Identification of apoptotic changes in osteocytes in normal and pathological human bone

Bone

Volumn 20, Issue 3, 1997, Pages 273-282

  Noble, B S ^a   Stevens, H ^a   Loveridge, N ^a   Reeve, J ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Apoptosis; Bone modeling; Bone remodeling; DNA fragmentation; Human bone; In situ; Osteocyte

Indexed keywords

DNA FRAGMENT; LACTATE DEHYDROGENASE;

ADULT; AGAR GEL ELECTROPHORESIS; APOPTOSIS; ARTICLE; BIOMECHANICS; BONE GROWTH; BONE MATRIX; BONE REMODELING; BONE TISSUE; BONE TURNOVER; CALVARIA; CELL SIZE; CELL VIABILITY; CHROMATIN; CHROMATIN CONDENSATION; CONTROLLED STUDY; DNA DETERMINATION; DNA NICK TRANSLATION; ELECTRON MICROSCOPY; FEMUR HEAD; HUMAN; HUMAN CELL; ILIAC CREST; INFANT; MICROSCOPY; OSTEOCYTE; OSTEOPHYTE; TRANSMISSION ELECTRON MICROSCOPY;

ADULT; APOPTOSIS; BONE DEVELOPMENT; BONE REMODELING; CHROMATIN; DNA FRAGMENTATION; ELECTROPHORESIS, AGAR GEL; FEMALE; HIP FRACTURES; HUMANS; INFANT; MICROSCOPY, ELECTRON; MIDDLE AGED; OSTEOARTHRITIS; OSTEOCYTES;

EID: 0030951831     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/S8756-3282(96)00365-1     Document Type: Article

References (53)

