Triggering of the dsRNA sensors TLR3, MDA5, and RIG-I induces CD55 expression in synovial fibroblasts

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Karpus, Olga N ^a   Heutinck, Kirstin M ^a   Wijnker, Paul J M ^a   Tak, Paul P ^b   Hamann, Jörg ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CD97 ANTIGEN; CYTOKINE; DECAY ACCELERATING FACTOR; DISEASE MODIFYING ANTIRHEUMATIC DRUG; DOUBLE STRANDED RNA; INTERLEUKIN 1BETA; MELANOMA DIFFERENTIATION ASSOCIATED PROTEIN 5; METHOTREXATE; NONSTEROID ANTIINFLAMMATORY AGENT; POLYINOSINIC POLYCYTIDYLIC ACID; RETINOIC ACID INDUCIBLE PROTEIN I; TOLL LIKE RECEPTOR 3; UNCLASSIFIED DRUG; CD97 PROTEIN, HUMAN; DDX58 PROTEIN, HUMAN; DEAD BOX PROTEIN; IFIH1 PROTEIN, HUMAN; IL1B PROTEIN, HUMAN; INTERFERON INDUCING AGENT; LEUKOCYTE ANTIGEN; TLR3 PROTEIN, HUMAN;

ADULT; AGED; ARTICLE; CELL DEATH; CELL ISOLATION; CELL VIABILITY; CLINICAL ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME REGULATION; FEMALE; FIBROBLAST; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; OSTEOARTHRITIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PSORIATIC ARTHRITIS; RHEUMATOID ARTHRITIS; SPONDYLARTHRITIS; SYNOVIOCYTE; ARTHRITIS; BIOSYNTHESIS; CELL COMMUNICATION; CELL CULTURE; CLINICAL TRIAL; DRUG EFFECT; IMMUNOLOGY; LEUKOCYTE; METABOLISM; MIDDLE AGED; PATHOLOGY; SYNOVIUM; UPREGULATION;

ADULT; AGED; AGED, 80 AND OVER; ANTIGENS, CD; ANTIGENS, CD55; ARTHRITIS; CELL COMMUNICATION; CELLS, CULTURED; DEAD-BOX RNA HELICASES; FEMALE; FIBROBLASTS; HUMANS; INTERFERON INDUCERS; INTERLEUKIN-1BETA; LEUKOCYTES; MALE; MIDDLE AGED; POLY I-C; RNA, DOUBLE-STRANDED; SYNOVIAL MEMBRANE; TOLL-LIKE RECEPTOR 3; UP-REGULATION;

EID: 84861012395     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0035606     Document Type: Article

References (58)

1. Tak PP, Bresnihan B, (2000) The pathogenesis and prevention of joint damage in rheumatoid arthritis: advances from synovial biopsy and tissue analysis. Arthritis Rheum 43: 2619-2633.
2. Noss EH, Brenner MB, (2008) The role and therapeutic implications of fibroblast-like synoviocytes in inflammation and cartilage erosion in rheumatoid arthritis. Immunol Rev 223: 252-270.
3. Bartok B, Firestein GS, (2010) Fibroblast-like synoviocytes: key effector cells in rheumatoid arthritis. Immunol Rev 233: 233-255.
4. Neumann E, Lefevre S, Zimmermann B, Gay S, Muller-Ladner U, (2010) Rheumatoid arthritis progression mediated by activated synovial fibroblasts. Trends Mol Med 16: 458-468.
5. Medof ME, Walter EI, Rutgers JL, Knowles DM, Nussenzweig V, (1987) Identification of the complement decay-accelerating factor (DAF) on epithelium and glandular cells and in body fluids. J Exp Med 165: 848-864.
6. Stevens CR, Mapp PI, Revell PA, (1990) A monoclonal antibody (Mab 67) marks type B synoviocytes. Rheumatol Int 10: 103-106.
7. Edwards JC, Wilkinson LS, (1996) Distribution in human tissues of the synovial lining-associated epitope recognised by monoclonal antibody 67. J Anat 188: 119-127.
