Antigens of Osteoclasts Phenotypic Definition of a Specialized Hemopoietic Cell Lineage

  • M. H. Helfrich
  • M. A. Horton
Part of the Blood Cell Biochemistry book series (BLBI, volume 5)


Immunological approaches have readily found a place in the analysis of hemopoietic differentiation and led to the definition of cellular subpopulations which previously had only been identified by applying functional criteria. Increasingly, the techniques of monoclonal antibody technology, biochemical analysis, and, more recently, molecular cloning have been applied to questions of bone cell biology. In this chapter we review the current literature on the expression of antibody-defined antigens of osteoclasts, bone-resorbing cells of hemopoietic origin. The definition of the immunophenotype of human osteoclasts is considered primarily, but, where relevant, features of avian and rodent cells are also discussed. Our knowledge of the function of the majority of osteoclast antigens is limited; we do, however, speculate about a role in bone for some molecules, for example, aminopeptidase N (CD13), CD9, ICAM-1 (CD54), and the transferrin receptor (CD71). A section on adhesive molecules, mainly integrins, is included as they were among the first “specific” markers of human osteoclasts to be reported (the vitronectin receptor, CD51, by Horton et al., 1985a) and the definition of their functional activity in osteoclasts is well advanced. Finally, we review the application of immunological techniques to the phenotypic analysis of cells of the mononuclear phagocyte system and compare their characteristics with those of osteoclasts, particularly as there has been considerable dispute over their exact interrelationship.


Bone Resorption Giant Cell Giant Cell Tumor Mononuclear Phagocyte System Hemopoietic Cell 


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  1. Alvarez, J. I., Teitelbaum, S. L., Chappel, J. C., Cheresh, D. A., Sander, D., Farach-Carson, M. C., Robey, P. G., and Ross, F. P., 1990, Osteoclast attachment to bone and its subsequent resorption depend upon the vitronectin receptor, J. Bone Miner. Res. 5: S154 (Abstract No. 321).Google Scholar
  2. Andreesen, R., Brugger, W., Scheibenbogen, C., Kreutz, M., Leser, H. G., Rehm, A., and Lohr, G. W., 1990, Surface phenotype analysis of human monocyte to macrophage maturation, J. Leukocyte Biol. 47: 490–497.PubMedGoogle Scholar
  3. Agel, N. M., Clark, M., Jones, D. B., Arnot, J., and Waldmann, H., 1987, Identification of cells of the human mononuclear phagocyte system with rat monoclonal antibodies, J. Pathol. 152: 265–273.CrossRefGoogle Scholar
  4. Agel, N. M., Pringle, J. A. S., and Horton, M. A., 1988, Cellular heterogeneity in giant cell tumour of bone (osteoclastoma): An immunohistological study of 16 cases, Histopathology 13: 675–685.CrossRefGoogle Scholar
  5. Ashmun, R. A., and Look, A. T., 1990, Metalloprotease activity of CD 13/aminopeptidase N on the surface of human myeloid cells, Blood 75: 462–469.Google Scholar
  6. Athanasou, N. A., and Quinn, J., 1990, Immunophenotypic differences between osteoclasts and macrophage polykaryons: Immunohistological distinction and implications for osteoclast ontogeny and function, J. Clin. Pathol. 43: 997–1003.PubMedCrossRefGoogle Scholar
  7. Athanasou, N. A., Quinn, J., and McGee, J. 0.-D., 1988a, Immunocytochemical analysis of the human osteoclast: Phenotypic relationship to other marrow-derived cells, Bone Miner. 3: 317–333.Google Scholar
  8. Athanasou, N. A., Pulford, K. A. F., Quinn, J., Gatter, K. C., Mason, D. Y., and McGee, J. 0., 1988b, A monoclonal antimacrophage antibody (3MA-134) which reacts with human osteoclasts in decalcified paraffin embedded bone sections, Calcif. Tissue Int. 42 (Suppl.): A1.Google Scholar
