Bone microdamage and cell apoptosis

European Cells and Materials

Volumn 6, Issue , 2003, Pages 46-55

  Noble, Brendon ^a   Alini, M ^b   Richards, R G ^b  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b NONE

Author keywords

Apoptosis; Bone; Microdamage; Osteoclast; Osteocyte; Signaling; Targeted bone resorption

Indexed keywords

AGING; APOPTOSIS; BONE INJURY; BONE REMODELING; CELL STRUCTURE; HUMAN; NONHUMAN; OSTEOCLAST; OSTEOCYTE; REVIEW; SCANNING ELECTRON MICROSCOPY; SIGNAL TRANSDUCTION; BIOLOGICAL MODEL; BONE; CYTOLOGY; OSTEOLYSIS; PHYSIOLOGY; ULTRASTRUCTURE;

AGING; APOPTOSIS; BONE AND BONES; BONE RESORPTION; HUMANS; MODELS, BIOLOGICAL; OSTEOCLASTS; OSTEOCYTES; SIGNAL TRANSDUCTION;

EID: 3042793422     PISSN: 14732262     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (120)

1. Adams CS, Shapiro IM (2002) The fate of the terminally differentiated chondrocyte: evidence for microenvironmental regulation of chondrocyte apoptosis. Crit Rev Oral Biol Med 13: 465-473.
2. Ajubi NE, Klein-Nulend J, Nijweide PJ, Vrijheid-Lammers T, Alblas MJ, Burger EH (1996) Pulsating fluid flow increases prostaglandin production by cultured chicken osteocytes - A cytoskeleton-dependent process. Biochem Biophys Res Commun 225: 62-68.
3. Andrade-Rozental AF, Rozental R, Hopperstad MG, Wu JK, Vrionis FD, Spray DC (2000) Gap junctions: the "kiss of death" and the "kiss of life". Brain Res Rev 32: 308-315.
4. Beppu M (2001) Mechanism of removal of aged cells, oxidized cells and apoptotic cells through carbohydrate chains. Seikagaku 73: 196-200.
5. Brukner P, Bradshaw C, Khan KM, White S, Crossley K (1966) Stress fractures: a review of 180 cases. Clin J Sports Med 6: 85-89.
6. Burr DB (2001) Targeted and non-targeted remodeling. Bone 30: 582-584.
7. Burr DB, Martin RB, Schaffler MB, Radin EL (1985) Bone remodeling in response to in vivo fatigue microdamage. J Biomech 18: 189-200.
8. Burr DB, Martin RB (1993) Calculating the probability that microcracks initiate resorption spaces. J Biomech 26: 613-616.
9. Burr DB, Milgrom C, Fyhrie D, Forwood M, Nyska M, Finestone A, Hoshaw S, Saiag E, Simkin A (1996) In vivo measurement of human tibial strains during vigorous activity. Bone 18: 405-410.
10. Carter DR, Hayes WC (1977) Compact bone fatigue damage - I Residual strength and stiffness. J Biomech 10: 325-327.
11. Chan G, Duque G (2002) Age-related bone loss: old bone, new facts. Gerontology 48: 62-71.
12. Chang MK, Bergmark C, Laurila A, Horkko S, Han KH, Friedman P, Dennis EA, Witztum JL (1999) Monoclonal antibodies against oxidized low-density lipoprotein bind to apoptotic cells and inhibit their phagocytosis by elicited macrophages: evidence that oxidation-specific epitopes mediate macrophage recognition. Proc Natl Acad Sci USA 96: 6353-6358.
13. Cline AD, Jansen GR, Melby CL (1998) Stress fractures in female army recruits: implications of bone density, calcium intake and exercise. J Am Coll Nutr 17: 128-135.
14. Compagni A, Christofori G (2000) Recent advances in research on multistage tumorigenesis. Br J Cancer 83: 1-5.
15. Deckwerth TL, East RM, Knudson CM, Korsmeyer SJ, Johnson EM Jr (1998) Placement of the Bcl2 family member bax in the death pathway of sympathetic neurons activated by trophic factor deprivation. Exp Neurol 152: 150-162.
