Transforming growth factor (TGF)-β signalling is increased in rheumatoid synovium but TGF-β blockade does not modify experimental arthritis

Clinical and Experimental Immunology

Volumn 174, Issue 2, 2013, Pages 245-255

  Gonzalo Gil, E ^a   Criado, G ^a   Santiago, B ^a   Dotor, J ^b   Pablos, J L ^a   Galindo, M ^a  

^a HOSPITAL UNIVERSITARIO 12 DE OCTUBRE   (Spain)

^b Digna Biotech   (Spain)

Author keywords

Collagen induced arthritis; Rheumatoid arthritis; Treg; Th17; Transforming growth factor beta (TGF )

Indexed keywords

ANTIBODY; COLLAGEN TYPE 2; GAMMA INTERFERON; INTERLEUKIN 17; INTERLEUKIN 4; INTERLEUKIN 6; SMAD2 PROTEIN; SMAD3 PROTEIN; SMAD7 PROTEIN; SYNTHETIC PEPTIDE; T LYMPHOCYTE RECEPTOR DELTA CHAIN; T LYMPHOCYTE RECEPTOR GAMMA CHAIN; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTHRITIS; ARTICLE; CARTILAGE INJURY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; DISEASE COURSE; DISEASE SEVERITY; DRUG EFFECT; HUMAN; HUMAN TISSUE; IMMUNIZATION; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; LYMPHOCYTE FUNCTION; MALE; MOUSE; NONHUMAN; OSTEOARTHRITIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REGULATORY T LYMPHOCYTE; RHEUMATOID ARTHRITIS; SIGNAL TRANSDUCTION; SYNOVIUM; T LYMPHOCYTE SUBPOPULATION; TH1 CELL; TH17 CELL; TH2 CELL;

COLLAGEN-INDUCED ARTHRITIS; RHEUMATOID ARTHRITIS; TH17; TRANSFORMING GROWTH FACTOR-BETA (TGF-Β); TREG;

ANIMALS; ARTHRITIS, EXPERIMENTAL; ARTHRITIS, RHEUMATOID; AVIAN PROTEINS; CHICKENS; COLLAGEN TYPE II; DISEASE PROGRESSION; HUMANS; IMMUNIZATION; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED DBA; MODELS, ANIMAL; PEPTIDES; SIGNAL TRANSDUCTION; SMAD PROTEINS; SYNOVIAL MEMBRANE; TRANSFORMING GROWTH FACTOR BETA;

EID: 84885163129     PISSN: 00099104     EISSN: 13652249     Source Type: Journal    
DOI: 10.1111/cei.12179     Document Type: Article

References (50)

