Estrogen inhibits bone resorption by directly inducing apoptosis of the bone-resorbing osteoclasts

Journal of Experimental Medicine

Volumn 186, Issue 4, 1997, Pages 489-495

  Kameda, Takashi ^a   Mano, Hiroshi ^b   Yuasa, Tatsuhisa ^b   Mori, Yoshihisa ^b   Miyazawa, Koshi ^b   Shiokawa, Miho ^b   Nakamaru, Yukiya ^b   Hiroi, Emi ^b   Hiura, Kenji ^b   Kameda, Akira ^a   Yang, Na N ^c   Hakeda, Yoshiyuki ^b   Kumegawa, Masayoshi ^b  

^a NIPPON DENTAL UNIVERSITY   (Japan)

^b MEIKAI UNIVERSITY SCHOOL OF DENTISTRY   (Japan)

^c ELI LILLY AND COMPANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR; N BUTYL 11 (3,17BETA DIHYDROXYESTRA 1,3,5(10) TRIEN 7ALPHA YL) N METHYLUNDECANAMIDE; TAMOXIFEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; DATA ANALYSIS; DOSE RESPONSE; ESTROGEN DEFICIENCY; ESTROGEN THERAPY; MAMMAL; MENOPAUSE; NONHUMAN; OSTEOCLAST; OSTEOLYSIS; OSTEOPOROSIS; OVARIECTOMY; PRIORITY JOURNAL; RABBIT;

ANIMALS; APOPTOSIS; BONE RESORPTION; ESTROGENS; OSTEOCLASTS; RABBITS; RECEPTORS, ESTROGEN;

EID: 0030750208     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.186.4.489     Document Type: Article

References (38)