8. Lublin DM, Atkinson JP, (1989) Decay-accelerating factor: biochemistry, molecular biology, and function. Annu Rev Immunol 7: 35-58.
9. Song WC, (2006) Complement regulatory proteins and autoimmunity. Autoimmunity 39: 403-410.
10. Hamann J, Eichler W, Hamann D, Kerstens HM, Poddighe PJ, et al. (1995) Expression cloning and chromosomal mapping of the leukocyte activation antigen CD97, a new seven-span transmembrane molecule of the secretion receptor superfamily with an unusual extracellular domain. J Immunol 155: 1942-1950.
11. Hamann J, Vogel B, van Schijndel GMW, van Lier RAW, (1996) The seven-span transmembrane receptor CD97 has a cellular ligand (CD55, DAF). J Exp Med 184: 1185-1189.
12. Eichler W, Hamann J, Aust G, (1997) Expression characteristics of the human CD97 antigen. Tissue Antigens 50: 429-438.
13. Lin HH, Stacey M, Saxby C, Knott V, Chaudhry Y, et al. (2001) Molecular analysis of the epidermal growth factor-like short consensus repeat domain-mediated protein-protein interactions: dissection of the CD97-CD55 complex. J Biol Chem 276: 24160-24169.
14. Yona S, Lin HH, Siu WO, Gordon S, Stacey M, (2008) Adhesion-GPCRs: emerging roles for novel receptors. Trends Biochem Sci 33: 491-500.
15. Hamann J, Wishaupt JO, van Lier RA, Smeets TJ, Breedveld FC, et al. (1999) Expression of the activation antigen CD97 and its ligand CD55 in rheumatoid synovial tissue. Arthritis Rheum 42: 650-658.
16. Kop EN, Kwakkenbos MJ, Teske GJ, Kraan MC, Smeets TJ, et al. (2005) Identification of the epidermal growth factor-TM7 receptor EMR2 and its ligand dermatan sulfate in rheumatoid synovial tissue. Arthritis Rheum 52: 442-450.
17. Hoek RM, de Launay D, Kop EN, Yilmaz-Elis AS, Lin F, et al. (2010) Deletion of either CD55 or CD97 ameliorates arthritis in mouse models. Arthritis Rheum 62: 1036-1042.
18. Gerlag DM, Tak PP, (2009) How to perform and analyse synovial biopsies. Best Pract Res Clin Rheumatol 23: 221-232.
19. Arnett FC, Edworthy SM, Bloch DA, McShane DJ, Fries JF, et al. (1988) The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum 31: 315-324.
20. Dougados M, van der Linden S, Juhlin R, Huitfeldt B, Amor B, et al. (1991) The European Spondylarthropathy Study Group preliminary criteria for the classification of spondylarthropathy. Arthritis Rheum 34: 1218-1227.
21. Taylor W, Gladman D, Helliwell P, Marchesoni A, Mease P, et al. (2006) Classification criteria for psoriatic arthritis: development of new criteria from a large international study. Arthritis Rheum 54: 2665-2673.
22. Altman R, Asch E, Bloch D, Bole G, Borenstein D, et al. (1986) Development of criteria for the classification and reporting of osteoarthritis. Classification of osteoarthritis of the knee. Diagnostic and Therapeutic Criteria Committee of the American Rheumatism Association. Arthritis Rheum 29: 1039-1049.
23. Stacey M, Chang GW, Sanos SL, Chittenden LR, Stubbs L, et al. (2002) EMR4, a novel epidermal growth factor (EGF)-TM7 molecule up-regulated in activated mouse macrophages, binds to a putative cellular ligand on B lymphoma cell line A20. J Biol Chem 277: 29283-29293.
24. Takeuchi O, Akira S, (2010) Pattern recognition receptors and inflammation. Cell 140: 805-820.
25. Imaizumi T, Tanaka H, Matsumiya T, Yoshida H, Tanji K, et al. (2010) Retinoic acid-inducible gene-I is induced by double-stranded RNA and regulates the expression of CC chemokine ligand (CCL) 5 in human mesangial cells. Nephrol Dial Transplant 25: 3534-3539.
