IL-6 signal blockade ameliorates the enhanced osteoclastogenesis and the associated joint destruction in a novel FcγRIIB-deficient rheumatoid arthritis mouse model

Modern Rheumatology

Volumn 25, Issue 2, 2015, Pages 270-277

  Ohtsuji, Mareki ^a,b   Lin, Qingshun ^b   Nishikawa, Keiko ^b   Ohtsuji, Naomi ^b   Okazaki, Hideki ^b,c   Tsurui, Hiromichi ^b   Amano, Hirofumi ^b   Shirai, Toshikazu ^b   Nishimoto, Norihiro ^d   Nishimura, Hiroyuki ^a   Hirose, Sachiko ^b  

^a TOIN UNIVERSITY OF YOKOHAMA   (Japan)

^b JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c Musashigaoka College   (Japan)

^d Osaka Rheumatology Clinic   (Japan)

Author keywords

Interleukin 6; MCP 1; OPG; Osteoclastogenesis; RANKL

Indexed keywords

ACID PHOSPHATASE TARTRATE RESISTANT ISOENZYME; AUTOANTIBODY; CYCLIC CITRULLINATED PEPTIDE ANTIBODY; FC RECEPTOR IIB; FRACTALKINE; INTERLEUKIN 17; INTERLEUKIN 4; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; OSTEOCLAST DIFFERENTIATION FACTOR; OSTEOPROTEGERIN; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE; FC RECEPTOR; INTERLEUKIN 6 RECEPTOR; MONOCLONAL ANTIBODY; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR KAPPA B;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANKLE; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; DISEASE SEVERITY; DOWN REGULATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; HISTOLOGY; HISTOPATHOLOGY; JOINT DESTRUCTION; MOUSE; NONHUMAN; OSTEOCLASTOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RHEUMATOID ARTHRITIS; SCORING SYSTEM; UPREGULATION; ANIMAL; ARTHRITIS, RHEUMATOID; DISEASE MODEL; DRUG EFFECTS; GENETICS; IMMUNOLOGY; JOINT; METABOLISM; OSTEOCLAST; PATHOLOGY; SEVERITY OF ILLNESS INDEX;

ANIMALS; ANTIBODIES, MONOCLONAL; ARTHRITIS, RHEUMATOID; AUTOANTIBODIES; CYTOKINES; DISEASE MODELS, ANIMAL; JOINTS; MICE; OSTEOCLASTS; OSTEOPROTEGERIN; RANK LIGAND; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR-KAPPA B; RECEPTORS, IGG; RECEPTORS, INTERLEUKIN-6; SEVERITY OF ILLNESS INDEX;

EID: 84924408032     PISSN: 14397595     EISSN: 14397609     Source Type: Journal    
DOI: 10.3109/14397595.2014.950035     Document Type: Article

References (45)

