Decoy receptor 3 attenuates collagen-induced arthritis by modulating T cell activation and B cell expansion

Journal of Rheumatology

Volumn 38, Issue 12, 2011, Pages 2522-2535

  Cheng, Chia Pi ^a   Sytwu, Huey Kang ^a   Chang, Deh Ming ^b  

^a NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

^b TRI SERVICE GENERAL HOSPITAL   (Taiwan)

Author keywords

B cell expansion; Collagen induced arthritis; Decoy receptor 3; T cell activation

Indexed keywords

COLLAGEN; COLLAGEN TYPE 2; DECOY RECEPTOR 3; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G2A; IMMUNOGLOBULIN G2A ANTIBODY; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 1ALPHA; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; PLASMID DNA; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 2; TRANSCRIPTION FACTOR FOXP3; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTHROPOMETRIC PARAMETERS; ANTIBODY BLOOD LEVEL; ARTICLE; B LYMPHOCYTE; CARBOXYFLUORESCEIN SUCCINIMIDYL ESTER ASSAY; CD19+ B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL ASSAY; CELL EXPANSION; CELL POPULATION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE SEVERITY; ENZYME LINKED IMMUNOSORBENT ASSAY; EXPERIMENTAL MODEL; FLOW CYTOMETRY; HYDRODYNAMICS BASED TRANSFECTION; HYPERPLASIA; IMMUNIZATION; IMMUNOGLOBULIN BLOOD LEVEL; IMMUNOHISTOCHEMISTRY; IMMUNOMODULATION; IN VITRO STUDY; IN VIVO STUDY; INGUINAL LYMPH NODE; LYMPHOCYTE; LYMPHOCYTE PROLIFERATION; MALE; MOUSE; NONHUMAN; PAW THICKNESS; PLASMID; PRIORITY JOURNAL; PROTECTION; PROTEIN ANALYSIS; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RHEUMATOID ARTHRITIS; SCORING SYSTEM; SPLEEN CELL; SYNOVIUM; T LYMPHOCYTE ACTIVATION; TH1 CELL; TH17 CELL; TH2 CELL;

ANIMALS; ARTHRITIS, EXPERIMENTAL; AUTOANTIBODIES; B-LYMPHOCYTES; COLLAGEN TYPE II; CYTOKINES; IMMUNOGLOBULIN G; LYMPH NODES; LYMPHOCYTE ACTIVATION; MALE; MICE; MICE, INBRED DBA; RECEPTORS, TUMOR NECROSIS FACTOR, MEMBER 6B; SPLEEN; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES;

EID: 82755162911     PISSN: 0315162X     EISSN: 14992752     Source Type: Journal    
DOI: 10.3899/jrheum.110245     Document Type: Article

References (55)

