Role of osteoclasts and interleukin-17 in the pathogenesis of rheumatoid arthritis: Crucial 'human osteoclastology'

Journal of Bone and Mineral Metabolism

Volumn 30, Issue 2, 2012, Pages 125-135

  Kotake, Shigeru ^a   Yago, Toru ^a   Kawamoto, Manabu ^a   Nanke, Yuki ^a  

^a TOKYO WOMEN'S MEDICAL UNIVERSITY   (Japan)

Author keywords

Interleukin 17 (IL 17); Osteoclast; Osteoclastology; Rheumatoid arthritis; Th17

Indexed keywords

DISEASE MODIFYING ANTIRHEUMATIC DRUG; GAMMA INTERFERON; INTERLEUKIN 17; INTERLEUKIN 23; INTERLEUKIN 6 RECEPTOR; IXEKIZUMAB; OSTEOCLAST DIFFERENTIATION FACTOR; T CELL LEUKEMIA TRANSLOCATION ASSOCIATED PROTEIN; TEPRENONE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; VITAMIN K GROUP;

COLONY FORMING UNIT GM; CYTOKINE PRODUCTION; DISEASE ASSOCIATION; DRUG MECHANISM; HUMAN; HUMAN VERSUS ANIMAL COMPARISON; IMMUNE RESPONSE; LYMPHOCYTE FUNCTION; NONHUMAN; OSTEOCLAST; OSTEOCLASTOGENESIS; OSTEOPOROSIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS INHIBITION; REVIEW; RHEUMATOID ARTHRITIS; T LYMPHOCYTE; TH17 CELL; UNSPECIFIED SIDE EFFECT;

ANIMALS; ARTHRITIS, RHEUMATOID; BONE RESORPTION; DISEASE MODELS, ANIMAL; HUMANS; INTERLEUKIN-17; OSTEOCLASTS; T-LYMPHOCYTES;

EID: 84859833805     PISSN: 09148779     EISSN: 14355604     Source Type: Journal    
DOI: 10.1007/s00774-011-0321-5     Document Type: Review

References (75)