  9. Athanasou, N. A., Quinn, J., and McGee, J. O’D., 1989a, Reactivity of Workshop mAb of the myeloid, platelet, and non-lineage (CD45, 45R, CD 11 a, b, c) series with cells in bone and synovium, in Leucocyte Typing IV. White Cell Differentiation Antigens ( W. Knapp, B. Dörken, W. R. Gilks, E. P. Rieber, R. E. Schmidt, H. Stein, and A. E. G. Kr. von dem Borne, eds.), pp. 921–923, Oxford University Press, Oxford.Google Scholar
  10. Athanasou, N. A., Wells, C. A., Quinn, J., Ferguson, D. P., Heryet, A., and McGee, J. O., 1989b, The origin and nature of stromal osteoclast-like multinucleated giant cells in breast carcinoma: Implications of tumour osteolysis and macrophage biology, Br. J. Cancer 59: 491–498.PubMedCrossRefGoogle Scholar
  11. Athanasou, N. A., Alvarez, J. I., Ross, F. P., Quinn, J., and Teitelbaum, S. L., 1992, Species differences in the immunophenotype of osteoclasts and mononuclear phagocytes, Calcif. Tissue Int. 50: 427–432.PubMedCrossRefGoogle Scholar
  12. Athanasou, N. A., Puddle, B., Quinn, J., and Woods, C. G., 1991, Use of monoclonal antibodies to recognise osteoclasts in routinely processed bone biopsy specimens, J. Clin. Pathol. 44: 664–666.PubMedCrossRefGoogle Scholar
  13. Backe, E., Schwarting, R., Gerdes, J., Ernst, M., and Stein, H., 1991, BerMac3: New monoclonal antibody that defines human monocyte/macrophage differentiation antigen, J. Clin. Pathol. 44: 936–945.PubMedCrossRefGoogle Scholar
  14. Bossy, B., and Reichardt, L. F., 1990, Chicken integrin a subunit molecular analysis reveals high conservation of structural domains and association with multiple ß subunits in embryo fibroblasts, Biochemistry 29: 10191–10198.PubMedCrossRefGoogle Scholar
  15. Chambers, T. J., and Horton, M. A., 1984, Failure of cells of the mononuclear phagocyte series to resorb bone, Calcif. Tissue Int. 36: 556–558.PubMedCrossRefGoogle Scholar
  16. Chambers, T. J., Fuller, K., Darby, J. A., Pringle, J. A. S., and Horton, M. A., 1986, Monoclonal antibodies against osteoclasts inhibit bone resorption in vitro, Bone Miner. 1: 127–135.PubMedGoogle Scholar
  17. Chilosi, M., Giliol, E., Lestani, M., Menestrina, F., and Fiore-Donati, L., 1988, Immunohistochemical characterization of osteoclasts and osteoclast-like cells with monoclonal antibody MB1 on paraffin-embedded tissues, J. Pathol. 156: 251–254.PubMedCrossRefGoogle Scholar
  18. Clover, J., Dodds, R. A., and Gowen, M., 1992, Integrin subunit expression by human osteoblasts and osteoclasts in situ and in culture, J. Cell Sci. 103: 267–271.PubMedGoogle Scholar
  19. Coombe, D. R., and Rider, C. C., 1989, Lymphocyte homing receptors cloned—a role for anionic polysaccharides in lymphocyte adhesion, Immunol. Today 10: 289–291.PubMedCrossRefGoogle Scholar
  20. Cottrell, B., and Jones, D., 1990, Functional and phenotypic changes associated with the in vitro development of human monocytes into macrophages, FEMS Microbiol. Immunol. 2: 333–337.PubMedCrossRefGoogle Scholar
  21. Davies, J. D., 1990, The use of monoclonal antibodies to identify and characterise functional antigens on osteoclasts, Ph.D. Thesis, University of London.Google Scholar
  22. Davies, J., Warwick, J., Totty, N., Philp, R., Helfrich, M., and Horton, M., 1989, The osteoclast functional antigen implicated in the regulation of bone resorption is biochemically related to the vitronectin receptor, J. Cell Biol. 109: 1817–1826.PubMedCrossRefGoogle Scholar
