Effects of Estrogen, Aging and Oxidative Stress on Bone Remodelling in a View of Molecular Mechanisms

골개형(Bone Remodelling)의 분자생물학적 기전에 대한 노화, 에스트로젠 및 산화적 스트레스의 영향

  • Park, Yeong-Chul (Center for Bio-Safety Catholic University of Daegu) ;
  • Koh, Young-Do (Department of Orthopaedic Surgery, Medical College, Ewha Women University) ;
  • Han, Jung-Ho (Medical Research Center, Seoul National University) ;
  • Kim, Mi-Kyung (Marine Science Research Center, Yeungnam University)
  • 박영철 (대구가톨릭대학교 바이오안전성센터) ;
  • 고영도 (이화여자대학교 의과대학 정형외과(목동병원)) ;
  • 한정호 (서울대학교 의학연구원) ;
  • 김미경 (영남대학교 해양과학연구센터)
  • Published : 2006.09.30

Abstract

Bone is a dynamic tissue that is constantly being remodelled. Resolution of bone and formation of new bone are closely linked, so that bone mass remains constant. With age, this process becomes unlinked with an imbalance in bore resorption and formation that results in a net loss of bone. Especially, osteoporosis is a disease characterized by low bone mass with age. One form of aging-related primary osteoporosis is postulated with the reduction of circulating estrogen, rapid bone loss occurs as a result of enhanced bore remodelling with an excess of resorption over bore formation. The oxidative stress is also involved in the pathogenesis of osteoporosis. Oxidative stress by cytokines, such as IL-a and TNF-${\alpha}$, inhibits osteoblast function in vitro and stimulates osteoblast apoptosis resulting in an imbalance in bore remodelling. The present article reviews the current perspectives on the interaction between bone remodelling and factors such as estrogen and oxidative stress, providing an interpretation of bone diseases in a view of molecular mechanisms.

Keywords

References

  1. Abe, M. (2006): Bone disease in multiple myeloma and its mechanism. Clin Calcium., 16, 33-39
  2. Allan, E.H., Hilton, D.J., Brown, M.A., Evely, R.S,, Yumita, S., Metcalf, D., Gough, N.M., Ng, K.W., Nicola, N.A. and Martin, T.J. (1990): Osteoblasts display receptors for and responses to leukemia-inhibitory factor. Cell Physiol., 145, 110-119 https://doi.org/10.1002/jcp.1041450116
  3. Allan, E.H., Hamilton, J.A., Medcalf, R.L., Kubota, M. and Martin, T.J. (1986): Cyclic AMP-dependent and -independent effects on tissue-type plasminogenactivator activity in osteogenic sarcoma cells; evidence from phosphodiesterase inhibition and parathyroid hormone antagonists. Biochim. Biophys. Acta, 888, 199-207 https://doi.org/10.1016/0167-4889(86)90022-4
  4. Ashton, B.A., Allen, T.D., Howlett, C.R., Eaglesom, C.C., Hattori, A. and Owen, M. (1980): Formation of bone and cartilage by marrow stromal cells in diffusion chambers in vivo. Clin. Orthop. Relat. Res., 151, 294-307
  5. Bai, X.C., Lu, D., Liu, A.L., Zhang, Z.M., Li, X.M., Zou, Z.P., Zeng, W.S., Cheng, B.L. and Luo, S.Q. (2005): Reactive oxygen species stimulates receptor activator of NF-kappaB ligand expression in osteoblast. J. Biol. Chem., 280, 17497-17506 https://doi.org/10.1074/jbc.M409332200
  6. Balasch, J. (2003): Sex steroids and bone: current perspectives. Hum. Reprod. Update., 9, 207-222 https://doi.org/10.1093/humupd/dmg017
  7. Bax, B.E., Alam, A.S.M.T. and Banerji, B. (1992): Stimulation of osteoclastic bone resorption by hydrogen peroxide. Biochem. Biophysics. Res. Commun., 183, 1153-1158 https://doi.org/10.1016/S0006-291X(05)80311-0
  8. Bancroft, J. and Cawood, E.H. (1996): Androgens and the menopause; a study of 40-60-year-old women. Clin. Endocrinol., 45, 577-587 https://doi.org/10.1046/j.1365-2265.1996.00846.x
  9. Beard, C.J., Key. L., Newburger, P.E., Ezekowitz, R.A., Arceci, R., Miller, B., Proto, P., RyanT, Anast, C. and Simons, E.R. (1986): Neutrophil defect associated with malignant infantile osteopetrosis. J. Lab. Clin. Med., 108, 498-505
  10. Beckman, J.S., Beckman, T.W., Chen, J., Marshall, P.A. and Freeman, B.A., (1990): Apparent hydroxyl radical production by peroxynitrite: implication for endothelial injury from nitric oxide and superoxide. Proc. Natl. Acad. Sci., 17, 1620-1624
  11. Bellosta, S. and Bernini, F. (2005): Modulation of macrophage function and metabolism. Handb. Exp. Pharmacol., 170, 665-95 https://doi.org/10.1007/3-540-27661-0_25
  12. Benayahu, D., Kletter, Y., Zipori, D. and Wientroub, S. (1989): Bone marrow-derived stromal cell line expressing osteoblastic phenotype in vitro and osteogenic capacity in vivo. J. Cell. Physiol., 140, 1-7 https://doi.org/10.1002/jcp.1041400102
  13. Bergmann, P., Nijs-De Wolf, N., Pepersack, T. and Corvilain, J. (1990): Release of parathyroid hormonelike peptides by fetal rat long bones in culture. J. Bone. Miner. Res., 5, 741-753 https://doi.org/10.1002/jbmr.5650050711
  14. Blair, H.C., Robinson, L.J. and Zaidi, M. (2005): Osteoclast signalling pathways. Biochem. Biophys. Res. Commun., 328, 728-738 https://doi.org/10.1016/j.bbrc.2004.11.077
  15. Boyce, B.F., Aufdemorte, T.B., Garrett, I.R., Yates, A.J. and Mundy, G.R. (1989): Effects of interleukin-1 on bone turnover in normal mice. Endocrinology, 125, 1142-1150 https://doi.org/10.1210/endo-125-3-1142
