The prothrombinase activity of FGL2 contributes to the pathogenesis of experimental arthritis

References

• Jenkins JK, Hardy KJ, McMurray RW. The pathogenesis of rheumatoid arthritis: a guide to therapy. Am J Med Sci 2002;323:171–80.
   PubMed Web of Science ®Google Scholar
• Goldring SR. Pathogenesis of bone and cartilage destruction in rheumatoid arthritis. Rheumatology (Oxford) 2003;42(Suppl 2): ii11–16.
   PubMedGoogle Scholar
• Smith JB, Haynes MK. Rheumatoid arthritis – a molecular understanding. Ann Intern Med 2002;136:908–22.
   PubMed Web of Science ®Google Scholar
• Weyand CM. New insights into the pathogenesis of rheumatoid arthritis. Rheumatology (Oxford) 2000;39(Suppl 1):3–8.
   PubMed Web of Science ®Google Scholar
• Chang X, Yamada R, Sawada T, Suzuki A, Kochi Y, Yamamoto K. The inhibition of antithrombin by peptidylarginine deiminase 4 may contribute to pathogenesis of rheumatoid arthritis. Rheumatology (Oxford) 2005;44:293–8.
   PubMed Web of Science ®Google Scholar
• Chang X, Yamada R, Yamamoto K. Inhibition of antithrombin by hyaluronic acid may be involved in the pathogenesis of rheumatoid arthritis. Arthritis Res Ther 2005;7:R268–73.
   Web of Science ®Google Scholar
• Flick MJ, LaJeunesse CM, Talmage KE, Witte DP, Palumbo JS, Pinkerton MD, Fibrin(ogen) exacerbates inflammatory joint disease through a mechanism linked to the integrin alphaMbeta2 binding motif. J Clin Invest 2007;117:3224–35.
   PubMed Web of Science ®Google Scholar
• Marty I, Peclat V, Kirdaite G, Salvi R, So A, Busso N. Amelioration of collagen-induced arthritis by thrombin inhibition. J Clin Invest 2001;107:631–40.
   PubMed Web of Science ®Google Scholar
• Varisco PA, Peclat V, van Ness K, Bischof-Delaloye A, So A, Busso N. Effect of thrombin inhibition on synovial inflammation in antigen induced arthritis. Ann Rheum Dis 2000;59:781–7.
   PubMed Web of Science ®Google Scholar
• Davidson CJ, Hirt RP, Lal K, Snell P, Elgar G, Tuddenham EG, Molecular evolution of the vertebrate blood coagulation network. Thromb Haemost 2003;89:420–8.
   PubMed Web of Science ®Google Scholar
• Chan CW, Chan MW, Liu M, Fung L, Cole EH, Leibowitz JL, Kinetic analysis of a unique direct prothrombinase, fgl2, and identification of a serine residue critical for the prothrombinase activity. J Immunol 2002;168:5170–7.
   PubMed Web of Science ®Google Scholar
• Schwartz BS, Levy GA, Fair DS, Edgington TS. Murine lymphoid procoagulant activity induced by bacterial lipopolysaccharide and immune complexes is a monocyte prothrombinase. J Exp Med 1982;155:1464–79.
   PubMed Web of Science ®Google Scholar
• Ruegg CR, Chiquet-Ehrismann R, Alkan SS. Tenascin, an extracellular matrix protein, exerts immunomodulatory activities. Proc Natl Acad Sci USA 1989;86:7437–41.
   PubMed Web of Science ®Google Scholar
• Smiley ST, King JA, Hancock WW. Fibrinogen stimulates macrophage chemokine secretion through toll-like receptor 4. J Immunol 2001;167:2887–94.
   PubMed Web of Science ®Google Scholar
• Thurston G, Suri C, Smith K, McClain J, Sato TN, Yancopoulos GD, Leakage-resistant blood vessels in mice transgenically overexpressing angiopoietin-1. Science 1999;286:2511–14.
   PubMed Web of Science ®Google Scholar
• Liu X, Piela-Smith TH. Fibrin(ogen)-induced expression of ICAM-1 and chemokines in human synovial fibroblasts. J Immunol 2000;165:5255–61.
   PubMed Web of Science ®Google Scholar
• Sitrin RG, Pan PM, Srikanth S, Todd RF III. Fibrinogen activates NF-kappa B transcription factors in mononuclear phagocytes. J Immunol 1998;161:1462–70.
   PubMed Web of Science ®Google Scholar
• Liu M, Leibowitz JL, Clark DA, Mendicino M, Ning Q, Ding JW, Gene transcription of fgl2 in endothelial cells is controlled by Ets-1 and Oct-1 and requires the presence of both Sp1 and Sp3. Eur J Biochem 2003;270:2274–86.
   PubMedGoogle Scholar
• Chan CW, Kay LS, Khadaroo RG, Chan MW, Lakatoo S, Young KJ, Soluble fibrinogen-like protein 2/fibroleukin exhibits immunosuppressive properties: suppressing T cell proliferation and inhibiting maturation of bone marrow-derived dendritic cells. J Immunol 2003;170:4036–44.