  23. D’Souza, S. E., Ginsberg, M. H., Burke, T. A., and Plow, E. F., 1990, The ligand binding site of the platelet integrin receptor GPIIb-IIIa is proximal to the second calcium binding domain of its alpha subunit, J. Biol. Chem. 265: 3440–3446.PubMedGoogle Scholar
  24. Duijvestijn, A., and Hamann, A., 1989, Mechanisms and regulation of lymphocyte migration, Immunol. Today 10: 23–28.PubMedCrossRefGoogle Scholar
  25. Flanagan, A. M., and Chambers, T. J., 1989, Osteoclasts are present in the giant cell variant of malignant fibrous histiocytoma, J. Pathol. 159: 53–57.PubMedCrossRefGoogle Scholar
  26. Flanagan, A. M., Horton, M. A., Dorey, E. L., Evely, R. S., Moseley, J. M., Firkin, F. C., Chambers, T. J., Helfrich, M. H., and Martin, T. J., 1992, An assessment of the ability of human bone marrow cultures to generate osteoclasts, Int. J. Pathol. 73: 387–401.Google Scholar
  27. Fuller, K., and Chambers, T. J., 1987, Generation of osteoclasts in cultures of rabbit bone marrow and spleen cells, J. Cell. Physiol. 132: 441–452.PubMedCrossRefGoogle Scholar
  28. Goldberg, R. D., Michelassi, F., and Montag, A. G., 1991, Osteoclast-like giant cell tumor of the pancreas: Immunophenotypic similarity to giant cell tumor of bone, Hum. Pathol. 22: 618–622.PubMedCrossRefGoogle Scholar
  29. Gordon, S., Keshav, S., and Chung, L. P., 1988, Mononuclear phagocytes: Tissue distribution and functional heterogeneity, Curr. Opin. Immunol. 1: 26–35.PubMedCrossRefGoogle Scholar
  30. Greywoode, G. I. N., McCarthy, S. P., and McGee, J. O’D., 1990, Labelling of cells of the mononuclear phagocyte system in routinely processed archival biopsy specimens with monoclonal antibody EBM/ 11, J. Clin. Pathol. 43: 992–996.Google Scholar
  31. Hato, T., Ikeda, K., Yasukawa, M., Watanabe, A., and Kobayashi, Y., 1988, Exposure of platelet fibrinogen receptors by a monoclonal antibody to CD9 antigen, Blood 72: 224–229.PubMedGoogle Scholar
  32. Hattersley, G., and Chambers, T. J., 1989, Calcitonin receptors as markers for osteoclastic differentiation: Correlation between generation of bone resorptive cells and cells that express calcitonin receptors in mouse bone marrow cultures, Endocrinology 125: 1606–1612.PubMedCrossRefGoogle Scholar
  33. Hattersley, G., Kerby, J. A., and Chambers, T. J., 1991, Identification of osteoclast precursors in multilineage colonies, Endocrinology 128: 259–262.PubMedCrossRefGoogle Scholar
  34. Helfrich, M. H., and Horton, M. A., 1992, Adhesion to bone matrix protein by chick osteoclasts differs from that by rat osteoclasts, in Bone Biology and Skeletal Disorders, ( C. C. Whitehead, ed.), p. 361, Carfax Publishing Co., United Kingdom.Google Scholar
  35. Helfrich, M. H., Nesbitt, S. A., and Horton, M. A., 1992a, Integrins on rat osteoclasts: Characterisation of two monoclonal antibodies (F4 and F11) to rat $3, J. Bone Miner. Res. 7: 345–351.PubMedCrossRefGoogle Scholar
  36. Helfrich, M. H., Nesbitt, S. A., Dorey, E. L., and Horton, M. A., 1992b, Rat osteoclasts adhere to a wide range of RGD (Arg-Gly-Asp) peptide-containing proteins, including the bone sialoproteins and fibronectin via a $3 integrin, J. Bone Miner. Res. 7: 335–343.PubMedCrossRefGoogle Scholar
  37. Hemler, M. E., 1990, VLA proteins in the integrin family: Structures, functions, and their role on leukocytes, Annu. Rev. Immunol. 82: 365–400.CrossRefGoogle Scholar
  38. Hentunen, T. A., and Väänänen, H. K., 1989, Inhibition of bone resorption by osteoclast-recognizing monoclonal antibodies, J. Bone Miner. Res. 4 (Suppl. 1): S213.Google Scholar
  39. Hentunen, T. A., Tuukkanen, J., and Väänänen, H. K., 1990, Osteoclasts and a small population of peripheral blood cells share common surface antigens, Calcif. Tissue Int. 47: 8–17.PubMedCrossRefGoogle Scholar