  16. Boyce, B.F., Li, P., Yao, Z., Zhang, Q., Badell, I.R., Schwarz, E.M., O'Keefe, R.J. and Xing, L. (2005): TNF-alpha and pathologic bone resorption. Keio. J. Med., 54, 127-131 https://doi.org/10.2302/kjm.54.127
  17. Brandi, M.L., Hukkanen, M., Umeda, T., et al., (1995): Bidirectional regulation of osteoclast function by nitric oxide synthase isoforms. Proc. Natl. Acad. Sci., 92, 2954-2958
  18. Briot, K. and Roux, C. (2005): Epub 2005 Nov 28. Comment in: Gynecol Obstet Fertil., 33, 1009-1013
  19. Buttke, T.M. and Van Cleave, S. (1994): Adaptation of a cholesterol deficient human T cell line to growth with lanosterol. Biochem. Biophys. Res. Commun., 200, 206-212 https://doi.org/10.1006/bbrc.1994.1435
  20. Canalis, E., Centrella, M., Burch, W. and McCarthy, T.L. (1989): Insulin-like growth factorI mediates selective anabolic effects of parathyroidhormone in bone cultures. J. Clin. Invest., 83, 60-65 https://doi.org/10.1172/JCI113885
  21. Canalis, E., McCarthy, T.L. and Centrella, M. (1989): Effects of platelet-derived growth factor on bone formation in vitro. J. Cell. Physiol., 140, 530-537 https://doi.org/10.1002/jcp.1041400319
  22. Carlsten, H. (2005): Immune responses and bone loss: the estrogen connection. Immunol. Rev., 208, 194-206 https://doi.org/10.1111/j.0105-2896.2005.00326.x
  23. Chenu, C., Valentin-Opran, A., Chavassieux, P., Saez, S., Meunier, P.J. and Delmas, P.D. (1990): Insulin like growth factor I hormonal regulation by growth hormone and by 1,25(OH)2D3 and activity on human osteoblast-like cells in short-term cultures. Bone., 11, 81-86 https://doi.org/10.1016/8756-3282(90)90054-3
  24. Cheng, M.Z., Rawlinson, S.C., Pitsillides, A.A., Zaman, G., Mohan, S., Baylink, D.J. and Lanyon, L.E. (2002): Human osteoblasts' proliferative responses to strain and 17betaestradiol are mediated by the estrogen receptor and the receptor for insulin-like growth factor I. J. Bone. Miner. Res., 17, 593-602 https://doi.org/10.1359/jbmr.2002.17.4.593
  25. Clezardin, P. (2000): Bone hyperresorption in bone metastases. Presse Med., 29, 487-491
  26. Cosman, F. and Lindsay, R. (1998): Is parathyroid hormone a therapeutic option for osteoporosis? A review of the clinical evidence. Calcif. Tissue. Int., 62, 475-480 https://doi.org/10.1007/s002239900464
  27. Cutolo, M., Sulli, A., Barone, A., Seriolo, B. and Accardo, S. (1993): Macrophages, synovial tissue and rheumatoid arthritis. Clin. Exp. Rheumatol., 11, 331-339
  28. Daci, E., Everts, V., Torrekens, S., Van Herck, E., Tigchelaar- Gutterr, W., Bouillon, R. and Carmeliet, G. (2003): Increased bone formation in mice lacking plasminogen activators. J. Bone. Miner. Res., 18, 1167-1176 https://doi.org/10.1359/jbmr.2003.18.7.1167
  29. Damoulis, P.D. and Hauschka, P.V. (1994): Cytokines induce nitric oxide production in mouse osteoblasts. Biochem. Biophys. Res. Commun., 201, 924-931 https://doi.org/10.1006/bbrc.1994.1790
  30. Darden, A.G., Ries, W.L., Wolf, W.C., Rodriguiz, R.M. and Key, L.L. Jr. (1996): Osteoclastic superoxide production and bone resorption: stimulation and inhibition by modulators of NADPH oxidase. J. Bone. Miner. Res., 11, 671-675 https://doi.org/10.1002/jbmr.5650110515
  31. Datta, H.K., Rathod, H., Manning, P., Turnbull, Y. and McNeil, C.J. (1996): Parathyroid hormone induces superoxide anion burst in the osteoclast: evidence for the direct instantaneous activation of the osteoclast by the hormone. J. Endocrinol., 149, 269-277 https://doi.org/10.1677/joe.0.1490269
  32. Dinarello, C.A. (1994) The interleukin-1 family: 10 years of discovery. FASEB J., 8, 1314-1325 https://doi.org/10.1096/fasebj.8.15.8001745
  33. Farrell, A.J., Blake, D.R., Palmer, R.M. and Moncada, S. (1992): Increased concentrations of nitrite in synovial fluid and serum samples suggest increased nitric oxide synthesis in rheumatic diseases. Ann. Rheum. Dis., 51, 1219-1222 https://doi.org/10.1136/ard.51.11.1219
  34. Feyen, J.H., Elford, P., Di Padova, F.E. and Trechsel, U. (1989): Interleukin-6 is produced by bone and modulated by parathyroid hormone. J. Bone. Miner. Res., 4, 633-8 https://doi.org/10.1002/jbmr.5650040422
  35. Felix, R., Fleisch, H. and Elford, P.R. (1989): Bone-resorbing cytokines enhance release of macrophage colony-stimulating activity by the osteoblastic cell MC3T3-E1. Calcif. Tissue. Int., 44, 356-360 https://doi.org/10.1007/BF02556317
  36. Filvaroff, E. and Derynck, R. (1998): Bone remodelling: a signalling system for osteoclast regulation. Curr. Biol., 8, R679-R682 https://doi.org/10.1016/S0960-9822(98)70434-8
  37. Friedenstein, A.J., Deriglasova, U.F., Kulagina, N.N., Panasuk, A.F., Rudakowa, S.F., Luria, E.A. and Ruadkow, I.A. (1974): Precursors for fibroblasts in different populations of hematopoietic cells as detected by the in vitro colony assay method. Exp. Hematol., 2, 83-92
  38. Evans, D.M. and Ralston, S.H. (1996): Nitric oxide and bone. J. Bone. Miner. Res., 11, 300-305 https://doi.org/10.1002/jbmr.5650110303
