Bone
Volume 33, Issue 4 , Pages 721-732 , October 2003

Inhibition of RANKL-induced osteoclast formation in mouse bone marrow cells by IL-12: involvement of IFN-γ possibly induced from non-T cell population

  • Noriko Nagata

      Affiliations

    • Division of Orthodontic and Biomedical Engineering, Department of Developmental and Reconstructive Medicine, Nagasaki University Graduate School of Biomedical Sciences, 1-7-1 Sakamoto, Nagasaki 852-8588, Japan
    • Division of Microbiology and Oral Infection, Department of Developmental and Reconstructive Medicine, Nagasaki University Graduate School of Biomedical Sciences, 1-7-1 Sakamoto, Nagasaki 852-8588, Japan
    • ,
  • Hideki Kitaura

      Affiliations

    • Division of Orthodontic and Biomedical Engineering, Department of Developmental and Reconstructive Medicine, Nagasaki University Graduate School of Biomedical Sciences, 1-7-1 Sakamoto, Nagasaki 852-8588, Japan
    • ,
  • Noriaki Yoshida

      Affiliations

    • Division of Orthodontic and Biomedical Engineering, Department of Developmental and Reconstructive Medicine, Nagasaki University Graduate School of Biomedical Sciences, 1-7-1 Sakamoto, Nagasaki 852-8588, Japan
    • ,
  • Koji Nakayama

      Affiliations

    • Division of Microbiology and Oral Infection, Department of Developmental and Reconstructive Medicine, Nagasaki University Graduate School of Biomedical Sciences, 1-7-1 Sakamoto, Nagasaki 852-8588, Japan
    • Corresponding Author InformationCorresponding author. Fax: +81-95-849-7650.

Received 3 December 2002 ,Revised 8 March 2003 ,Accepted 5 June 2003.