  40. Hentunen, T. A., Lakkakorpi, P. T., Rautiala, T., and Väänänen, K., 1991, Inhibition of bone resorption by a monoclonal antibody that reacts with a 150 kD membrane protein in chicken osteoclasts, J. Bone Miner. Res. 6: 1091–1097.PubMedCrossRefGoogle Scholar
  41. Horejsi, V., 1991, A novel family of leukocyte surface antigens, Immunol. Today 12: 287.PubMedCrossRefGoogle Scholar
  42. Horton, M., 1990, Current status review. Vitronectin receptor: Tissue specific expression or adaptation to culture, Int. J. Exp. Pathol. 71: 741–759.PubMedGoogle Scholar
  43. Horton, M. A., 1988, Osteoclast-specific antigens, LS/ Atlas Sci. Immunol. 1: 35–43.Google Scholar
  44. Horton, M. A., and Chambers, T. J., 1986, Human osteoclast specific antigens are expressed by osteoclasts in a wide range of non-human species, Br. J. Exp. Pathol. 67: 95–104.PubMedGoogle Scholar
  45. Horton, M. A., and Davies, J., 1989, Perspectives: Adhesion receptors in bone, J. Bone Miner. Res. 4: 803–808.Google Scholar
  46. Horton, M. A., and Helfrich, M. H., 1992, Antigenic markers of osteoclasts, in Biology and Physiology of the Osteoclast ( B. R. Rifkin and C. Gay, eds.), pp. 33–54, CRC Press, Boca Raton, Fla.Google Scholar
  47. Horton, M. A., Rimmer, E. F., Lewis, D., Pringle, J. A. S., Fuller, K., and Chambers, T. J., 1984, Cell surface characterisation of the human osteoclast: Phenotypic relationship to other bone marrow cell types, J. Pathol. 144: 281–294.PubMedCrossRefGoogle Scholar
  48. Horton, M. A., Lewis, D., McNulty, K., Pringle, J. A. S., and Chambers, T. J., 1985a, Monoclonal antibodies to osteoclastomas (giant cell bone tumours): Definition of osteoclast-specific antigens, Cancer Res. 45: 5663–5669.PubMedGoogle Scholar
  49. Horton, M. A., Rimmer, E. F., Moore, A., and Chambers, T. J., 1985b, On the origin of the osteoclast: The cell surface phenotype of rodent osteoclasts, Calcif. Tissue Int. 37: 46–50.PubMedCrossRefGoogle Scholar
  50. Horton, M. A., Dorey, E., Helfrich, M. H., and Simpson, A. F. P., 1989, Cluster analysis of platelet and myeloid antibody panels: Contribution of immunohistological analysis of osteoclasts and other tissues, in Leucocyte Typing IV. White Cell Differentiation Antigens ( W. Knapp, B. Dörken, W. R. Gilks, E. P. Reiber, R. E. Schmidt, H. Stein, and A. E. G. Kr. von dem Borne, eds.), pp. 979–981, Oxford University Press, Oxford.Google Scholar
  51. Horton, M. A., Taylor, M. L., Arnett, T. R., and Helfrich, M. H., 1991, Arg-Gly-Asp (RGD) peptides and the antivitronectin receptor antibody 23C6 inhibit cell spreading and dentine resorption by osteoclasts, Exp. Cell Res. 195: 368–375.PubMedCrossRefGoogle Scholar
  52. Horton, M. A., Dorey, E. L., Nesbitt, S., Samanen, J., Ali, F. E., Stadel, J. M., Nichols, A., Greig, R., and Helfrich, M. H., 1993, Modulation of vitronectin receptor-mediated osteoclast adhesion by Arg-GlyAsp peptide analogs: a structure-function analysis, J Bone Min. Res. 8: 241–249.Google Scholar
  53. Hume, D. A., Loutit, J. F., and Gordon, S., 1984, The mononuclear phagocyte system of the mouse defined by immunohistochemical localization of antigen F4/80: Macrophages of bone and associated connective tissue, J. Cell Sci. 66: 189–194.PubMedGoogle Scholar
  54. Hunkapiller, T., and Hood, L., 1989, Diversity of the immunoglobulin gene superfamily, Adv. Immunol. 44: 1–63.PubMedCrossRefGoogle Scholar
  55. Hynes, R., 1987, Integrins: A family of cell surface receptors, Cell 48: 549–554.PubMedCrossRefGoogle Scholar
  56. Hynes, R. 0., 1992, Integrins: versatility, modulation and signaling in cell adhesion, Cell 69: 11–25.Google Scholar