  39. Gallagher, J.C., Riggs, B.L., Jerpbak, C.M. and Arnaud, C.D. (1980): The effect of age on serum immunoreactive parathyroid hormone in normal and osteoporotic women. J. Lab. Clin. Med., 95, 373-385
  40. Garrett, I.R., Boyce, B.F., Oreffo, R.O.C., Bonewald, L., Poser, J. and Mundy, G.R, (1990): Oxygen-derived free radicals stimulate osteoclastic bone resorption in rodent bone in vitro and in vivo. J. Clin. Invest., 85, 632-639 https://doi.org/10.1172/JCI114485
  41. Girasole, G., Jilka, R.L., Passeri, G., Boswell, S., Boder, G., Williams, D.C. and Manolagas, S.C. (1992): beta-estradiol inhibits interleukin-6 production by bone marrowderived stromal cells and osteoblasts in vitro: a potential mechanism for the antiosteoporotic effect of estrogens. J. Clin. Invest., 89, 883-891 https://doi.org/10.1172/JCI115668
  42. Grills, B.L., Gallagher, J.A., Allan, E.H., Yumita, S. and Martin, T.J. (1990): Identification of plasminogen activator in osteoclasts. J. Bone. Miner. Res., 5, 499-505 https://doi.org/10.1002/jbmr.5650050512
  43. Gowen, M., Chapman, K., Littlewood, A., Hughes, D., Evans, D. and Russell, G. (1990): Production of tumor necrosis factor by human osteoblasts is modulated by othercytokines, but not by osteotropic hormones. Endocrinology, 126, 1250-1255 https://doi.org/10.1210/endo-126-2-1250
  44. Greenwald, R.A. and Rifkin, B.R. (1992): Reactive oxygen species as potential mediators of osteoclast action. In: Rifkin, B.R. and Gay, C.V. (eds.), Biology and physiology of the osteoclast. CRC press., 315-336
  45. Hagenaars, C.E., van der Kraan, A.A., Kawilarang-de Haas, E.W., Visser, J.W. and Nijweide, P.J. (1989): Osteoclast formation from cloned pluripotent hemopoietic stem cells. Bone. Miner., 6, 179-189 https://doi.org/10.1016/0169-6009(89)90049-4
  46. Hall, T.J., Jeker, H. and Schaueblin, M. (1995): Taxol inhibits osteoclastic bone resorption. Calcif. Tissue. Int., 57, 463-465 https://doi.org/10.1007/BF00301951
  47. Halleen, J.M., Raisanen, S.R., Alatalo, S.L. and Vaananen, H.K. (2003): Potential function for the ROS-generating activity of TRACP. J. Bone. Miner. Res., 18, 1908-1911 https://doi.org/10.1359/jbmr.2003.18.10.1908
  48. Hamilton, J.A., Lingelbach, S., Partridge, N.C. and Martin, T.J. (1985): Regulation of plasminogen activator production by bone-resorbing hormones in normal and malignant osteoblasts. Endocrinology, 116, 2186-2191 https://doi.org/10.1210/endo-116-6-2186
  49. Hattersley, G., Kerby, J.A. and Chambers, T.J. (1991): Identification of osteoclast precursors in multilineage hemopoietic colonies. Endocrinology, 128, 259-262 https://doi.org/10.1210/endo-128-1-259
  50. Higuchi, C. and Nakase, T. (2005): Osteoporosis and bone morphogenetic protein (BMP). Nippon. Rinsho., 63, 439-443
  51. Horowitz, M.C., Coleman, D.L., Ryaby, J.T. and Einhorn, T.A. (1989): Osteotropic agents induce the differential secretion of granulocyte-macrophagecolony-stimulating factor by the osteoblast cell line MC3T3-E1. J. Bone. Miner. Res., 4, 911-921 https://doi.org/10.1002/jbmr.5650040616
  52. Horowitz, M., Wishart, J.M., O'Loughlin, P.D., Morris, H.A., Need, A.G. and Nordin, B.E. (1992): Osteoporosis and Klinefelter's syndrome. Clin. Endocrinol., 36, 113-118 https://doi.org/10.1111/j.1365-2265.1992.tb02910.x
  53. Howard, G.A., Bottemiller, B.L., Turner, R.T., Rader, J.I. and Baylink, D.J. (1981): Parathyroid hormone stimulates bone formation and resorption in organ culture: evidence for a coupling mechanism. Proc. Natl. Acad. Sci., 78, 3204-3208
  54. Hughes, F.J., Turner, W., Belibasakis, G. and Martuscelli, G. (2006): Effects of growth factors and cytokines on osteoblast differentiation. Periodontol. 2000., 41, 68-72
  55. Ikegami, A., Inoue, S., Hosoi, T., Kaneki, M., Mizuno, Y., Akedo, Y., Ouchi, Y. and Orimo, H. (1994): Cell cycledependent expression of estrogen receptor and effect of estrogen on proliferation of synchronized human osteoblast- like osteosarcoma cells. Endocrinology, 135, 782-789 https://doi.org/10.1210/en.135.2.782
  56. Ishimi, Y., Miyaura, C., Jin, C.H., Akatsu, T., Abe, E., Nakamura, Y., Yamaguchi, A., Yoshiki, S., Matsuda, T., Hirano, T., et al. (1990) IL-6 is produced by osteoblasts and induces bone resorption. J. Immunol., 145, 3297-3303
  57. Jilka, R.L., Hangoc, G., Girasole, G., Passeri, G., Williams, D.C., Abrams, J.S., Boyce, B., Broxmeyer, H. and Manolagas, S.C. (1992): Increased osteoclast development after estrogen loss: mediation byinterleukin-6. Science, 257, 88-91 https://doi.org/10.1126/science.1621100
  58. Johnson, R.A., Boyce, B.F., Mundy, G.R. and Roodman, G.D. (1989): Tumors producing human tumor necrosis factor induced hypercalcemia and osteoclastic bone resorption in nude mice. Endocrinology, 124, 1424-1427 https://doi.org/10.1210/endo-124-3-1424
  59. Joyce, M.E., Roberts, A.B., Sporn, M.B. and Bolander, M.E. (1990): Transforming growth factor-beta and the initiation of chondrogenesis and osteogenesis in the rat femur. J. Cell. Biol., 110, 2195-2207 https://doi.org/10.1083/jcb.110.6.2195