1. Aletaha D, Neogi T, Silman AJ, Funovits J, Felson DT, Bingham CO 3rd, et al. 2010 rheumatoid arthritis classification criteria: an American College of Rheumatology/European League Against Rheumatism collaborative initiative. Ann Rheum Dis 2010;69:1580-8.
2. 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.
3. Del Nagro CJ, Kolla RV, Rickert RC. A critical role for complement C3d and the B cell coreceptor (CD19/CD21) complex in the initiation of inflammatory arthritis. J Immunol 2005;175:5379-89. (Pubitemid 41456424)
4. Doncarli A, Stasiuk LM, Fournier C, Abehsira-Amar O. Conversion in vivo from an early dominant Th0/Th1 response to a Th2 phenotype during the development of collagen-induced arthritis. Eur J Immunol 1997;27:1451-8. (Pubitemid 27254838)
5. 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;204:41-7. (Pubitemid 46148754)
6. Ranges GE, Sriram S, Cooper SM. Prevention of type II collagen-induced arthritis by in vivo treatment with anti-L3T4. J Exp Med 1985;162:1105-10. (Pubitemid 16248214)
7. Svensson L, Jirholt J, Holmdahl R, Jansson L. B cell-deficient mice do not develop type II collagen-induced arthritis (CIA). Clin Exp Immunol 1998;111:521-6. (Pubitemid 28160894)
8. Hughes C, Wolos JA, Giannini EH, Hirsch R. Induction of T helper cell hyporesponsiveness in an experimental model of autoimmunity by using nonmitogenic anti-CD3 monoclonal antibody. J Immunol 1994;153:3319-25. (Pubitemid 24292558)
9. Yanaba K, Hamaguchi Y, Venturi GM, Steeber DA, St. Clair EW, Tedder TF. B cell depletion delays collagen-induced arthritis in mice: arthritis induction requires synergy between humoral and cell-mediated immunity. J Immunol 2007;179:1369-80.
10. Ashkenazi A. Targeting death and decoy receptors of the tumour-necrosis factor superfamily. Nat Rev Cancer 2002;2:420-30. (Pubitemid 37328939)
11. Migone TS, Zhang J, Luo X, Zhuang L, Chen C, Hu B, et al. TL1A is a TNF-like ligand for DR3 and TR6/DcR3 and functions as a T cell costimulator. Immunity 2002;16:479-92. (Pubitemid 34260924)
12. Yu KY, Kwon B, Ni J, Zhai Y, Ebner R, Kwon BS. A newly identified member of tumor necrosis factor receptor superfamily (TR6) suppresses LIGHT-mediated apoptosis. J Biol Chem 1999;274:13733-6.
13. Pitti RM, Marsters SA, Lawrence DA, Roy M, Kischkel FC, Dowd P, et al. Genomic amplification of a decoy receptor for Fas ligand in lung and colon cancer. Nature 1998;396:699-703. (Pubitemid 29003951)
14. Zhang J, Salcedo TW, Wan X, Ullrich S, Hu B, Gregorio T, et al. Modulation of T-cell responses to alloantigens by TR6/DcR3. J Clin Invest 2001;107:1459-68. (Pubitemid 32522040)
15. Roth W, Isenmann S, Nakamura M, Platten M, Wick W, Kleihues P, et al. Soluble decoy receptor 3 is expressed by malignant gliomas and suppresses CD95 ligand-induced apoptosis and chemotaxis. Cancer Res 2001;61:2759-65. (Pubitemid 32685866)
16. Bai C, Connolly B, Metzker ML, Hilliard CA, Liu X, Sandig V, et al. Overexpression of M68/DcR3 in human gastrointestinal tract tumors independent of gene amplification and its location in a four-gene cluster. Proc Natl Acad Sci USA 2000;97:1230-5. (Pubitemid 30080841)
17. Sung HH, Juang JH, Lin YC, Kuo CH, Hung JT, Chen A, et al. Transgenic expression of decoy receptor 3 protects islets from spontaneous and chemical-induced autoimmune destruction in nonobese diabetic mice. J Exp Med 2004;199:1143-51. (Pubitemid 38619910)
18. Ka SM, Sytwu HK, Chang DM, Hsieh SL, Tsai PY, Chen A. Decoy receptor 3 ameliorates an autoimmune crescentic glomerulonephritis model in mice. J Am Soc Nephrol 2007;18:2473-85. (Pubitemid 47378864)
19. Mueller AM, Pedre X, Killian S, David M, Steinbrecher A. The decoy receptor 3 (DcR3, TNFRSF6B) suppresses Th17 immune responses and is abundant in human cerebrospinal fluid. J Neuroimmunol 2009;209:57-64.
