Citrullination enhances the pro-inflammatory response to fibrin in rheumatoid arthritis synovial fibroblasts

Annals of the Rheumatic Diseases

Volumn 72, Issue 8, 2013, Pages 1400-1406

  Sanchez Pernaute, Olga ^a,b   Filkova, Maria ^a   Gabucio, Antonio ^b   Klein, Martin ^a   MacIejewska Rodrigues, Hanna ^a   Ospelt, Caroline ^a   Brentano, Fabia ^a   Michel, Beat A ^a   Gay, Renate E ^a   Herrero Beaumont, Gabriel ^b   Gay, Steffen ^a   Neidhart, Michel ^a   Juengel, Astrid ^a  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^b HOSPITAL UNIVERSITARIO FUNDACIÓN JIMÉNEZ DÍAZ   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIGEN; CITRULLINE; CYTOKINE; FIBRIN; INTERLEUKIN 6; INTERLEUKIN 8; MESSENGER RNA; PROTEIN ARGININE DEIMINASE; PROTEIN ARGININE DEIMINASE 2; PROTEIN ARGININE DEIMINASE 4; TOLL LIKE RECEPTOR 4; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ANALYTIC METHOD; ARTICLE; CELL CULTURE; CITRULLINATION; CYTOKINE RELEASE; ENZYME LINKED IMMUNOSORBENT ASSAY; FIBRIN DEPOSITION; FIBROBLAST; GENE EXPRESSION; GENE EXPRESSION PROFILING; HUMAN; MACROMOLECULE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RHEUMATOID ARTHRITIS;

ANT-CCP; CHEMOKINES; FIBROBLASTS; RHEUMATOID ARTHRITIS;

ARTHRITIS, RHEUMATOID; CELL SURVIVAL; CELLS, CULTURED; CITRULLINE; CYTOKINES; FIBRIN; FIBROBLASTS; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; HUMANS; HYDROLASES; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RECOMBINANT PROTEINS; RNA, MESSENGER; RNA, SMALL INTERFERING; SYNOVIAL MEMBRANE; TOLL-LIKE RECEPTORS; UP-REGULATION;

EID: 84880135608     PISSN: 00034967     EISSN: 14682060     Source Type: Journal    
DOI: 10.1136/annrheumdis-2012-201906     Document Type: Article

References (49)

