686 (1984).Google Scholar
  114. 114.
    P.A. Price, M.R. Urist, and Y. Otawara, Matrix Gla protein, a new -carboxyglutarnic acid-containing protein which is associated with the organic matrix of bone, Biochem. Biophys. Res. Comm. 117: 765771 (1983).Google Scholar
  115. 115.
    A.S. Posner, Bone mineral and the mineralization process, in: “Bone and mineral research/5”, W.A. Peck, ed., Elsevier, Amsterdam, New York, Oxford (1987).Google Scholar
  116. 116.
    M.J. Glimcher, and S.M. Krane, The organization and structure of bone, and the mechanism of calcification, in: “Treatise on collagen; v. 2, Biology of collagen”, B.S. Gould, ed., Academic Press, London and New York (1968).Google Scholar
  117. 117.
    A. Ascenzi, E. Bonucci, and D. Steve Bocciarelli, An electron microscope study of osteon calcification, J. Ultrastruct. Res. 12: 287–303 (1965).Google Scholar
  118. 118.
    A. Ascenzi, E. Bonucci, and D. Steve Bocciarelli, An electron microscope study on primary periosteal bone, J. Ultrastruct. Res. 18: 605–618 (1967).Google Scholar
  119. 119.
    E. Bonucci, The structural basis of calcification, in: “Ultra-structure of the connective tissue matrix”, A. Ruggeri and P.M. Motta, eds., Martinus Nijhoff Publ., Boston, The Hague, Dordrecht, Lancaster (1984).Google Scholar
  120. 120.
    M.J. Glimcher, Molecular biology of mineralized tissues with particular reference to bone, Rev. Mod. Phys. 31: 359–393 (1959).Google Scholar
  121. 121.
    M.J. Glimcher, Composition, structure, and organization of bone and other mineralized tissues and the mechanism of calcification, in: “Handbook of physiology: Endocrinology”, v. 7, R.O. Greep, E.B. Astwood, eds., Am. Physiol. Soc., Washington (1976).Google Scholar
  122. 122.
    M.U. Nylen, D.B. Scott, and V.M. Mosley, Mineralization of turkey leg tendon. II. Collagen-mineral relations revealed by electron and X-ray microscopy, in: “Calcification in biological systems”, R.F. Sognnaes, ed., Am. Ass. Adv. Sci., Washington (1960).Google Scholar
  123. 123.
    W.J. Landis, A study of calcification in the leg tendons from the domestic turkey, J. Ultrastruct. Molec. Struct. Res. 94: 217–238 (1986).CrossRefGoogle Scholar
  124. 124.
    A.L. Arsenault, Crystal-collagen relationships in calcified turkey leg tendons visualized by selected-area dark field electron microscopy, Calcif. Tiss. Int. 43: 202–212 (1988).Google Scholar
  125. 125.
    E. Bonucci, Is there a calcification factor common to all calcifying matrices?, Scann. Microsc. 1: 1089–1102 (1987).Google Scholar
  126. 126.
    S.Y. Ali, Calcification of cartilage, in: “Cartilage”, v. 1, B.K. Hall, ed., Academic Press, New York, London (1983).Google Scholar
  127. 127.
    B. De Bernard, N. Stagni, I. Colautti, F. Vittur, and E. Bonucci, Glycosaminoglycans and endochondral calcification, Clin. Orthop. 126: 285–291 (1977).Google Scholar
  128. 128.
    E. Bonucci, G. Silvestrini, R. Di Grezia, The ultrastructure of the organic phase associated with the inorganic substance in calcified tissues, Clin. Orthop. 233: 243–261 (1988).Google Scholar
  129. 129.
    E. Bonucci, and J. Reurink, The fine structure of decalcified cartilage and bone: a comparison between decalcification procedures performed before and after embedding, Calcif. Tiss. Res. 25: 179–190 (1978).Google Scholar
  130. 130.
    E. Bonucci, Fine structure of early cartilage calcification, J. Ultrastruct. Res. 20: 33–50 (1967).Google Scholar
  131. 131.
    E. Bonucci, Further investigation on the organic-inorganic relationships in calcifying cartilage, Calcif. Tiss. Res. 3: 38–54 (1969).Google Scholar
  132. 132.
    E. Bonucci, The locus of initial calcification in cartilage and bone, Clin. Orthop. 78: 108–139 (1971).Google Scholar
  133. 133.
    E. Bonucci, The organic-inorganic relationships in calcified organic matrices, In: “Physico-chimie et crystallographie des apatites d’intéret biologique”, Coll. Int. CRNS n. 230, Paris (1975).Google Scholar
  134. 134.
    B. De Bernard, P. Bianco, E. Bonucci, M. Costantini, G.C. Lunazzi, P. Martinuzzi, C. Modricky, L. Moro, E. Panfili, P. Pollesello, N. Stagni, and F. Vittur, Biochemical and immunohistochemical evidence that in cartilage an alkaline phosphatase is a Ca2+-binding glycoprotein, J. Cell Biol. 103: 1615–1623 (1986).PubMedCrossRefGoogle Scholar
  135. 135.
    A.L. Boskey, The role of calcium-phospholipids, phosphate complexes in tissue mineralization, Metab. Bone Dis. Rel. Res. 1: 137142 (1978).Google Scholar
  136. 136.
    H.C. Anderson, Matrix vesicles of cartilage and bone, in: “The biochemistry and physiology of bone”, 2nd ed., v. 4, G.H. Bourne, ed., Academic Press, New York, San Francisco, London (1976).Google Scholar
  137. 137.
    H.C. Anderson, Mineralization by matrix vesicles, Scann. Electr. Micr. 2: 953–964 (1984).Google Scholar
  138. 138.
    E. Bonucci, Matrix vesicles: their role in calcification, in: “Dentin and dentinogenesis”, A. Linde, ed., CRC Press, Boca Raton (1984).Google Scholar
  139. 139.
    E. Bonucci, Fine structure and histochemistry of “calcifying globules” in epiphyseal cartilage, Z. Zellfor. 103: 192–217 (1978)CrossRefGoogle Scholar
  140. 140.
    E. Bonucci, Matrix vesicles formation in cartilage of scorbutic guinea pigs: electron microscope study of serial sections, Metab. Bone Dis. Rel. Res. 1: 205–212 (1978).Google Scholar
  141. 141.
    J.E. Hale, and R.E. Wuthier, The mechanism of matrix vesicle formation, J. Biol. Chem. 262: 1916–1925 (1987).Google Scholar
  142. 142.
    F.M. McLean, P.J. Keller, B.R. Genge, S.A. Walters, and R.E. Wuthier, Disposition of preformed mineral in matrix vesicles. Internal localization and association with alkaline phosphatase, J. Biol. Chem. 262: 10481–10488 (1987).Google Scholar

Copyright information

© Springer Science+Business Media New York 1990

Authors and Affiliations

  • Ermanno Bonucci
    • 1
  1. 1.Department of Human Biopathology, Section of Pathological AnatomyLa Sapienza UniversityRomeItaly

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