26. Kariko K, Ni H, Capodici J, Lamphier M, Weissman D, (2004) mRNA is an endogenous ligand for Toll-like receptor 3. J Biol Chem 279: 12542-12550.
27. Heutinck KM, Kassies J, Florquin S, ten Berge IJ, Hamann J, et al. (2012) SerpinB9 expression in human renal tubular epithelial cells is induced by triggering of the viral dsRNA sensors TLR3, MDA5 and RIG-I. Nephrol Dial Transplant 27.
28. Halme J, Sachse M, Vogel H, Giese T, Klar E, et al. (2009) Primary human hepatocytes are protected against complement by multiple regulators. Mol Immunol 46: 2284-2289.
29. Ahmad SR, Lidington EA, Ohta R, Okada N, Robson MG, et al. (2003) Decay-accelerating factor induction by tumour necrosis factor-alpha, through a phosphatidylinositol-3 kinase and protein kinase C-dependent pathway, protects murine vascular endothelial cells against complement deposition. Immunology 110: 258-268.
30. Tak PP, Smeets TJ, Daha MR, Kluin PM, Meijers KA, et al. (1997) Analysis of the synovial cell infiltrate in early rheumatoid synovial tissue in relation to local disease activity. Arthritis Rheum 40: 217-225.
31. Hyc A, Osiecka-Iwan A, Strzelczyk P, Moskalewski S, (2003) Effect of IL-1beta, TNF-alpha and IL-4 on complement regulatory protein mRNA expression in human articular chondrocytes. Int J Mol Med 11: 91-94.
32. Nasu J, Mizuno M, Uesu T, Takeuchi K, Inaba T, et al. (1998) Cytokine-stimulated release of decay-accelerating factor (DAF;CD55) from HT-29 human intestinal epithelial cells. Clin Exp Immunol 113: 379-385.
33. Spiller OB, Criado-Garcia O, Rodriguez De CS, Morgan BP, (2000) Cytokine-mediated up-regulation of CD55 and CD59 protects human hepatoma cells from complement attack. Clin Exp Immunol 121: 234-241.
34. Farina GA, York MR, Di MM, Collins CA, Meller S, et al. (2010) Poly(I:C) drives type I IFN- and TGFbeta-mediated inflammation and dermal fibrosis simulating altered gene expression in systemic sclerosis. J Invest Dermatol 130: 2583-2593.
35. Brentano F, Schorr O, Gay RE, Gay S, Kyburz D, (2005) RNA released from necrotic synovial fluid cells activates rheumatoid arthritis synovial fibroblasts via Toll-like receptor 3. Arthritis Rheum 52: 2656-2665.
36. Lundberg AM, Drexler SK, Monaco C, Williams LM, Sacre SM, et al. (2007) Key differences in TLR3/poly I:C signaling and cytokine induction by human primary cells: a phenomenon absent from murine cell systems. Blood 110: 3245-3252.
37. Ospelt C, Brentano F, Rengel Y, Stanczyk J, Kolling C, et al. (2008) Overexpression of toll-like receptors 3 and 4 in synovial tissue from patients with early rheumatoid arthritis: toll-like receptor expression in early and longstanding arthritis. Arthritis Rheum 58: 3684-3692.
38. Imaizumi T, Arikawa T, Sato T, Uesato R, Matsumiya T, et al. (2008) Involvement of retinoic acid-inducible gene-I in inflammation of rheumatoid fibroblast-like synoviocytes. Clin Exp Immunol 153: 240-244.
39. Carrion M, Juarranz Y, Perez-Garcia S, Jimeno R, Pablos JL, et al. (2011) RNA sensors in human osteoarthritic and rheumatoid synovial fibroblasts. Immune regulation by vasoactive intestinal peptide. Arthritis Rheum 63: 1626-1636.
40. Paone A, Starace D, Galli R, Padula F, De Cesaris P, et al. (2008) Toll-like receptor 3 triggers apoptosis of human prostate cancer cells through a PKC-alpha-dependent mechanism. Carcinogenesis 29: 1334-1342.