References 

  1. Burger EH, Van der Meer JW, Van de Gevel JS, Gribnau JC, Thesingh GW, Van Furth R. In vitro formation of osteoclasts from long-term cultures of bone marrow mononuclear phagocytes. J Exp Med. 1982;156:1604–1614
  2. Scheven BA, Visser JW, Nijweide PJ. In vitro osteoclast generation from different bone marrow fractions, including a highly enriched haematopoietic stem cell population. Nature. 1986;321:79–81
  3. Lee SK, Lorenzo JA. Parathyroid hormone stimulates TRANCE and inhibits osteoprotegerin messenger ribonucleic acid expression in murine bone marrow cultures (correlation with osteoclast-like cell formation). Endocrinology. 1999;140:3552–3561
  4. Anderson DM, Maraskovsky E, Billingsley WL, Dougall WC, Tometsko ME, Roux ER, et al. A homologue of the TNF receptor and its ligand enhance T-cell growth and dendritic-cell function. Nature. 1997;390:175–179
  5. Teitelbaum SL. Bone resorption by osteoclasts. Science. 2000;289:1504–1508
  6. Udagawa N, Takahashi N, Jimi E, Matsuzaki K, Tsurukai T, Itoh K, et al. Osteoblasts/stromal cells stimulate osteoclast activation through expression of osteoclast differentiation factor/RANKL but not macrophage colony-stimulating factor. Bone. 1999;25:517–523
  7. Yasuda H, Shima N, Nakagawa N, Yamaguchi K, Kinosaki M, Mochizuki S, et al. Osteoclast differentiation factor is a ligand for osteoprotegerin/osteoclastogenesis-inhibitory factor and is identical to TRANCE/RANKL. Proc Natl Acad Sci USA. 1998;95:3597–3602
  8. Wani MR, Fuller K, Kim NS, Choi Y, Chambers T. Prostaglandin E2 cooperates with TRANCE in osteoclast induction from hemopoietic precursors (synergistic activation of differentiation, cell spreading, and fusion). Endocrinology. 1999;140:1927–1935
  9. Wong BR, Rho J, Arron J, Robinson E, Orlinick J, Chao M, et al. 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. 1997;272:25190–25194
  10. Lacey DL, Timms E, Tan HL, Kelley MJ, Dunstan CR, Burgess T, et al. Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell. 1998;93:165–176
  11. Kong YY, Yoshida H, Sarosi I, Tan HL, Timms E, Capparelli C, et al. OPGL is a key regulator of osteoclastogenesis, lymphocyte development and lymph-node organogenesis. Nature. 1999;397:315–323
  12. Tanaka S, Takahashi N, Udagawa N, Tamura T, Akatsu T, Stanley ER, et al. Macrophage colony-stimulating factor is indispensable for both proliferation and differentiation of osteoclast progenitors. J Clin Invest. 1993;91:257–263
  13. Wiktor JW, Bartocci A, Ferrante AJ, Ahmed AA, Sell KW, Pollard JW, et al. Total absence of colony-stimulating factor 1 in the macrophage-deficient osteopetrotic (op/op) mouse. Proc Natl Acad Sci USA. 1990;87:4828–4832
  14. Kobayashi K, Takahashi N, Jimi E, Udagawa N, Takami M, Kotake S, et al. Tumor necrosis factor α stimulates osteoclast differentiation by a mechanism independent of the ODF/RANKL-RANK interaction. J Exp Med. 2000;191:275–286
  15. Lam J, Takeshita S, Barker JE, Kanagawa O, Ross FP, Teitelbaum SL. TNF-α induces osteoclastogenesis by direct stimulation of macrophages exposed to permissive levels of RANK ligand. J Clin Invest. 2000;106:1481–1488
  16. Pfeilschifter J, Chenu C, Bird A, Mundy GR, Roodman GD. Interleukin-1 and tumor necrosis factor stimulate the formation of human osteoclastlike cells in vitro. J Bone Miner Res. 1989;4:113–118
  17. Fox SW, Fuller K, Bayley KE, Lean JM, Chambers TJ. TGF-β 1 and IFN-γ direct macrophage activation by TNF-α to osteoclastic or cytocidal phenotype. J Immunol. 2000;165:4957–4963
  18. Gao Y, Morita I, Maruo N, Kubota T, Murota S, Aso T. Expression of IL-6 receptor and GP130 in mouse bone marrow cells during osteoclast differentiation. Bone. 1998;22:487–493
  19. Ishimi Y, Miyaura C, Jin CH, Akatsu T, Abe E, Nakamura Y, et al. IL-6 is produced by osteoblasts and induces bone resorption. J Immunol. 1990;145:3297–3303
  20. Kotake S, Udagawa N, Takahashi N, Matsuzaki K, Itoh K, Ishiyama S, et al. IL-17 in synovial fluids from patients with rheumatoid arthritis is a potent stimulator of osteoclastogenesis. J Clin Invest. 1999;103:1345–1352