  60. Kania, D.M., Binkley, N., Checovich, M., Havighurst, T., Schilling, M. and Ershler, W.B. (1995): Elevated plasma levels of interleukin-6 in postmenopausal women do not correlatewith bone density. J. Am. Geriatr. Soc., 43, 236-239 https://doi.org/10.1111/j.1532-5415.1995.tb07328.x
  61. Kassem, M., Okazaki, R., De Leon, D., Harris, S.A., Robinson, J.A., Spelsberg, T.C., Conover, C.A. and Riggs, B.L. (1996): Potential mechanism of estrogen-mediated decrease in bone formation: estrogen increases production of inhibitory insulin-like growth factor-binding protein-4. Proc. Assoc. Am. Physicians., 108, 155-164
  62. Key, L.L. Jr., Ries, W.L., Taylor, R.G., Hays, B.D. and Pitzer, B.L. (1990): Oxygen derived free radicals in osteoclasts: the specificity and location of the nitroblue tetrazolium reaction. Bone., 11, 115-119 https://doi.org/10.1016/8756-3282(90)90058-7
  63. Kerby, J.A., Hattersley, G., Collins, D.A. and Chambers, T.J. (1992): Derivation of osteoclasts from hematopoietic colony- forming cells in culture. J. Bone. Miner. Res., 7, 353-362 https://doi.org/10.1002/jbmr.5650070316
  64. Kitching, R., Qi, S., Li, V., Raouf, A., Vary, C.P. and Seth, A. (2002): Coordinate gene expression patterns during osteoblast maturation and retinoicacid treatment of MC3T3-E1 cells. J. Bone. Miner. Metab., 20, 269-280 https://doi.org/10.1007/s007740200039
  65. Kindle, L., Rothe, L., Kriss, M., Osdoby, P. and Collin-Osdoby, P. (2006): Human microvascular endothelial cell activation by IL-1 and TNF-alpha stimulates the adhesion and transendothelial migration of circulating human $CD14^+$ monocytesthat develop with RANKL into functional osteoclasts. J. Bone. Miner. Res., 21, 193-206 https://doi.org/10.1359/JBMR.051027
  66. Kitazawa, R., Kimble, R.B., Vannice, J.L., Kung, V.T. and Pacifici, R. (1994): Interleukin-1 receptor antagonist and tumor necrosis factor binding protein decrease osteoclast formation and bone resorption in ovariectomized mice. J. Clin. Invest., 94, 2397-2406 https://doi.org/10.1172/JCI117606
  67. Kitazawa, S. and Kitazawa, R. (2005): Regulatory mechanism of bone morphogenetic protein gene expression. Nippon Rinsho., 63, 409-413
  68. Kimble, R.B., Srivastava, S., Ross, F.P., Matayoshi, A. and Pacifici, R. (1996): Estrogen deficiency increases the ability of stromal cells to support murine osteoclastogenesis via an interleukin-1and tumor necrosis factor-mediated stimulation of macrophage colony-stimulating factor production. J. Biol. Chem., 271, 28890-28897 https://doi.org/10.1074/jbc.271.46.28890
  69. Kneissel, M., Boyde, A. and Gasser, J.A. (2001): Bone tissue and its mineralization in aged estrogen-depleted rats after long-term intermittent treatment with parathyroid hormone (PTH) analog SDZ PTS893 or human PTH(1-34). Bone., 28, 237-250 https://doi.org/10.1016/S8756-3282(00)00409-9
  70. Kobayashi, S., Inoue, S., Hosoi, T., Ouchi, Y., Shiraki, M. and Orimo, H. (1996): Association of bone mineral density with polymorphism of the estrogen receptorgene. J. Bone. Miner. Res., 11, 306-311 https://doi.org/10.1002/jbmr.5650110304
  71. Komm, B.S., Terpening, C.M., Benz, D.J., Graeme, K.A., Gallegos, A., Korc, M., Greene, G.L., O'Malley, B.W. and Haussler, M.R. (1988): Estrogen binding, receptor mRNA, and biologic response in osteoblast-like osteosarcoma cells. Science, 241, 81-84 https://doi.org/10.1126/science.3164526
  72. Korach, K.S., Levy, L.A. and Sarver, P.J. (1987): Estrogen receptor stereochemistry: receptor binding and hormonal responses. J. Steroid. Biochem., 27, 281-290 https://doi.org/10.1016/0022-4731(87)90319-0
  73. Kurabayashi, T., Matsushita, H., Tomita, M., Kato, N., Kikuchi, M., Nagata, H., Honda, A., Yahata, T. and Tanaka, K. (2004): Association of vitamin D and estrogen receptor gene polymorphism with theeffects of longterm hormone replacement therapy on bone mineral density. J. Bone. Miner. Metab., 22, 241-247 https://doi.org/10.1007/s00774-003-0474-y
  74. Kurihara, N. (1990): The origin of osteoclasts. Bull Kanagawa Dent Coll., 18, 161-164
  75. Lerner, U.H. (2006): Bone Remodeling in Post-menopausal Osteoporosis. J. Dent. Res., 85, 584-595 https://doi.org/10.1177/154405910608500703
  76. Libermann, T.A. and Baltimore, D. (1990): Activation of interleukin- 6 gene expression through the NF-kappa B transcriptionfactor. Mol. Cell. Biol., 10, 2327-2334 https://doi.org/10.1128/MCB.10.5.2327
  77. Liehr, J.G. and Roy, D. (1990): Free radical generation by redox cycling of estrogens. Free Radic. Biol. Med., 8, 415-423 https://doi.org/10.1016/0891-5849(90)90108-U
  78. Livshits, G. (2006): Quantitative genetics of circulating molecules associated with bone metabolism:a review. J. Musculoskelet Neuronal Interact., 6, 47-61
  79. Lorenzo, J.A., Sousa, S.L., Fonseca, J.M., Hock, J.M. and Medlock, E.S. (1987): Colony-stimulating factors regulate the development of multinucleated osteoclasts from recently replicated cells in vitro. J. Clin. Invest., 80, 160-164 https://doi.org/10.1172/JCI113042