1. Shimizu S, Shiozawa S, Shiozawa K, Imura S, Fujita T (1985) Quantitative histologic studies on the pathogenesis of periarticular osteoporosis in rheumatoid arthritis. Arthritis Rheum 28:25-31 (Pubitemid 15193018)
2. Firestein GS (1998) Rheumatoid arthritis and pannus. Klippel JH, Dieppe (eds) Rheumatology, 2nd edn. Mosby, London, pp 5.13. 1-5.13.24
3. Kotake S, Nanke Y, Yago T, Kawamoto M, Yamanaka H (2009) Human osteoclastogenic T cells and human osteoclastology. EDITORIAL. Arthritis Rheum 60:3158-3163
4. Kotake S, Yago T, Kawamoto M, Nanke Y (2010) Effects of NSAIDs on differentiation and function of human and murine osteoclasts -crucial 'Human Osteoclastology'. Pharmaceuticals 3:1394-1410
5. Testa NG, Allen TD, Lajtha LG, Onions D, Jarret O (1981) Generation of osteoclasts in vitro. J Cell Sci 47:127-137 (Pubitemid 11134478)
6. Ibbotson KJ, Roodman GD, McManus LM, Mundy GR (1984) Identification and characterization of osteoclast-like cells and their progenitors in cultures of feline marrow mononuclear cells. J Cell Biol 99:471-480 (Pubitemid 14065173)
7. MacDonald BR, Takahashi N, McManus LM, Holahan J, Mundy GR, Roodman GD (1987) Formation of multinucleated cells that respond to osteotropic hormones in long term human bone marrow cultures. Endocrinology 120:2326-2333
8. Takahashi N, Yamana H, Yoshiki S, Roodman GD, Mundy GR, Jones SJ, Boyde A, Suda T (1988) Osteoclast-like cell formation and its regulation by osteotropic hormones in mouse bone marrow cultures. Endocrinology 122:1373-1382 (Pubitemid 18091966)
9. Hattersley G, Chambers TJ (1989) Calcitonin receptors as markers for osteoclastic differentiation: correlation between generation of bone-resorptive cells and cells that express calcitonin receptors in mouse bone marrow cultures. Endocrinology 125:1606-1612 (Pubitemid 19224017)
10. Takahashi N, Akatsu T, Udagawa N, Sasaki T, Yamaguchi A, Moseley JM, Martin TJ, Suda T (1988) Osteoblastic cells are involved in osteoclast formation. Endocrinology 123:2600-2602
11. Udagawa N, Takahashi N, Akatsu T, Tanaka H, Sasaki T, Nishihara T, Koga T, Martin TJ, Suda T (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
12. Suda T, Udagawa N, Nakamura I, Miyaura C, Takahashi N (1995) Modulation of osteoclast differentiation by local factors. Bone 17:87S-91S
13. Udagawa N, Kotake S, Kamatani N, Takahashi N, Suda T (2002) The molecular mechanism of osteoclastogenesis in rheumatoid arthritis. Arthritis Res 4:281-289 (Pubitemid 34947141)
14. Lam J, Nelson CA, Ross FP, Teitelbaum SL, Fremont DH (2001) Crystal structure of the TRANCE/RANKL cytokine reveals determinants of receptor-ligand specificity. J Clin Invest 108: 971-979 (Pubitemid 32946071)
15. Ochi T, Hakomori S, Adachi M, Owaki H, Okamura M, Ono Y, Yamasaki K, Fujimoto M, Wakitani S, Ono K (1988) The presence of a myeloid cell population showing strong reactivity with monoclonal antibody directed to difucosyl type 2 chain in epiphyseal bone marrow adjacent to joints affected with rheumatoid arthritis (RA) and its absence in the corresponding normal and non-RA bone marrow. J Rheumatol 15:1609-1615 (Pubitemid 19027777)
16. Kotake S, Higaki M, Sato K, Himeno S, Morita H, Kim K-J, Nara N, Miyasaka N, Nishioka K, Kashiwazaki S (1992) Detection of myeloid precursors (granulocyte/macrophage colony forming units) in the bone marrow adjacent to rheumatoid arthritis joints. J Rheumatol 19:1511-1516