  57. Indig, F. E., Benayallu, D., Fried, A., Wientroub, S., and Blumberg, S., 1990, Neutral endopeptidase (EC is highly expressed on osteoblastic cells and other marrow stromal cell types, Biochem.Google Scholar
  58. Biophys. Res. Commun. 172:620–626.Google Scholar
  59. James, I. E., Walsh, S., Dodds, R. A., and Gowen, M., 1991, Production and characterization of osteoclastselective monoclonal antibodies which distinguish between multinucleated cells derived from different human tissues, J. Histochem. Cytochem. 39: 905–914.PubMedCrossRefGoogle Scholar
  60. Ketcham, C. M., Roberts, R. M., Simmen, R. C. M., and Nick, H. S., 1989, Molecular cloning of the type 5, iron-containing, tartrate-resistant acid phosphatase from human placenta, J. Biol. Chem. 264: 557–563.PubMedGoogle Scholar
  61. Knapp, W., Dörken, B., Gilks, W. R., Reiber, E. P., Schmidt, R. E., Stein, H., and von dem Borne, A. E. G. Kr. (eds.), 1989, Leucocyte Typing IV. White Cell Differentiation Antigens, Oxford University Press, Oxford.Google Scholar
  62. Kukita, T., and Roodman, G. D., 1989, Development of a monoclonal antibody to osteoclasts formed in vitro which recognizes mononuclear osteoclast precursors in the marrow, Endocrinology 125: 630–637.PubMedCrossRefGoogle Scholar
  63. Kukita, T., McManus, L. M., Miller, M., Civin, C., and Roodman, G. D., 1989, Osteoclast-like cells formed in long-term human bone marrow cultures express a similar surface phenotype as authentic osteoclasts, Lab. Invest. 60: 532–538.PubMedGoogle Scholar
  64. Kurihara, N., Bertolini, D., Suda, T., Akayama, Y., and Roodman, G. D., 1990, IL-6 stimulated osteoclast-like multinucleated cell formation in long-term human cultures by inducing IL-1 release, J. Immunol. 144: 4226–4230.PubMedGoogle Scholar
  65. Lakkakorpi, P. T., Horton, M. A., Helfrich, M. H., Karhukorpi, E.-K., and Väänänen, H. K., 1991, Vitronectin receptor has a role in bone resorption but does not mediate tight sealing zone attachment of osteoclasts to the bone surface, J. Cell Biol. 115: 1179–1186.PubMedCrossRefGoogle Scholar
  66. Lanza, F., Wolf, D., Fox, C. F., Kieffer, N., Seyer, J. M., Fried, V. A., Coughlin, S. R., Phillips, D. R., and Jennings, L. K., 1991, cDNA cloning and expression of platelet p24/CD9. Evidence for a new family of multiple membrane spanning proteins, J. Biol. Chem. 266: 10638–10645.Google Scholar
  67. Lasky, L. A., 1991, Lectin cell adhesion molecules (LEC-CAMS): A new family of cell adhesion proteins involved with inflammation, J. Cell. Biochem. 45: 139–146.PubMedCrossRefGoogle Scholar
  68. Leenen, P. J. M., Melis, M., Kraal, G., Hoogeveen, A. T., and van Ewijk, W., 1989, Monoclonal antibody ER-BMDM 1 recognizes a macrophage and dendritic cell differentiation antigen with aminopeptidase activity, in Phenotypical analysis of murine macrophage differentiation (P. J. M. Leenen, Ph.D. Thesis ), University of Rotterdam.Google Scholar
  69. MacDonald, B. R., Mundy, G. R., Clark, S., Wang, E. A., Kuehl, T. J., Stanley, E. R., and Roodman, G. D., 1986, Effects of human recombinant CSF-GM and high purified CSF-1 on the formation of multinucleated cells with osteoclast characteristics in longterm bone marrow cultures, J. Bone Miner. Res. 1: 227–233.PubMedCrossRefGoogle Scholar
  70. MacDonald, B. R., Takahashi, N., McManus, L. M., Holohan, J., Mundy, G. R., and Roodman, G. D., 1987, Formation of multinucleated cells that respond to osteotropic hormones in long term human marrow cultures, Endocrinology 120: 2326–2333.PubMedCrossRefGoogle Scholar
  71. Marcantonio, E. E., and Hynes, R. 0., 1988, Antibodies to the conserved cytoplasmic domain of the integrin ß subunit react with proteins in vertebrates, invertebrates, and fungi, J. Cell Biol. 106: 1765–1772.Google Scholar
