Commitment and differentiation of osteoclast precursor cells by the sequential expression of c-Fms and receptor activator of nuclear factor κB (RANK) receptors

Journal of Experimental Medicine

Volumn 190, Issue 12, 1999, Pages 1741-1754

  Arai, Fumio ^a,b   Miyamoto, Takeshi ^a   Ohneda, Osamu ^a   Inada, Tornohisa ^a   Sudo, Tetsuo ^c   Brasel, Kenneth ^d   Miyata, Takashi ^b   Anderson, Dirk M ^d   Suda, Toshio ^a  

^a KUMAMOTO UNIV SCHOOL OF MEDICINE   (Japan)

^b MEIKAI UNIVERSITY SCHOOL OF DENTISTRY   (Japan)

^c TORAY INDUSTRIES INC   (Japan)

^d AMGEN INC   (United States)

Author keywords

Commitment; M CSF; Macrophage; Osteoclastogenesis; RANK ligand

Indexed keywords

COLONY STIMULATING FACTOR 1; OSTEOCLAST DIFFERENTIATION FACTOR;

ANIMAL CELL; ARTICLE; BONE MARROW; CELL DIFFERENTIATION; CELL PROLIFERATION; FEMALE; HEMATOPOIETIC STEM CELL; MACROPHAGE; MOUSE; NONHUMAN; OSTEOCLAST; PRIORITY JOURNAL; STEM CELL;

ANIMALS; CARRIER PROTEINS; CELL DIFFERENTIATION; CELL LINEAGE; HEMATOPOIETIC STEM CELLS; LIGANDS; MACROPHAGE COLONY-STIMULATING FACTOR; MACROPHAGES; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; OSTEOCLASTS; RANK LIGAND; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR-KAPPA B; RECEPTOR, MACROPHAGE COLONY-STIMULATING FACTOR; RECEPTORS, TUMOR NECROSIS FACTOR;

EID: 0033398996     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.190.12.1741     Document Type: Article

References (51)