1. Lindsay, R., D.M. Hart, J.M. Aitken, E.B. MacDonald, J.B. Anderson, and A.C. Clarke. 1976. Long-term prevention of postmenopausal osteoporosis by oestrogen. Evidence for an increased bone mass after delayed onset of oestrogen treatment. Lancet. 1:1038-1041.
2. Ettinger, B., H.K. Genant, and C.E. Cann. 1985. Long-term estrogen replacement therapy prevents bone loss and fractures. Ann. Intern. Med. 102:319-324.
3. Heaney, R.P., R.R. Recker, and P.D. Saville. 1978. Menopausal changes in bone remodeling. J. Lab. Clin. Med. 92: 964-970.
4. Selby, P.L., M. Peacock, S.A. Barkworth, W.B. Brown, and G.A. Taylor. 1985. Early effects of ethinyloestradiol and norethisterone treatment in post-menopausal women on bone resorption and calcium regulating hormones. Clin. Sci. (Lond.). 69:265-271.
5. Vaes, G. 1988. Cellular biology and biochemical mechanism of bone resorption. A review of recent developments on the formation, activation, and mode of action of osteoclasts. Clin. Orthop. Relat. Res. 231:239-271.
6. Dewhirst, F.E., P.P. Stashenko, J.E. Mole, and T. Tsurumachi. 1985. Purification and partial sequence of human osteoclast-activating factor: identity with interleukin 1 beta. J. Immunol. 135:2562-2568.
7. Pfeilschifter, J., C. Chenu, A. Bird, G.R. Mundy, and G.D. Roodman. 1989. Interleukin-1 and tumor necrosis factor stimulate the formation of human osteoclast-like cells in vitro. J. Bone Miner. Res. 4:113-118.
8. Bertolini, D.R., G.E. Nedwin, T.S. Bringman, D.D. Smith, and G.R. Mundy. 1986. Stimulation of bone resorption and inhibition of bone formation in vitro by human tumour necrosis factors. Nature (Lond.). 319:516-518.
9. Lowik, C.W., G. van der Pluijm, H. Bloys, K. Hoekman, O.L. Bijvoet, L.A. Aarden, and S.E. Papapoulos. 1989. Parathyroid hormone (PTH) and PTH-like protein (PLP) stimulate interleukin-6 production by osteogenic cells: a possible role of interleukin-6 in osteoclastogenesis. Biochem. Biophys. Res. Commun. 162:1546-1552.
10. Chambers, T.J., N.A. Athanasou, and K. Fuller. 1984. Effect of parathyroid hormone and calcitonin on the cytoplasmic spreading of isolated osteoclasts. J. Endocrinol. 102:281-286.
11. Zaidi, M., H.K. Datta, B.S. Moonga, and I. MacIntyre. 1990. Evidence that the action of calcitonin on rat osteoclasts is mediated by two G proteins acting via separate post-receptor pathways. J. Endocrinol. 126:473-481.
12. 2 inhibits osteoclastic bone resorption by inducing osteoclast apoptosis. Biochem. Biophys. Res. Commun. 220:515-519.
13. Hughes, D.E., K.R. Wright, H.L. Uy, A. Sasaki, T. Yoneda, G.D. Roodman, G.R. Mundy, and B.F. Boyce. 1995. Bisphosphonates promote apoptosis in murine osteoclasts in vivo and in vitro. J. Bone Miner. Res. 10:1478-1487.
14. Wyllie, A.H., J.F. Kerr, and A.R. Currie. 1980. Cell death: the significance of apoptosis. Int. Rev. Cytol. 6:251-306.
15. Wyllie, A.H., R.G. Morris, A.L. Smith, and D. Dunlop. 1984. Chromatin cleavage in apoptosis: association with condensed chromatin morphology and dependence on macromolecular synthesis. J. Pathol. 142:67-77.
16. Pacifici, R., L. Rifas, S. Teitelbaum, E. Slatopolsky, R. McCracken, M. Bergfeld, W. Lee, L.V. Avioli, and W.A. Peck. 1987. Spontaneous release of interleukin 1 from human blood monocytes reflects bone formation in idiopathic osteoporosis. Proc. Natl. Acad. Sci. USA. 84:4616-4620.
17. Cohen-Solal M.E., A.M. Graulet, M.A. Denne, J. Gueris, D. Baylink, and M.C. de Vernejoul. 1993. Peripheral monocyte culture supernatants of menopausal women can induce bone resorption: involvement of cytokines. J. Clin. Endocrinol. Metab. 77:1648-1653.
18. Jilka, R.L., G. Hangoc, G. Girasole, G. Passeri, D.C. Williams, J.S. Abrams, B. Boyce, H. Broxmeyer, and S.C. Manolagas. 1992. Increased osteoclast development after estrogen loss: mediation by interleukin-6. Science (Wash. DC). 257:88-91.
19. Ikeda, T., C. Shigeno, R. Kasai, H. Kohno, S. Ohta, H. Okumura, J. Konishi, and T. Yamamuro. 1993. Ovariectomy decreases the mRNA levels of transforming growth factor-beta 1 and increases the mRNA levels of osteocalcin in rat bone in vivo. Biochem. Biophys. Res. Commun. 194:1228-1233.