  21. Riancho JA, Zarrabeitia MT, Mundy GR, Yoneda T, Gonzalez MJ. Effects of interleukin-4 on the formation of macrophages and osteoclast-like cells. J Bone Miner Res. 1993;8:1337–1344
  22. Wei S, Wang MW, Teitelbaum SL, Ross FP. Interleukin-4 reversibly inhibits osteoclastogenesis via inhibition of NF-κB and mitogen-activated protein kinase signaling. J Biol Chem. 2002;277:6622–6630
  23. Hong MH, Williams H, Jin CH, Pike JW. The inhibitory effect of interleukin-10 on mouse osteoclast formation involves novel tyrosine-phosphorylated proteins. J Bone Miner Res. 2000;15:911–918
  24. Owens JM, Gallagher AC, Chambers TJ. IL-10 modulates formation of osteoclasts in murine hemopoietic cultures. J Immunol. 1996;157:936–940
  25. Onoe Y, Miyaura C, Kaminakayashiki T, Nagai Y, Noguchi K, Chen QR, et al. IL-13 and IL-4 inhibit bone resorption by suppressing cyclooxygenase-2-dependent prostaglandin synthesis in osteoblasts. J Immunol. 1996;156:758–764
  26. Horwood NJ, Udagawa N, Elliott J, Grail D, Okamura H, Kurimoto M, et al. Interleukin 18 inhibits osteoclast formation via T cell production of granulocyte macrophage colony-stimulating factor. J Clin Invest. 1998;101:595–603
  27. Udagawa N, Horwood NJ, Elliott J, Mackay A, Owens J, Okamura H, et al. Interleukin-18 (interferon-γ-inducing factor) is produced by osteoblasts and acts via granulocyte/macrophage colony-stimulating factor and not via interferon-gamma to inhibit osteoclast formation. J Exp Med. 1997;185:1005–1012
  28. Fox SW, Chambers TJ. Interferon-γ directly inhibits TRANCE-induced osteoclastogenesis. Biochem Biophys Res Commun. 2000;276:868–872
  29. Takayanagi H, Ogasawara K, Hida S, Chiba T, Murata S, Sato K, et al. T-cell-mediated regulation of osteoclastogenesis by signalling cross-talk between RANKL and IFN-gamma. Nature. 2000;408:600–605
  30. Cooper AM, Roberts AD, Rhoades ER, Callahan JE, Getzy DM, Orme IM. The role of interleukin-12 in acquired immunity to Mycobacterium tuberculosis infection. Immunology. 1995;84:423–432
  31. Flynn JL, Goldstein MM, Triebold KJ, Sypek J, Wolf S, Bloom BR. IL-12 increases resistance of BALB/c mice to Mycobacterium tuberculosis infection. J Immunol. 1995;155:2515–2524
  32. Bost KL, Clements JD. In vivo induction of interleukin-12 mRNA expression after oral immunization with Salmonella dublin or the B subunit of Escherichia coli heat-labile enterotoxin. Infect Immun. 1995;63:1076–1083
  33. Bost KL, Clements JD. Intracellular Salmonella dublin induces substantial secretion of the 40-kilodalton subunit of interleukin-12 (IL-12) but minimal secretion of IL-12 as a 70-kilodalton protein in murine macrophages. Infect Immun. 1997;65:3186–3192
  34. Afonso LC, Scharton TM, Vieira LQ, Wysocka M, Trinchieri G, Scott P. The adjuvant effect of interleukin-12 in a vaccine against Leishmania major. Science. 1994;263:235–237
  35. Heinzel FP, Schoenhaut DS, Rerko RM, Rosser LE, Gately MK. Recombinant interleukin 12 cures mice infected with Leishmania major. J Exp Med. 1993;177:1505–1509
  36. Macatonia SE, Hosken NA, Litton M, Vieira P, Hsieh CS, Culpepper JA, et al. Dendritic cells produce IL-12 and direct the development of Th1 cells from naive CD4+ T cells. J Immunol. 1995;154:5071–5079
  37. Cassatella MA, Meda L, Gasperini S, D'Andrea A, Ma X, Trinchieri G. Interleukin-12 production by human polymorphonuclear leukocytes. Eur J Immunol. 1995;25:1–5
  38. Tabel H, Kaushik RS, Uzonna J. Experimental African trypanosomiasis (differences in cytokine and nitric oxide production by macrophages from resistant and susceptible mice). Pathobiology. 1999;67:273–276
  39. Becher B, Blain M, Antel JP. CD40 engagement stimulates IL-12 p70 production by human microglial cells (basis for Th1 polarization in the CNS). J Neuroimmunol. 2000;102:44–50
  40. Becher B, Blain M, Giacomini PS, Antel JP. Inhibition of Th1 polarization by soluble TNF receptor is dependent on antigen-presenting cell-derived IL-12. J Immunol. 1999;162:684–688
  41. Suzumura A, Sawada M, Takayanagi T. Production of interleukin-12 and expression of its receptors by murine microglia. Brain Research. 1998;787:139–142
