Downregulation of TGF-βRII in T effector cells leads to increased resistance to TGF-β-mediated suppression of autoimmune responses in type I diabetes

Autoimmunity

Volumn 45, Issue 4, 2012, Pages 310-319

  Kawamoto, Koichi ^a   Pahuja, Anil ^a   Nettles, Adam ^a   Honkanen Scott, Minna ^a   Bansal Pakala, Pratima ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

GAD65; NOD; regulatory T cell; Th1; Th17; Tregs; Type 1 diabetes

Indexed keywords

GAMMA INTERFERON; GLUTAMATE DECARBOXYLASE 65; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; CYTOKINE PRODUCTION; DISEASE COURSE; DISEASE PREDISPOSITION; DOWN REGULATION; EFFECTOR CELL; FEMALE; IMMUNE RESPONSE; INSULIN DEPENDENT DIABETES MELLITUS; LYMPHOCYTE COUNT; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE; TH1 CELL;

ANIMALS; AUTOANTIGENS; AUTOIMMUNITY; CELLS, CULTURED; DIABETES MELLITUS, TYPE 1; DISEASE PROGRESSION; FEMALE; GLUTAMATE DECARBOXYLASE; INTERFERON-GAMMA; MALE; MICE; MICE, INBRED NOD; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; T-LYMPHOCYTES, REGULATORY; TH1 CELLS; TRANSFORMING GROWTH FACTOR BETA;

EID: 84859864752     PISSN: 08916934     EISSN: 1607842X     Source Type: Journal    
DOI: 10.3109/08916934.2012.664667     Document Type: Article

References (48)