16. Devas MB (1961) Compression stress fractures in man and the greyhound. J Bone Joint Surg 43B: 540-551.
17. Dini L, Sutuori F, Lentini A, Oliverio S, Piacentini M (1992) The clearance of apoptotic cells in the liver is mediated by the asialo-glycoprotein receptor. FEBS Lett 296: 174-178.
18. Dockrell DH (2001) Apoptotic cell death in the pathogenesis of infectious diseases. J Infect 42: 227-234.
19. Dunstan CR, Somers NM, Evans RA (1993) Osteocyte death and hip fracture. Calcif Tissue Int 53: S113-S118.
20. Duvall E, Wyllie AG, Morris RG (1985) Macrophage recognition of cells undergoing programmed cell death (apoptosis). Immunology 56: 351-358.
21. Evan G, Littlewood T (1998) A matter of life and cell death. Science 281: 1317-1322.
22. Fadok VA, Bratton DL, Konowal A, Freed PW, Westcott JY, Henson PM (1998) Macrophages that have ingested apoptotic cells in vitro inhibit proinfammatory cytokine production sthrough autocrine/paracrine mechanisms involving TGF-β, PGE2 and PAF. J Clin Invest 101: 890-898.
23. Fadok VA, Bratton DL, Rose DM, Pearson A, Ezekewitz RA, Henson PM (2000) A receptor for phosphatidylserine-specific clearance of apoptotic cells. Nature 405: 85-90.
24. Fadok VA, de Cathelineau A, Daleke DL, Henson PM, Bratton DL (2001) Loss of phospholipid asymmetry and surface exposure of phosphatidylserine is required for phagocytosis of apopotic cells by macrophages and fibroblasts. J Biol Chem 276: 1071-1077.
25. Fraser A, McCarthy N, Evan GI (1996) Biochemistry of cell death. Curr Opin Neurobiol 6: 71-80.
26. Frisch SM, Francis H (1994) Desruption of epithelial cell-matrix interactions induces apoptosis. J Cell Biol 124: 619-626.
27. Frisch SM, Vuori K, Ruoslahti E, Chan-Hui PY (1996) Control of adhesion-dependent cell survival by focal adhesion kinase. J Cell Biol 134: 793-799.
28. Frost HM (1960a) Presence of microscopic cracks in vivo in bone. Henry Ford Hospital Med Bull 8: 25-35.
29. Frost HM (1960b) In vivo osteocyte death. J Bone Joint Surg 42: 138-143.
30. Frost HM (1985) Bone microdamage: Factors that impair its repair. In: Current Concepts of Bone Fragility. Uhtofff HD (ed). Springer-Verlag, Berlin. pp 123-148.
31. Grassme H, Jendrossek V, Gulbins E (2001) Molecular mechanisms of bacteria induced apoptosis. Apoptosis 6: 441-445.
32. Gregory CD (2000) CD14-dependent clearance of apoptotic cells: relevance to the immune system. Curr Opin Immunol 12: 27-34.
33. Gruber HE, Ivey JL, Thompson ER, Chesnut CH 3rd, Baylink DJ (1986) Osteoblast and osteoclast cell number and cell activity in postmenopausal osteoporosis. Miner Electrolyte Metab 12: 246-254.
34. Hamon Y, Broccardo C, Chambenoit O, Luciani MF, Toti F, Chaslin S, Freyssinet JM, Devaux PF, McNeish J, Marguet D, Chimini G (2000) ABC1 promotes engulfment of apoptitic cells and transbilayer redistribution of phosphatidylserine. Nat Cell Biol 2: 399-406.
35. Heemels M (2000) Nature Insight: Apoptosis. Nature 407: 769.
36. Heino TJ, Hentunen TA, Vaananen HK (2002) Osteocytes inhibit osteoclastic bone resorption through transforming growth factor-beta: enhancement by estrogen. J Cell Biochem 85: 185-197.
37. Hengartner MO (2000) The biochemistry of apoptosis. Nature 407: 770-776.
38. Hirano T, Turner CH, Forwood MR, Johnston CC, Burr DB (2000) Does suppression of bone turnover impair mechanical properties by allowing microdamage accumulation. Bone 27: 13-20.
39. Hogg N, Browning J, Howard T, Winterford C, Fitzpatrick D, Gobe G (1999) Apoptosis in vascular endothelial cells caused by serum deprivation, oxidative stress and transforming growth factor-beta. Endothelium 7: 35-39.
