Ultrastructural biology and pathology of the osteoclast

  • Sandy C. MarksJr
  • Steven N. Popoff
Chapter
Part of the Electron Microscopy in Biology and Medicine book series (EMBM, volume 7)

Abstract

The osteoclast is usually described as a large, multinucleated cell next to bone surfaces [1,2], and this will be our definition for this review. However, recent observations suggest that we may soon be able to identify a spectrum of relatives of the conventional osteoclast. The origin of osteoclasts from the fusion in skeletal tissues of circulating mononuclear precursors [1,3] provides the potential for the existence of mononuclear cells capable of bone resorption. New knowledge of cell-surface and other features characteristic of osteoclasts increases the possibility of eventually identifying the mononuclear precursors of multinucleated osteoclasts and even mononulcear osteoclasts. An example is the recent demonstration in developing bone of mononuclear cells with certain enzymatic features of osteoclasts (tartrate-resistant acid phosphatase) that have been interpreted as osteoclast precursors [4,5]. Thus, we are likely to have more discriminating criteria for identification of a veriety of osteoclastic cells in the near future.

Keywords

Osteoporosis Adenosine Prostaglandin Indomethacin Methacrylate 

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References

  1. 1.
    Marks SC Jr: The origin of osteoclasts: Evidence, clinical implications and investigative challenges of an extra-skeletal source. J Oral Path 12: 226 - 256, 1983.PubMedCrossRefGoogle Scholar
  2. 2.
    Bonucci E: New knowledge on the origin, function and fate of osteoclasts. Clin Orthop 158: 252 - 269, 1981.PubMedGoogle Scholar
  3. 3.
    Chambers TJ: The cellular basis of bone resorption. Clin Orthop 151: 283 - 293, 1980.PubMedGoogle Scholar
  4. 4.
    Baron R, Tran Van P, Nefussi JR, Vignery A: Kinetic and cytochemical identification of osteoclasts precursors and their differentiation into multinucleated osteoclasts. Am J Pathol 122: 363 - 378, 1986.PubMedGoogle Scholar
  5. 5.
    van de Wijngaert FP, Burger EH: Demonstration of tartrate-resistant acid phosphatase in un-decalcified, glycolmethacrylate-embedded mouse bone: A possible marker for (pre) osteoclasts identification. J Histochem Cytochem 34: 1317 - 1323, 1986.CrossRefGoogle Scholar
  6. 6.
    Lucht U: Osteoclasts and their relationship to bone as studied by electron microscopy. Z Zellforsch Mikrosk Anat 145: 75 - 87, 1972.CrossRefGoogle Scholar
  7. 7.
    Malkani K, Luxembourger MM, Rebel A: Cytoplasmic modifications at the contact zone of osteoclasts and cal¬cified tissue in the diaphyseal growing plate of foetal guinea-pig tibia. Cdlcif Tissue Res 11: 258 - 264, 1973.CrossRefGoogle Scholar
  8. 8.
    Marks SC Jr, Popoff SN: Bone cell biology — the re¬gulation of development, structure and function in the skeleton. Am J Anat 183: 1 - 44, 1988.PubMedCrossRefGoogle Scholar
  9. 9.
    Lucht U: Acid phosphatase of osteoclasts demonstrated by electron microscopic histochemistry. Histochemie 29: 103 - 117, 1971.Google Scholar
  10. 10.
    Lucht U: Absorption of peroxidase by osteoclasts as studied by electron microscope histochemistry. Histo¬chemie 29: 274 - 286, 1972.Google Scholar
  11. 11.
    Lucht U: Osteoclasts and their relationship to bone as studied by electron microscopy. Z Zellforsch 135: 211 - 228, 1972.PubMedCrossRefGoogle Scholar
  12. 12.
    Lucht U, Norgaard JO: Export of protein from the osteoclast as studied by electron microscopic autoradio¬graphy. Cell Tissue Res 168: 89 - 99, 1976.PubMedCrossRefGoogle Scholar
  13. 13.