20. Chen SJ, Wang YL, Kao JH, Wu SF, Lo WT, Wu CC, et al. Decoy receptor 3 ameliorates experimental autoimmune encephalomyelitis by directly counteracting local inflammation and downregulating Th17 cells. Mol Immunol 2009;47:567-74.
21. Yang CR, Wang JH, Hsieh SL, Wang SM, Hsu TL, Lin WW. Decoy receptor 3 (DcR3) induces osteoclast formation from monocyte/macrophage lineage precursor cells. Cell Death Differ 2004;11 Suppl 1:S97-107.
22. Wu SF, Liu TM, Lin YC, Sytwu HK, Juan HF, Chen ST, et al. Immunomodulatory effect of decoy receptor 3 on the differentiation and function of bone marrow-derived dendritic cells in nonobese diabetic mice: from regulatory mechanism to clinical implication. J Leukoc Biol 2004;75:293-306.
23. Hayashi S, Miura Y, Nishiyama T, Mitani M, Tateishi K, Sakai Y, et al. Decoy receptor 3 expressed in rheumatoid synovial fibroblasts protects the cells against Fas-induced apoptosis. Arthritis Rheum 2007;56:1067-75. (Pubitemid 46608631)
24. Bamias G, Siakavellas SI, Stamatelopoulos KS, Chryssochoou E, Papamichael C, Sfikakis PP. Circulating levels of TNF-like cytokine 1A (TL1A) and its decoy receptor 3 (DcR3) in rheumatoid arthritis. Clin Immunol 2008;129:249-55.
25. Rosloniec EF, Cremer M, Kang A, Myers LK, Brand DD. Collagen-induced arthritis. Curr Protoc Immunol 2010;15:1-25.
26. Brand DD, Latham KA, Rosloniec EF. Collagen-induced arthritis. Nat Protoc 2007;2:1269-75. (Pubitemid 46901304)
27. Liu F, Song Y, Liu D. Hydrodynamics-based transfection in animals by systemic administration of plasmid DNA. Gene Ther 1999;6:1258-66. (Pubitemid 29359019)
28. Baharav E, Bar-Yehuda S, Madi L, Silberman D, Rath-Wolfson L, Halpren M, et al. Antiinflammatory effect of A3 adenosine receptor agonists in murine autoimmune arthritis models. J Rheumatol 2005;32:469-76. (Pubitemid 40381417)
29. Kamel OW, van de Rijn M, Weiss LM, Del Zoppo GJ, Hench PK, Robbins BA, et al. Brief report: reversible lymphomas associated with Epstein-Barr virus occurring during methotrexate therapy for rheumatoid arthritis and dermatomyositis. N Engl J Med 1993;328:1317-21. (Pubitemid 23131374)
30. Symmons DP, Ahern M, Bacon PA, Hawkins CF, Amlot PL, Jones EL, et al. Lymphoproliferative malignancy in rheumatoid arthritis: a study of 20 cases. Ann Rheum Dis 1984;43:132-5. (Pubitemid 14125171)
31. Tada Y, Ho A, Koh DR, Mak TW. Collagen-induced arthritis in CD4- or CD8-deficient mice: CD8+ T cells play a role in initiation and regulate recovery phase of collagen-induced arthritis. J Immunol 1996;156:4520-6. (Pubitemid 26165856)
32. Kelchtermans H, De Klerck B, Mitera T, Van Balen M, Bullens D, Billiau A, et al. Defective CD4+CD25+ regulatory T cell functioning in collagen-induced arthritis: an important factor in pathogenesis, counter-regulated by endogenous IFN-gamma. Arthritis Res Ther 2005;7:R402-15.
33. Wooley PH, Luthra HS, Krco CJ, Stuart JM, David CS. Type II collagen-induced arthritis in mice. II. Passive transfer and suppression by intravenous injection of anti-type II collagen antibody or free native type II collagen. Arthritis Rheum 1984; 27:1010-7. (Pubitemid 14004763)
34. Holmdahl R, Rubin K, Klareskog L, Larsson E, Wigzell H. Characterization of the antibody response in mice with type II collagen-induced arthritis, using monoclonal anti-type II collagen antibodies. Arthritis Rheum 1986;29:400-10. (Pubitemid 16127275)
35. Takahashi M, Miura Y, Hayashi S, Tateishi K, Fukuda K, Kurosaka M. DcR3-TL1A signalling inhibits cytokine-induced proliferation of rheumatoid synovial fibroblasts. Int J Mol Med 2011;28:423-7.
36. Edwards JR, Sun SG, Locklin R, Shipman CM, Adamopoulos IE, Athanasou NA, et al. LIGHT (TNFSF14), a novel mediator of bone resorption, is elevated in rheumatoid arthritis. Arthritis Rheum 2006;54:1451-62.