   PubMed Web of Science ®Google Scholar
• Shalev I, Liu H, Koscik C, Bartczak A, Javadi M, Wong KM, Targeted deletion of fgl2 leads to impaired regulatory T cell activity and development of autoimmune glomerulonephritis. J Immunol 2008;180:249–60.
   PubMed Web of Science ®Google Scholar
• Marsden PA, Ning Q, Fung LS, Luo X, Chen Y, Mendicino M, The Fgl2/fibroleukin prothrombinase contributes to immunologically mediated thrombosis in experimental and human viral hepatitis. J Clin Invest 2003;112:58–66.
   PubMed Web of Science ®Google Scholar
• Clark DA, Foerster K, Fung L, He W, Lee L, Mendicino M, The fgl2 prothrombinase/fibroleukin gene is required for lipopolysaccharide-triggered abortions and for normal mouse reproduction. Mol Hum Reprod 2004;10:99–108.
   PubMed Web of Science ®Google Scholar
• Brand DD, Kang AH, Rosloniec EF. Immunopathogenesis of collagen arthritis. Springer Semin Immunopathol 2003;25:3–18.
   PubMed Web of Science ®Google Scholar
• Terato K, Hasty KA, Cremer MA, Stuart JM, Townes AS, Kang AH. Collagen-induced arthritis in mice. Localization of an arthritogenic determinant to a fragment of the type II collagen molecule. J Exp Med 1985;162:637–46.
   Google Scholar
• Kurosaka D, Yoshida K, Yasuda J, Yasuda C, Noda K, Furuya K, The effect of endostatin evaluated in an experimental animal model of collagen-induced arthritis. Scand J Rheumatol 2007;36:434–41.
   PubMed Web of Science ®Google Scholar
• Lee SW, Kim JH, Park MC, Park YB, Lee SK. Adiponectin mitigates the severity of arthritis in mice with collagen-induced arthritis. Scand J Rheumatol 2008;37:260–8.
   PubMed Web of Science ®Google Scholar
• Rampersad RR, Esserman D, McGinnis MW, Lee DM, Patel DD, Tarrant TK. S100A9 is not essential for disease expression in an acute (K/BxN) or chronic (CIA) model of inflammatory arthritis. Scand J Rheumatol 2009;38:445–9.
   PubMed Web of Science ®Google Scholar
• Schmitt-Sody M, Metz P, Klose A, Gottschalk O, Zysk S, Hausdorf J, In vivo interactions of platelets and leucocytes with the endothelium in murine antigen-induced arthritis: the role of P-selectin. Scand J Rheumatol 2007;36:311–19.
   PubMed Web of Science ®Google Scholar
• Anthony DD, Haqqi TM. Collagen-induced arthritis in mice: an animal model to study the pathogenesis of rheumatoid arthritis. Clin Exp Rheumatol 1999;17:240–4.
   PubMed Web of Science ®Google Scholar
• Myers LK, Rosloniec EF, Cremer MA, Kang AH. Collagen-induced arthritis, an animal model of autoimmunity. Life Sci 1997;61:1861–78.
   PubMed Web of Science ®Google Scholar
• Gorczynski RM, Chen Z, Yu K, Hu J. CD200 immunoadhesin suppresses collagen-induced arthritis in mice. Clin Immunol 2001;101:328–34.
   PubMed Web of Science ®Google Scholar
• Pan M, Kang I, Craft J, Yin Z. Resistance to development of collagen-induced arthritis in C57BL/6 mice is due to a defect in secondary, but not in primary, immune response. J Clin Immunol 2004;24:481–91.
   PubMed Web of Science ®Google Scholar
• Terato K, Hasty KA, Reife RA, Cremer MA, Kang AH, Stuart JM. Induction of arthritis with monoclonal antibodies to collagen. J Immunol 1992;148:2103–8.
   PubMed Web of Science ®Google Scholar
• Cho YG, Cho ML, Min SY, Kim HY. Type II collagen autoimmunity in a mouse model of human rheumatoid arthritis. Autoimmun Rev 2007;7:65–70.
   PubMed Web of Science ®Google Scholar
• Rowley MJ, Nandakumar KS, Holmdahl R. The role of collagen antibodies in mediating arthritis. Mod Rheumatol 2008;18:429–41.
   PubMed Web of Science ®Google Scholar
• Busso N, Peclat V, Van Ness K, Kolodziesczyk E, Degen J, Bugge T, Exacerbation of antigen-induced arthritis in urokinase-deficient mice. J Clin Invest 1998;102:41–50.
   PubMed Web of Science ®Google Scholar
• Clemmensen I, Holund B, Andersen RB. Fibrin and fibronectin in rheumatoid synovial membrane and rheumatoid synovial fluid. Arthritis Rheum 1983;26:479–85.
   PubMed Web of Science ®Google Scholar
• Weinberg JB, Pippen AM, Greenberg CS. Extravascular fibrin formation and dissolution in synovial tissue of patients with osteoarthritis and rheumatoid arthritis. Arthritis Rheum 1991;34:996–1005.
   PubMed Web of Science ®Google Scholar
• Bokarewa MI, Morrissey JH, Tarkowski A. Tissue factor as a proinflammatory agent. Arthritis Res 2002;4:190–5.