    Pierce AM, Lindskog S: Evidences for capping of Fc receptors on osteoclasts. Cale Tiss 1nt 39: 109 - 116, 1986.CrossRefGoogle Scholar
  14. 14.
    Hammarstrom LE, Hanker JS, Toverud SU: Cellular differences in acid phosphatase isoenzymes in bone and teeth. Clin Orthop 78: 151 - 167, 1971.PubMedCrossRefGoogle Scholar
  15. 15.
    Minkin C: Bone acid phosphatase: Tartrate-resistant acid phosphatase as a marker of osteoclast function. Calc Tissue Int 34: 285 - 290, 1982.CrossRefGoogle Scholar
  16. 16.
    Mostafa YA, Meyer RA Jr, Latorraca R: A simple and rapid method for osteoclast identification using a histo- chemical method for acid phosphatase. Histochem J 14: 409 - 413, 1982.PubMedCrossRefGoogle Scholar
  17. 17.
    Chappard D, Alexandre C, Riffat G: Histochemical iden¬tification of osteoclasts. Review of current methods and reappraisal of a simple procedure for routine diagnosis on decalcified human iliac bone biopsies. Basic Appl Histo¬chem 27: 75 - 85, 1983.Google Scholar
  18. 18.
    Andersson G, Ek-Rylander B, Hammarstrom LE: Puri¬fication and characterization of a vanadate-sensitive nuc¬leotide tri- and diphosphatase with acid pH optimum from rat bone. Arch Biochem Biophys 228: 431 - 438, 1984.PubMedCrossRefGoogle Scholar
  19. 19.
    Andersson GN, Ek-Rylander B, Hammarstrom LE, Lindskog S, Toverud SU: Immunocytochemical localiza¬tion of tartrate-resistant and vanadate-sensitive acid nuc¬leotide tri- and diphosphatase. J Histochem Cvtochem 34: 293 - 298, 1986.CrossRefGoogle Scholar
  20. 20.
    Sundquist KT, Leppilampi M, Jarvelin K, Kumpulainen T, Vàànànen HK: Carbonic anhydrase isoenzymes in isolated rat peripheral monocytes, tissue macrophages and osteoclasts. Bone 8: 33 - 38, 1987.Google Scholar
  21. 21.
    Anderson RE, Schraer H, Gay CV: Ultrastructural immunocytochemical localization of carbonic anhydrase in normal and calcitonin-treated chick osteoclasts. Anat Rec 204: 9 - 20, 1982.PubMedCrossRefGoogle Scholar
  22. 22.
    Marie PJ, Hott M: Histomorphometric identification of carbonic anhydrase in fetal rat bone embedded in glyco- methacrylate. J Histochem Cytochem 35: 245 - 250, 1987.PubMedCrossRefGoogle Scholar
  23. 23.
    Vaiinanen HK, Parvinen EK: High active isoenzyme of carbonic anhydrase in rat calvaria osteoclasts. Histoche¬mistry 78: 481 - 485, 1983.CrossRefGoogle Scholar
  24. 24.
    Minkin C, Jennings JM: Carbonic anhydrase and bone remodeling: Sulfonamide inhibition of bone resorption in organ culture. Science 176: 1031 - 1033, 1972.PubMedCrossRefGoogle Scholar
  25. 25.
    Sly WS, Hewett-Emmett D, Whyte MP, Lu Y-SL, Tashian RE: Carbonic anhydrase II deficiency identified as the primary defect in the autosomal recessive syndrome of osteopetrosis with renal tubular acidosis and cerebral calcification. Proc Natl Acad Sci USA 80: 2752 - 2756, 1983.PubMedCrossRefGoogle Scholar
  26. 26.
    Baron R, Neff L, Louvard D, Courtoy PJ: 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, 1985.PubMedCrossRefGoogle Scholar
  27. 27.