  80. Lowik, C.W.G.M., Nibbering, P.H., Van der Ruit, M. and Papapoulos, S.E. (1994): Inducible production of nitric oxide in osteoblast-like cells and in fetal bone explants is associated with supression of osteoclastic bone resorption. J. Clin. Invest., 93, 1465-1472 https://doi.org/10.1172/JCI117124
  81. MacIntyre, I., Zaidi, M. and Alam, A.S. (1991): Osteoclastic inhibition: An action of nitric oxide not mediated by cyclic GMP. Proc. Natl. Acad. Sci., 88, 2936-2940
  82. Malaval, L., Liu, F., Vernallis, A.B. and Aubin, J.E. (2005): GP130/OSMR is the only LIF/IL-6 family receptor complex to promote osteoblast differentiation of calvaria progenitors. J. Cell. Physiol., 204, 585-593 https://doi.org/10.1002/jcp.20312
  83. Marshall, M.J., Holt, I. and Davie, M.W. (1996): Inhibition of prostaglandin synthesis leads to a change in adherence of mouseosteoclasts from bone to periosteum. Calcif. Tissue. Int., 59, 207-213 https://doi.org/10.1007/s002239900110
  84. Masi, L. and Brandi, M.L. (2001): Physiopathological basis of bone turnover. J. Nucl. Med., 45, 2-6
  85. Massicotte, F., Fernandes, J.C., Martel-Pelletier, J., Pelletier, J.P. and Lajeunesse, D., (2006): Epub 2005 Oct 27. Modulation of insulin-like growth factor 1 levels in human osteoarthritic subchondral bone osteoblasts. Bone., 38, 333-341 https://doi.org/10.1016/j.bone.2005.09.007
  86. Matemba, S.F., Lie, A. and Ransjo, M. (2006): Regulation of osteoclastogenesis by gap junction communication. J. Cell. Biochem., 25, [Epub ahead of print]
  87. McCulloch, C.A., Strugurescu, M., Hughes, F., Melcher, A.H. and Aubin, J.E. (1991): Osteogenic progenitor cells in rat bone marrow stromal populations exhibit self-renewal in culture. Blood., 77, 1906-1911
  88. Mee, A.P., Gordon, M.T., May, C., Bennett, D., Anderson, D.C. and Sharpe, P.T. (1993): Canine distemper virus transcripts detected in the bone cells of dogs with metaphyseal osteopathy. Bone,, 14, 59-67 https://doi.org/10.1016/8756-3282(93)90257-B
  89. Minuto, F., Palermo, C., Arvigo, M. and Barreca, A.M. (2005): The IGF system and bone. J. Endocrinol. Invest., 28, 8-10 https://doi.org/10.1007/BF03345522
  90. Monaca, S., Palmer, R.M.J. and Higgs, E.A. (1991): Nitric Oxide: Physiology, pathophysiology and pharmacology. Phamacol. Rev., 43, 109-142
  91. Nagashima, M., Sakai, A., Uchida, S., Tanaka, S., Tanaka, M. and Nakamura, T. (2005): Bisphosphonate (YM529) delays the repair of cortical bone defect afterdrill-hole injury by reducing terminal differentiation of osteoblasts in themouse femur. Bone., 36, 502-511 https://doi.org/10.1016/j.bone.2004.11.013
  92. Nakamura, M., Udagawa, N., Yamamoto, Y. and Nakamura, H. (2006): BMP and osteoclastogenesis. Clin. Calcium., 16, 89-95
  93. Oktem, G., Uslu, S., Vatansever, S.H., Aktug, H., Yurtseven, M.E. and Uysal, A. (2006): Epub 2005 Dec 15. Evaluation of the relationship between inducible nitric oxide synthase (iNOS) activity and effects of melatonin in experimental osteoporosis in the rat. Surg. Radiol. Anat., 28, 157-162 https://doi.org/10.1007/s00276-005-0065-9
  94. Onuma, E., Azuma, Y., Saito, H., Tsunenari, T., Watanabe, T., Hirabayashi, M., Sato, K., Yamada-Okabe, H. and Ogata, E. (2005): Increased renal calcium reabsorption by parathyroid hormone-related protein is acausative factor in the development of humoral hypercalcemia of malignancyrefractory to osteoclastic bone resorption inhibitors. Clin. Cancer. Res., 11, 4198-4203 https://doi.org/10.1158/1078-0432.CCR-04-2531
  95. Oursler, M.J., Collin-Osdoby, P., Li, L., Schmitt, E. and Osdoby, P. (1991): Evidence for an immunological and functional relationship between superoxide dismutase and a high molecular weight osteoclast plasma membrane glycoprotein. J. Cell. Biochem., 46, 331-344 https://doi.org/10.1002/jcb.240460408
  96. Oursler, M.J., Bradley, E.W. and Elfering, S.L. (2005): Epub 2004 Sep 1.Native, not nitrated, cytochrome c and mitochondria- derived hydrogen peroxidedrive osteoclast apoptosis. J. Physiol. Cell. Physiol., 288, C156-C168
  97. Pacifici, R. (1993): Estrogen, cytokines, and pathogenesis of postmenopausal osteoporosis. J. Clin. Endocrinol. Metab., 77, 1135-1141 https://doi.org/10.1210/jc.77.5.1135
  98. Pacifici, R. (1996): Estrogen, cytokines, and pathogenesis of postmenopausal osteoporosis. J. Bone. Miner. Res., 11, 1043-1451 https://doi.org/10.1002/jbmr.5650110802
  99. Pacifici, R. (1998): Cytokines, estrogen, and postmenopausal osteoporosis the second decade. Endocrinology, 139, 2659-2661 https://doi.org/10.1210/en.139.6.2659
  100. Pacifici, R. (1995): Estrogen replacement therapy in osteoporosis: advances and controversies. Endocr. Pract., 1, 27-32 https://doi.org/10.4158/EP.1.1.27
  101. Pacifici, R., Brown, C., Puscheck, E., Friedrich, E., Slatopolsky, E., Maggio, D., McCracken, R. and Avioli, L.V. (1991): Effect of surgical menopause and estrogen replacement on cytokine release from human blood mononuclear cells. Proc. Natl. Acad. Sci., 88, 5134-5138
