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Original Article

Tumor Necrosis Factor Stimulates Osteoclast Differentiation by a Mechanism Independent of the Odf/Rankl–Rank Interaction

^a Department of Biochemistry, School of Dentistry, Showa University, Tokyo 142-8555, Japan
^b The Institute of Rheumatology, Tokyo Women's Medical University, Tokyo 162-0054, Japan
^c Research Institute of Life Science, Snow Brand Milk Products Co., Ltd., Tochigi 329-0512, Japan
^d St. Vincent's Institute of Medical Research, Fitzroy, Victoria 3065, Australia
Department of Biochemistry, School of Dentistry, Showa University, 1-5-8 Hatanodai, Shinagawa-ku, Tokyo 142-8555, Japan.81-3-3784-555581-3-3784-8162

suda{at}showa-u.ac.jp

Osteoclast differentiation factor (ODF, also called RANKL/TRANCE/OPGL) stimulates the differentiation of osteoclast progenitors of the monocyte/macrophage lineage into osteoclasts in the presence of macrophage colony-stimulating factor (M-CSF, also called CSF-1). When mouse bone marrow cells were cultured with M-CSF, M-CSF–dependent bone marrow macrophages (M-BMM) appeared within 3 d. Tartrate-resistant acid phosphatase–positive osteoclasts were also formed when M-BMM were further cultured for 3 d with mouse tumor necrosis factor (TNF-) in the presence of M-CSF. Osteoclast formation induced by TNF- was inhibited by the addition of respective antibodies against TNF receptor 1 (TNFR1) or TNFR2, but not by osteoclastogenesis inhibitory factor (OCIF, also called OPG, a decoy receptor of ODF/RANKL), nor the Fab fragment of anti–RANK (ODF/RANKL receptor) antibody. Experiments using M-BMM prepared from TNFR1- or TNFR2-deficient mice showed that both TNFR1- and TNFR2-induced signals were important for osteoclast formation induced by TNF-. Osteoclasts induced by TNF- formed resorption pits on dentine slices only in the presence of IL-1. These results demonstrate that TNF- stimulates osteoclast differentiation in the presence of M-CSF through a mechanism independent of the ODF/RANKL–RANK system. TNF- together with IL-1 may play an important role in bone resorption of inflammatory bone diseases.

Key Words: bone resorption • tumor necrosis factor receptor • nuclear factor-B • macrophage colony-stimulating factor • interleukin-1

Abbreviations used in this paper: 1,25(OH)₂D₃, 1,25-dihydroxyvitamin D₃; JNK, c-Jun NH₂-terminal kinase; M-BMM, M-CSF–dependent bone marrow macrophages; M-CSF, macrophage CSF; NF-B, nuclear factor B; OCIF, osteoclastogenesis inhibitory factor; ODF, osteoclast differentiation factor; OPGL, osteoprotegerin ligand; RANKL, receptor activator of NF-B ligand; RT-PCR, reverse-transcriptase PCR; TRAP, tartrate-resistant acid phosphatase.