    Akisaka T, Gay CV: Ultracytochemical evidence for a proton-pump adenosine triphosphatase in chick osteo¬clasts. Cell Tissue Res 245: 507 - 512, 1986.PubMedCrossRefGoogle Scholar
  28. 28.
    Baron R, Neff L, Roy C, Boisvert A, Caplan M: Evidence for a high and specific concentration of (Na+, K+) ATPase in the plasma membrane of the osteoclast. Cell 46: 311 - 320, 1986.PubMedCrossRefGoogle Scholar
  29. 29.
    Akisaka T, Gay CV: An ultracytochemical investigation of ouabain-sensitive p-nitrophenylphosphatase in chick osteoclasts. Cell Tiss Res 244: 57 - 62, 1986.CrossRefGoogle Scholar
  30. 30.
    Miller SC: Osteoclast cell-surface changes during the egg- laying cycle in Japanese quail. J Cell Biol 75: 104 - 118, 1977.PubMedCrossRefGoogle Scholar
  31. 31.
    Miller SC, Bowman BM, Myers RL: Morphological and ultrastructural aspects of the activation of avian medullary bone osteoclasts by parathyroid hormone. Anat Rec 208: 223 - 231, 1984.PubMedCrossRefGoogle Scholar
  32. 32.
    Reynolds JJ, Pavlovitch H, Balsan S: 1,25-dihydroxyc- holecalciferol increases bone resorption in thyroparathy- roidectomized mice. Calc Tissue Res 21: 207 - 212, 1976.CrossRefGoogle Scholar
  33. 33.
    Tanaka Y, DeLuca HF: Bone mineral mobilization acti¬vity of 1,25-dihydroxycholecalciferol, a metabolite of vita¬min D. Arch Biochem Biophys 146: 574 - 578, 1971.PubMedCrossRefGoogle Scholar
  34. 34.
    Miller SC: Rapid activation of the medullary bone osteo¬clast cell surface by parathyroid hormone. J Cell Biol 76: 615 - 618, 1978.PubMedCrossRefGoogle Scholar
  35. 35.
    Holtrop ME, Raisz LG: Comparison of the effects of 1,25-dihydroxycholecalciferol, prostaglandin E2, and os- teoclast-activating factor with parathyroid hormone on the ultrastructure of osteoclasts in cultured long bones of fetal rats. Calcif Tissue Int 29: 201 - 205, 1979.PubMedCrossRefGoogle Scholar
  36. 36.
    Raisz LG: Stimulation of bone resorption by parathyroid hormone in tissue culture. Nature 197: 1015 - 1016, 1963.PubMedCrossRefGoogle Scholar
  37. 37.
    Raisz LG, Trummel CL, Holick MD, DeLuca HF: 1,25- dihydroxycholecalciferol: A potent stimulator of bone resorption in tissue culture. Science 175: 768 - 769, 1972.PubMedCrossRefGoogle Scholar
  38. 38.
    Miller SC, Bowman BM, Myers RL: Morphological and ultrastructural aspects of the activation of avian medullary bone osteoclasts by parathyroid hormone. Anat Rec 208: 223 - 231, 1984.PubMedCrossRefGoogle Scholar
  39. 39.
    Addison WC: The distribution of nuclei in imprints of feline osteoclasts. J Anat 129: 63 - 68, 1979.PubMedGoogle Scholar
  40. 40.
    Weisbrode SE, Capen CC, Norman AW: Ultrastructural evaluation of the effects of 1,25-dihydroxyvitamin D3 on bone of thyroparathyroidectomised rats fed a low calcium diet. Am J Pathol 92: 459 - 472, 1978.PubMedGoogle Scholar
  41. 41.
    Marie PJ, Travers R: Continuous infusion of 1,25-dihy- droxyvitamin D3 stimulates bone turnover in the normal young mouse. Calcif Tissue Int 35: 418 - 425, 1983.PubMedCrossRefGoogle Scholar
  42. 42.