  42. Bost KL, Ramp WK, Nicholson NC, Bento JL, Marriott I, Hudson MC. Staphylococcus aureus infection of mouse or human osteoblasts induces high levels of interleukin-6 and interleukin-12 production. J Infect Dis. 1999;180:1912–1920
  43. Horwood NJ, Elliott J, Martin TJ, Gillespie MT. IL-12 alone and in synergy with IL-18 inhibits osteoclast formation in vitro. J Immunol. 2001;166:4915–4921
  44. Takahashi N, Yamana H, Yoshiki S, Roodman GD, Mundy GR, Jones SJ, et al. Osteoclast-like cell formation and its regulation by osteotropic hormones in mouse bone marrow cultures. Endocrinology. 1988;122:1373–1382
  45. Takeshita S, Kaji K, Kudo A. Identification and characterization of the new osteoclast progenitor with macrophage phenotypes being able to differentiate into mature osteoclasts. J Bone Miner Res. 2000;15:1477–1488
  46. MacDonald HR, Blanc C, Lees RK, Sordat B. Abnormal distribution of T cell subsets in athymic mice. J Immunol. 1986;136:4337–4339
  47. Kuroda E, Kito T, Yamashita U. Reduced expression of STAT4 and IFN-gamma in macrophages from BALB/c mice. J Immunol. 2002;168:5477–5482
  48. Kitaura H, Nagata N, Fujimura Y, Hotokezaka H, Yoshida N, Nakayama K. Effect of IL-12 on TNFα mediated osteoclast formation in bone marrow cells (apoptosis mediated by Fas/Fas ligand interaction). J Immunol. 2002;169:4732–4738
  49. Goedert S, Germann T, Hoehn P, Koelsch S, Palm N, Rude E, et al. Th1 development of naive CD4+ T cells is inhibited by co-activation with anti-CD4 monoclonal antibodies. J Immunol. 1996;157:566–573
  50. Kobayashi M, Fitz L, Ryan M, Hewick RM, Clark SC, Chan S, et al. Identification and purification of natural killer cell stimulatory factor (NKSF), a cytokine with multiple biologic effects on human lymphocytes. J Exp Med. 1989;170:827–845
  51. Yoshimoto T, Takeda K, Tanaka T, Ohkusu K, Kashiwamura S, Okamura H, et al. IL-12 up-regulates IL-18 receptor expression on T cells, Th1 cells, and B cells (synergism with IL-18 for IFN-γ production). J Immunol. 1998;161:3400–3407
  52. Simonet WS, Lacey DL, Dunstan CR, Kelley M, Chang MS, Luthy R, et al. Osteoprotegerin (a novel secreted protein involved in the regulation of bone density). Cell. 1997;89:309–319
  53. Yasuda H, Shima N, Nakagawa N, Mochizuki SI, Yano K, Fujise N, et al. Identity of osteoclastogenesis inhibitory factor (OCIF) and osteoprotegerin (OPG) (a mechanism by which OPG/OCIF inhibits osteoclastogenesis in vitro). Endocrinology. 1998;139:1329–1337
  54. Grĉević D, Lee SK, Maruŝić A, Lorenzo JA. Depletion of CD4 and CD8 T lymphocytes in mice in vivo enhances 1,25-dihydroxyvitamin D3-stimulated osteoclast-like cell formation in vitro by a mechanism that is dependent on prostaglandin synthesis. J Immunol. 2000;165:4231–4238
  55. Leite-de-Moraes MC, Herbelin A, Gouarin C, Koezuka Y, Schneider E, Dy M. Fas/Fas ligand interactions promote activation-induced cell death of NK T lymphocytes. J Immunol. 2000;165:4367–4371
  56. Airoldi I, Guglielmino R, Carra G, Corcione A, Gerosa F, Taborelli G, et al. The interleukin-12 and interleukin-12 receptor system in normal and transformed human B lymphocytes. Haematologica. 2002;87:434–442
  57. Fukao T, Matsuda S, Koyasu S. Synergistic effects of IL-4 and IL-18 on IL-12-dependent IFN-γ production by dendritic cells. J Immunol. 2000;164:64–71
  58. Puddu P, Fantuzzi L, Borghi P, Varano B, Rainaldi G, Guillemard E, et al. IL-12 induces IFN-γ expression and secretion in mouse peritoneal macrophages. J Immunol. 1997;159:3490–3497
  59. Manabe N, Kawaguchi H, Chikuda H, Miyaura C, Inada M, Nagai R, et al. Connection between B lymphocyte and osteoclast differentiation pathways. J Immunol. 2001;167:2625–2631
  60. Yamada N, Niwa S, Tsujimura T, Iwasaki T, Sugihara A, Futani H, et al. Interleukin-18 and interleukin-12 synergistically inhibit osteoclastic bone-resorbing activity. Bone. 2002;30:901–908

PII: S8756-3282(03)00213-8

doi: 10.1016/S8756-3282(03)00213-8

Bone
Volume 33, Issue 4 , Pages 721-732 , October 2003

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