40. Ii M, Kurata H, Itoh N, Yamashima I, Kawasaki T (1990) Molecular cloning and sequence analysis of cDNA encoding the macrophage lectin specific for galactose and N-acetylgalactosamine. J Biol Chem 265: 11295-11298.
41. Inaoka T, Lean J, Bessho T, Chow J, Mackay A, Kokubo T (1995) Sequential analysis of gene expression after an osteogenic stimulus: c-fos expression is induced in osteocyes. Biochem Biophys Res Commun 217: 264-270.
42. Kakizaki I, Altmann F (1971) The osteocytes of the labyrinthine capsule. Arch Otolaryng 94: 139-149.
43. Kamijou T, Nakajima T, Ozawa H (1994) Effects of osteocytes on osteoinduction in the autogenous rib graft in the rat mandible. Bone 15: 629-637.
44. Kawata A, Miyauchi A, Kikuni-Takagaki Y (1998) Mechanisms of bone formation in vitro by stretched osteocytes. Jap J Med Electronics Biol Eng 36: 252-258.
45. Kenzora JE, Steele RE, Yosipovitch ZH, Glimcher MJ (1978) Experimental osteonecrosis of the femoral head in adult rabbits. Clin Orthop 130: 8-46.
46. Kerr JF, Wyllie AH, Currie AR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26: 239-257.
47. Klein-Nulend J, Semeins CM, Ajubi NE, Nijweide PJ, Burger EG (1995) Pulsating fluid flow increases nitric oxide (NO) synthesis by osteocytes but not periosteal fibroblasts - Correlation with prostaglandin upregulation. Biochem Biophys Res Commun 217: 640-648.
48. Kulms D, Schwarz T (2002) Molecular mechanisms involved in UV-induced apoptotic cell death. Skin Pharmacol Appl Skin Physiol 15: 342-347.
49. Lane NE, Thompson JM, Haupt D, Kimmel DB, Modin G, Kinnery JH (1998) Acute changes in trabecular bone connectivity and osteoclast activity in the ovariectomized rat in vivo. J Bone Miner Res 13: 229-236.
50. Lanyon LE (1992) Control of bone architecture by functional load bearing. J Bone Miner Res 7: S369-S375.
51. Lean JM, Jagger CJ, Chambers TJ, Chow JWM (1995) Increased insulin-like growth factor I mRNA expression in rate osteocytes in response to mechanical stimulation. Am J Physiol Endocrinol Metab 268: E318-E327.
52. Leri A, Caludio PP, Li Q, Wang X, Reiss K, Wang S, Malhotra A, Kajstura J, Anversa P (1998) Stretch-mediated release of angiotensin II induces myocyte apoptosis by activating p53 that enhances the local renin-angiotensin system and decreases the Bcl-2-to-Bax protein ratio in the cell. J Clin Invest 101: 1326-1342.
53. Li J, Mashiba T, Burr DB (2001) Bisphosphonate treatment suppresses not only stochastic remodeling but also the targeted repair of microdamage. Calcif Tissue Int 69: 281-286.
54. Lozupone E, Palumbo C, Favia A, Ferretti M, Palazzini S, Cantatore FP. (1996) Intermittent compressive load stimulates osteogenesis and improves osteocyte viability in bones cultured "in vitro". Clin Rheumatol. 15: 563-72.
55. Luciani MF, Chimini G (1996) The ATP binding cassette transporter ABC1, is required for the engulfment of corpses generated by apoptotic cell death. EMBO J 15: 226-235.
56. Maejima-Ikeda A, Aoki M, Tsuritani K, Kamioka K, Hiura K, Miyoshi T, Hara H, Takano-Yamamoto T, Kumegawa M (1997) Chick osteocyte-derived protein inhibits osteoclastic bone resorption. Biochem J 15: 245-250.
57. Marotti G, Farneti D, Remaggi F, Tartari F (1998) Morphometric investigation on osteocytes in human auditory ossicles. Ann Anatomy 180: 449-453.