1. Ash, P., J.F. Loutit, and K.M. Townsend. 1980. Osteoclasts derived from haematopoietic stem cells. Nature. 283:669-670.
2. Scheven, B.A., J.W. Visser, and P.J. Nijweide. 1986. In vitro osteoclast generation from different bone marrow fractions, including a highly enriched haematopoietic stem cell population. Nature. 321:79-81.
3. Kurihara, N., T. Suda, Y. Miura, H. Nakauchi, H. Kodama, K. Hiura, Y. Hakeda, and M. Kumegawa. 1989. Generation of osteoclasts from isolated heinatopoietic progenitor cells. Blood. 74:1295-1302.
4. Roodman, G.D. 1996. Advances in bone biology: the osteoclast. Endocr. Rev. 17:308-332.
5. Manolagas, S.C., and R.L. Jilka. 1995. Bone marrow, cytokines, and bone remodeling. Emerging insights into the pathophysiology of osteoporosis. N. Engl. J. Med. 332:305-311.
6. Udagawa, N., N. Takahashi, T. Akatsu, H. Tanaka, T. Sasaki, T. Nishihara, T. Koga, T.J. Martin, and T. Suda. 1990. Origin of osteoclasts: mature monocytes and macrophages are capable of differentiating into osteoclasts under a suitable microenvironment prepared by bone marrow-derived stromal cells. Proc. Natl. Acad. Sci. USA. 87:7260-7264.
7. Kurihara, N., C. Chenu, M. Miller, C. Civin, and G.D. Roodman. 1990. Identification of committed mononuclear precursors for osteoclast-like cells formed in long term human marrow cultures. Endocrinology. 126:2733-2741.
8. Takahashi, N., N. Udagawa, S. Tanaka, H. Murakami, I. Owan, T. Taniura, and T. Suda. 1994. Postmitotic osteoclast precursors are mononuclear cells which express macrophage-associated phenotypes. Dev. Biol. 163:212-221.
9. Wang, Z.Q., C. Ovitt, A.E. Grigoriadis, U. Mohle-Steinlein, U. Ruther, and E.F. Wagner. 1992. Bone and haematopoietic defects in mice lacking c-fos. Nature. 360:741-745.
10. Grigoriadis, A.E., Z.Q. Wang, M.G. Cecchini, W. Hofstetter, R. Felix, H.A. Fleisch, and E.F. Wagner. 1994. c-Fos: a key regulator of osteoclast-macrophage lineage determination and bone remodeling. Science. 266:443-448.
11. Takahashi, N., T. Akatsu, N. Udagawa, T. Sasaki, A. Yamaguchi, J.M. Moseley, T.J. Martin, and T. Suda. 1988. Osteoblastic cells are involved in osteodast formation. Endocrinology. 123:2600-2602.
12. Udagawa, N., N. Takahashi, T. Akatsu, T. Sasaki, A. Yamaguchi, H. Kodama, T.J. Martin, and T. Suda. 1989. The bone marrow-derived stromal cell lines MC3T3-G2/PA6 and ST2 support osteoclast-like cell differentiation in cocultures with mouse spleen cells. Endocrinology. 125:1805-1813.
13. Quinn, J.M., J. Elliott, M.T. Gillespie, and T.J. Martin. 1998. A combination of osteoclast differentiation factor and macrophage-colony stimulating factor is sufficient for both human and mouse osteoclast formation in vitro. Endocrinology. 139:4424-4427.
14. Lagasse, E., and I.L. Weissman. 1997. Enforced expression of Bcl-2 in monocytes rescues macrophages and partially reverses osteopetrosis in op/op mice. Cell. 89:1021-1031.
15. Suda, T., S. Tanaka, and N. Takahashi. 1993. Macrophage colony-stimulating factor (M-CSF) is essential for differentiation rather than proliferation of osteoclast progenitors. Osteoporos. Int. 3:111-113.
16. Tanaka, S., N. Takahashi, N. Udagawa, T. Tamura, T. Akatsu, E.R. Stanley, T. Kurokawa, and T. Suda. 1993. Macrophage colony-stimulating factor is indispensable for both proliferation and differentiation of osteoclast progenitors. J. Clin. Invest. 91:257-263.
17. Yoshida, H., S. Hayashi, T. Kunisada, M. Ogawa, S. Nishikawa, H. Okamura, T. Sudo. L.D. Shultz, and S. Nishikawa. 1990. The murine mutation osteopetrosis is in the coding region of the macrophage colony stimulating factor gene. Nature. 345:442-444.
18. Kodama, H., M. Nose, S. Niida, and A. Yamasaki. 1991. Essential role of macrophage colony-stimulating factor in the osteoclast differentiation supported by stromal cells. J. Exp. Med. 173:1291-1294.
