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

Scandinavian Journal of Rheumatology

Volumn 40, Issue 4, 2011, Pages 269-278

  Melnyk, M C ^a   Shalev, I ^a   Zhang, J ^a   Bartczak, A ^a   Gorczynski, R M ^a,b   Selzner, N ^a   Inman, R ^c   Marsden, P A ^d   Phillips, M J ^a   Clark, D A ^a,e   Levy, G A ^a,f  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY HEALTH NETWORK   (Canada)

^d ST MICHAEL'S HOSPITAL   (Canada)

^e MCMASTER UNIVERSITY   (Canada)

^f TORONTO GENERAL HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD CLOTTING FACTOR 10A; CD200 ANTIGEN; FIBRIN; MEMBRANE ASSOCIATED FIBRINOGEN LIKE PROTEIN 2; MEMBRANE PROTEIN; MESSENGER RNA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTHRITIS; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; FIBRIN DEPOSITION; GENE EXPRESSION REGULATION; HINDLIMB; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; JOINT CAVITY; KNOCKOUT MOUSE; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; SYNOVIUM;

ANIMALS; ANTIGENS, CD; ARTHRITIS, EXPERIMENTAL; DISEASE MODELS, ANIMAL; FIBRIN; FIBRINOGEN; IMMUNOSUPPRESSIVE AGENTS; MICE; MICE, INBRED C57BL; MICE, INBRED DBA; MICE, KNOCKOUT; SIGNAL TRANSDUCTION; SYNOVIAL MEMBRANE; THROMBOPLASTIN; UP-REGULATION;

EID: 80051994927     PISSN: 03009742     EISSN: 15027732     Source Type: Journal    
DOI: 10.3109/03009742.2010.536163     Document Type: Article

References (56)