    Holtrop ME, Raisz LG, Simmons HA: The effects of parathyroid hormone, colchicine, and calcitonin on the ultrastructure and the activity of osteoclasts in organ culture. J Cell Biol 60: 346 - 355, 1974.PubMedCrossRefGoogle Scholar
  43. 43.
    Rouleau MF, Warshawsky H, Goltzman D: Parathyroid hormone binding in vivo to renal, hepatic, and skeletal tissues of the rat using a radioautographic approach. Endocrinology 118: 919 - 931, 1986.PubMedCrossRefGoogle Scholar
  44. 44.
    Silve CH, Hradek GT, Jones AL, Arnaud CD: Parathy¬roid hormone receptor in intact embryonic chicken bone: Characterization and cellular localization. J Cell Biol 94: 379 - 386, 1982.PubMedCrossRefGoogle Scholar
  45. 45.
    Kream BE, Jose M, Yamada S, DeLuca HF: A specific high-affinity binding macromolecule for 1,25-dihydroxy¬vitamin D3 in fetal bone. Science 197: 1086 - 1088, 1977.PubMedCrossRefGoogle Scholar
  46. 46.
    Manolagas SC, Taylor CM, Anderson DC: Highly specific binding of 1,25-dihydroxycholecalciferol in bone cytosol. J Endocrinol 80: 35 - 39, 1979.PubMedCrossRefGoogle Scholar
  47. 47.
    Chambers, TJ, McSheehy PMJ, Thomson BM, Fuller K: The effect of calcium-regulating hormones and prostag¬landins on bone resorption by osteoclasts disaggregated from neonatal rabbit bones. Endocrinology 116: 234 - 239, 1985.PubMedCrossRefGoogle Scholar
  48. 48.
    Rodan GA, Martin TJ: Role of osteoblasts in hormonal control of bone resorption — A hypothesis. Calcif Tissue Int 33: 349 - 351, 1981.PubMedCrossRefGoogle Scholar
  49. 49.
    Rao LG, Murray TM, Heersche JNM: Immunohisto- chemical demonstration of parathyroid hormone binding to specific cell types in fixed rat bone tissue. Endocrino¬logy 113: 805 - 810, 1983.CrossRefGoogle Scholar
  50. 50.
    Narbaitz R, Stumpf WE, Sar M, Huang S, DeLuca HF: Autoradiographic localization of target cells for 1,25-dihy- droxyvitamin D3 in bones from fetal rats. Calcif Tissue Int 35: 177 - 182, 1983.PubMedCrossRefGoogle Scholar
  51. 51.
    McSheehy PMJ, Chambers TJ: Osteoblastic cells mediate osteoclastic responsiveness to parathyroid hormone. En-docrinology 118: 824 - 828, 1986.Google Scholar
  52. 52.
    Wong GL: Paracrine interactions in bone-secreted pro¬ducts of osteoblasts permits osteoclasts to respond to parathyroid hormone. J Biol Chem 259: 4019 - 4022, 1984.PubMedGoogle Scholar
  53. 53.
    McSheehy PMJ, Chambers TJ: Osteoblast-like cells in the presence of parathyroid hormone release soluble factor that stimulates osteoclastic bone resorption. Endocrino¬logy 119: 1654 - 1659, 1986.CrossRefGoogle Scholar
  54. 54.
    Chambers TJ, Athanasou NA, Fuller K: Effect of para¬thyroid hormone and calcitonin on the cytoplasmic spreading of isolated osteoclasts. J Endocrinol 102: 281 - 286, 1984.PubMedCrossRefGoogle Scholar
  55. 55.
    Chambers TJ: Osteoblasts release osteoclasts from cal- citonin-induced quiescence. J Cell Sci 57: 247 - 260, 1982.PubMedGoogle Scholar
  56. 56.
    Wong GL: Skeletal effects of parathyroid hormone. Bone Min 4: 103 - 129, 1986.Google Scholar
  57. 57.