1. Ishikawa H, Hirata S, Andoh Y, et al. An immunohistochemical and immunoelectron microscopic study of adhesion molecules in synovial pannus formation in rheumatoid arthritis. Rheumatol Int 1996;16:53-60. (Pubitemid 26318575)
2. 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.
3. 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)
4. Konttinen YT, Bergroth V, Nordstrom D, et al. Cellular immunohistopathology of acute, subacute, and chronic synovitis in rheumatoid arthritis. Ann Rheum Dis 1985;44:549-55. (Pubitemid 15001296)
5. Schumacher HR, Kitridou RC. Synovitis of recent onset. A clinicopathologic study during the first month of disease. Arthritis Rheum 1972;15:465-85.
6. Sanchez-Pernaute O, Largo R, Calvo E, et al. A fibrin based model for rheumatoid synovitis. Ann Rheum Dis 2003;62:1135-8. (Pubitemid 37500617)
7. Sanchez-Pernaute O, Lopez-Armada MJ, Calvo E, et al. Fibrin generated in the synovial fluid activates intimal cells from their apical surface: a sequential morphological study in antigen-induced arthritis. Rheumatology (Oxford) 2003;42:19-25. (Pubitemid 36131562)
8. Altieri DC, Agbanyo FR, Plescia J, et al. A unique recognition site mediates the interaction of fibrinogen with the leukocyte integrin Mac-1 (CD11b/CD18). J Biol Chem 1990;265:12119-2.
9. Rubel C, Gomez S, Fernandez GC, et al. Fibrinogen-CD11b/CD18 interaction activates the NF-kappa B pathway and delays apoptosis in human neutrophils. Eur J Immunol 2003;33:1429-38. (Pubitemid 36609162)
10. Flick MJ, LaJeunesse CM, Talmage KE, 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)
11. Szaba FM, Smiley ST. Roles for thrombin and fibrin(ogen) in cytokine/chemokine production and macrophage adhesion in vivo. Blood 2002;99:1053-9. (Pubitemid 34525570)
12. Smiley ST, King JA, Hancock WW. Fibrinogen stimulates macrophage chemokine secretion through toll-like receptor 4. J Immunol 2001;167:2887-94. (Pubitemid 32768923)
13. Sokolove J, Zhao X, Chandra PE, et al. Immune complexes containing citrullinated fibrinogen costimulate macrophages via Toll-like receptor 4 and Fcgamma receptor. Arthritis Rheum 2011;63:53-62.
14. Honda K, Taniguchi T. Toll-like receptor signaling and IRF transcription factors. IUBMB Life 2006;58:290-5. (Pubitemid 43880018)
15. Bianchi ME. DAMPs, PAMPs and alarmins: all we need to know about danger. J Leukoc Biol 2007;81:1-5. (Pubitemid 46028489)
16. Sacre SM, Andreakos E, Kiriakidis S, et al. The Toll-like receptor adaptor proteins MyD88 and Mal/TIRAP contribute to the inflammatory and destructive processes in a human model of rheumatoid arthritis. Am J Pathol 2007;170:518-25. (Pubitemid 47339389)
17. Choe JY, Crain B, Wu SR, et al. Interleukin 1 receptor dependence of serum transferred arthritis can be circumvented by toll-like receptor 4 signaling. J Exp Med 2003;197:537-42. (Pubitemid 36278608)
18. Joosten LA, Koenders MI, Smeets RL, et al. Toll-like receptor 2 pathway drives streptococcal cell wall-induced joint inflammation: critical role of myeloid differentiation factor 88. J Immunol 2003;171:6145-53. (Pubitemid 37467237)
19. Abdollahi-Roodsaz S, Joosten LA, Roelofs MF, et al. Inhibition of Toll-like receptor 4 breaks the inflammatory loop in autoimmune destructive arthritis. Arthritis Rheum 2007;56:2957-67. (Pubitemid 47502742)
20. Sebbag M, Chapuy-Regaud S, Auger I, et al. Clinical and pathophysiological significance of the autoimmune response to citrullinated proteins in rheumatoid arthritis. Joint Bone Spine 2004;71:493-502. (Pubitemid 39626716)
21. Masson-Bessiere C, Sebbag M, Girbal-Neuhauser E, et al. The major synovial targets of the rheumatoid arthritis-specific antifilaggrin autoantibodies are deiminated forms of the alpha- and beta-chains of fibrin. J Immunol 2001;166:4177-84. (Pubitemid 32224951)
22. Vossenaar ER, Smeets TJ, Kraan MC, et al. The presence of citrullinated proteins is not specific for rheumatoid synovial tissue. Arthritis Rheum 2004;50:3485-94. (Pubitemid 39488673)
23. Vallbracht I, Rieber J, Oppermann M, et al. Diagnostic and clinical value of anti-cyclic citrullinated peptide antibodies compared with rheumatoid factor isotypes in rheumatoid arthritis. Ann Rheum Dis 2004;63:1079-84. (Pubitemid 39120358)
24. Forslind K, Ahlmen M, Eberhardt K, et al. Prediction of radiological outcome in early rheumatoid arthritis in clinical practice: role of antibodies to citrullinated peptides (anti-CCP). Ann Rheum Dis 2004;63:1090-5. (Pubitemid 39120360)
25. Zhao X, Okeke NL, Sharpe O, et al. Circulating immune complexes contain citrullinated fibrinogen in rheumatoid arthritis. Arthritis Res Ther 2008;10:R94.
26. Qi J, Goralnick S, Kreutzer DL. Fibrin regulation of interleukin-8 gene expression in human vascular endothelial cells. Blood 1997;90:3595-602. (Pubitemid 27473429)