1. Walsh MC, Kim N, Kadono Y, Rho J, Lee SY, Lorenzo J, Choi Y. Osteoimmunology: interplay between the immune system and bone metabolism. Annu Rev Immunol. 2006; 24: 33-63.
2. Takayanagi H. Osteoimmunology and the effect of the immune system on bone. Nat Rev Rheumatol. 2009; 5(12): 667-76.
3. 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(2): 309-19.
4. Mclnnes J B, Schett G. Cytokines in the pathogeneses of rheumatoid arthritis. Nat Rev Immunol. 2007; 7(6): 429-42.
5. Breedveld F C, Emery P, Keystone E, Patel K, Furst D E, Kalden J R, et al. Infl iximab in active early rheumatoid arthritis. Ann Rheum Dis. 2004; 63(2): 149-55.
6. Fleischmann RM, Schechtman J, Bennett R, Handel ML, Burmester GR, Tesser J, et al. Anakinra, a recombinant human interleukin-1 receptor antagonist (r-metHuIL-1ra), in patients with rheumatoid arthritis: A large, international, multicenter, placebocontrolled trial. Arthr Rheum. 2003; 48(4): 927-34.
7. Voll RE, Kalden JR. Do we need new treatment that goes beyond tumor necrosis factor blockers for rheumatoid arthritis? Ann N Y Acad Sci. 2005; 1051: 799-810.
8. van den Berg W B, M clnnes I B. T h17 cells and IL-17 A-Focus on immunopathology and immunotherapeutics. Semin Arthritis Rheum. 2013; 43(2): 158-70.
9. Thorbecke GJ, Shah R, Leu CH, Kuruvilla AP, Hardison AM, Palladino MA. Involvement of endogenous tumor necrosis factor α and transforming growth factor β during induction of collagen type II arthritis in mice. Proc Natlacad Sci USA. 1992; 89(16): 7375-9.
10. Piguet PF, Grau GE, Vesin C, Loetscher H, Gentz R, Lesslauer W. Evolution of collagen arthritis in mice is arrested by treatment with antitumour necrosis factor (TNF) antibody or a recombinant soluble TNF receptor. Immunology. 1992; 77(4): 510-4.
11. Campbell I K, O‘Donnell K, Lawlor K E, Wicks I P. Severe inflammatory arthritis and lymphadenopathy in the absence of TNF. J Clin Invest. 2001; 107(12): 1519-27.
12. Ji H, Pettit A, Ohmura K, Oriz-Lopez A, Duchatelle V, Degott C, et al. Critical roles for interleukin 1 and tumor necrosis factor α in antibody-induced arthritis. J Exp Med. 2002; 196(1): 77-85.
13. Hirota K, Hashimoto M, Yoshitomi H, Tanaka S, Nomura T, Yamaguchi T, et al. T cell self-reactivity forms a cytokine milieu for spontaneous development of IL-17+ Th cells that cause autoimmune arthritis. J Exp Med. 2007; 204(1): 41-7.
14. Nakae S, Saijo S, Horai R, Sudo K, Mori S, Iwakura Y. IL-17 production from activated T cells is required for the spontaneous development of arthritis in mice defi cient in IL-1 receptor antagonist. Proc Natlacad Sci USA. 2003; 100(10): 5986-90.
15. Nakae S, Nambu A, Sodo K, Iwakura Y. Suppression of immune induction of collagen-induced arthritis in IL-17-defi cient mice. J Immunol. 2003; 171(11): 6173-7.
16. Doodes PD, Cao Y, Hamel KM, Wang Y, Farkas B, Iwakura Y, et al. Development of proteoglycan-induced arthritis is independent of IL-17. J Immunol. 2008; 181(1): 329-37.
17. Mima T, Nishimoto N. Clinical value of blocking IL-6 receptor. C urr Opin Rheumatol. 2009; 21(3): 224-30.
18. Smolen J S, Beaulieu A, Rubbert-Roth A, Ramos-Remus C, Rovensky J, Alecock E, et al. Effect of interleukin-6 receptor inhibition with tocilizumab in patients with rheumatoid arthritis (OPTION study): a double-blind, placebo-controlled, randomised trial. Lancet. 2008; 371(9617): 987-97.
19. Dougados M, Kissel K, Sheeran T, Tak P P, Conaghan P G, M ola E M, et al. Adding tocilizumab or switching to tocilizumab monotherapy in methotrexate inadequate responders: 24-week symptomatic and structural results of a 2-year randomised controlled strategy trial in rheumatoid arthritis (ACT-RAY). Ann Rheum Dis. 2013; 72(1): 43-50.
20. Takagi N, Mihara M, Moriya Y, Nishimoto N, Yoshizaki K, Kishimoto T, et al. Blockage of interleukin-6 receptor ameliorates joint disease in murine collagen-induced arthritis. Arthr Rheum. 1998; 41(12): 2117-21.
21. Kagari T, Doi H, Shimozato T. The importance of IL-1β and TNF-α, and the non-involvement of IL-6, in the development of monoclonalantibody-induced arthritis. J Immunol. 2002; 169(9): 1459-66.
22. Sato-Hayashizaki A, Ohtsuji M, Lin Q, Hou R, Ohtsuji N, Nishikawa K, et al. Presumptive role of 129 strain-derived Sle16 locus in rheumatoid arthritis in a new mouse model with Fc γ receptor Type IIb-defi cient C57BL/6 genetic background. Arthr Rheum. 2011; 63(10): 2930-8.