1. Aarden, E. M., Burger, E. H., and Nijweide, P. Function of osteocytes in bone. J Cell Biochem 55:287-299; 1994.
2. Aaron, J. E. Osteocyte types in developing mouse calvarium. Calcif Tissue Res 12:259-279; 1973.
3. Arends, M. J., Morris, R. G., and Wyllie, A. H. Apoptosis - the role of the endonuclease. Am J Pathol 136:593-608; 1990.
4. Boyde, A., Hendel, P., Hendel, R., Maconnachie, E., and Jones, S. J. Human cranial bone structure and the healing of cranial bone grafts: A study using backscattered electron imaging and confocal microscopy. Anat Embryol 181: 235-251; 1990.
5. Burger, E. H., KleinNulend, J., Van der Plas, A., and Nijweide, P. J. Function of osteocytes in bone: Their role in mechanotransduction. J Nutr 125(Suppl): 2020S-2023S; 1995.
6. Cohen, G. M., Sun, X., Snowden, R. T., Dinsdale, D., and Skilleter, D. N. Key morphological features of apoptosis may occur in the absence of internucleosomal fragmentation. Biochem J 286:331-334; 1992.
7. Compston, J. E., Yamaguchi, K., Croucher, P. I., Garrahan, N. J., Lindsay, P. C., and Shaw, R. W. The effects of gonadotrophin-releasing hormone agonists on iliac crest cancellous bone structure in women with endometriosis. Bone 16:261-267; 1995.
8. Darzynkiewicz, Z., Bruno, S., Del Bino, G., Gorczyca, W., Hotz, M. A., Lassota, P., and Traganos, F. Features of apoptotic cells measured by flow cytometry. Cytometry 13:795-808; 1992.
9. Dini, L., Coppola, M., Ruzittu, M. T., and Ghibelli, L. Multiple pathways for apoptotic nuclear fragmentation. Exp Cell Res 223:340-347; 1996.
10. Dunstan, C. R., Evans, R. A., Hills, E., Wong, S. Y. P., and Higgs, R. J. E. D. Bone death in hip fracture in the elderly. Calcif Tissue Int 47:270-275; 1990.
11. Dunstan, C. R., Somers, N. M., and Evans, R. A. Osteocyte death and hip fracture. Calcif Tissue Int 53(Suppl 1):S113-S117; 1993.
12. Duvall, E., Wyllie, A. H., and Morris, R. G. Macrophage recognition of cells undergoing programmed cell death (apoptosis). Immunology 56:351-358; 1985.
13. El Haj, A. J., Minter, S. L., Rawlinson, S. C. F., Suswillo, R., and Lanyon, L. E. Cellular responses to mechanical loading in vitro. J Bone Miner Res 5:923-932; 1990.
14. Elmardi, A. S., Katchburian, M. V., and Katchburian, E. Electron microscopy of developing calvaria reveals images that suggest that osteoclasts engulf and destroy osteocytes during bone resorption. Calcif Tissue Int 46:239-245; 1990.
15. Evan, G. I., Brown, L., Whyte, M., and Harrington, E. Apoptosis and the cell cycle. Curr Opin Cell Biol 7:825-834; 1995.
16. Fadok, V. A., Voelker, D. R., Campbell, P. A., Cohen, J. J., Bratton, D. L., and Henson, P. M. Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J Immunol 148:2207-2216; 1992.
17. Farquharson, C., Whitehead, C., Rennie, S., Thorp, B., and Loveridge, N. Cell proliferation and enzyme activities associated with the development of avian tibial dyschondroplasia: An in situ biochemical study. Bone 13:59-67; 1992.
18. Fehsel, K., KolbBachofen, V., and Kolb, H. Analysis of TNF alpha induced DNA strand breaks at the single cell level. Am J Pathol 139:251-254; 1991.
19. Fehsel, K., Kroncke, K. D., Kolb, H., and KolbBachoten, V. In situ nick-translation detects focal apoptosis in thymuses of glucocorticoid- and lipopolysaccharide-treated mice. J Histochem Cytochem 42:613-619; 1994.
20. Fesus, L., Thomazy, V., Autuori, F., Ceru, M., Tarcsa, E., and Piacentini, M. Apoptotic hepatocytes become insoluble in detergents and chaotropic agents as a result of transglutaminase action. FEBS Lett 245:150-154; 1989.
21. Fournel, S., Genestier, L., Rouault, J., Lizard, G., Flacher, M., Assossou, O., and Revillard, J. Apoptosis without decrease of cell DNA content. FEBS Lett 367:188-192; 1995.
22. Frost, H. M. In vivo osteocyte death. J Bone Joint Surg [Am] 42:138-143; 1960.
23. Gold, R., Schmied, M., Giegerich, G., Breitschopf, H., Hartung, H. P., Tyka, K. V., and Lassmann, H. Differentiation between cellular apoptosis and necrosis by the combined use of in situ tailing and nick translation techniques. Lab Invest 71:219-225; 1994.
24. Gorczyca, W., Gong, J., and Darzynkiewiez, Z. Detection of DNA strand breaks in individual apoptotic cells by the in situ terminal deoxynucleotidyl transferase and nick translation assays. Cancer Res 53:1945-1951; 1993.
25. Hatori, M., Klatte, K. J., Teixeira, C. C., and Shapiro, I. M. End labelling of fragmented DNA in the avian growth plate: Evidence of apoptosis in terminally differentiated chondrocytes. J Bone Miner Res 10:1960-1968; 1995.
26. Henson, F. M. D., Davies, M. E., Skepper, J. N., and Jeffcott, L. B. Localisation of alkaline phosphatase in equine growth cartilage. J Anat 187:151-159; 1995.