58. Martin LJ (2001) Neuronal cell death in nervious system development, disease and injury. Int J Mol Med 7: 455-478.
59. Mashiba T, Hirano T, Turner CH, Forwood MR, Johnston CC, Burr DB (2000) Suppressed bone turnover by bisphosphonates increases microdamage accumulation and reduces some biomechanical properties in dog rib. Bone Miner Res 15: 613-620.
60. Mashiba T, Turner CH, Hirano T, Forwood MR, Jacob DS, Johnston CC, Burr DB (2001) Effects of high-dose etidronate treatment on microdamage accumulation and biomechanical properties in beagle bone occurrence of spontaneous fractures. Bone 29: 271-278.
61. Mason DJ, Suva LJ, Genever PG, Patton AJ, Steuckle S, Hillam RA, Skerry TM (1997) Mechanically regulated expression of a neural glutamate transporter in bone: A role for excitatory amino acids as osteotropic agents? Bone 20: 199-205.
62. Matsumoto T, Nakayama K, Kodama Y, Fuse H, Nakamura T, Fukumoto S (1998) Effect of mechanical unloading and reloading on periosteal bone formation and gene expression in tail-suspended rapidly growing rats. Bone 22: 89S-93S.
63. McBryde AM (1975) Stress fractures in athletes. J Sports Med 3: 212-217.
64. McNeill PL (2002) Repairing a torn cell surface: make way, lysosomes to the rescue. J Cell Sci 115: 873-879.
65. McNeill PL, Steinhardt RA (1997) Loss restoration and maintenance of plasma membrane integrity. J Cell Biol 137: 1-4.
66. Meier P, Finch A, Evan G (2000) Apoptosis in development. Nature 407: 796-801.
67. Mevorach D, Mascarenhas JO, Gershov D, Elkon KB (1998) Complement-dependent clearance of apoptotic cells by human macrophages. J Exp Med 188: 2313-2320.
68. Moffatt OD, Devitt A, Bell ED, Simmons DL, Gregory CD (1999) Macrophage recognition of ICAM-3 on apoptotic leukocytes. J Immunol 162: 6800-6810.
69. Monroe DG, Jin DF, Sanders MM (2000) Estrogen opposes the apoptotic effects of bone morphogenetic protein 7 on tissue remodeling. Mol Cell Biol 20: 4626-4634.
70. Mori S, Burr DB (1993) Increased intracortical remodeling following fatigue damage. Bone 14: 103-109.
71. Mori S, Harruff R, Ambrosius W, Burr DB (1997) Trabecular bone volume and microdamage accumulation in the femoral heads of women with a without femoral neck fractures. Bone 21: 521-526.
72. Muir P, Johnson KA, Ruaux-Mason CP (1999) Microdamage in a naturally occurring canine fatigue fracture. Bone 25: 571-576.
73. Mullender MG, Huiskes R, Versleyen H, Buma P (1996a) Osteocyte density and histomorphometric parameters in cancellous bone of the proximal femur in five mammalian species. J Orthop Res 14: 972-979.
74. Mullender MG, van der Meer DD, Huiskes R, Lips P (1996) Osteocyte density changes in aging and osteoporosis. Bone 18: 109-113.
75. Nguyen-Ba G, Vasseur P (1999) Epigenetic events during the process of cell transformation induced by carcinogens. Oncol Rep 6: 925-932.
76. Noble BS, Stevens H, Loveridge N, Reeve J (1997a) Identification of apoptotic changes in osteocytes in normal and pathological human bone. Bone 20: 273-282.
77. Noble BS, Stevens H, Mosley JR, Pitsillides AA, Reeve J, Lanyon L (1997b) Osteocyte apoptosis and functional strain in bone. J Bone Miner Res 12: 5.
78. Noble BS, Peet N, Stevens HY, Brabbs A, Mosley JR, Reilly GC, Reeve J, Skerry TM, Lanyon LE (2003) Mechanical loading: biphasic osteocyte survival and targeting of osteoclasts for bone destruction in rat cortical bone. Am J Physiol Cell Physiol 284: C934-C943.
79. Norman TL, Wang Z (1997) Microdamage of human cortical bone: incidence and morphology in long bones. Bone 20: 375-379.
80. Norrdin RW, Kawcak CE, Capwell BA, Mcilwraith CW (1998) Subchondral bone failure in an equine model of overload arthrosis. Bone 22: 133-139.