1. Siegel RM, Katsumata M, Komori S, Wadsworth S, Gill-Morse L, Jerrold-Jones S, Bhandoola A, Greene MI, Yui K. Mechanisms of autoimmunity in the context of T-cell tolerance: insights from natural and transgenic animal model systems. Immunol Rev 1990;118:165-192.
2. Roep BO. T-cell responses to autoantigens in IDDM. The search for the Holy Grail. The search for the Holy Grail. Diabetes 1996;45:1147-1156.
3. Wing K, Sakaguchi S. Regulatory T cells exert checks and balances on self tolerance and autoimmunity. Nat Immunol 2010;11:7-13.
4. Tang Q, Henriksen KJ, Bi M, Finger EB, Szot G, Ye J, Masteller EL, McDevitt H, Bonyhadi M, Bluestone JA. In vitro-expanded antigen-specific regulatory T cells suppress autoimmune diabetes. J Exp Med 2004;199:1455-1465. (Pubitemid 38780401)
5. Masteller EL, Warner MR, Tang Q, Tarbell KV, McDevitt H, Bluestone JA. Expansion of functional endogenous antigen-specific CD4 + CD25 + regulatory T cells from nonobese diabetic mice. J Immunol 2005;175:3053-3059. (Pubitemid 41170524)
6. Tarbell KV, Yamazaki S, Olson K, Toy P, Steinman RM. CD25 + CD4 + T cells, expanded with dendritic cells presenting a single autoantigenic peptide, suppress autoimmune diabetes. J Exp Med 2004;199:1467-1477. (Pubitemid 38780402)
7. Kukreja A, Cost G, Marker J, Zhang C, Sun Z, Lin-Su K, Ten S, Sanz M, Exley M, Wilson B, et al. Multiple immunoregulatory defects in type-1 diabetes. J Clin Invest 2002;109: 131-140. (Pubitemid 34052549)
8. Lindley S, Dayan CM, Bishop A, Roep BO, Peakman M, Tree TI. Defective suppressor function in CD4(+)CD25(+) T-cells from patients with type 1 diabetes. Diabetes 2005;54: 92-99. (Pubitemid 40105099)
9. Pop SM, Wong CP, Culton DA, Clarke SH, Tisch R. Single cell analysis shows decreasing FoxP3 and TGFbeta1 coexpressing CD4 + CD25 + regulatory T cells during autoimmune diabetes. J Exp Med 2005;201:1333-1346. (Pubitemid 40629075)
10. Berzins SP, Venanzi ES, Benoist C, Mathis D. T-cell compartments of prediabetic NOD mice. Diabetes 2003;52: 327-334. (Pubitemid 36173186)
11. Brusko T, Wasserfall C, McGrail K, Schatz R, Viener HL, Schatz D, Haller M, Rockell J, Gottlieb P, Clare-Salzler M, et al. No alterations in the frequency of FOXP3 + regulatory T-cells in type 1 diabetes. Diabetes 2007;56:604-612. (Pubitemid 46348451)
12. Gregori S, Giarratana N, Smiroldo S, Adorini L. Dynamics of pathogenic and suppressor T cells in autoimmune diabetes development. J Immunol 2003;171:4040-4047. (Pubitemid 37238678)
13. You S, Belghith M, Cobbold S, Alyanakian MA, Gouarin C, Barriot S, Garcia C, Waldmann H, Bach JF, Chatenoud L. Autoimmune diabetes onset results from qualitative rather than quantitative age-dependent changes in pathogenic T-cells. Diabetes 2005;54:1415-1422. (Pubitemid 40586672)
14. D'Alise AM, Auyeung V, Feuerer M, Nishio J, Fontenot J, Benoist C, Mathis D. The defect in T-cell regulation in NOD mice is an effect on the T-cell effectors. Proc Natl Acad Sci USA 2008;105:19857-19862.
15. Tree TI, Roep BO, Peakman M. A mini meta-analysis of studies on CD4 + CD25 + T cells in human type 1 diabetes: report of the Immunology of Diabetes Society T Cell Workshop. Ann NY Acad Sci 2006;1079:9-18. (Pubitemid 44968695)
16. Mellanby RJ, Thomas D, Phillips JM, Cooke A. Diabetes in non-obese diabetic mice is not associated with quantitative changes in CD4 + CD25 + Foxp3 + regulatory T cells. Immunology 2007;121:15-28. (Pubitemid 46537670)
17. Li MO, Flavell RA. TGF-beta: a master of all T cell trades. Cell 2008;134:392-404.
18. You S, Thieblemont N, Alyanakian MA, Bach JF, Chatenoud L. Transforming growth factor-beta and T-cell-mediated immunoregulation in the control of autoimmune diabetes. Immunol Rev 2006;212:185-202. (Pubitemid 44116709)
19. Gregg RK, Jain R, Schoenleber SJ, Divekar R, Bell JJ, Lee HH, Yu P, Zaghouani H. A sudden decline in active membrane-bound TGF-beta impairs both T regulatory cell function and protection against autoimmune diabetes. J Immunol 2004; 173:7308-7316. (Pubitemid 39628168)
20. Belghith M, Bluestone JA, Barriot S, Megret J, Bach JF, Chatenoud L. TGF-beta-dependent mechanisms mediate restoration of self-tolerance induced by antibodies to CD3 in overt autoimmune diabetes. Nat Med 2003;9:1202-1208. (Pubitemid 37173706)
21. Chen G, Han G, Wang J, Wang R, Xu R, Shen B, Qian J, Li Y. Essential roles of TGF-beta in anti-CD3 antibody therapy: reversal of diabetes in nonobese diabetic mice independent of Foxp3 + CD4 + regulatory T cells. J Leukoc Biol 2008;83: 280-287. (Pubitemid 351225608)
22. Ludviksson BR, Seegers D, Resnick AS, Strober W. The effect of TGF-beta1 on immune responses of naive versus memory CD4 + Th1/Th2 T cells. Eur J Immunol 2000;30: 2101-2111. (Pubitemid 30456207)
23. Chen W, Jin W, Hardegen N, Lei KJ, Li L, Marinos N, McGrady G, Wahl SM. Conversion of peripheral CD4 + CD25- naive T cells to CD4 + CD25 + regulatory T cells by TGF-beta induction of transcription factor Foxp3. J Exp Med 2003;198:1875-1886. (Pubitemid 38032120)
24. Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, Oukka M, Weiner HL, Kuchroo VK. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 2006;441:235-238.
25. Dai YD, Jensen KP, Lehuen A, Masteller EL, Bluestone JA, Wilson DB, Sercarz EE. A peptide of glutamic acid decarboxylase 65 can recruit and expand a diabetogenic T cell clone, BDC2.5, in the pancreas. J Immunol 2005;175: 3621-3627. (Pubitemid 41292021)
26. Tree TI, Duinkerken G, Willemen S, de Vries RR, Roep BO. HLA-DQ-regulated T-cell responses to islet cell autoantigens insulin and GAD65. Diabetes 2004;53:1692-1699. (Pubitemid 38857026)
27. van Halteren AG, Tysma OM, van EE, Mathieu C, Roep BO. 1alpha,25-dihydroxyvitamin D3 or analogue treated dendritic cells modulate human autoreactive T cells via the selective induction of apoptosis. J Autoimmun 2004;23:233-239. (Pubitemid 40288105)
28. Raimondi G, Sumpter TL, Matta BM, Pillai M, Corbitt N, Vodovotz Y, Wang Z, Thomson AW. Mammalian target of rapamycin inhibition and alloantigen-specific regulatory T cells synergize to promote long-term graft survival in immunocompetent recipients. J Immunol 2010;184:624-636.
29. Schneider A, Rieck M, Sanda S, Pihoker C, Greenbaum C, Buckner JH. The effector T cells of diabetic subjects are resistant to regulation via CD4 + FOXP3 + regulatory T cells. J Immunol 2008;181:7350-7355.
30. Pietropaolo M, Peakman M, Pietropaolo SL, Zanone MM, Foley TP, Jr., Becker DJ, Trucco M. Combined analysis of GAD65 and ICA512(IA-2) autoantibodies in organ and non-organ-specific autoimmune diseases confers high specificity for insulin-dependent diabetes mellitus. J Autoimmun 1998;11: 1-10. (Pubitemid 28080723)
31. Li L, Wang B, Frelinger JA. T-cell promiscuity in autoimmune diabetes. Diabetes 2008;57:2099-2106.
32. Shevach EM, Davidson TS, Huter EN, Dipaolo RA, Andersson J. Role of TGF-Beta in the induction of Foxp3 expression and T regulatory cell function. J Clin Immunol 2008;28:640-646.
33. 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.
34. Lee YK, Mukasa R, Hatton RD, Weaver CT. Developmental plasticity of Th17 and Treg cells. Curr Opin Immunol 2009; 21:274-280.
35. Negoro T, Iinuma F, Tobe T, Watanabe M. Induction of CD4 + regulatory T cells by 12-O-tetradecanoylphorbol 13-acetate in mice. Part 1: The strain difference in this induction. Int Immunopharmacol 2001;1:1153-1163. (Pubitemid 32434431)
36. Fahlen L, Read S, Gorelik L, Hurst SD, Coffman RL, Flavell RA, Powrie F. T cells that cannot respond to TGF-beta escape control by CD4(+)CD25(+) regulatory T cells. J Exp Med 2005;201:737-746. (Pubitemid 40395119)
37. D'Alise AM, Ergun A, Hill JA, Mathis D, Benoist C. A cluster of coregulated genes determines TGF-beta-induced regulatory T-cell (Treg) dysfunction in NOD mice. Proc Natl Acad Sci USA 2011;108:8737-8742.
38. Shull MM, Ormsby I, Kier AB, Pawlowski S, Diebold RJ, Yin M, Allen R, Sidman C, Proetzel G, Calvin D, et al. Targeted disruption of the mouse transforming growth factor-beta 1 gene results in multifocal inflammatory disease. Nature 1992; 359:693-699.
39. Gorelik L, Flavell RA. Abrogation of TGFbeta signaling in T cells leads to spontaneous T cell differentiation and autoimmune disease. Immunity 2000;12:171-181. (Pubitemid 30398631)
40. Li MO, Wan YY, Flavell RA. T cell-produced transforming growth factor-beta1 controls T cell tolerance and regulates Th1- and Th17-cell differentiation. Immunity 2007;26: 579-591. (Pubitemid 46756347)
41. Weaver CT, Harrington LE, Mangan PR, Gavrieli M, Murphy KM. Th17: an effector CD4 T cell lineage with regulatory T cell ties. Immunity 2006;24:677-688. (Pubitemid 43867371)
42. Wang B, Andre I, Gonzalez A, Katz JD, Aguet M, Benoist C, MathisD. Interferon-gamma impacts at multiple points during the progression of autoimmune diabetes. Proc Natl Acad Sci USA 1997;94:13844-13849. (Pubitemid 28009672)
43. Hultgren B, Huang X, Dybdal N, Stewart TA. Genetic absence of gamma-interferon delays but does not prevent diabetes in NOD mice. Diabetes 1996;45:812-817. (Pubitemid 26166778)
44. Emamaullee JA, Davis J, Merani S, Toso C, Elliott JF, Thiesen A, Shapiro AM. Inhibition of Th17 cells regulates autoimmune diabetes in NOD mice. Diabetes 2009;58: 1302-1311.
45. Fitzpatrick F, Lepault F, Homo-Delarche F, Bach JF, Dardenne M. Influence of castration, alone or combined with thymectomy, on the development of diabetes in the nonobese diabetic mouse. Endocrinology 1991;129: 1382-1390.
46. Ivakine EA, Fox CJ, Paterson AD, Mortin-Toth SM, Canty A, Walton DS, Aleksa K, Ito S, Danska JS. Sex-specific effect of insulin-dependent diabetes 4 on regulation of diabetes pathogenesis in the nonobese diabetic mouse. J Immunol 2005;174:7129-7140. (Pubitemid 40705679)
47. Xiao BG, Liu X, Link H. Antigen-specific T cell functions are suppressed over the estrogen-dendritic cell-indoleamine 2,3-dioxygenase axis. Steroids 2004;69:653-659. (Pubitemid 39297704)
48. Zoller AL, Kersh GJ. Estrogen induces thymic atrophy by eliminating early thymic progenitors and inhibiting proliferation of beta-selected thymocytes. J Immunol 2006;176: 7371-7378. (Pubitemid 43849038)