27. Hughes, D. E., Wright, K. R., Uy, H. L., Sasaki, A., Yoneda, T., Roodman, G. D., Mundy, G. R., and Boyce, B. F. Bisphosphonates promote apoptosis in murine osteoclasts in vitro and in vivo. J Bone Miner Res 10:1478-1487; 1995.
28. Kameda, T., Ishikawa, H., and Tsutsui, T. Detection and characterisation of apoptosis in osteoclasts in vitro. Biochem Biophys Res Commun 207:753-760; 1995.
29. KleinNulend, J., Van der Plas, A., Semeins, C. M., Ajubi, N. E., Frangos, J. A., Nijweide, P. J., and Burger, E. H. Sensitivity of osteocytes to biomechanical stress in vitro. FASEB J 9:441-445; 1995.
30. Lanyon, L. E. Osteocytes, strain detection, bone modeling and remodeling. Calcif Tissue Int 53:5102-5107; 1993.
31. Lewinson, D. and Silbermann, M. Chondroclasts and endothelial cells collaborate in the process of cartilage resorption. Anat Rec 233:504-514; 1992.
32. Midgley, C. A., Owens, B., Briscoc, C. V., Thomas, D. B., Lane, D. P., and Hall, P. A. Coupling between gamma irradiation, P53 induction, and the apoptotic response depends upon cell type in vivo. J Cell Sci 108:1843-1848; 1995.
33. Noble, B. S., Milne, J., and Loveridge, N. Apoptosis in growing rat bone: Preliminary studies. Bone 16:689; 1995.
34. Noble, B. S., Stevens, H., Reeve, J., and Loveridge, N. Apoptosis in normal and pathological human bone. J Bone Miner Res 10:5264; 1995.
35. Oberhammer, F., Wilson, J. W., Dive, C., Morris, I. D., Hickman, J. A., Wakeling, A. E., Walker, P. R., and Sikorska, M. Apoptotic death in epithelial cells: Cleavage of DNA to 300 and/or 50 kb fragments prior to or in the absence of internucleosomal fragmentation. EMBO J 12:3679-3684; 1993.
36. Osborne, B. A. and Schwartz, L. M. Essential genes that regulate apoptosis. Trends Cell Biol 4:394-399; 1994.
37. Parfitt, A. M. Bone age, mineral density, and fatigue damage. Calcif Tissue Int 53(Suppl 1):S82-S86: 1993.
38. 3H] uridine levels in osteocytes following a single short period of dynamic loading in vivo. Calcif Tissue Int 43:92-96; 1988.
39. Preston, G. A., Lang, J. E., Maronpot, R. R., and Barrett, J. C. Regulation of apoptosis by low serum in cells of different stages of neoplastic progression: Enhanced susceptibility after loss of a senescence gene and decreased susceptibility after loss of a tumour suppressor gene. Cancer Res 54:4214-4223: 1994.
40. Rittmaster, R. S., Manning, A. P., Wright, A. S., Thomas, L. N., Whitefield, S., Norman, R. W., Lazier, C. B., and Rowden, G. Evidence for atrophy and apoptosis in the ventral prostrate of rats given the 5α-reductase inhibitor finasteride. Endocrinology 136:741-748; 1995.
41. Roach, H. I., Erenpreisa, J., and Aigner, T. Osteogenic differentiation of hypertrophic chondrocytes involves cell divisions and apoptosis. J Cell Biol 131: 483-494; 1995.
42. Savill, J., Dransfield, I., Hogg, N., and Haslett, C. Vitronectin receptor-mediated phagocytosis of cells undergoing apoptosis. Nature 343:170-173; 1990.
43. Simmons D. J. and Gynpas, M. D. Mechanisms of bone formation in vivo. In: Hall, B. K., Ed. Bone, Vol. I: The osteoblast and osteocyte. Caldwell, NJ: Telford; 1990; 193-302.
44. Skerry, T. M., Bitensky, L., Chayen, J., and Lanyon, L. E. Early strain-related changes in enzyme activity in osteocytes following bone loading in vivo. J Bone Miner Res 4:783-788; 1989.
45. Smeyne, R. J., Vendrell, M., Hayward, M., Baker, S. J., Miao, G. G., Schilling, K., Robertson, L. M., Curran, T., and Morgan, J. I. Continuous c-fos expression precedes programmed cell death in vivo. Nature 363:166-169; 1993.
46. Tanaka, K., Matsuo, T., Ohta, M., Sato, T., Tezuka, K., Nijweide, P. J., Katoh, Y., Hakeda, Y., and Kumegawa, M. Time-lapse microcinematography of osteocytes. Miner Electrolyte Metab 21:189-192; 1995.
47. Tomei, L. D., Shapiro, J. P., and Cope, F. O. Apoptosis in C3H/10T1/2 mouse embryonic cells: Evidence tor internucleosomal DNA modification in the absence of double-strand cleavage. Proc Natl Acad Sci USA 90:853-857; 1993.
48. Tonna, E. A. An electron microscope study of osteocyte release during osteoclasis in mice of different ages. Clin Orthop Rel Res 87:311-317; 1972.
49. Wong, S. Y. P., Evans, R. A., Needs, C., Dunstan, C. R., Hills, E., and Garvan, J. The pathogenesis of osteoarthritis of the hip. Clin Orthop Rel Res 214:305-312; 1987.
50. Wyllie, A. H. Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 284:555-556; 1980.
51. Wyllie, A. H., Kerr, J. F. R., and Currie, A. R. Cell death: The significance of apoptosis. Int Rev Cytol 68:251-306; 1980.
52. Zimmermann, B. Degeneration of osteoblasts involved in intramembranous ossification of fetal rat calvaria. Cell Tissue Res 267:75-84; 1992.
53. Zimmermann, B. Occurrence of osteoblast necroses during ossification of long bone cortices in mouse fetuses. Cell Tissue Res 275:345-353; 1994.