    Chambers TJ, Fuller K: Bone cells predispose bone sur¬faces to resorption by exposure of mineral to osteoclastic contact. J Cell Sci 76: 155 - 165, 1985.PubMedGoogle Scholar
  58. 58.
    Gunness-Hey M, Hock JM: Increased trabecular bone mass in rats treated with human synthetic parathyroid hormone. Metab Bone Dis Rel Res 5: 177 - 181, 1984.CrossRefGoogle Scholar
  59. 59.
    Jowsey J, Riggs BL, Kelly PJ, Hoffman DL: Calcium and salmon calcitonin in treatment of osteoporosis. J Clin Endocrinol Metab 47: 633 - 639, 1978.PubMedCrossRefGoogle Scholar
  60. 60.
    Mills BG, Harontinian AM, Hoist P, Bordier PJ, Tun- Chot S: Ultrastructural and cellular changes at the costo- chondral junction following in vivo treatment with cal¬citonin or calcium chloride in the rabbit. In: Endocrino¬logy 1971. S Taylor (ed), London: Heineman, p 79, 1972.Google Scholar
  61. 61.
    Hedlund T, Hulth A, Johnell O: Early effects of parathor¬mone and calcitonin on the number of osteoclasts and on serum-calcium in rats. Acta Orthop Scand 54: 802 - 804, 1983.PubMedCrossRefGoogle Scholar
  62. 62.
    Baron R, Vignery A: Behavior of osteoclasts during a rapid change in their number induced by high doses of parathyroid hormone or calcitonin in intact rats. Metab Bone Dis Rel Res 2: 339 - 346, 1981.CrossRefGoogle Scholar
  63. 63.
    Kallio DM, Garant PR, Minkin C: Ultrastructural effects of calcitonin on osteoclasts in tissue culture. J Ultrastruct Res 39: 205 - 216, 1972.PubMedCrossRefGoogle Scholar
  64. 64.
    Rao LG, Heersche JNM, Marchuk LL, Sturtridge W: Immunohistochemical demonstration of calcitonin bind¬ing to specific cell types in fixed rat bone tissue. Endo¬crinology 108: 1972 - 1978, 1981.CrossRefGoogle Scholar
  65. 65.
    Warshawsky H, Goltzman D, Rouleau MF, Bergeron JJM: Direct in vivo demonstration by radioautography of specific binding sites for calcitonin in skeletal and renal tissues of the rat. J Cell Biol 85: 682 - 694, 1980.PubMedCrossRefGoogle Scholar
  66. 66.
    Nicholson GC, Mosely JM, Sexton PM, Mendelsohn FAO, Martin TJ: Abundant calcitonin receptors in isolated rat osteoclasts. J Clin Invest 78: 355 - 360, 1986.PubMedCrossRefGoogle Scholar
  67. 67.
    Horton, JE, Raisz LG, Simmons HA, Oppenheim JJ, Mergenhagen SE: Bone resorbing activity in supernatant fluid from cultured human peripheral blood leucocytes. Science 177: 793 - 795, 1972.PubMedCrossRefGoogle Scholar
  68. 68.
    Raisz LG, Luben RA, Mundy GR, Dietrich JW, Horton JE, Trummel CL: Effect of osteoclast activating factor from human leukocytes on bone metabolism. J Clin Invest 56: 408 - 413, 1975.PubMedCrossRefGoogle Scholar
  69. 69.
    Sato K, Fujii Y, Kasono K, Saji M, Tsushima T, Shizume K: Stimulation of prostaglandin E2 and bone resorption by recombinant human interleukin 1 alpha in fetal mouse bones. Biochem Biophys Res Comm 138: 618 - 624, 1986.PubMedCrossRefGoogle Scholar
  70. 70.
    Gowen M, Wood DD, Ihrie EJ, McGuire MKB, Russell RGG: An interleukin 1 like factor stimulates bone resorp¬tion in vitro. Nature 306: 378 - 380, 1983.PubMedCrossRefGoogle Scholar
  71. 71.