19. Kodama, H., A. Yamasaki, M. Nose, S. Niida, Y. Ohgame, M. Abe, M. Kumegawa, and T. Suda. 1991. Congenital osteoclast deficiency in osteopetrotic (op/op) mice is cured by injections of macrophage colony-stimulating factor. J. Exp. Med. 173:269-272.
20. Hofstetter, W., A. Wetterwald, M.C. Cecchini, R. Felix, H. Fleisch, and C. Mueller. 1992. Detection of transcripts for the receptor for macrophage colony-stimulating factor, c-fms, in murine osteoclasts. Proc. Natl. Acad. Sci. USA. 89:9637-9641.
21. Lacey, D.L., E. Timms, H.L. Tan, M.J. Kelley, C.R. Dunstan, T. Burgess, R. Elliott, A. Colombero, G. Elliott, S. Scully, et al. 1998. Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell. 93: 165-176.
22. Yasuda, H., N. Shima, N. Nakagawa, K. Yamaguchi, M. Kinosaki, S. Mochizuki, A. Tomoyasu, K. Yano, M. Goto, A. Murakami, et al. 1998. Osteoclast differentiation factor is a ligand for osteoprotegerin/osteoclastogenesis-inhibitory factor and is identical to TRANCE/RANKL. Proc. Natl. Acad. Sci. USA. 95:3597-3602.
23. Wong, B.R., J. Rho, J. Arron, E. Robinson, J. Orlinick, M. Chao, S. Kalachikov, E. Cayani, F.S. Bartlett, 3rd, W.N. Frankel, et al. 1997. TRANCE is a novel ligand of the tumor necrosis factor receptor family that activates c-Jun N-terminal kinase in T cells. J. Biol. Chem. 272:25190-25194.
24. Anderson, D.M., E. Maraskovsky, W.L. Billingsley, W.C. Dougall, M.E. Tometsko, E.R. Roux, M.C. Teepe, R.F. DuBose, D. Cosman, and L. Galibert. 1997. A homologue of the TNF receptor and its ligand enhance T-cell growth and dendritic-cell function. Nature. 390:175-179.
25. Yeh, W.C., A. Shahinian, D. Speiser, J. Kraunus, F. Billia, A. Wakeham, J.L. de la Pompa, D. Ferrick. B. Hum, N. Iscove, et al. 1997. Early lethality, functional NF-κB activation, and increased sensitivity to TNF-induced cell death in TRAF2-deficient mice. Immunity. 7:715-725.
26. Galibert, E., M.E. Tometsko, D.M. Anderson, D. Cosman, and W.C. Dougall. 1998. The involvement of multiple tumor necrosis factor receptor (TNFR)-associated factors in the signaling mechanisms of receptor activator of NF-κB, a member of the TNFR superfamily. J. Biol. Chem. 273:34120-34127.
27. Wong, B.R., R. Josien, S.Y. Lee, M. Vologodskaia, R.M. Steinman, and Y. Choi. 1998. The TRAF family of signal transducers mediates NF-κB activation by the TRANCE receptor. J. Biol. Chem. 273:28355-28359.
28. Hsu, H., D.L. Lacey, C.R. Dunstan, I. Solovyev, A. Colombero, E. Timms, H.L. Tan, G. Elliott, M.J. Kelley, I. Sarosi, et al. 1999. Tumor necrosis factor receptor family member RANK mediates osteoclast differentiation and activation induced by osteoprotegerin ligand. Proc. Natl. Acad. Sci. USA. 96:3540-3545.
29. Lomaga, M.A., W.Y. Wen-Chen, I. Sarosi, D.S. Duncan, C. Furlonger, A. Ho, S. Morony, C. Capparelli, G. Van, S. Kaufman, et al. 1999. TRAF6 deficiency results in osteopetrosis and defective interleukin-1, CD40, and LPS signaling. Genes Dev. 13:1015-1024.
30. Iotsova, V., J. Caamano, J. Loy, Y. Yang, A. Lewin, and R. Bravo. 1997. Osteopetrosis in mice lacking NF-κB1 and NF-κB2. Nat. Med. 3:1285-1289.
31. Franzoso, G., L. Carlson, L. Xing, L. Poljak, E.W. Shores, K.D. Brown, A. Leonardi, T. Tran, B.F. Boyce, and U. Siebenlist. 1997. Requirement for NF-κB in osteoclast and B-cell development. Genes Dev. 11:3482-3496.
32. Kong, Y.Y., H. Yoshida, I. Sarosi, H.L. Tan, E. Timms, C. Capparelli, S. Morony, A.J. Oliveira-dos-Santos, G. Van, A. Itie, et al. 1999. OPGL is a key regulator of osteoclastogenesis, lymphocyte development and lymph-node organogenesis. Nature. 397:315-323.
33. Takakura, N., X.L. Huang, T. Naruse, I. Hamaguchi, D.J. Dumont, G.D. Yancopoulos, and T. Suda. 1998. Critical role of the TIE2 endothelial cell receptor in the development of definitive hematopoiesis. Immunity. 9:677-686.
34. Spangrude, G.J., S. Heimfeld, and I.L. Weissman. 1988. Purification and characterization of mouse hematopoietic stem cells. Science. 241:58-62.