© 2000 The Rockefeller University Press

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• Crotti, T N, Smith, M D, Weedon, H, Ahern, M J, Findlay, D M, Kraan, M, Tak, P P, Haynes, D R (2002). Receptor activator NF-{kappa}B ligand (RANKL) expression in synovial tissue from patients with rheumatoid arthritis, spondyloarthropathy, osteoarthritis, and from normal patients: semiquantitative and quantitative analysis. Ann Rheum Dis 61: 1047-1054 [Abstract] [Full Text]  
• Armstrong, A. P., Tometsko, M. E., Glaccum, M., Sutherland, C. L., Cosman, D., Dougall, W. C. (2002). A RANK/TRAF6-dependent Signal Transduction Pathway Is Essential for Osteoclast Cytoskeletal Organization and Resorptive Function. J. Biol. Chem. 277: 44347-44356 [Abstract] [Full Text]  
• Kitaura, H., Nagata, N., Fujimura, Y., Hotokezaka, H., Yoshida, N., Nakayama, K. (2002). Effect of IL-12 on TNF-{alpha}-Mediated Osteoclast Formation in Bone Marrow Cells: Apoptosis Mediated by Fas/Fas Ligand Interaction. J. Immunol. 169: 4732-4738 [Abstract] [Full Text]  
• Hirayama, T., Danks, L., Sabokbar, A., Athanasou, N. A. (2002). Osteoclast formation and activity in the pathogenesis of osteoporosis in rheumatoid arthritis. Rheumatology (Oxford) 41: 1232-1239 [Abstract] [Full Text]  
• Jones, D H., Kong, Y-Y, Penninger, J M (2002). Role of RANKL and RANK in bone loss and arthritis. Ann Rheum Dis 61: ii32-39 [Abstract] [Full Text]  
• Akune, T., Ogata, N., Hoshi, K., Kubota, N., Terauchi, Y., Tobe, K., Takagi, H., Azuma, Y., Kadowaki, T., Nakamura, K., Kawaguchi, H. (2002). Insulin receptor substrate-2 maintains predominance of anabolic function over catabolic function of osteoblasts. JCB 159: 147-156 [Abstract] [Full Text]  
• Lane, N E, Rehman, Q (2002). Osteoporosis in the rheumatic disease patient. Lupus 11: 675-679 [Abstract]  
• Danks, L, Sabokbar, A, Gundle, R, Athanasou, N A (2002). Synovial macrophage-osteoclast differentiation in inflammatory arthritis. Ann Rheum Dis 61: 916-921 [Abstract] [Full Text]  
• Albagha, O. M.E., Tasker, P. N., McGuigan, F. E.A., Reid, D. M., Ralston, S. H (2002). Linkage disequilibrium between polymorphisms in the human TNFRSF1B gene and their association with bone mass in perimenopausal women. Hum Mol Genet 11: 2289-2295 [Abstract] [Full Text]  
• Ragab, A. A., Nalepka, J. L., Bi, Y., Greenfield, E. M. (2002). Cytokines synergistically induce osteoclast differentiation: support by immortalized or normal calvarial cells. Am. J. Physiol. Cell Physiol. 283: C679-C687 [Abstract] [Full Text]  
• Li, X., Udagawa, N., Itoh, K., Suda, K., Murase, Y., Nishihara, T., Suda, T., Takahashi, N. (2002). p38 MAPK-Mediated Signals Are Required for Inducing Osteoclast Differentiation But Not for Osteoclast Function. Endocrinology 143: 3105-3113 [Abstract] [Full Text]  
• Takami, M., Kim, N., Rho, J., Choi, Y. (2002). Stimulation by Toll-Like Receptors Inhibits Osteoclast Differentiation. J. Immunol. 169: 1516-1523 [Abstract] [Full Text]  
• Hayashi, T., Kaneda, T., Toyama, Y., Kumegawa, M., Hakeda, Y. (2002). Regulation of Receptor Activator of NF-kappa B Ligand-induced Osteoclastogenesis by Endogenous Interferon-beta (INF-beta ) and Suppressors of Cytokine Signaling (SOCS). THE POSSIBLE COUNTERACTING ROLE OF SOCSs IN IFN-beta -INHIBITED OSTEOCLAST FORMATION. J. Biol. Chem. 277: 27880-27886 [Abstract] [Full Text]  
• Ji, H., Pettit, A., Ohmura, K., Ortiz-Lopez, A., Duchatelle, V., Degott, C., Gravallese, E., Mathis, D., Benoist, C. (2002). Critical Roles for Interleukin 1 and Tumor Necrosis Factor {alpha} in Antibody-induced Arthritis. JEM 196: 77-85 [Abstract] [Full Text]  
• Jiang, Y., Mehta, C. K., Hsu, T.-Y., Alsulaimani, F. F. H. (2002). Bacteria Induce Osteoclastogenesis via an Osteoblast-Independent Pathway. Infect. Immun. 70: 3143-3148 [Abstract] [Full Text]  
• Matsumoto, Y., Tanaka, K., Hirata, G., Hanada, M., Matsuda, S., Shuto, T., Iwamoto, Y. (2002). Possible Involvement of the Vascular Endothelial Growth Factor-Flt-1-Focal Adhesion Kinase Pathway in Chemotaxis and the Cell Proliferation of Osteoclast Precursor Cells in Arthritic Joints. J. Immunol. 168: 5824-5831 [Abstract] [Full Text]  
• Nakamura, I., Kadono, Y., Takayanagi, H., Jimi, E., Miyazaki, T., Oda, H., Nakamura, K., Tanaka, S., Rodan, G. A., Duong, L. T. (2002). IL-1 Regulates Cytoskeletal Organization in Osteoclasts Via TNF Receptor-Associated Factor 6/c-Src Complex. J. Immunol. 168: 5103-5109 [Abstract] [Full Text]  
• Neale, S.D., Schulze, E., Smith, R., Athanasou, N.A. (2002). The influence of serum cytokines and growth factors on osteoclast formation in Paget's disease. QJM 95: 233-240 [Abstract] [Full Text]  
• Fuller, K., Murphy, C., Kirstein, B., Fox, S. W., Chambers, T. J. (2002). TNF{alpha} Potently Activates Osteoclasts, through a Direct Action Independent of and Strongly Synergistic with RANKL. Endocrinology 143: 1108-1118 [Abstract] [Full Text]  
• Wei, S., Wang, M. W.-H., Teitelbaum, S. L., Ross, F. P. (2002). Interleukin-4 Reversibly Inhibits Osteoclastogenesis via Inhibition of NF-kappa B and Mitogen-activated Protein Kinase Signaling. J. Biol. Chem. 277: 6622-6630 [Abstract] [Full Text]  

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