  102. Pacifici, R., Rifas, L., McCracken, R. and Avioli, L.V. (1990): The role of interleukin-1 in postmenopausal bone loss. Exp. Gerontol., 25, 309-316 https://doi.org/10.1016/0531-5565(90)90067-C
  103. Park, Y.G., Kang, S.K., Kim, W.J., Lee, Y.C. and Kim, C.H. (2004): Effects of TGF-beta, TNF-alpha, IL-beta and IL-6 alone or in combination, and tyrosine kinase inhibitor on cyclooxygenase expression, prostaglandin E2production and bone resorption in mouse calvarial bone cells. J. Biochem. Cell. Biol., 36, 2270-2280 https://doi.org/10.1016/j.biocel.2004.04.019
  104. Passeri, M., Pedrazzoni, M., Pioli, G., Butturini, L., Ruys, A.H. and Cortenraad, M.G., (1993): Effects of nandrolone decanoate on bone mass in established osteoporosis. Maturitas., 17, 211-219 https://doi.org/10.1016/0378-5122(93)90049-N
  105. Pfeilschifter, J., Chenu, C., Bird, A., Mundy, G.R. and Roodman, G.D. (1989): Interleukin-1 and tumor necrosis factor stimulate the formation of human osteoclast like cells in vitro. J. Bone. Miner. Res., 4, 113-118 https://doi.org/10.1002/jbmr.5650040116
  106. Poole, K.E. and Reeve, J. (2005): Parathyroid hormone - a bone anabolic and catabolic agent. Curr. Opin. Pharmacol., 5, 612-617 https://doi.org/10.1016/j.coph.2005.07.004
  107. Pottratz, S.T., Bellido, T., Mocharla, H., Crabb, D. and Manolagas, S.C. (1994): beta-Estradiol inhibits expression of human interleukin-6 promoter-reporter constructs by a receptor-dependent mechanism. J. Clin. Invest., 93, 944-950 https://doi.org/10.1172/JCI117100
  108. Raisz, L.G. (2005): Pathogenesis of osteoporosis: concepts, conflicts, and prospects. J. Clin. Invest., 115, 3318-3325 https://doi.org/10.1172/JCI27071
  109. Ralston, S.H., Ho, L.P., Helfrich, M., Grabowski, P.S., Johnston, P.W. and Benjamin, N. (1995) Nitric oxide: a cytokine induced regulator of bone resorption. J. Bone. Miner. Res., 10, 1040-1049 https://doi.org/10.1002/jbmr.5650100708
  110. Ralston, S.H., Tood, D., Helfrich, M.H., Benjamin, N. and Gabowski, P. (1994): Human osteoblast-like cells produce nitric oxide and express inducible nitric oxide synthese. Endocrinology, 135, 330-336 https://doi.org/10.1210/en.135.1.330
  111. Ray, A., Prefontaine, K.E. and Ray, P. (1994): Down-modulation of interleukin-6 gene expression by 17 beta-estradiol in the absence of high affinity DNA binding by the estrogen receptor. J. Biol. Chem., 269, 12940-12946
  112. Reddy, S.V. and Crit, Rev. (2004): Regulatory mechanisms operative in osteoclasts. Eukaryot. Gene. Expr., 14, 255-270 https://doi.org/10.1615/CritRevEukaryotGeneExpr.v14.i4.20
  113. Reddy, V.B., Gattuso, P., Abraham, K.P., Moncada, R. and Castelli, M.J. (1991): Computed tomography-guided fine needle aspiration biopsy of deep-seated lesions. A fouryear experience. Acta Cytol., 35, 753-756
  114. Reid, L.R., Lowe, C., Cornish, J., Skinner, S.J., Hilton, D.J., Willson, T.A., Gearing, D.P. and Martin, T.J. (1990): Leukemia inhibitory factor: a novel bone-active cytokine. Endocrinology. 126, 1416-1420 https://doi.org/10.1210/endo-126-3-1416
  115. Reeves, J.D. and Hinzman, G.W. (1979): A benign cause of abnormal bone scan in Hodgkin's disease: case report. Mil. Med., 144, 825-826 https://doi.org/10.1093/milmed/144.12.825
  116. Riancho, J.A., Salas, E., Zarrabeitia, M.T., Olmos, J.M., Amado, J.A., Fernandez-Luna, J.L. and Gonzalez-Macias, J. (1995): Expression and functional role of nitric oxide synthase in osteoblast-like cells. J. Bone. Miner. Res., 10, 439-446 https://doi.org/10.1002/jbmr.5650100315
  117. Riancho, J.A., Zarrabeitia, M.T., Fernandez-Luna, J.L. and Gonzalez-Macias, J. (1995): Mechanisms controlling nitric oxide synthesis in osteoblasts. Mol. Cell. Endocrinol., 107, 87-92 https://doi.org/10.1016/0303-7207(94)03428-V
  118. Ries, W.L., Key, L.L. and Rodriguiz, R.M. (1992): Nitroblue tetrazolium reduction and bone resorption by osteoclasts in vitro inhibited by a maganase-based superoxide dismutase mimic. J. Bone. Miner. Res., 7, 931-939 https://doi.org/10.1002/jbmr.5650070810
  119. Richelson, L.S., Wahner, H.W., Melton, L. and Riggs, B.L. (1984): Relative contributions of aging and estrogen deficiency to postmenopausal bone loss. N. Engl. J. Med., 311, 1273-1275 https://doi.org/10.1056/NEJM198411153112002
  120. Rickard, D.J., Subramaniam, M. and Spelsberg, T.C. (1999): Molecular and cellular mechanisms of estrogen action on the skeleton. J. Cell. Biochem., Suppl 32-33, 123-132
  121. Riggs, B.L., Wahner, H.W., Dunn, W.L., Mazess, R.B., Offord, K.P. and Melton, L.J. (1981): Differential changes in bone mineral density of the appendicular and axial skeleton with aging: relationship to spinal osteoporosis. Clin. Invest., 67, 328-335 https://doi.org/10.1172/JCI110039
  122. Robey, P.G., Young, M.F., Flanders, K.C., Roche, N.S., Kondaiah, P., Reddi, A.H., Termine, J.D., Sporn, M.B. and Roberts, A.B. (1987): Osteoblasts synthesize and respond to transforming growth factor-type beta(TGF-beta) in vitro. J. Cell. Biol., 105, 457-463 https://doi.org/10.1083/jcb.105.1.457