37. Zhang J, Wang X, Fahmi H, Wojcik S, Fikes J, Yu Y, et al. Role of TL1A in the pathogenesis of rheumatoid arthritis. J Immunol 2009;183:5350-7.
38. Kim WU, Kwok SK, Hong KH, Yoo SA, Kong JS, Choe J, et al. Soluble Fas ligand inhibits angiogenesis in rheumatoid arthritis. Arthritis Res Ther 2007;9:R42.
39. Fava RA, Notidis E, Hunt J, Szanya V, Ratcliffe N, Ngam-Ek A, et al. A role for the lymphotoxin/LIGHT axis in the pathogenesis of murine collagen-induced arthritis. J Immunol 2003;171:115-26. (Pubitemid 36745279)
40. Tamada K, Shimozaki K, Chapoval AI, Zhu G, Sica G, Flies D, et al. Modulation of T-cell-mediated immunity in tumor and graft-versus-host disease models through the LIGHT co-stimulatory pathway. Nat Med 2000;6:283-9. (Pubitemid 30148620)
41. Cantwell MJ, Hua T, Zvaifler NJ, Kipps TJ. Deficient Fas ligand expression by synovial lymphocytes from patients with rheumatoid arthritis. Arthritis Rheum 1997;40:1644-52. (Pubitemid 27426158)
42. Cheung TC, Coppieters K, Sanjo H, Oborne LM, Norris PS, Coddington A, et al. Polymorphic variants of LIGHT (TNF superfamily-14) alter receptor avidity and bioavailability. J Immunol 2010;185:1949-58.
43. Hernandez-Garcia C, Fernandez-Gutierrez B, Morado IC, Banares AA, Jover JA. The CD69 activation pathway in rheumatoid arthritis synovial fluid T cells. Arthritis Rheum 1996;39:1277-86. (Pubitemid 26270085)
44. Sancho D, Gomez M, Viedma F, Esplugues E, Gordon-Alonso M, Garcia-Lopez MA, et al. CD69 downregulates autoimmune reactivity through active transforming growth factor-beta production in collagen-induced arthritis. J Clin Invest 2003;112:872-82. (Pubitemid 38063745)
45. Rueda B, Fernandez-Gutierrez B, Balsa A, Pacual-Salcedo D, Lamas JR, Raya E, et al. Investigation of CD69 as a new candidate gene for rheumatoid arthritis. Tissue Antigens 2008;72:206-10.
46. Sancho D, Gomez M, Martinez Del Hoyo G, Lamana A, Esplugues E, Lauzurica P, et al. CD69 targeting differentially affects the course of collagen-induced arthritis. J Leukoc Biol 2006;80:1233-41. (Pubitemid 44904962)
47. Takemura S, Klimiuk PA, Braun A, Goronzy JJ, Weyand CM. T cell activation in rheumatoid synovium is B cell dependent. J Immunol 2001;167:4710-8. (Pubitemid 32954353)
48. Sato K, Suematsu A, Okamoto K, Yamaguchi A, Morishita Y, Kadono Y, et al. Th17 functions as an osteoclastogenic helper T cell subset that links T cell activation and bone destruction. J Exp Med 2006;203:2673-82. (Pubitemid 44833343)
49. Alonzi T, Fattori E, Lazzaro D, Costa P, Probert L, Kollias G, et al. Interleukin 6 is required for the development of collagen-induced arthritis. J Exp Med 1998;187:461-8. (Pubitemid 28093348)
50. Mangan PR, Harrington LE, O'Quinn DB, Helms WS, Bullard DC, Elson CO, et al. Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 2006;441:231-4.
51. Hirano T, Yasukawa K, Harada H, Taga T, Watanabe Y, Matsuda T, et al. Complementary DNA for a novel human interleukin (BSF-2) that induces B lymphocytes to produce immunoglobulin. Nature 1986;324:73-6. (Pubitemid 16008419)
52. Nimmerjahn F, Ravetch JV. Fc-gamma receptors: old friends and new family members. Immunity 2006;24:19-28. (Pubitemid 43077197)
53. Nimmerjahn F, Ravetch JV. Divergent immunoglobulin G subclass activity through selective Fc receptor binding. Science 2005;310:1510-2. (Pubitemid 41746349)
54. Nimmerjahn F, Bruhns P, Horiuchi K, Ravetch JV. Fc-gamma-RIV: a novel FcR with distinct IgG subclass specificity. Immunity 2005;23:41-51. (Pubitemid 41019656)
55. Lindenau S, Scholze S, Odendahl M, Dorner T, Radbruch A, Burmester GR, et al. Aberrant activation of B cells in patients with rheumatoid arthritis. Ann NY Acad Sci 2003;987:246-8. (Pubitemid 36584029)