35. Okada, S., H. Nakauchi, K. Nagayoshi, S. Nishikawa, Y. Miura, and T. Suda. 1992. In vivo and in vitro stem cell function of c-kit-and Sca-1-positive murine hematopoietic cells. Blood. 80:3044-3050.
36. Morrison, S.J., H.D. Hemmati, A.M. Wandycz, and I.L. Weissman. 1995. The purification and characterization of fetal liver hematopoietic stem cells. Proc. Natl. Acad. Sci. USA. 92:10302-10306.
37. Takakura, N., H. Kodama, S. Nishikawa, and S.I. Nishikawa. 1996. Preferential proliferation of murine colony-forming units in culture in a chemically defined condition with a macrophage colony-stimulating factor-negative stroinal cell clone. J. Exp. Med. 184:2301-2309.
38. Sariban, E., T. Mitchell, and D. Kufe. 1985. Expression of the c-fms proto-oncogene during human monocytic differentiation. Nature. 316:64-66.
39. Reddy, M.A., B.S. Yang, X. Yue, C.J. Barnett, I.L. Ross, M.J. Sweet, D.A. Hume, and M.C. Ostrowski. 1994. Opposing actions of c-ets/PU.1 and c-myb protooncogene products in regulating the macrophage-specific promoters of the human and mouse colony-stimulating factor-1 receptor (c-fms) genes. J. Exp. Med. 180:2309-2319.
40. Zhang, D.E., C.J. Hetherington, H.M. Chen, and D.G. Tenen. 1994. The macrophage transcription factor PU.1 directs tissue-specific expression of the macrophage colony-stimulating factor receptor. Mol. Cell. Biol. 14:373-381.
41. Zhang, D.E., K. Fujioka, C.J. Hetherington, L.H. Shapiro, H.M. Chen, A.T. Look, and D.G. Tenen. 1994. Identification of a region which directs the monocytic activity of the colony-stimulating factor 1 (macrophage colony-stimulating factor) receptor promoter and binds PEBP2/CBF (AML1). Mol. Cell. Biol. 14:8085-8095.
42. Yamane, T., T. Kunisada, H. Yamazaki, T. Era, T. Nakano, and S.I. Hayashi. 1997. Development of osteoclasts from embryonic stem cells through a pathway that is c-fms but not c-kit dependent. Blood. 911:3516-3523.
43. Hayashi, S., A. Miyamoto, T. Yamane, H. Kataoka, M. Ogawa, S. Sugawara, S. Nishikawa, S. Nishikawa, T. Sudo, H. Yamazaki, et al. 1997. Osteoclast precursors in bone marrow and peritoneal cavity. J. Cell. Physiol. 170:241-247.
44. Lee, M.Y., J.L. Lottsfeldt, and K.L. Fevold. 1992. Identification and characterization of osteoclast progenitors by clonal analysis of hematopoietic cells. Blood. 80:1710-1716.
45. Muguruma, Y., and M.Y. Lee. 1998. Isolation and characterization of murine clonogenic osteoclast progenitors by cell surface phenotype analysis. Blood. 91:1272-1279.
46. Tsukii, K., N. Shima, S. Mochizuki, K. Yamaguchi, M. Kinosaki, K. Yano, O. Shibata, N. Udagawa, H. Yasuda, T. Suda, et al. 1998. Osteoclast differentiation factor mediates an essential signal for bone resorption induced by 1 alpha, 25-dihydroxyvitamin D3, prostaglandin E2, or parathyroid hormone in the microenvironment of bone. Biochem. Biophys. Res. Commun. 246:337-341.
47. Simonet, W.S., D.L. Lacey, C.R. Dunstan, M. Kelley, M.S. Chang, R. Lüthy, H.Q. Nguyen, S. Wooden, L. Bennett, T. Boone, et al. 1997. Osteoprotegerin: a novel secreted protein involved in the regulation of bone density. Cell. 89:309-319.
48. Yasuda, H., N. Shima, N. Nakagawa, S.I. Mochizuki, K. Yano, N. Fujise, Y. Sato, M. Goto, K. Yamaguchi, M. Kuriyama, et al. 1998. Identity of osteoclastogenesis inhibitory factor (OCIF) and osteoprotegerin (OPG): a mechanism by which OPG/OCIF inhibits osteoclastogenesis in vitro. Endocrinology. 139:1329-1337.
49. Fuller, K., B. Wong, S. Fox, Y. Choi, and T.J. Chambers. 1998. TRANCE is necessary and sufficient for osteoblast-mediated activation of bone resorption in osteoclasts. J. Exp. Med. 188:997-1001.
50. Begg, S.K., and I. Bertoncello. 1993. The hematopoietic deficiencies in osteopetrotic (op/op) mice are not permanent, but progressively correct with age. Exp. Hematol. 21:493-495.
51. Begg, S.K., J.M. Radley, J.W. Pollard, O.T. Chisholm, E.R. Stanley, and I. Bertoncello. 1993. Delayed hematopoietic development in osteopetrotic (op/op) mice. J. Exp. Med. 177: 237-242.