    Bertolini DR, Nedwin GE, Bringman TS, Smith DD, Mundy GR: Stimulation of bone resorption and inhibition of bone formation in vitro by human tumour necrosis factors. Nature 319: 516 - 518, 1986.Google Scholar
  72. 72.
    Stashenko P, Dewhirst FE, Peros WJ, Kent RL, Ago JM: Synergistic interactions between interleukin 1, tumor nec¬rosis factor, and lymphotoxin in bone resorption. J Im¬munol 138: 1464 - 1468, 1987.Google Scholar
  73. 73.
    Dewhirst FE, Ago JM, Peros WJ, Stashenko P: Synerg¬ism between parathyroid hormone and interleukin 1 in stimulating bone resorption in organ culture. J Bone Min Res 2: 127 - 134, 1987.CrossRefGoogle Scholar
  74. 74.
    Gowen M, Mundy GR: Actions of recombinant inter¬leukin 1, interleukin 2, and interferon-y on bone resorp¬tion in vitro. J Immunol 136: 2478 - 2482, 1986.PubMedGoogle Scholar
  75. 75.
    Peterlik M, Hoffmann O, Swetly P, Klaushofer K, Koller K: Recombinant y-interferon inhibits prostaglandin-me- diated and parathyroid hormone-induced bone resorption in cultured neonatal mouse calvaria. Fed Eur Biochem Soc 185: 287 - 290, 1985.CrossRefGoogle Scholar
  76. 76.
    Centrella M, Canalis E: Isolation of EGF-dependent transforming growth factor (TGF -like) activity from cul¬ture medium conditioned by fetal rat calvariae. J Bone Min Res 2: 29 - 42, 1987.CrossRefGoogle Scholar
  77. 77.
    Pfeilschifter J, Mundy GR: Modulation of type (3 trans¬forming growth factor activity in bone cultures by osteo¬tropic hormones. Proc Natl Acad Sci USA 84: 2024 - 2028, 1987.PubMedCrossRefGoogle Scholar
  78. 78.
    Tashjian AJ Jr, Voelkel EF, Lazzaro M, Singer FR, Roberts AB, Derynck R, Winkler ME, Levine L: a and (3 human transforming growth factors stimulate prostag¬landin production and bone resorption in cultured mouse calvaria. Proc Natl Acad Sci USA 82: 4535 - 4538, 1985.PubMedCrossRefGoogle Scholar
  79. 79.
    Centrella M, Massague J, Canalis E: Human platelet- derived transforming growth factor-(3 stimulates parame¬ters of bone growth in fetal rat calvariae. Endocrinology 119: 2306 - 2312, 1986.PubMedCrossRefGoogle Scholar
  80. 80.
    Hauschka PV, Mavrakos AE, Iafrati MD, Doleman SE, Klagsbrun M: Growth factors in bone matrix. J Biol Chem 261: 12665 - 12674, 1986.PubMedGoogle Scholar
  81. 81.
    Canalis E, Peck WA, Raisz LG: Stimulation of DNA and collagen synthesis by autologous growth factor in cul¬tured fetal rat calvariae. Science 210: 1021 - 1023, 1980.PubMedCrossRefGoogle Scholar
  82. 82.
    Drivdahl RH, Puzas JE, Howard GA, Baylink DJ: Regu¬lation of DNA synthesis in chick calvaria cells by factors from bone organ cultures. Proc Soc Exp Biol Med 168: 143 - 150, 1981.PubMedGoogle Scholar
  83. 83.
    Canalis E, Centrella Mr Isolation of a nontranforming bone-derived growth factor from medium conditioned by fetal rat calvariae. Endocrinology 118: 2002 - 2008, 1986.PubMedCrossRefGoogle Scholar
  84. 84.
    Linkhart S, Mohan S, Linkhart TA, Kumegawa M, Bay- link DJ: Human skeletal growth factor stimulates collagen synthesis and inhibits proliferation in a clonal osteoblast cell line (MC3T3-E1). J Cell Physiol 128: 307 - 312, 1986.PubMedCrossRefGoogle Scholar
  85. 85.