1. Rooney M, Condell D, Quinlan W etal. Analysis of the histologic variation of synovitis in rheumatoid arthritis. Arthritis Rheum 1988; 31:956-963.
2. Massague J. The transforming growth factor-beta family. Annu Rev Cell Biol 1990; 6:597-641.
3. Heldin CH, Miyazono K, ten Dijke P. TGF-beta signalling from cell membrane to nucleus through SMAD proteins. Nature 1997; 390:465-471.
4. Moustakas A, Pardali K, Gaal A, Heldin CH. Mechanisms of TGF-beta signaling in regulation of cell growth and differentiation. Immunol Lett 2002; 82:85-91.
5. Monteleone G, Kumberova A, Croft NM, McKenzie C, Steer HW, MacDonald TT. Blocking Smad7 restores TGF-beta1 signaling in chronic inflammatory bowel disease. J Clin Invest 2001; 108:601-609.
6. Elliott RL, Blobe GC. Role of transforming growth factor beta in human cancer. J Clin Oncol 2005; 23:2078-2093.
7. Varga J, Pasche B. Transforming growth factor beta as a therapeutic target in systemic sclerosis. Nat Rev Rheumatol 2009; 5:200-206.
8. Shull MM, Ormsby I, Kier AB etal. Targeted disruption of the mouse transforming growth factor-beta 1 gene results in multifocal inflammatory disease. Nature 1992; 359:693-699.
9. Liu Y, Zhang P, Li J, Kulkarni AB, Perruche S, Chen W. A critical function for TGF-beta signaling in the development of natural CD4+CD25+Foxp3+ regulatory T cells. Nat Immunol 2008; 9:632-640.
10. Nakamura K, Kitani A, Strober W. Cell contact-dependent immunosuppression by CD4(+)CD25(+) regulatory T cells is mediated by cell surface-bound transforming growth factor beta. J Exp Med 2001; 194:629-644.
11. Bettelli E, Carrier Y, Gao W etal. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 2006; 441:235-238.
12. Mangan PR, Harrington LE, O'Quinn DB etal. Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 2006; 441:231-234.
13. Yang L, Anderson DE, Baecher-Allan C etal. IL-21 and TGF-beta are required for differentiation of human T(H)17 cells. Nature 2008; 454:350-352.
14. Acosta-Rodriguez EV, Napolitani G, Lanzavecchia A, Sallusto F. Interleukins 1beta and 6 but not transforming growth factor-beta are essential for the differentiation of interleukin 17-producing human T helper cells. Nat Immunol 2007; 8:942-949.
15. Ghoreschi K, Laurence A, Yang XP etal. Generation of pathogenic T(H)17 cells in the absence of TGF-beta signalling. Nature 2010; 467:967-971.
16. Ivanov II, McKenzie BS, Zhou L etal. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 2006; 126:1121-1133.
17. Yang XO, Pappu BP, Nurieva R etal. T helper 17 lineage differentiation is programmed by orphan nuclear receptors ROR alpha and ROR gamma. Immunity 2008; 28:29-39.
18. Kehrl JH, Wakefield LM, Roberts AB etal. Production of transforming growth factor beta by human T lymphocytes and its potential role in the regulation of T cell growth. J Exp Med 1986; 163:1037-1050.
19. Cheon H, Yu SJ, Yoo DH, Chae IJ, Song GG, Sohn J. Increased expression of proinflammatory cytokines and metalloproteinase-1 by TGF-beta1 in synovial fibroblasts from rheumatoid arthritis and normal individuals. Clin Exp Immunol 2002; 127:547-552.
20. Brandes ME, Allen JB, Ogawa Y, Wahl SM. Transforming growth factor beta 1 suppresses acute and chronic arthritis in experimental animals. J Clin Invest 1991; 87:1108-1113.
21. Kuruvilla AP, Shah R, Hochwald GM, Liggitt HD, Palladino MA, Thorbecke GJ. Protective effect of transforming growth factor beta 1 on experimental autoimmune diseases in mice. Proc Natl Acad Sci USA 1991; 88:2918-2921.
22. Allen JB, Manthey CL, Hand AR, Ohura K, Ellingsworth L, Wahl SM. Rapid onset synovial inflammation and hyperplasia induced by transforming growth factor beta. J Exp Med 1990; 171:231-247.
23. Sancho D, Gomez M, Viedma F etal. CD69 downregulates autoimmune reactivity through active transforming growth factor-beta production in collagen-induced arthritis. J Clin Invest 2003; 112:872-882.
24. Thorbecke GJ, Shah R, Leu CH, Kuruvilla AP, Hardison AM, Palladino MA. Involvement of endogenous tumor necrosis factor alpha and transforming growth factor beta during induction of collagen type II arthritis in mice. Proc Natl Acad Sci USA 1992; 89:7375-7379.
25. Sakuma M, Hatsushika K, Koyama K etal. TGF-beta type I receptor kinase inhibitor down-regulates rheumatoid synoviocytes and prevents the arthritis induced by type II collagen antibody. Int Immunol 2007; 19:117-126.
26. Nakae S, Nambu A, Sudo K, Iwakura Y. Suppression of immune induction of collagen-induced arthritis in IL-17-deficient mice. J Immunol 2003; 171:6173-6177.