81. Nunamaker DM, Butterweck DM, Provost MT (1990) Fatigue fractures in thoroughbred racehourses: relationships with age, peak bone strain and training. J Orthop Res 8: 604-611.
82. Parfitt AM (1994) The two faces of growth: benefits and risks to bone integrity. Osteoporosis Int 4: 382-398.
83. Parfitt AM (2001) Trageted and non targeted bone remodeling: Relationship to BMU origination and progression. Bone 30: 585-587.
84. Pelengaris SA, Evan GI (1997) Matters of life and cell death. Rev Neurol (Paris) 153: 470-477.
85. Pitsillides AA, Rawlings SCF, Suswillo RFL, Bourrin S, Zaman G, Lanyon LE (1995) Mechanical strain-induced NO production by bone cells: A possible role in adaptive bone (re)modeling? FASEB J 9: 1614-1622.
86. Rawlinson SCF, Mosley JR, Suswillo RFL, Pitsillides AA, Lanyon LE (1995) Calvarial and limb bone cells in organ and monolayer culture do not show the same early responses to dynamic mechanical strain. J Bone Miner Res 10: 1225-1232.
87. Reilly GC, Currey JD (2000) The effects of damage and microcracking on the impact strength of bone. J Biomech 33: 337-43.
88. Ripps H (2002) Cell death in retinitis pigmentosa: gap junctions and the 'bystander' effect. Exp Eye Res 74: 327-336.
89. Rodan GA, Martin TJ (2000) Therapeutic approaches to bone diseases. Science 1: 1508-1514.
90. Rosen CJ (2000) Pathogenesis of osteoporosis. Baillieres Best Pract Res Clin Endocrinol Metab 14: 181-193.
91. Rubartelli A, Foggi A, Zocchi MK (1997) The selective engulfment of apoptotic bodies by dendritic cells is mediated by the avb3 integrin and requires intracellular and extracellular calcium. Eur J Immunol 27: 1893-1900.
92. Sanson M, Marcaud V, Robin E, Valery C, Sturtz F, Zalc B (2002) Connexin 43-mediated bystander effect in two rat glioma cell models. Cancer Gene Ther 9: 149-155.
93. Savill J, Fadok V (2000) Corpse clearance defines the meaning of cell death. Nature 407: 784-788.
94. Schaffler MB, Radin EL, Burr DB (1989) Mechanical and morphological effects of strain rate on fatigue of compact bone. Bone 10: 207-214.
95. Schaffler MB, Choi K, Milgrom C (1995a) Ageing and matrix microdamage accumulation in human compact bone. Bone 17: 521-525.
96. Schaffler MB, Boyce TM, Lundin-Cannon KD, Milgrom C, Fyhrie DP (1995b) Age related architectural changes and microdamage accumulation in the human femoral neck cortex. Trans Orthop Res Soc 20: 549.
97. Shibahara M, Nishida K, Asahara H, Yoshikawa T, Mitani S, Kondo Y, Inoue H (2000) Increased osteocyte apoptosis during the development of femoral head osteonecrosis in spontaneously hypertensive rats. Acta Med Okayama 54: 67-74.
98. Silvestrini G, Ballanti P, Patacchioli FR, Mocetti P, Di Grezia R, Wedard BM, Angelucci L, Bonucci E (2000) Evaluation of apoptosis and the glucocorticoid receptor in the cartilage growth plate and metaphyseal bone cells of rats after high-dose treatment with corticosterone. Bone 26: 33-42.
99. Stern M, Savill J, Haslett C (1996) Human monocyte-derived macrophage phagocytosis and senescent eosinophils undergoing apoptosis: mediation by avb3/CD36 thrombospondin recognition mechanism and lack of phlogistic response. Am J Pathol 149: 911-921.
100. Sun Y-Q, McLeod KJ, Rubin CT (1995) Mechanically induced periosteal bone formation is paralleled by the upregulation of collagen type one mRNA in osteocytes as measured by in situ reverse transcript-polymerase chain reaction. Calcif Tissue Int 57: 456-462.