17. Kotake S, Sato K, Kim K-J, Takahashi N, Udagawa N, Nakamura I, Yamaguchi A, Kishimoto T, Suda T, Kashiwazaki S (1996) Interleukin-6 and soluble interleukin-6 receptors in the synovial fluids from rheumatoid arthritis patients are responsible for osteoclast-like cell formation. J Bone Miner Res 11:88-95 (Pubitemid 26026748)
18. Tamura T, Udagawa N, Takahashi N, Miyaura C, Tanaka S, Yamada Y, Koishihara Y, Ohsugi Y, Kumaki K, Taga T, Kishimoto T, Suda T (1993) Soluble interleukin-6 receptor triggers osteoclast formation by interleukin 6. Proc Natl Acad Sci USA 90:11924-11928 (Pubitemid 24008752)
19. Chang JS, Quinn JM, Demaziere A, Bulstrode CJ, Francis MJ, Duthie RB, Athanasou NA (1992) Bone resorption by cells isolated from rheumatoid synovium. Ann Rheum Dis 51:1223-1229
20. Goronzy JJ, Weyand CM (2001) Mechanism of joint destruction. In: Klippel JH (ed) Primers on the rheumatic diseases, 12th edn. Arthritis Foundation®, Atlanta pp 215-216
21. Wilkinson LS, Pitsillides AA, Edwards JC (1993) Giant cells in arthritic synovium. Ann Rheum Dis 52:182-184 (Pubitemid 23094305)
22. Fujikawa Y, Shingu M, Torisu T, Itonaga I, Masumi S (1996) Bone resorption by tartrate-resistant acid phosphatase-positive multinuclear cells isolated from rheumatoid synovium. Br J Rheumatol 35:213-217
23. Kotake S, Udagawa N, Takahashi N, Matsuzaki K, Itoh K, Ishiyama S, Saito S, Inoue K, Kamatani N, Gillespie MT, Martin TJ, Suda T (1999) IL-17 in synovial fluids from patients with rheumatoid arthritis is a potent stimulator of osteoclastogenesis. J Clin Invest 103:1345-1352 (Pubitemid 29218305)
24. Kwan Tat S, Pelletier JP, Lajeunesse D, Fahmi H, Duval N, Martel-Pelletier J (2008) Differential modulation of RANKL isoforms by human osteoarthritic subchondral bone osteoblasts: influence of osteotropic factors. Bone 43:284-291
25. Stamp LK, James MJ, Cleland LG (2004) Paracrine upregulation of monocyte cyclooxygenase-2 by mediators produced by T lymphocytes: role of interleukin 17 and interferon-gamma. J Rheumatol 31:1255-1264 (Pubitemid 38879186)
26. Stamp LK, Cleland LG, James MJ (2004) Upregulation of synoviocyte COX-2 through interactions with T lymphocytes: role of interleukin 17 and tumor necrosis factor-alpha. J Rheumatol 31:1246-1254 (Pubitemid 38879185)
27. Yago T, Nanke Y, Ichikawa N, Kobashigawa T, Mogi M, Kamatani N, Kotake S (2009) IL-17 induces osteoclastogenesis from human monocytes alone in the absence of osteoblasts, which is potently inhibited by anti-TNF-alpha antibody: a novel mechanism of osteoclastogenesis by IL-17. J Cell Biochem 108:947-955
28. Lam J, Takeshita S, Barker JE, Kanagawa O, Ross FP, Teitelbaum SL (2000) TNF-alpha induces osteoclastogenesis by direct stimulation of macrophages exposed to permissive levels of RANK ligand. J Clin Invest 106:1481-1488 (Pubitemid 32038586)
29. Zou W, Hakim I, Tschoep K, Endres S, Bar-Shavit Z (2001) Tumor necrosis factor-alpha mediates RANK ligand stimulation of osteoclast differentiation by an autocrine mechanism. J Cell Biochem 83:70-83
30. Miranda-Carus ME, Benito-Miguel M, Balsa A, Cobo-Ibanez T, Perez de Ayala C, Pascual-Salcedo D, Martín-Mola E (2006) Peripheral blood T lymphocytes from patients with early rheumatoid arthritis express RANKL and interleukin-15 on the cell surface and promote osteoclastogenesis in autologous monocytes. Arthritis Rheum 54:1151-1164 (Pubitemid 43672928)