  123. Robling, A.G., Castillo, A.B., Turner, C.H. and Annu, R. (2006): Biomechanical and molecular regulation of bone remodeling. Biomed. Eng., 8, 455-498
  124. Rosen, C.J. (2000): Pathogenesis of osteoporosis. Baillieres Best Pract. Res. Clin. Endocrinol. Metab., 14, 181-193 https://doi.org/10.1053/beem.2000.0068
  125. Roodman, G.D. and Ann, N.Y. (2006): Regulation of osteoclast differentiation. Acad Sci., 1068, 100-109 https://doi.org/10.1196/annals.1346.013
  126. Sawicki, A. (1990): Effect of hydrochlorothiazide on calcium metabolism in postoperative hypoparathyroidism. Pol. Tyg. Lek., 45, 501-503
  127. Schreck, R. and Baeuerle, P.A. (1991): A role for oxygen radicals as second messengers. Trends Cell. Biol., 1, 39-42 https://doi.org/10.1016/0962-8924(91)90072-H
  128. Schreck, R.R. (1992): 9(2): ix-x.Comment on: Pediatr Hematol Oncol. Tumor suppressor gene (Rb and p53) mutations in osteosarcoma. Pediatr. Hematol. Oncol., 9, 125-137 https://doi.org/10.3109/08880019209018328
  129. Schmid, T.M., Popp, R.G. and Linsenmayer, T.F. (1990): Hypertrophic cartilage matrix. Type X collagen, supramolecular assembly, and calcification. Ann. N. Y. Acad Sci., 580, 64-73 https://doi.org/10.1111/j.1749-6632.1990.tb17918.x
  130. Schmidt, H.G., Wittek, F., Faschingbauer, M. and Fink, B. (1992): Treatment of chronic osteitis of the femur][Article in German. Unfallchirurg., 95, 562-565
  131. Seck. T., Diel, I., Bismar, H., Ziegler, R., Pfeilschifter, J. and Eur, J. (2001): Serum V parathyroid hormone, but not menopausal status, is associated with the expression of osteoprotegerin and RANKL mRNA in human bone samples. Endocrinol., 145, 199-205
  132. Silverton, S. (1994): Osteoclast radicals. J. Cell. Biochem., 56, 367-373 https://doi.org/10.1002/jcb.240560313
  133. Silverton. S.F., Mesaros, S., Markham, G.D. and Malinski, T. (1995): Osteoclast radical interactions: NADPH causes pulsatile release of NO and stimulates superoxide production. Endocrinology, 136, 5244-5247 https://doi.org/10.1210/en.136.11.5244
  134. Sontakke, A.N. and Tare, R.S. (2002): A duality in the roles of reactive oxygen species with respect to bone metabolism. Clin. Chim. Acta., 318, 145-148 https://doi.org/10.1016/S0009-8981(01)00766-5
  135. Sorimachi, K., Akimoto, K., Hattori, Y., Ieiri, T. and Niwa, A. (1999): Secretion of TNF-alpha, IL-8 and nitric oxide by macrophages activated with polyanions, and involvement of interferon-gamma in the regulation of cytokine secretion. Cytokine., 11, 571-578 https://doi.org/10.1006/cyto.1998.0472
  136. Srivastava, S., Weitzmann, M.N., Kimble, R.B., Rizzo, M., Zahner, M., Milbrandt, J., Ross, F.P. and Pacifici, R. (1998): Estrogen blocks M-CSF gene expression and osteoclast formation by regulating phosphorylation of Egr- 1 and its interaction with Sp-1. J. Clin. Invest., 102, 1850-1859 https://doi.org/10.1172/JCI4561
  137. Stein, B. and Yang, M.X. (1995): Repression of the interleukin- 6 promoter by estrogen receptor is mediated by NFkappa B and C/EBP beta. Mol. Cell. Biol., 15, 4971-4979 https://doi.org/10.1128/MCB.15.9.4971
  138. Steinbeck, M.J., Appel, W.H., Jr., Verhoeven, A.J. and Karnovsky, M.J. (1994): NADPH-oxidase expression and in situ production of superoxide by osteoclasts actively resorbing bone. Cell Biol., 126, 765-772 https://doi.org/10.1083/jcb.126.3.765
  139. Stilgren, L.S., Abrahamsen, B., Abdallah, B.M. and Jorgensen, N.R. (2005): The cytokine system of bone tissue][Article in Danish. Ugeskr Laeger., 167, 874-878
  140. Su, X., Liao, E.Y., Peng, J., Liu, S.P., Dai, R.C., Zhong, N.D. (2004): Effects of parathyroid hormone on osteoprotegerin expression and osteoprotegerin ligand and their related cytokines in human osteoblasts. Xue Xue Bao Yi Xue Ban., 29, 562-565
  141. Subbiah, M.T., Kessel, B., Agrawal, M., Rajan, R., Abplanalp, W. and Rymaszewski, Z. (1993): Antioxidant potential of specific estrogens on lipid peroxidation. J. Clin. Endocrinol. Metab., 77, 1095-1097 https://doi.org/10.1210/jc.77.4.1095
  142. Suda. T., Ueno, Y., Fujii, K. and Shinki, T. (2003): Vitamin D and bone. J. Cell. Biochem., 88, 259-266 https://doi.org/10.1002/jcb.10331
  143. Suda, N., Morita, I., Kuroda, T. and Murota, S. (1993): Participation of oxidative stress in the process of osteoclast differentiation. Biochim. Biophys. Acta., 1157, 318-323 https://doi.org/10.1016/0304-4165(93)90116-P
  144. Sugioka, K., Shimosegawa, Y. and Nakano. M. (1987): Estrogens as natural antioxidants of membrane phospholipid peroxidation. FEBS Lett., 210, 37-39 https://doi.org/10.1016/0014-5793(87)81293-0
  145. Suva, L.J., Ernst, M. and Rodan, G.A. (1991): Retinoic acid increases zif268 early gene expression in rat preosteoblastic cells. Mol. Cell. Biol., 11, 2503-2510 https://doi.org/10.1128/MCB.11.5.2503