  72. Maxfield, S. R., Moulder, K., Koning, F., Elbe, S., Stingl, G., Coligan, J. E., Shevach, E. M., and Yokovama, W. M., 1989, Murine T cells express a cell surface receptor for multiple extracellular matrix protein. Identification and characterization with monoclonal antibodies, J. Exp. Med. 169: 2173–2190.PubMedCrossRefGoogle Scholar
  73. McEver, R. P., 1991, GMP-140: A receptor for neutrophils and monocytes on activated platelets, J. Cell. Biochem. 45: 156–161.PubMedCrossRefGoogle Scholar
  74. McMichael, A. J., Beverley, P. L. C., Cobbold, S., Crumpton, M. J., Gilks, W., Gotch, F. M., Hogg, N., Horton, M. A., Ling, N., MacLennan, I. C. M., Mason, D. Y., Milstein, C., Spiegelhalter, D., and Waldmann, H. (eds.), 1987, Leucocyte Typing III. White Cell Differentiation Antigens, Oxford University Press, Oxford.Google Scholar
  75. Miyauchi, A., Alvarez, J., Greenfield, E. M., Teti, A., Grano, M., Colucci, S., Zambonin-Zallone, A., Ross, F. P., Teitebaum, S. L., Cheresh, D., and Hruska, K. A., 1991, Recognition of osteopontin and related peptides by an avß3 integrin stimulates immediate cell signals in osteoclasts, J. Biol. Chem. 266: 20369–20374.PubMedGoogle Scholar
  76. Most, J., Neumayer, H. P., and Dierich, M. P., 1990, Cytokine-induced generation of multinucleated giant cells in vitro requires interferon-gamma and expression on LFA-1, Eur. J. Immunol. 20: 1661–1667.PubMedCrossRefGoogle Scholar
  77. Moulder, K., Roberts, K., Shevach, E. M., and Coligan, J. E., 1991, The mouse vitronectin receptor is a T cell activation antigen, J. Exp. Med. 173: 343–347.PubMedCrossRefGoogle Scholar
  78. Nelson, P. N., Pringle, J. A. S., and Chambers, T. J., 1991, Production and characterisation of new monoclonal antibodies to human osteoclasts, Calcif. Tissue Int. 49: 317–320.PubMedCrossRefGoogle Scholar
  79. Nesbitt, S., Hart, I., and Horton, M. A., 1989, Epitope analysis of the vitronectin receptor (CD51), in Leucocyte Typing IV. White Cell Differentiation Antigens ( W. Knapp, B. Dörken, W. R. Gilks, E. P. Reiber, R. E. Schmidt, H. Stein, and A. E. G. Kr. von dem Borne, eds.), pp. 1037, Oxford University Press, Oxford.Google Scholar
  80. Nesbitt, S., Nesbit, A., Helfrich, M., and Horton, M., 1993, Biochemical characterisation of human osteoclast integrins: osteoclasts express a v 03,a20, and a„ß,integrins, J. Biol. Chem.,in press.Google Scholar
  81. Nijweide, P. J., Vrijheid-Lammers, T., Mulder, R. J., and Blok, J., 1985, Cell surface antigens on osteoclasts and related cells in the quail studied with monoclonal antibodies, Histochemistry 83:315–324. Osborn, L., 1990, Leukocyte adhesion to endothelium in inflammation, Cell 62: 3–6.Google Scholar
  82. Oursler, M. J., and Osdoby, P., 1988, Osteoclast development in marrow cultured in calvaria-conditioned media, Dev. Biol. 127: 170–178.PubMedCrossRefGoogle Scholar
  83. Oursler, M. J., Bell, L. V., Clevinger, B., and Osdoby, P., 1985, Identification of osteoclast-specific monoclonal antibodies, J. Cell Biol. 100: 1592–1600.PubMedCrossRefGoogle Scholar
  84. Oursler, M. J., Li, L., and Osdoby, P., 1989, Characterization of an osteoclast membrane protein related to superoxide dismutase, J. Bone Miner. Res. 4 (Suppl. 1): S265.Google Scholar
  85. Parravicini, C. L., Soligo, D., Berti, E., Cattoretti, G., Gaiera, G., and Vago, L., 1989, Immunohistochemical reactivity of anti-platelet mAb in normal human tissues and bone marrow, in Leucocyte Typing IV. White Cell Differentiation Antigens ( W. Knapp, B. Dörken, W. R. Gilks, E. P. Reiber, R. E. Schmidt, H. Stein, and A. E. G. Kr. von dem Borne, eds.), pp. 981–985, Oxford University Press, Oxford.Google Scholar