41. Peng S, Geng J, Sun R, Tian Z, Wei H, (2009) Polyinosinic-polycytidylic acid liposome induces human hepatoma cells apoptosis which correlates to the up-regulation of RIG-I like receptors. Cancer Sci 100: 529-536.
42. Besch R, Poeck H, Hohenauer T, Senft D, Hacker G, et al. (2009) Proapoptotic signaling induced by RIG-I and MDA-5 results in type I interferon-independent apoptosis in human melanoma cells. J Clin Invest 119: 2399-2411.
43. Weber A, Kirejczyk Z, Besch R, Potthoff S, Leverkus M, et al. (2010) Proapoptotic signalling through Toll-like receptor-3 involves TRIF-dependent activation of caspase-8 and is under the control of inhibitor of apoptosis proteins in melanoma cells. Cell Death Differ 17: 942-951.
44. Tormo D, Checinska A, Alonso-Curbelo D, Perez-Guijarro E, Canon E, et al. (2009) Targeted activation of innate immunity for therapeutic induction of autophagy and apoptosis in melanoma cells. Cancer Cell 16: 103-114.
45. Heutinck KM, Rowshani AT, Kassies J, Claessen N, Bemelman FJ, et al. (2012) The viral dsRNA sensors TLR3, MDA5 and RIG-I incuce anti-viral, pro-inflammatory and pro-apoptotic responses in human renal tubular epithelial cells. Kidney Int 82.
46. Lallemand C, Blanchard B, Palmieri M, Lebon P, May E, et al. (2007) Single-stranded RNA viruses inactivate the transcriptional activity of p53 but induce NOXA-dependent apoptosis via post-translational modifications of IRF-1, IRF-3 and CREB. Oncogene 26: 328-338.
47. Cha HS, Rosengren S, Boyle DL, Firestein GS, (2006) PUMA regulation and proapoptotic effects in fibroblast-like synoviocytes. Arthritis Rheum 54: 587-592.
48. Dinarello CA, (2011) Interleukin-1 in the pathogenesis and treatment of inflammatory diseases. Blood 117: 3720-3732.
49. Stahl HD, Hubner B, Seidl B, Liebert UG, van der Heijden IM, et al. (2000) Detection of multiple viral DNA species in synovial tissue and fluid of patients with early arthritis. Ann Rheum Dis 59: 342-346.
50. Munz C, Lunemann JD, Getts MT, Miller SD, (2009) Antiviral immune responses: triggers of or triggered by autoimmunity? Nat Rev Immunol 9: 246-258.
51. Becker J, Winthrop KL, (2010) Update on rheumatic manifestations of infectious diseases. Curr Opin Rheumatol 22: 72-77.
52. Kariko K, Ni H, Capodici J, Lamphier M, Weissman D, (2004) mRNA is an endogenous ligand for Toll-like receptor 3. J Biol Chem 279: 12542-12550.
53. Cavassani KA, Ishii M, Wen H, Schaller MA, Lincoln PM, et al. (2008) TLR3 is an endogenous sensor of tissue necrosis during acute inflammatory events. J Exp Med 205: 2609-2621.
54. Lai Y, Di Nardo A, Nakatsuji T, Leichtle A, Yang Y, et al. (2009) Commensal bacteria regulate Toll-like receptor 3-dependent inflammation after skin injury. Nat Med 15: 1377-1382.
55. Zimmermann B, Fischer S, Stürz H, Rehart S, Lehr A, et al. (2012) Expression of extracellular RNA in synovial tissue and RNase activity in synovial fluid of rheumatoid arthritis patients. Ann Rheum Dis 71: A89.
56. Wang Y, Zhang HX, Sun YP, Liu ZX, Liu XS, et al. (2007) Rig-I-/- mice develop colitis associated with downregulation of G alpha i2. Cell Res 17: 858-868.
57. Dann A, Poeck H, Croxford AL, Gaupp S, Kierdorf K, et al. (2012) Cytosolic RIG-I-like helicases act as negative regulators of sterile inflammation in the CNS. Nat Neurosci 15: 98-106.
58. Buckley CD, (2011) Why does chronic inflammation persist: An unexpected role for fibroblasts. Immunol Lett 138: 12-14.