  146. Takahashi, N., Yamana, H., Yoshiki, S., Roodman, G.D., Mundy, G.R., Jones, S.J., Boyde, A. and Suda, T. (1988): Osteoclast-like cell formation and its regulation by osteotropic hormones inmouse bone marrow cultures. Endocrinology, 122, 1373-1382 https://doi.org/10.1210/endo-122-4-1373
  147. Takata, S., Yamashita, Y., Masaki, K., Morimoto, K. and Nakano, M. (1993): Effects of bed rest on bone metabolism in patients with femoral neck fracture. Ann. Physiol. Anthropol., 12, 321-325 https://doi.org/10.2114/ahs1983.12.321
  148. Togari, A., Arakawa, S., Arai, M. and Matsumoto, S. (1993): Alteration of in vitro bone metabolism and tooth formation by zinc. Gen. Pharmacol., 24, 1133-1140 https://doi.org/10.1016/0306-3623(93)90360-A
  149. Torring, O., Firek, A.F. and Conover, C.A. (1991): Parathyroid hormone and parathyroid hormone-related peptide stimulate insulin-like growth factor-binding protein secretion by rat osteoblast-like cells through a adenosine 3',5'-monophosphate- dependent mechanism. Endocrinology, 128, 1006-1014 https://doi.org/10.1210/endo-128-2-1006
  150. Troen, B.R. (2003): Molecular mechanisms underlying osteoclast formation and activation. Exp. Gerontol., 38, 605-614 https://doi.org/10.1016/S0531-5565(03)00069-X
  151. Turner, R.T. and Eliel, L.P. (1978): Nuclear estrogen receptor in the reproductive tract of laying Japanese quail. Gen. Comp. Endocrinol., 34, 141-148 https://doi.org/10.1016/0016-6480(78)90204-6
  152. Udagawa, N., Takahashi, N., Akatsu, T., Tanaka, H., Sasaki, T., Nishihara, T., Koga, T., Martin, T.J. and Suda, T. (1990): Origin of osteoclasts: mature monocytes and macrophages are capable of differentiating into osteoclasts under a suitable microenvironment prepared bybone marrow- derived stromal cells. Proc. Natl. Acad. Sci., 87, 7260-7264
  153. van't Hof, R.J. and Ralston, S.H. (2001): Nitric oxide and bone. Immunology, 103, 255-261 https://doi.org/10.1046/j.1365-2567.2001.01261.x
  154. Veille, J.C., Li, P., Eisenach, J.C., Massmann, A.G., Figueroa, J.P. and Am, J. (1996): Effects of estrogen on nitric oxide biosynthesis and vasorelaxant activity in sheep uterine and renal arteries in vitro. Obstet Gynecol., 174, 1043-1049 https://doi.org/10.1016/S0002-9378(96)70348-4
  155. Venema, R.C., Nishida, K., Alexander, R.W., Harrison, D.G. and Murphy, T.J. (1994): Organization of the bovine gene encoding the endothelial nitric oxide synthase. Biochim. Biophys. Acta, 1218, 413-420 https://doi.org/10.1016/0167-4781(94)90195-3
  156. Vidal, K., van den, Broek, P., Lorget, F. and Donnet-Hughes, A. (2004) Osteoprotegerin in human milk: a potential role in the regulation of bone metabolism and immune development. Pediatr. Res., 55, 1001-1008 https://doi.org/10.1203/01.pdr.0000127014.22068.15
  157. Weusten, J.J., Blankenstein, M.A., Gmelig-Meyling, F.H., Schuurman, H.J., Kater, L. and Thijssen, J.H. (1986): Presence of oestrogen receptors in human blood mononuclear cells and thymocytes. Acta Endocrinol. (Copenh), 112, 409-414
  158. Weiner, C.P., Lizasoain, I., Baylis, S.A., Knowles, R.G., Charles, I.G. and Moncada, S. (1994): Induction of calcium- dependent nitric oxide synthases by sex hormones. Proc. Natl. Acad. Sci., 91, 5212-5216
  159. Yamazaki, H., Kunisada, T., Yamane, T. and Hayashi, S.I. (2001): Presence of osteoclast precursors in colonies cloned in the presence of hematopoietic colony-stimulating factors. Exp. Hematol., 29, 68-76 https://doi.org/10.1016/S0301-472X(00)00626-3
  160. Yates, A.J., Gutierrez, G.E., Smolens, P., Travis, P.S., Katz, M.S., Aufdemorte, T.B., Boyce, B.F., Hymer, T.K., Poser, J.W. and Mundy, G.R. (1988): Effects of a synthetic peptide of a parathyroid hormone-related protein on calcium homeostasis, renal tubular calcium reabsorption, and bone metabolism in vivo and in vitro in rodents. J. Clin. Invest., 81, 932-938 https://doi.org/10.1172/JCI113406
  161. Yalin, S., Bagis, S., Polat, G., Dogruer, N., Cenk, Aksit, S., Hatungil, R. and Erdogan, C. (2005): Is there a role of free oxygen radicals in primary male osteoporosis? Clin. Exp. Rheumatol., 23, 689-692
  162. Yang, S., Madyastha, P., Bingel, S., Ries, W. and Key, L.L. (2001): A new superoxide -generating oxidase in murine osteoclasts. J. Biol. Chem., 276, 5452-5458 https://doi.org/10.1074/jbc.M001004200
  163. Zaidi, M., Alam, A.S., Bax, B.E., Shankar, V.S., Bax, C.M., Gill, J.S., Pazianas, M., Huang, C.L., Sahinoglu, T. and Moonga, B.S. (1993): Role of the endothelial cell in osteoclast control: new perspectives. Bone., 14, 97-102 https://doi.org/10.1016/8756-3282(93)90234-2
  164. Zarrabeitia, M.T., Riancho, J.A., Amado, J.A. and Gonzalez- Macias, J. (1991): Lack of effect of human parathyroid hormone and calcitonin on cytokine and prostaglandin secretion by blood mononuclear cells. Methods Find. Exp. Clin. Pharmacol., 13, 541-544
  165. Zhou, H., Hammonds, R.G., Jr, Findlay, D.M., Fuller, P.J., Martin, T.J. and Ng, K.J. (1991): Retinoic acid modulation of mRNA levels in malignant, nontransformed, and immortalized osteoblasts. Bone. Miner. Res., 6, 767-777 https://doi.org/10.1002/jbmr.5650060715