27. Lubberts E, Koenders MI, Oppers-Walgreen B etal. Treatment with a neutralizing anti-murine interleukin-17 antibody after the onset of collagen-induced arthritis reduces joint inflammation, cartilage destruction, and bone erosion. Arthritis Rheum 2004; 50:650-659.
28. Chabaud M, Durand JM, Buchs N etal. Human interleukin-17: a T cell-derived proinflammatory cytokine produced by the rheumatoid synovium. Arthritis Rheum 1999; 42:963-970.
29. Shahrara S, Huang Q, Mandelin AM II, Pope RM. TH-17 cells in rheumatoid arthritis. Arthritis Res Ther 2008; 10:R93.
30. Yamada H, Nakashima Y, Okazaki K etal. Th1 but not Th17 cells predominate in the joints of patients with rheumatoid arthritis. Ann Rheum Dis 2008; 67:1299-1304.
31. Dotor J, Lopez-Vazquez AB, Lasarte JJ etal. Identification of peptide inhibitors of transforming growth factor beta 1 using a phage-displayed peptide library. Cytokine 2007; 39:106-115.
32. Inglis JJ, Criado G, Medghalchi M etal. Collagen-induced arthritis in C57BL/6 mice is associated with a robust and sustained T-cell response to type II collagen. Arthritis Res Ther 2007; 9:R113.
33. Ito Y, Usui T, Kobayashi S etal. Gamma/delta T cells are the predominant source of interleukin-17 in affected joints in collagen-induced arthritis, but not in rheumatoid arthritis. Arthritis Rheum 2009; 60:2294-2303.
34. Brennan FM, Chantry D, Turner M, Foxwell B, Maini R, Feldmann M. Detection of transforming growth factor-beta in rheumatoid arthritis synovial tissue: lack of effect on spontaneous cytokine production in joint cell cultures. Clin Exp Immunol 1990; 81:278-285.
35. Bira Y, Tani K, Nishioka Y etal. Transforming growth factor beta stimulates rheumatoid synovial fibroblasts via the type II receptor. Mod Rheumatol 2005; 15:108-113.
36. Pohlers D, Beyer A, Koczan D, Wilhelm T, Thiesen HJ, Kinne RW. Constitutive upregulation of the transforming growth factor-beta pathway in rheumatoid arthritis synovial fibroblasts. Arthritis Res Ther 2007; 9:R59.
37. Marinova-Mutafchieva L, Gabay C, Funa K, Williams RO. Remission of collagen-induced arthritis is associated with high levels of transforming growth factor-beta expression in the joint. Clin Exp Immunol 2006; 146:287-293.
38. Wahl SM, Allen JB, Costa GL, Wong HL, Dasch JR. Reversal of acute and chronic synovial inflammation by anti-transforming growth factor beta. J Exp Med 1993; 177:225-230.
39. Arribillaga L, Dotor J, Basagoiti M etal. Therapeutic effect of a peptide inhibitor of TGF-beta on pulmonary fibrosis. Cytokine 2011; 53:327-333.
40. Gil-Guerrero L, Dotor J, Huibregtse IL etal. In vitro and in vivo down-regulation of regulatory T cell activity with a peptide inhibitor of TGF-beta1. J Immunol 2008; 181:126-135.
41. Serrati S, Margheri F, Pucci M etal. TGFbeta1 antagonistic peptides inhibit TGFbeta1-dependent angiogenesis. Biochem Pharmacol 2009; 77:813-825.
42. Loureiro J, Aguilera A, Selgas R etal. Blocking TGF-beta1 protects the peritoneal membrane from dialysate-induced damage. J Am Soc Nephrol 2011; 22:1682-1695.
43. Zarranz-Ventura J, Fernandez-Robredo P, Recalde S etal. Transforming growth factor-beta inhibition reduces progression of early choroidal neovascularization lesions in rats: p17 and p144 peptides. PLoS ONE 2013; 8:e65434.
44. Veldhoen M, Hocking RJ, Flavell RA, Stockinger B. Signals mediated by transforming growth factor-beta initiate autoimmune encephalomyelitis, but chronic inflammation is needed to sustain disease. Nat Immunol 2006; 7:1151-1156.
45. Lee Y, Awasthi A, Yosef N etal. Induction and molecular signature of pathogenic TH17 cells. Nat Immunol 2012; 13:991-999.
46. Kulkarni AB, Huh CG, Becker D etal. Transforming growth factor beta 1 null mutation in mice causes excessive inflammatory response and early death. Proc Natl Acad Sci USA 1993; 90:770-774.
47. Christ M, McCartney-Francis NL, Kulkarni AB etal. Immune dysregulation in TGF-beta 1-deficient mice. J Immunol 1994; 153:1936-1946.
48. Ouyang W, Beckett O, Ma Q, Li MO. Transforming growth factor-beta signaling curbs thymic negative selection promoting regulatory T cell development. Immunity 2010; 32:642-653.
49. Morgan ME, Sutmuller RP, Witteveen HJ etal. CD25+ cell depletion hastens the onset of severe disease in collagen-induced arthritis. Arthritis Rheum 2003; 48:1452-1460.
50. Marie JC, Letterio JJ, Gavin M, Rudensky AY. TGF-beta1 maintains suppressor function and Foxp3 expression in CD4+CD25+ regulatory T cells. J Exp Med 2005; 201:1061-1067.