   PubMedGoogle Scholar
• Ghanekar A, Mendicino M, Liu H, He W, Liu M, Zhong R, Endothelial induction of fgl2 contributes to thrombosis during acute vascular xenograft rejection. J Immunol 2004;172:5693–701.
   PubMed Web of Science ®Google Scholar
• Mendicino M, Liu M, Ghanekar A, He W, Koscik C, Shalev I, Targeted deletion of Fgl-2/fibroleukin in the donor modulates immunologic response and acute vascular rejection in cardiac xenografts. Circulation 2005;112:248–56.
   PubMed Web of Science ®Google Scholar
• Mauritz NJ, Holmdahl R, Jonsson R, Van der Meide PH, Scheynius A, Klareskog L. Treatment with gamma-interferon triggers the onset of collagen arthritis in mice. Arthritis Rheum 1988;31:1297–304.
   PubMed Web of Science ®Google Scholar
• Liu M, Mendicino M, Ning Q, Ghanekar A, He W, McGilvray I, Cytokine-induced hepatic apoptosis is dependent on FGL2/fibroleukin: the role of Sp1/Sp3 and STAT1/PU.1 composite cis elements. J Immunol 2006;176:7028–38.
   PubMed Web of Science ®Google Scholar
• Ding JW, Ning Q, Liu MF, Lai A, Leibowitz J, Peltekian KM, Fulminant hepatic failure in murine hepatitis virus strain 3 infection: tissue-specific expression of a novel fgl2 prothrombinase. J Virol 1997;71:9223–30.
   PubMed Web of Science ®Google Scholar
• Li C, Fung LS, Chung S, Crow A, Myers-Mason N, Phillips MJ, Monoclonal antiprothrombinase (3D4.3) prevents mortality from murine hepatitis virus (MHV-3) infection. J Exp Med 1992;176:689–97.
   PubMed Web of Science ®Google Scholar
• Boissier MC, Chiocchia G, Bessis N, Hajnal J, Garotta G, Nicoletti F, Biphasic effect of interferon-gamma in murine collagen-induced arthritis. Eur J Immunol 1995;25:1184–90.
   PubMed Web of Science ®Google Scholar
• Holmdahl R, Tarkowski A, Jonsson R. Involvement of macrophages and dendritic cells in synovial inflammation of collagen induced arthritis in DBA/1 mice and spontaneous arthritis in MRL/lpr mice. Autoimmunity 1991;8:271–80.
   PubMed Web of Science ®Google Scholar
• Weinberg JB, Wortham TS, Misukonis MA, Patton KL, Chitneni SR. Synovial mononuclear phagocytes in rheumatoid arthritis and osteoarthritis: quantitative and functional aspects. Immu nol Invest 1993;22:365–74.
   PubMed Web of Science ®Google Scholar
• Liu H, Shalev I, Manuel J, He W, Leung E, Crookshank J, The FGL2-FcgammaRIIB pathway: a novel mechanism leading to immunosuppression. Eur J Immunol 2008;383114–26.
   Web of Science ®Google Scholar
• Shalev I, Wong KM, Foerster K, Zhu Y, Chan C, Maknojia A, The novel CD4+CD25+ regulatory T cell effector molecule fibrinogen-like protein 2 contributes to the outcome of murine fulminant viral hepatitis. Hepatology 2009;49:387–97.
   PubMed Web of Science ®Google Scholar
• Fontenot JD, Rasmussen JP, Gavin MA, Rudensky AY. A function for interleukin 2 in Foxp3-expressing regulatory T cells. Nat Immunol 2005;6:1142–51.
   PubMed Web of Science ®Google Scholar
• Herman AE, Freeman GJ, Mathis D, Benoist C. CD4+CD25+ T regulatory cells dependent on ICOS promote regulation of effector cells in the prediabetic lesion. J Exp Med 2004; 199:1479–89.
   PubMed Web of Science ®Google Scholar
• Williams LM, Rudensky AY. Maintenance of the Foxp3-dependent developmental program in mature regulatory T cells requires continued expression of Foxp3. Nat Immunol 2007; 8:277–84.
   PubMed Web of Science ®Google Scholar
• Zhou L, Wang H, Zhong X, Jin Y, Mi QS, Sharma A, The IL-10 and IFN-gamma pathways are essential to the potent immunosuppressive activity of cultured CD8+ NKT-like cells. Genome Biol 2008;9:R119.
   PubMed Web of Science ®Google Scholar
• Morgan ME, Sutmuller RP, Witteveen HJ, van Duivenvoorde LM, Zanelli E, Melief CJ, CD25+ cell depletion hastens the onset of severe disease in collagen-induced arthritis. Arthritis Rheum 2003;48:1452–60.
   PubMed Web of Science ®Google Scholar
• Morgan ME, Flierman R, van Duivenvoorde LM, Witteveen HJ, van Ewijk W, van Laar JM, Effective treatment of collagen-induced arthritis by adoptive transfer of CD25+ regulatory T cells. Arthritis Rheum 2005;52:2212–21.
   PubMed Web of Science ®Google Scholar