1. Jenkins JK, Hardy KJ, McMurray RW. The pathogenesis of rheumatoid arthritis: a guide to therapy. Am J Med Sci 2002;323:171-80 (Pubitemid 34651586)
2. Goldring SR. Pathogenesis of bone and cartilage destruction in rheumatoid arthritis. Rheumatology (Oxford) 2003;42(Suppl 2): ii11-16 (Pubitemid 37220895)
3. Smith JB, Haynes MK. Rheumatoid arthritis - a molecular understanding. Ann Intern Med 2002;136:908-22 (Pubitemid 34625703)
4. Weyand CM. New insights into the pathogenesis of rheumatoid arthritis. Rheumatology (Oxford) 2000;39(Suppl 1):3-8 (Pubitemid 30352937)
5. 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 (Pubitemid 40361283)
6. 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
7. Flick MJ, LaJeunesse CM, Talmage KE, Witte DP, Palumbo JS, Pinkerton MD, et al. Fibrin(ogen) exacerbates inflammatory joint disease through a mechanism linked to the integrin alphaMbeta2 binding motif. J Clin Invest 2007;117:3224-35 (Pubitemid 350096980)
8. 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 (Pubitemid 32205184)
9. 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
10. Davidson CJ, Hirt RP, Lal K, Snell P, Elgar G, Tuddenham EG, et al. Molecular evolution of the vertebrate blood coagulation network. Thromb Haemost 2003;89:420-8 (Pubitemid 36329230)
11. Chan CW, Chan MW, Liu M, Fung L, Cole EH, Leibowitz JL, et al. 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 (Pubitemid 34495983)
12. 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 (Pubitemid 12102091)
13. Ruegg CR, Chiquet-Ehrismann R, Alkan SS. Tenascin, an extracellular matrix protein, exerts immunomodulatory activities. Proc Natl Acad Sci USA 1989;86:7437-41 (Pubitemid 19254471)
14. Smiley ST, King JA, Hancock WW. Fibrinogen stimulates macrophage chemokine secretion through toll-like receptor 4. J Immunol 2001;167:2887-94 (Pubitemid 32768923)
15. Thurston G, Suri C, Smith K, McClain J, Sato TN, Yancopoulos GD, et al. Leakage-resistant blood vessels in mice transgenically overexpressing angiopoietin-1. Science 1999;286:2511-14
16. Liu X, Piela-Smith TH. Fibrin(ogen)-induced expression of ICAM-1 and chemokines in human synovial fibroblasts. J Immunol 2000;165:5255-61
17. 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 (Pubitemid 28380578)
18. Liu M, Leibowitz JL, Clark DA, Mendicino M, Ning Q, Ding JW, et al. 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 (Pubitemid 36605577)
19. Chan CW, Kay LS, Khadaroo RG, Chan MW, Lakatoo S, Young KJ, et al. 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 (Pubitemid 36428165)
20. Shalev I, Liu H, Koscik C, Bartczak A, Javadi M, Wong KM, et al. Targeted deletion of fgl2 leads to impaired regulatory T cell activity and development of autoimmune glomerulonephritis. J Immunol 2008;180:249-60
21. Marsden PA, Ning Q, Fung LS, Luo X, Chen Y, Mendicino M, et al. The Fgl2/fibroleukin prothrombinase contributes to immunologically mediated thrombosis in experimental and human viral hepatitis. J Clin Invest 2003;112:58-66 (Pubitemid 38056376)
22. Clark DA, Foerster K, Fung L, He W, Lee L, Mendicino M, et al. The fgl2 prothrombinase/fibroleukin gene is required for lipopolysaccharide- triggered abortions and for normal mouse reproduction. Mol Hum Reprod 2004;10:99-108 (Pubitemid 38196511)
23. Brand DD, Kang AH, Rosloniec EF. Immunopathogenesis of collagen arthritis. Springer Semin Immunopathol 2003;25:3-18 (Pubitemid 37000035)
24. 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 (Pubitemid 15249965)
25. Kurosaka D, Yoshida K, Yasuda J, Yasuda C, Noda K, Furuya K, et al. The effect of endostatin evaluated in an experimental animal model of collagen-induced arthritis. Scand J Rheumatol 2007;36:434-41 (Pubitemid 350293527)
26. 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
27. 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
28. Schmitt-Sody M, Metz P, Klose A, Gottschalk O, Zysk S, Hausdorf J, et al. 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 (Pubitemid 47346919)
29. 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 (Pubitemid 29195833)
30. Myers LK, Rosloniec EF, Cremer MA, Kang AH. Collageninduced arthritis, an animal model of autoimmunity. Life Sci 1997;61:1861-78 (Pubitemid 27461519)
31. Gorczynski RM, Chen Z, Yu K, Hu J. CD200 immunoadhesin suppresses collagen-induced arthritis in mice. Clin Immunol 2001;101:328-34
32. 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 (Pubitemid 39221666)
33. 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
34. 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
35. Rowley MJ, Nandakumar KS, Holmdahl R. The role of collagen antibodies in mediating arthritis. Mod Rheumatol 2008;18:429-41
36. Busso N, Peclat V, Van Ness K, Kolodziesczyk E, Degen J, Bugge T, et al. Exacerbation of antigen-induced arthritis in urokinase- deficient mice. J Clin Invest 1998;102:41-50 (Pubitemid 28323828)
37. Clemmensen I, Holund B, Andersen RB. Fibrin and fibronectin in rheumatoid synovial membrane and rheumatoid synovial fluid. Arthritis Rheum 1983;26:479-85 (Pubitemid 13120236)
38. 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
39. Bokarewa MI, Morrissey JH, Tarkowski A. Tissue factor as a proinflammatory agent. Arthritis Res 2002;4:190-5 (Pubitemid 34460758)
40. Ghanekar A, Mendicino M, Liu H, He W, Liu M, Zhong R, et al. Endothelial induction of fgl2 contributes to thrombosis during acute vascular xenograft rejection. J Immunol 2004;172:5693-701 (Pubitemid 38542073)
41. Mendicino M, Liu M, Ghanekar A, He W, Koscik C, Shalev I, et al. Targeted deletion of Fgl-2/fibroleukin in the donor modulates immunologic response and acute vascular rejection in cardiac xenografts. Circulation 2005;112:248-56 (Pubitemid 40982308)
42. 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
43. Liu M, Mendicino M, Ning Q, Ghanekar A, He W, McGilvray I, et al. 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 (Pubitemid 43787884)
44. Ding JW, Ning Q, Liu MF, Lai A, Leibowitz J, Peltekian KM, et al. Fulminant hepatic failure in murine hepatitis virus strain 3 infection: tissue-specific expression of a novel fgl2 prothrombinase. J Virol 1997;71:9223-30 (Pubitemid 27492364)
45. Li C, Fung LS, Chung S, Crow A, Myers-Mason N, Phillips MJ, et al. Monoclonal antiprothrombinase (3D4.3) prevents mortality from murine hepatitis virus (MHV-3) infection. J Exp Med 1992;176:689-97
46. Boissier MC, Chiocchia G, Bessis N, Hajnal J, Garotta G, Nicoletti F, et al. Biphasic effect of interferon-gamma in murine collagen-induced arthritis. Eur J Immunol 1995;25:1184-90
47. 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
48. Weinberg JB, Wortham TS, Misukonis MA, Patton KL, Chitneni SR. Synovial mononuclear phagocytes in rheumatoid arthritis and osteoarthritis: quantitative and functional aspects. Immunol Invest 1993;22:365-74 (Pubitemid 23218133)
49. Liu H, Shalev I, Manuel J, He W, Leung E, Crookshank J, et al. The FGL2-FcgammaRIIB pathway: a novel mechanism leading to immunosuppression. Eur J Immunol 2008;383114-26
50. Shalev I, Wong KM, Foerster K, Zhu Y, Chan C, Maknojia A, et al. 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
51. 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 (Pubitemid 41541792)
52. 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 (Pubitemid 38780403)
53. 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 (Pubitemid 46745377)
54. Zhou L, Wang H, Zhong X, Jin Y, Mi QS, Sharma A, et al. 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
55. Morgan ME, Sutmuller RP, Witteveen HJ, van Duivenvoorde LM, Zanelli E, Melief CJ, et al. CD25+ cell depletion hastens the onset of severe disease in collagen-induced arthritis. Arthritis Rheum 2003;48:1452-60 (Pubitemid 36554546)
56. Morgan ME, Flierman R, van Duivenvoorde LM, Witteveen HJ, van Ewijk W, van Laar JM, et al. Effective treatment of collageninduced arthritis by adoptive transfer of CD25+ regulatory T cells. Arthritis Rheum 2005;52:2212-21 (Pubitemid 40994344)