31. Lubberts E, Koenders MI, Oppers-Walgreen B, van den Bersselaar L, Coenen-de Roo CJ, Joosten LA et al (2004) Treatment with a neutralizing anti-murine interleukin-17 antibody after the onset of collagen-induced arthritis reduces joint inflammation, cartilage destruction, and bone erosion. Arthritis Rheum 50:650-659 (Pubitemid 38198849)
32. Nakae S, Saijo S, Horai R, Sudo K, Mori S, Iwakura Y (2003) IL-17 production from activated T cells is required for the spontaneous development of destructive arthritis in mice deficient in IL-1 receptor antagonist. Proc Natl Acad Sci USA 100: 5986-5990 (Pubitemid 36576918)
33. Sarkar S, Tesmer LA, Hindnavis V, Endres JL, Fox DA (2007) Interleukin-17 as a molecular target in immune-mediated arthritis: immunoregulatory properties of genetically modified murine dendritic cells that secrete interleukin-4. Arthritis Rheum 56:89-100 (Pubitemid 46106181)
34. Raza K, Falciani F, Curnow SJ, Ross EJ, Lee CY, Akbar AN et al (2005) Early rheumatoid arthritis is characterized by a distinct and transient synovial fluid cytokine profile of T cell and stromal cell origin. Arthritis Res Ther 7:R784-R795
35. Furuzawa-Carballeda J, Vargas-Rojas MI, Cabral AR (2007) Autoimmune inflammation from the Th17 perspective. Autoimmun Rev 6:169-175 (Pubitemid 46187336)
36. Harrington LE, Hatton RD, Mangan PR, Turner H, Murphy TL, Murphy KM et al (2005) Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol 6:1123-1132 (Pubitemid 41541790)
37. Park H, Li Z, Yang XO, Chang SH, Nurieva R, Wang YH et al (2005) A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol 6:1133-1141 (Pubitemid 41541791)
38. Acosta-Rodriguez EV, Rivino L, Geginat J, Jarrossay D, Gattorno M, Lanzavecchia A et al (2007) Surface phenotype and antigenic specificity of human interleukin 17-producing T helper memory cells. Nat Immunol 8:639-646 (Pubitemid 46785128)
39. Ye P, Rodriguez FH, Kanaly S, Stocking KL, Schurr J, Schwarzenberger P et al (2001) Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colony-stimulating factor expression, neutrophil recruitment, and host defense. J Exp Med 194:519-527 (Pubitemid 32835046)
40. Happel KI, Dubin PJ, Zheng M, Ghilardi N, Lockhart C, Quinton LJ et al (2005) Divergent roles of IL-23 and IL-12 in host defense against Klebsiella pneumoniae. J Exp Med 202:761-769 (Pubitemid 41345965)
41. Rudner XL, Happel KI, Young EA, Shellito JE (2007) Interleukin-23 (IL-23)-IL-17 cytokine axis in murine Pneumocystis carinii infection. Infect Immun 75:3055-3061 (Pubitemid 46870190)
42. Sato K, Suematsu A, Okamoto K, Yamaguchi A, Morishita Y, Kadono Y et al (2006) Th17 functions as an osteoclastogenic helper T cell subset that links T cell activation and bone destruction. J Exp Med 203:2673-2682 (Pubitemid 44833343)
43. Hirota K, Hashimoto M, Yoshitomi H, Tanaka S, Nomura T, Yamaguchi T et al (2007) T cell self-reactivity forms a cytokine milieu for spontaneous development of IL-17? Th cells that cause autoimmune arthritis. J Exp Med 204:41-47 (Pubitemid 46148754)
44. Genovese M, Van den Bosch F, Roberson S, Bojin S, Biagini I, Ryan P, Sloan-Lancaster J (2010) LY2439821, a Humanized anti-IL-17 monoclonal antibody, in the treatment of patients with rheumatoid arthritis. Arthritis Rheum 62:929-939
45. Kokkonen H, Söderström I, Rocklöv J, Hallmans G, Lejon K, Rantapää Dahlqvist S (2010) Up-regulation of cytokines and chemokines predates the onset of rheumatoid arthritis. Arthritis Rheum 62:383-391