  86. Quinn, J., Athanasou, N. A., and McGee, J. O’D., 1991, Extracellular matrix receptor and platelet antigens on osyteoclasts and foreign body giant cells, Histochemistry 96: 169–176.Google Scholar
  87. Radzun, H. J., Kreipe, H., Bodewadt, S., Hausmann, M.-L., Barth, J., and Parwaresch, M. R., 1987, KiM8 monoclonal antibody reactive with an intracytoplasmic antigen of monocyte/macrophage lineage, Blood 69: 1320–1327.PubMedGoogle Scholar
  88. Reinholt, F. P., Hultenby, K., Oldberg, A., and Heinegard, D., 1990, Osteopontin—a possible anchor of osteoclasts to bone, Proc. Natl. Acad. Sci. USA 87: 4473–4475.PubMedCrossRefGoogle Scholar
  89. Rifkin, B. R., and Gay, C. (eds.), 1992, Biology and Physiology of the Osteoclast,CRC Press, Boca Raton, Fla., in press.Google Scholar
  90. Ruitishauser, U., and Jessell, T. M., 1988, Cell adhesion molecules in vertebrate neural development, Physiol. Rev. 68: 819–857.Google Scholar
  91. Sato, M., Sardana, M. K., Grasser, W. A., Garsky, V. M., Murray, J. M., and Gould, R. J., 1990, Echistatin is a potent inhibitor of bone resorption in culture, J. Cell Biol. 111: 1713–1723.PubMedCrossRefGoogle Scholar
  92. Schneider, G. B., and Relfson, M., 1988, The effects of transplantation of granulocyte–macrophage progenitors on bone resorption in osteopetrotic rats, J. Bone Miner. Res. 3: 225–232.PubMedCrossRefGoogle Scholar
  93. Slupsky, J. R., Seehafer, J. G., Tang, S.-S., Masellis Smith, A., and Shaw, A. R. E., 1989, Evidence that monoclonal antibodies against CD9 antigen induce specific association between CD9 and the platelet glycoprotein IIb–IIIa complex, J. Biol. Chem. 264: 12289–12293.PubMedGoogle Scholar
  94. Sminia, T., and Dijkstra, C. D., 1986, The origin of osteoclasts: An immunohistochemical study on macrophages and osteoclasts in embryonic rat bone, Calcif. Tissue Int. 39: 263–266.PubMedCrossRefGoogle Scholar
  95. Springer, T. A., and Lasky, L. A., 1991, Sticky sugars for selectins, Nature (London) 349:196–197. Stoolman, L. M., 1989, Adhesion molecules controlling lymphocyte migration, Cell 56: 907–910.Google Scholar
  96. Takahashi, N., Akatsu, T., Udagawa, N., Sasaki, T., Yamaguchi, A., Moseley, J. M., Martin, T. J., and Suda, T., 1988, Osteoblastic cells are involved in osteoclast formation, Endocrinology 123: 2600–2602.PubMedCrossRefGoogle Scholar
  97. Takeichi, M., 1988, The cadherins: Cell—cell adhesion molecules controlling animal morphogenesis, Development 102: 639–655.PubMedGoogle Scholar
  98. Takeya, M., Tsuchiya, T., Shimokawa, Y., and Takahashi, K., 1991, A new monoclonal antibody, PM-2K, specifically recognises tissue macrophages but not blood monocytes, J. Pathol. 163: 315–321.PubMedCrossRefGoogle Scholar
  99. Werb, Z., Tremble, P. M., Behrendtsen, O., Crowley, E., and Damsky, C. H., 1989, Signal transduction through the fibronectin receptor induces collagenase and stromelysin gene expression, J. Cell Biol. 109: 877–889.PubMedCrossRefGoogle Scholar
  100. Zambonin-Zallone, A., Teti, A., Grano, M., Rubinacci, A., Abbadini, M., Gaboli, M., and Marchisio, P. C., 1989, Immunocytochemical distribution of extracellular matrix receptors in human osteoclasts: A $3 antigen is colocalized with vinculin and talin in the podosomes of osteoclastoma giant cells, Exp. Cell Res. 182: 645–652.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1993

Authors and Affiliations

  • M. H. Helfrich
    • 1
  • M. A. Horton
    • 1
  1. 1.Imperial Cancer Research Fund Haemopoiesis Research Group, Department of HaematologySt. Bartholomew’s HospitalLondonUK

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