Mechanisms underlying antigen-specific tolerance of stable and convertible Th17 cells during suppression of autoimmune diabetes

Diabetes

Volumn 61, Issue 8, 2012, Pages 2054-2065

  Wan, Xiaoxiao ^a   Guloglu, F Betul ^a,b   VanMorlan, Amie M ^a   Rowland, Linda M ^a   Jain, Renu ^a,c   Haymaker, Cara L ^a,d   Cascio, Jason A ^a   Dhakal, Mermagya ^a   Hoeman, Christine M ^a   Tartar, Danielle M ^a   Zaghouani, Habib ^a  

^a University of Missouri   (United States)

^b MATERIALS INSTITUTE   (Turkey)

^c MERCK RESEARCH LABORATORIES   (United States)

^d UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR3; EPITOPE; FAS LIGAND; IMMUNOGLOBULIN; RETINOID RELATED ORPHAN RECEPTOR GAMMA; TRANSCRIPTION FACTOR T BET;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL FATE; CONTROLLED STUDY; FEMALE; IMMUNOLOGICAL TOLERANCE; INSULIN DEPENDENT DIABETES MELLITUS; MOUSE; NONHUMAN; PANCREAS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR DOWN REGULATION; SPLEEN; TH1 CELL; TH17 CELL;

ANIMALS; CELL POLARITY; DIABETES MELLITUS, TYPE 1; DOWN-REGULATION; FAS LIGAND PROTEIN; IMMUNE TOLERANCE; MICE; MICE, INBRED NOD; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP F, MEMBER 3; RECEPTORS, CXCR3; TH1 CELLS; TH17 CELLS;

EID: 84864386564     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db11-1723     Document Type: Article

References (42)