46. Leipe J, Grunke M, Dechant C, Reindl C, Kerzendorf U, Schulze-Koops H, Skapenko A (2010) Role of Th17 cells in human autoimmune arthritis. Arthritis Rheum 62:2876-2885
47. Kochi Y, Okada Y, Suzuki A, Ikari K, Terao C et al (2010) A regulatory variant in CCR6 is associated with rheumatoid arthritis susceptibility. Nat Genet 42:515-519
48. Yago T, Nanke Y, Kawamoto M, Furuya T, Kobashigawa T, Kamatani N, Kotake S (2007) IL-23 induces human osteoclastogenesis via IL-17 in vitro, and anti-IL-23 antibody attenuates collagen-induced arthritis in rats. Arthritis Res Ther 9:R96-R107
49. Kong YY, Feige U, Sarosi I, Bolon B, Tafuri A et al (1999) Activated T cells regulate bone loss and joint destruction in adjuvant arthritis through osteoprotegerin ligand. Nature 402:304-309 (Pubitemid 129516268)
50. Horwood NJ, Kartsogiannis V, Quinn JM, Romas E, Martin TJ, Gillespie MT (1999) Activated T lymphocytes support osteoclast formation in vitro. Biochem Biophys Res Commun 265:144-150
51. Kotake S, Udagawa N, Hakoda M, Mogi M, Yano K, Tsuda E, Takahashi K, Furuya T, Ishiyama S, Kim K-J, Saito S, Nishikawa T, Takahashi N, Togari A, Tomatsu T, Suda T, Kamatani N (2001) Activated human T cells directly induce osteoclastogenesis from human monocytes: possible role of T cells in bone destruction in rheumatoid arthritis patients. Arthritis Rheum 44:1003-1012 (Pubitemid 32433604)
52. Geusens PP, Landewe RB, Garnero P, Chen D, Dunstan CR, Lems WF et al (2006) The ratio of circulating osteoprotegerin to RANKL in early rheumatoid arthritis predicts later joint destruction. Arthritis Rheum 54:1772-1777 (Pubitemid 43877926)
53. Mogi M, Otogoto J, Ota N, Togari A (2004) Differential expression of RANKL and osteoprotegerin in gingival crevicular fluid of patients with periodontitis. J Dent Res 83:166-169 (Pubitemid 41713803)
54. Vernal R, Dutzan N, Hernandez M, Chandia S, Puente J, Leon R et al (2006) High expression levels of receptor activator of nuclear factor-B ligand associated with human chronic periodontitis are mainly secreted by CD4 ? T lymphocytes. J Periodontol 77:1772-1780 (Pubitemid 44680243)
55. Teng YT, Nguyen H, Gao X, Kong YY, Gorczynski RM, Singh B et al (2000) Functional human T-cell immunity and osteoprotegerin ligand control alveolar bone destruction in periodontal infection. J Clin Invest 106:1259-1267
56. Kawai T, Paster BJ, Komatsuzawa H, Ernst CW, Goncalves RB, Sasaki H et al (2007) Cross-reactive adaptive immune response to oral commensal bacteria results in an induction of receptor activator of nuclear factor-jB ligand (RANKL)-dependent periodontal bone resorption in a mouse model. Oral Microbiol Immunol 22:208-215 (Pubitemid 46691094)
57. Fox SW, Fuller K, Bayley KE, Lean JM, Chambers TJ (2000) TGF-beta 1 and IFN-gamma direct macrophage activation by TNF-alpha to osteoclastic or cytocidal phenotype. J Immunol 165:4957-4963
58. Udagawa N, Horwood NJ, Elliott J, Mackay A, Owens J, Okamura H et al (1997) Interleukin-18 (interferon-gamma-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 185:1005-1012 (Pubitemid 27136793)
59. Takayanagi H, Ogasawara K, Hida S, Chiba T, Murata S, Sato K et al (2000) T-cell-mediated regulation of osteoclastogenesis by signalling cross-talk between RANKL and IFN-gamma. Nature 408:600-605
60. Kotake S, Nanke Y, Mogi M, Kawamoto M, Furuya T, Yago T, Kobashigawa T, Togari A, Kamatani N (2005) IFN-gamma-producing human T cells directly induce osteoclastogenesis from human monocytes via the expression of RANKL. Eur J Immunol 35:3353-3363 (Pubitemid 41672539)