27. Shin H, Katajima I, Nakajima T, et al. Thrombin receptor mediated signals induce expressions of interleukin 6 and granulocyte colony stimulating factor via NF-kappa B activation in synovial fibroblasts. Ann Rheum Dis 1999;58:55-60. (Pubitemid 29112951)
28. Vossenaar ER, Nijenhuis S, Helsen MM, et al. Citrullination of synovial proteins in murine models of rheumatoid arthritis. Arthritis Rheum 2003;48:2489-500. (Pubitemid 37129426)
29. Liu X, Piela-Smith TH. Fibrin(ogen)-induced expression of ICAM-1 and chemokines in human synovial fibroblasts. J Immunol 2000;165:5255-61.
30. Bini A, Wu D, Schnuer J, et al. Characterization of stromelysin 1 (MMP-3), matrilysin (MMP-7), and membrane type 1 matrix metalloproteinase (MT1-MMP) derived fibrin(ogen) fragments D-dimer and D-like monomer: NH2-terminal sequences of late-stage digest fragments. Biochemistry 1999;38:13928-6. (Pubitemid 29504224)
31. Shainoff JR, Stearns DJ, DiBello PM, et al. Characterization of a mode of specific binding of fibrin monomer through its amino-terminal domain by macrophages and macrophage cell-lines. Thromb Haemost 1990;63:193-203. (Pubitemid 20128181)
32. Alves CS, Burdick MM, Thomas SN, et al. The dual role of CD44 as a functional P-selectin ligand and fibrin receptor in colon carcinoma cell adhesion. Am J Physiol Cell Physiol 2008;294:C907-16. (Pubitemid 351507918)
33. Del Villar K, Miller CA. Down-regulation of DENN/MADD, a TNF receptor binding protein, correlates with neuronal cell death in Alzheimer's disease brain and hippocampal neurons. Proc Natl Acad Sci USA 2004;101:4210-5. (Pubitemid 38405908)
34. Oda K, Kitano H. A comprehensive map of the toll-like receptor signaling network. Mol Syst Biol 2006;2:2006.0015.
35. Brentano F, Kyburz D, Schorr O, et al. The role of Toll-like receptor signalling in the pathogenesis of arthritis. Cell Immunol 2005;233:90-6. (Pubitemid 41074060)
36. Midwood K, Sacre S, Piccinini AM, et al. Tenascin-C is an endogenous activator of Toll-like receptor 4 that is essential for maintaining inflammation in arthritic joint disease. Nat Med 2009;15:774-80.
37. Kuhns DB, Priel DA, Gallin JI. Induction of human monocyte interleukin (IL)-8 by fibrinogen through the toll-like receptor pathway. Inflammation 2007;30: 178-88. (Pubitemid 47573147)
38. Barrera V, Skorokhod OA, Baci D, et al. Host fibrinogen stably bound to hemozoin rapidly activates monocytes via TLR-4 and CD11b/CD18-integrin: a new paradigm of hemozoin action. Blood 2011;117:5674-82.
39. Sorensen I, Susnik N, Inhester T, et al. Fibrinogen, acting as a mitogen for tubulointerstitial fibroblasts, promotes renal fibrosis. Kidney Int 2011;80: 1035-44.
40. Motojima M, Matsusaka T, Kon V, et al. Fibrinogen that appears in Bowman's space of proteinuric kidneys in vivo activates podocyte Toll-like receptors 2 and 4 in vitro. Nephron Exp Nephrol 2010;114:e39-47.
41. Chun KH, Seong SY. CD14 but not MD2 transmit signals from DAMP. Int Immunopharmacol 2010;10:98-106.
42. Fan L, He D, Wang Q, et al. Citrullinated vimentin stimulates proliferation, pro-inflammatory cytokine secretion, and PADI4 and RANKL expression of fibroblast-like synoviocytes in rheumatoid arthritis. Scand J Rheumatol 2012;41:354-8.
43. Proost P, Loos T, Mortier A, et al. Citrullination of CXCL8 by peptidylarginine deiminase alters receptor usage, prevents proteolysis, and dampens tissue inflammation. J Exp Med 2008;205:2085-97.
44. Mortier A, Loos T, Gouwy M, et al. Posttranslational modification of the NH2-terminal region of CXCL5 by proteases or peptidylarginine Deiminases (PAD) differently affects its biological activity. J Biol Chem 2010;285:29750-9.
45. Sebbag M, Moinard N, Auger I, et al. Epitopes of human fibrin recognized by the rheumatoid arthritis-specific autoantibodies to citrullinated proteins. Eur J Immunol 2006;36:2250-63. (Pubitemid 44251769)
46. Okumura N, Haneishi A, Terasawa F. Citrullinated fibrinogen shows defects in FPA and FPB release and fibrin polymerization catalyzed by thrombin. Clin Chim Acta 2009;401:119-23.
47. Foulquier C, Sebbag M, Clavel C, et al. Peptidyl arginine deiminase type 2 (PAD-2) and PAD-4 but not PAD-1, PAD-3, and PAD-6 are expressed in rheumatoid arthritis synovium in close association with tissue inflammation. Arthritis Rheum 2007;56:3541-3.
48. van Beers JJ, Raijmakers R, Alexander LE, et al. Mapping of citrullinated fibrinogen B-cell epitopes in rheumatoid arthritis by imaging surface plasmon resonance. Arthritis Res Ther 2010;12:R219.
49. Darrah E, Rosen A, Giles JT, et al. Peptidylarginine deiminase 2, 3 and 4 have distinct specificities against cellular substrates: novel insights into autoantigen selection in rheumatoid arthritis. Ann Rheum Dis 2012;71:92-8.