    Farley JR, Masuda T, Wergedal JE, Baylink DJ: Human skeletal growth factor: Characterization of the mitogenic effect on bone cells in vitro. Biochemistry 21: 3508 - 3513, 1982.PubMedCrossRefGoogle Scholar
  86. 86.
    Samuelsson B, Granstrom E, Green K, Hamberg M, Hammarstrom S: Prostaglandins. Annu Rev Biochem 44: 669 - 695, 1980.CrossRefGoogle Scholar
  87. 87.
    Klein DC, Raisz LG: Prostaglandins: Stimulation of bone resorption in tissue culture. Endocrinology 86: 1436 - 1440, 1970.PubMedCrossRefGoogle Scholar
  88. 88.
    Schelling SH, Wolfe HJ, Tashjian AH Jr: Role of the osteoclast in prostaglandin E2-stimulated bone resorption. Lab Invest 42: 290 - 295, 1980.PubMedGoogle Scholar
  89. 89.
    Jee WSS, Ueno K, Kimmel DB, Woodbury DM, Price P, Woodbury LA: The role of bone cells in increasing meta¬physeal hard tissue in rapidly growing rats treated with prostaglandin E2. Bone 8: 171 - 178, 1987.PubMedCrossRefGoogle Scholar
  90. 90.
    Miller SC, Jee WSS: Ethane-l-hydroxy-1, 1-diphosphon- ate (EHDP) effects on growth and modeling of the rat tibia. Calcif Tissue Res 18: 215 - 231, 1975.PubMedCrossRefGoogle Scholar
  91. 91.
    Miller SC, Jee WSS: The effect of dichloromethylene diphosphonate, a pyrophosphate analog, on bone and bone cell structure in the growing rat. Anat Ree 193: 439 - 462, 1979.CrossRefGoogle Scholar
  92. 92.
    Singer FR Schiller AL, Pyle EB, Krane SM: Pagefs disease of bone. In: Metabolic Bone Disease, Vol II. LV Avioli, SM Krane (eds). New York: Academic Press, p 489 - 575, 1978.Google Scholar
  93. 93.
    Mills BG, Singer FR: Critical evaluation of viral antigen data in Pagefs disease of bone. Clin Orthop Rei Res 217: 16 - 25, 1987.Google Scholar
  94. 94.
    Marks SC Jr: Osteopetrosis — multiple pathways for the interception of osteoclast function. Appi Pathol 5: 172 - 183, 1987.Google Scholar
  95. 95.
    Mills GB, Yabe H, Singer FR: Osteoclasts in human osteopetrosis contain viral-nucleocapsid-like nuclear in¬clusions. J Bone Min Res 3: 101 - 106, 1988.CrossRefGoogle Scholar
  96. 96.
    Shapiro F, Glimcher MJ, Holtrop ME, Tashjian AH, Parsons DB, Kenzora JE: Human osteopetrosis. A histo¬logical, ultrastructural and biochemical study. J Bone Joint Surg 62A: 384 - 399, 1980.PubMedGoogle Scholar
  97. 97.
    Miller SC, Marks SC Jr: Osteoclast kinetics in osteopet- rotic (ia) rats cured by spleen cell transfers from normal littermates. Calcif Tissue Int 34: 422 - 427, 1982.PubMedCrossRefGoogle Scholar
  98. 98.
    Marks SC Jr: Morphological evidence for reduced bone resorption in osteopetrotic (op) mice. Am J Anat 163: 157 - 167, 1982.PubMedCrossRefGoogle Scholar

Copyright information

© Kluwer Academic Publishers 1990

Authors and Affiliations

  • Sandy C. MarksJr
    • 1
  • Steven N. Popoff
  1. 1.Department of Cell BiologyUniversity of Massachusetts Medical SchoolWorcesterUSA

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