101. Taylor D (1998) Fatigue of bone and bones: An analysis based on stressed volume. J Orthop Res 16: 163-169.
102. Taylor PR, Carugati A, Fadok VA, Cook HT, Andrews M, Carroll MC, Savill JS, Henson PM, Botto M, Walport MJ (2000) A hierarchical role for classical pathway complement proteins in the clearance of apoptotic cells in vivo. J Exp Med 192: 359-366.
103. Tesarik J, Maretinez F, Rienzi L, Iacobelli M, Ubaldi F, Mendoza C, Greco E (2002) In vitro effects of FSH and testosterone withdrawal on caspase activation and DNA fragmentation in different cell types of human seminiferous epithelium. Hum Reprod 17: 1811-1819.
104. Tomkinson A (1998) Effects of oestrogen on the maintenance of bone mass and bone cell viability. PhD Thesis Cambridge University.
105. Tomkinson A, Reeve J, Shaw RW, Noble BS (1997) The death of osteocytes via apoptosis accompanies estrogen withdrawal in human bone. J Clin Enocrinol Metab 82, 3128-3135.
106. Tomlin JL, Lawes TJ, Blunn GW, Goodship AE, Muir P (2000) Fractographic examination of racing greyhound central (navicular) tarsal bone failure surfaces using scanning electron microscopy. Calcif Tissue Int 67: 260-266.
107. Tremollieres FA, Pouilles JM, Ribot C (2001) Withdrawal of hormone replacement therapy is associated with significant vertebral bone loss in postmenopausal women. Osteoporosis Int 12: 385-390.
108. Ueki A, Isozaki Y, Tomokuni A, Hatayama T, Ueki H, Kusaka M, Shiwa M, Arikuni H, Takeshita T, Morimoto K (2002) Intramolecular epitope spreading among anti-caspase-8 autoantibodies in patients with sclerosis and systemic lupus erythematosus, as well as in healthy individuals. Clin Exp Immunol 129: 556-561.
109. Verborgt O, Gibson GJ, Schaffler MB (2000) Loss of osteocyte integrity in association with microdamage and bone remodeling after fatigue in vivo. J Bone Miner Res 15: 60-67.
110. Voll RE, Herrmann M, Rothe EA, Stach C, Kalden JR (1997) Immunosuppressive effects of apoptotic cells. Nature 390: 350-351.
111. Wang R, Zagariya A, Ang E, Ibarra-Sunga O, Uhal BD (1999) Fas-induced apoptosis of alveolar epithelial cells requires ANG II generation and receptor interaction. Am J Physiol 277: 1245-1250.
112. Warden SJ, Gutschlag FR, Wajswelner H, Crossley KM (2002) Aetiology of rib stress fractures in rowers. Sports Med 32: 819-836.
113. Weinstein RS, Jilka RL, Parfitt AM, Manolagas SC (1998) Inhibition of osteoblastogenesis and promotion of apoptosis of osteoblasts and osteocytes by glucocorticoids. Potential mechanisms of their deleterious effects on bone. J Clin Invest 102: 274-282.
114. Weinstein RS, Nicholas RW, Manolagas SC (2000) Apoptosis of osteocytes in glucocorticoid-induced osteonecrosis of the hip. J Clin Enocrinol Metab 85: 2907-2912.
115. Wong SY, Kariks J, Evans RA, Dunstan CR, Hills E (1985) The effect of age on bone composition and viability in the femoral head. J Bone Joint Surg Am 67: 274-283.
116. Wu YC, Horvitz HR (1998) The C. elegans cell corpse engulfment gene ced-7 encodes a protein similar to ABC transporters. Cell 93: 951-960.
117. Wyllie AH (1997) Apoptosis: an overview. Br Med Bull 53: 451-465.
118. Wyllie AH, Kerr JF, Currie AR (1980) Cell death: the significance of apoptosis. Int Rev Cytol 68: 251-306.
119. Yang P, Chen L, Zhou H, Zhong H, Wang H, Huang X, Kijlstra A (2002) Resistance of lymphocytes to Fas-mediated apoptosis in Behcet's disease and Vogt-Koyangi-Harada syndrome. Ocul Immunol Inflamm 10: 47-52.
120. Zhao S, Zhang YK, Harris S, Ahuja SS, Bonewald LF (2002) MLO-Y4 osteocyte-like cells support osteoclast formation and activation. J Bone Miner Res 17: 2068-2079.