23. Okazaki H, Lin Q, Nishikawa K, Ohtsuji N, Tsurui H, Ohtsuji M, et al. TNF α but not IL-17 is critical in the pathogenesis of rheumatoid arthritis spontaneously occurring in a unique Fc γ RIIB-defi cient mouse model. Modern Rheum. DOI: 10.3109/14397595.2014.886351
24. Takai T, Ono M, Hikida M, Ohmori H, Ravetch J V. A ugmented humoraland anaphylactic responses in Fc γ RII-defi cient mice. Nature. 1996; 379(6563): 346-9.
25. Tamura T, Udagawa N, Takahashi N, Miyaura C, Tanaka S, Yamada Y, et al. Soluble interleukin-6 receptor triggers osteoclast formation by interleukin-6. Proc Natlacad. Sci USA. 1993; 90(24): 11924-8.
26. Abe Y, Ohtsuji M, Ohtsuji N, Lin Q, Tsurui H, Nakae S, et al. Ankylosing enthesitis associated with up-regulated IFN-γ and IL-17 production in (BXSB × NZB) F1 male mice: a new mouse model. Mod Rheumatol. 2009; 19(3): 316-22.
27. Gordon S, Taylor PR. Monocyte and macrophage heterogeneity. Nat Rev Immunol. 2005; 5(12): 953-64.
28. Kikuchi S, Santiago-Raber M-L, A mano H, A mano E, F ossati-Jimack L, Moll T, et al. Contribution of NZB autoimmunity 2 to Y-linked autoimmune acceleration-induced monocytosis in association with murine systemic lupus. J Immunol. 2006; 176(5): 3240-7.
29. Iwamoto T, Okamoto H, Toyama Y, Momohara S. M olecular aspects of rheumatoid arthritis: chemokines in the joints of patients. FEBS J. 2008; 275(18): 4448-55.
30. Yu RY-L, Wang X, Pixley FJ, Yu J, Dent AL, Broxmeyer DH, et al. BCL-6 negatively regulated macrophage proliferation by suppressing autocrine IL-6 production. Blood. 2005; 105(4): 1777-84.
31. Steinman L. A brief history of T H 17, the fi rst major revision in the T H 1/T H 2 hypothesis of T cell-mediated tissue damage. Nat Med. 2007: 13(2); 139-45.
32. Bolland S, Ravetch J V. S pontaneous autoimmune disease in Fc γ RIIBdefi cient mice results from strain-specifi c epistasis. Immunity. 2000; 13(2): 277-85.
33. Akira S, Narazaki M, Taga T. Interleukin-6 family of cytokines and gp130. Blood. 1995; 86(4): 1243-54.
34. Rose-John S, Scheller J, Elson G, Jones SA. Interleukin-6 biology is coordinated by membrane-bound and soluble receptors: role in inflammation and cancer. J Leukoc Biol. 2006; 80(2): 227-36.
35. Dayer J -M, Choy E. T herapeutic targests in rheumatoid arthritis: the interleukn-6 receptor. Rheumatology. 2010; 49(1): 15-24.
36. Atsumi T, Ishihara K, Kamimura D, Ikushima H, Ohtani T, Hirota S, et al. A point mutation of Tyr-759 in interleukin 6 family cytokine receptor subunit gp130 causes autoimmune arthritis. J Exp Med. 2002; 196(7): 979-90.
37. Palmqvist P, Persson E, Conaway HH, U.H. Lerner UH. IL-6, leukemia inhibitory factor, and oncostatin M stimulate bone resorption and regulate the expression of receptor activator of NF-κ B in mouse calvariare. J Immunol. 2002; 169(6): 3353-62.
38. Hashizume M, Hayakawa N. Mihara M. IL-6 trans-signalling directly induces RANKL on fobroblast-like synovial cells and is involved in RANKL induction by TNF-α and IL-17. Rheumatology. 2008; 47(11): 1635-40.
39. Yun T J, Chaudhary P M, Shu G L, Frazer J K, Ewing M K, Schwartz SM, et al. OPG/FDCR-1, a TNF receptor family member, is expressed in lymphoid cells and is up-regulated by ligating CD40. J Immunol. 1998; 161(11): 6113-21.
40. Zannettio ACW, Holding CA, Diamond P, Atkins GJ, Kostakis P, Farrugia A, et al. Osteoprotegerin (0PG) is localized to the Weibel-Palade bodies of human vascular endothelial cells and is physically associated with von Willebrand factor. J Cell Physiol. 2005; 204(2): 714-23.
41. Catrina AI, af Klint E, Ernestam S, Catrina S-B, Makrygiannakis D, Botusan IR, et al. Anti-tumor necrosis factor therapy increases synovial osteoprotegerin expression in rheumatoid arthritis. Arthr Rheum. 2006; 54(1): 76-81.
42. Liu X H, Kirschenbaum A, Yao S, Levine A C. I nteractive effect of interleukin-6 and prostaglandin E2 on osteoclastogenesis via the OPG/ RANKL/RANK system. Annn N Y Acad Sci. 2006; 1068: 225-33.
43. Feldmann M, Brennan F M, Maini R N. R heumatoid Arthritis. C ell. 1996; 85(3): 307-10.
44. Nishimoto N, Terao K, Mima T, Nakahara H, Takagi N, Kakehi T. Mechanisms and pathologic signifi cances in increase in serum interleukin-6 (IL-6) and soluble receptor after administration of an anti-IL-6 receptor antibody, tocilizumab, in patients with rheumatoid arthritis and Castleman disease. Blood. 2008; 112(10): 3959-64.
45. Ducreux J, Durez P, G alant C, Toukap A N, Van de Eynde B, Houssiau FA, et al. Global molecular effects of tocilizumab therapy in rheumatoid arthritis synovium. Arthr Rheum. 2014; 66(1): 15-23.