61. Gao Y, Grassi F, Ryan MR, Terauchi M, Page K, Yang X et al (2007) IFN-gamma stimulates osteoclast formation and bone loss in vivo via antigen-driven T cell activation. J Clin Invest 117:122-132 (Pubitemid 46048459)
62. Stashenko P, Goncalves RB, Lipkin B, Ficarelli A, Sasaki H, Campos-Neto A (2007) Th1 immune response promotes severe bone resorption caused by Porphyromonas gingivalis. Am J Pathol 170:203-213 (Pubitemid 47339200)
63. Rifas L, Weitzmann MN (2009) A novel secreted osteoclastogenic factor of activated T cells (SOFAT) induced osteoclast formation in a RANKL-independent manner. Arthritis Rheum 60:3324-3335
64. Kotake S, Nanke Y, Kawamoto M, Yago T, Udagawa N, Ichikawa N, Kobashigawa T, Saito S, Momohara S, Kamatani N, Yamanaka H (2009) T-cell leukemia translocation-associated gene (TCTA) protein is required for human osteoclastogenesis. Bone 45:627-639
65. Kotake S, Yago T, Kawamoto M, Nanke Y (2009) The role of T-cell leukemia translocation-associated gene (TCTA) protein in human osteoclastogenesis. Jpn J Clin Immunol 32:466-471
66. Nanke Y, Kotake S, Ninomiya T, Furuya T, Ozawa H, Kamatani N (2005) Geranylgeranylacetone inhibits formation and function of human osteoclasts and prevents bone loss in tail-suspended rats and ovariectomized rats. Calcif Tissue Int 77:376-385 (Pubitemid 41830853)
67. Nanke Y, Kawamoto M, Yago T, Chiba J, Yamanaka H, Kotake S (2009) Geranylgeranylacetone, a non-toxic inducer of heat shock protein, induces cell death in fibroblast-like synoviocytes from patients with rheumatoid arthritis. Mod Rheumatol 19:379-383
68. Motoyoshi K, Suda T, Kusumoto K, Takaku F, Miura Y (1982) Granulocyte-macrophage colony-stimulating and binding activities of purified human urinary colony-stimulating factor to murine and human bone marrow cells. Blood 60:1378-1386 (Pubitemid 13211377)
69. Kanamaru F, Iwai H, Ikeda T, Nakajima A, Ishikawa I, Azuma M (2004) Expression of membrane-bound and soluble receptor activator of NF-kappaB ligand (RANKL) in human T cells. Immunol Lett 94:239-246 (Pubitemid 38953425)
70. Baecher-Allan C, Brown JA, Freeman GJ, Hafler DA (2001) CD4? CD25high regulatory cells in human peripheral blood. J Immunol 167:1245-1253 (Pubitemid 32703119)
71. Nanke Y, Kotake S, Goto M, Ujihara H, Matsubara M, Kamatani N (2008) Decreased percentages of regulatory T cells in peripheral blood of patients with Behcet's disease before ocular attack: a possible predictive marker of ocular attack. Mod Rheumatol 18:354-358
72. Amadi-Obi A, Yu CR, Liu X, Mahdi RM, Clarke GL, Nussenblatt RB et al (2007) TH17 cells contribute to uveitis and scleritis and are expanded by IL-2 and inhibited by IL-27/STAT1. Nat Med 13:711-718 (Pubitemid 46889754)
73. Annunziato F, Cosmi L, Liotta F, Maggi E, Romagnani S (2009) Human Th17 cells: are they different from murine Th17 cells? Eur J Immunol 39:637-640
74. Itonaga I, Sabokbar A, Neale SD, Athanasou NA (1999) 1, 25-Dihydroxyvitamin D(3) and prostaglandin E(2) act directly on circulating human osteoclast precursors. Biochem Biophys Res Commun 264:590-595 (Pubitemid 29516130)
75. Take I, Kobayashi Y, Yamamoto Y, Tsuboi H, Ochi T, Uematsu S, Okafuji N, Kurihara S, Udagawa N, Takahashi N (2005) Prostaglandin E2 strongly inhibits human osteoclast formation. Endocrinology 146:5204-5214 (Pubitemid 41653034)