20. Horowitz, M.C. 1993. Cytokines and estrogen in bone: anti-osteoporotic effects. Science (Wash. DC). 260:626-627.
21. Hughes, D.E., A. Dai, J.C. Tiffee, H.H. Li, G.R. Mundy, and B.F. Boyce. 1996. Estrogen promotes apoptosis of murine osteoclasts mediated by TGF-β. Nat. Med. 2:1132-1136.
22. Mano, H., T. Yuasa, T. Kameda, K. Miyazawa, Y. Nakamaru, M. Shiokawa, Y. Mori, T. Yamada, K. Miyata, H. Shindo, et al. 1996. Mammalian mature osteoclasts as estrogen target cells. Biochem. Biophys. Res. Commun. 223:637-642.
23. Oursler, M.J., L. Pederson, L. Fitzpatrick, B.L. Riggs, and T. Spelsberg. 1994. Human giant cell tumors of the bone (osteoclastomas) are estrogen target cells. Proc. Natl. Acad. Sci. USA. 91:5227-5231.
24. Oursler, M.J., P. Osdoby, J. Pyfferoen, B.L. Riggs, and T.C. Spelsberg. 1991. Avian osteoclasts as estrogen target cells. Proc. Natl. Acad. Sci. USA. 88:6613-6617.
25. Kakudo, S., K. Miyazawa, T. Kameda, H. Mano, Y. Mori, T. Yuasa, I. Nakamaru, M. Shiokawa, K. Nagahira, S. Tokunaga, et al. 1996. Isolation of highly enriched rabbit osteoclasts from collagen gels: a new assay system for bone-resorbing activity of mature osteoclasts. J. Bone Miner. Metab. 14: 129-136.
26. Takada, Y., M. Kusuda, K. Hiura, T. Sato, H. Mochizuki, Y. Nagao, M. Tomura, M. Yahiro, Y. Hakeda, H. Kawashima, and M. Kumegawa. 1992. A simple method to assess osteoclast-mediated bone resorption using unfractionated bone cells. Bone Miner. 17:347-359.
27. Kameda, T., H. Ishikawa, and T. Tsutsui. 1995. Detection and characterization of apoptosis in osteoclasts in vitro. Biochem. Biophys. Res. Commun. 207:753-760.
28. Iida, S., S. Kakudo, Y. Mori, M. Matsui, K. Magota, Y. Kitajima, N. Nakamura, H. Mano, Y. Hakeda, H. Azuma, et al. 1996. Human calcitonin has the same inhibitory effect on osteoclastic bone resorption by human giant cell tumor cells as salmon calcitonin. Calcif. Tissue Int. 59:100-104.
29. Warshawsky, H., and G. Moore. 1967. A technique for the fixation and decalcification of rat incisors for electron microscopy. J. Histochem. Cytochem. 15:542-549.
30. Tezuka, K., Y. Tezuka, A. Maejima, T. Sato, K. Nemoto, H. Kamioka, Y. Hakeda, and M. Kumegawa. 1994. Molecular cloning of a possible cysteine proteinase predominantly expressed in osteoclasts. J. Biol. Chem. 269:1106-1109.
31. Tezuka, K., T. Sato, H. Kamioka, P.J. Nijweide, K. Tanaka, T. Matsuo, M. Ohta, N. Kurihara, Y. Hakeda, and M. Kumegawa. 1992. Identification of osteopontin in isolated rabbit osteoclasts. Biochem. Biophys. Res. Commun. 186:911-917.
32. Walker, N.I., B.V. Harmon, G.C. Gobe, and J.F. Kerr. 1988. Patterns of cell death. Methods Achiev. Exp. Pathol. 13:18-54.
33. Halachmi, S., E. Marden, G. Martin, H. Mackay, C. Abbondanza, and M. Brown. 1994. Estrogen receptor-associated proteins: possible mediators of hormone-induced transcription. Science (Wash. DC). 264:1455-1458.
34. Kamei, Y., L. Xu, T. Heinzel, J. Torchia, R. Kurokawa, B. Gloss, S.-C. Lin, R.A. Heyman, D.W. Rose, C.K. Glass, and M.G. Rosenfeld. 1996. A CBP integrator complex mediates transcriptional activation and AP-1 inhibition by nuclear receptors. Cell. 85:403-414.
35. Arnett, T.R., R. Lindsay, J.M. Kilb, B.S. Moonga, M. Spowage, and D.W. Dempster. 1996. Selective toxic effects of tamoxifen on osteoclasts: comparison with the effects of oestrogen. J. Endocrinol. 149:503-508.
36. Friend, K.E., L.W. Ang, and M.A. Shupnik. 1995. Estrogen regulates the expression of several different estrogen receptor niRNA isoforms in rat pituitary. Proc. Natl. Acad. Sci. USA. 92:4367-4371.
37. Inoue, S., S. Hoshino, H. Miyoshi, M. Akishita, T. Hosoi, H. Orimo, and Y. Ouchi. 1996. Identification of a novel isoform of estrogen receptor, a potential inhibitor of estrogen action, in vascular smooth muscle cells. Biochem. Biophys. Res. Commun. 219:766-772.
38. Kuiper, G.G.J.M., E. Enmark, M. Pelto-Huikko, S. Nilsson, and J-Å. Gustafsson. 1996. Cloning of a novel estrogen receptor expressed in rat prostate and ovary. Proc. Natl. Acad. Sci. USA. 93:5925-5930.