1. Katz JD, Benoist C, Mathis D. T helper cell subsets in insulin-dependent diabetes. Science 1995;268:1185-1188
2. Rabinovitch A. Immunoregulatory and cytokine imbalances in the pathogenesis of IDDM. Therapeutic intervention by immunostimulation? Diabetes 1994;43:613-621 (Pubitemid 24138771)
3. Bach JF. Insulin-dependent diabetes mellitus as an autoimmune disease. Endocr Rev 1994;15:516-542
4. 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)
5. Serreze DV, Post CM, Chapman HD, Johnson EA, Lu B, Rothman PB. Interferon-gamma receptor signaling is dispensable in the development of autoimmune type 1 diabetes in NOD mice. Diabetes 2000;49:2007-2011
6. Trembleau S, Penna G, Gregori S, et al. Pancreas-infiltrating Th1 cells and diabetes develop in IL-12-deficient nonobese diabetic mice. J Immunol 1999;163:2960-2968 (Pubitemid 29399229)
7. Martin-Orozco N, Chung Y, Chang SH, Wang YH, Dong C. Th17 cells promote pancreatic inflammation but only induce diabetes efficiently in lymphopenic hosts after conversion into Th1 cells. Eur J Immunol 2009;39: 216-224
8. Bradshaw EM, Raddassi K, Elyaman W, et al. Monocytes from patients with type 1 diabetes spontaneously secrete proinflammatory cytokines inducing Th17 cells. J Immunol 2009;183:4432-4439
9. Jain R, Tartar DM, Gregg RK, et al. Innocuous IFNgamma induced by adjuvant-free antigen restores normoglycemia in NOD mice through inhibition of IL-17 production. J Exp Med 2008;205:207-218 (Pubitemid 351185727)
10. Emamaullee JA, Davis J, Merani S, et al. Inhibition of Th17 cells regulates autoimmune diabetes in NOD mice. Diabetes 2009;58:1302-1311
11. Honkanen J, Nieminen JK, Gao R, et al. IL-17 immunity in human type 1 diabetes. J Immunol 2010;185:1959-1967
12. Katz JD, Wang B, Haskins K, Benoist C, Mathis D. Following a diabetogenic T cell from genesis through pathogenesis. Cell 1993;74:1089-1100 (Pubitemid 23289465)
13. Judkowski V, Pinilla C, Schroder K, Tucker L, Sarvetnick N, Wilson DB. Identification of MHC class II-restricted peptide ligands, including a glutamic acid decarboxylase 65 sequence, that stimulate diabetogenic T cells from transgenic BDC2.5 nonobese diabetic mice. J Immunol 2001;166:908-917 (Pubitemid 32060245)
14. You S, Chen C, Lee WH, et al. Detection and characterization of T cells specific for BDC2.5 T cell-stimulating peptides. J Immunol 2003;170:4011-4020 (Pubitemid 36428162)
15. Bending D, De la Peña H, Veldhoen M, et al. Highly purified Th17 cells from BDC2.5NOD mice convert into Th1-like cells in NOD/SCID recipient mice. J Clin Invest 2009;119:565-572
16. Stadinski BD, Delong T, Reisdorph N, et al. Chromogranin A is an autoantigen in type 1 diabetes. Nat Immunol 2010;11:225-231
17. Nurieva R, Yang XO, Chung Y, Dong C. Cutting edge: in vitro generated Th17 cells maintain their cytokine expression program in normal but not lymphopenic hosts. J Immunol 2009;182:2565-2568
18. Gregg RK, Jain R, Schoenleber SJ, et al. 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)
19. Hu JK, Kagari T, Clingan JM, Matloubian M. Expression of chemokine receptor CXCR3 on T cells affects the balance between effector and memory CD8 T-cell generation. Proc Natl Acad Sci USA 2011;108:E118-E127
20. Lee YK, Turner H, Maynard CL, et al. Late developmental plasticity in the T helper 17 lineage. Immunity 2009;30:92-107
21. Zhou L, Chong MM, Littman DR. Plasticity of CD4+ T cell lineage differentiation. Immunity 2009;30:646-655
22. Hirota K, Duarte JH, Veldhoen M, et al. Fate mapping of IL-17-producing T cells in inflammatory responses. Nat Immunol 2011;12:255-263
23. Lexberg MH, Taubner A, Albrecht I, et al. IFN-γ and IL-12 synergize to convert in vivo generated Th17 into Th1/Th17 cells. Eur J Immunol 2010; 40:3017-3027
24. Bending D, Newland S, Krejcí A, Phillips JM, Bray S, Cooke A. Epigenetic changes at Il12rb2 and Tbx21 in relation to plasticity behavior of Th17 cells. J Immunol 2011;186:3373-3382
25. Tartar DM, VanMorlan AM, Wan X, et al. FoxP3+RORgammat+ T helper intermediates display suppressive function against autoimmune diabetes. J Immunol 2010;184:3377-3385
26. Gregg RK, Bell JJ, Lee HH, et al. IL-10 diminishes CTLA-4 expression on islet-resident T cells and sustains their activation rather than tolerance. J Immunol 2005;174:662-670 (Pubitemid 40094258)
27. Singh SP, Zhang HH, Foley JF, Hedrick MN, Farber JM. Human T cells that are able to produce IL-17 express the chemokine receptor CCR6. J Immunol 2008;180:214-221
28. Syrbe U, Siveke J, Hamann A. Th1/Th2 subsets: distinct differences in homing and chemokine receptor expression? Springer Semin Immunopathol 1999;21:263-285 (Pubitemid 30011439)
29. Koch MA, Tucker-Heard G, Perdue NR, Killebrew JR, Urdahl KB, Campbell DJ. The transcription factor T-bet controls regulatory T cell homeostasis and function during type 1 inflammation. Nat Immunol 2009;10:595-602
30. Beima KM, Miazgowicz MM, Lewis MD, Yan PS, Huang TH, Weinmann AS. T-bet binding to newly identified target gene promoters is cell type-independent but results in variable context-dependent functional effects. J Biol Chem 2006;281:11992-12000 (Pubitemid 43855463)
31. Reboldi A, Coisne C, Baumjohann D, et al. C-C chemokine receptor 6-regulated entry of TH-17 cells into the CNS through the choroid plexus is required for the initiation of EAE. Nat Immunol 2009;10:514-523
32. Hirota K, Yoshitomi H, Hashimoto M, et al. Preferential recruitment of CCR6-expressing Th17 cells to inflamed joints via CCL20 in rheumatoid arthritis and its animal model. J Exp Med 2007;204:2803-2812 (Pubitemid 350179551)
33. Chaudhry A, Rudra D, Treuting P, et al. CD4+ regulatory T cells control TH17 responses in a Stat3-dependent manner. Science 2009;326:986-991
34. Chaudhry A, Samstein RM, Treuting P, et al. Interleukin-10 signaling in regulatory T cells is required for suppression of Th17 cell-mediated inflammation. Immunity 2011;34:566-578
35. Huber S, Gagliani N, Esplugues E, et al. Th17 cells express interleukin-10 receptor and are controlled by Foxp3? and Foxp3+ regulatory CD4+ T cells in an interleukin-10-dependent manner. Immunity 2011;34:554-565
36. He YW, Deftos ML, Ojala EW, Bevan MJ. RORgamma t, a novel isoform of an orphan receptor, negatively regulates Fas ligand expression and IL-2 production in T cells. Immunity 1998;9:797-806 (Pubitemid 29024459)
37. Zhang Y, Xu G, Zhang L, Roberts AI, Shi Y. Th17 cells undergo Fas-mediated activation-induced cell death independent of IFN-gamma. J Immunol 2008; 181:190-196
38. Fang Y, Yu S, Ellis JS, Sharav T, Braley-Mullen H. Comparison of sensitivity of Th1, Th2, and Th17 cells to Fas-mediated apoptosis. J Leukoc Biol 2010; 87:1019-1028
39. Powell JD, Lerner CG, Schwartz RH. Inhibition of cell cycle progression by rapamycin induces T cell clonal anergy even in the presence of costimulation. J Immunol 1999;162:2775-2784 (Pubitemid 29309302)
40. Vanasek TL, Khoruts A, Zell T, Mueller DL. Antagonistic roles for CTLA-4 and the mammalian target of rapamycin in the regulation of clonal anergy: enhanced cell cycle progression promotes recall antigen responsiveness. J Immunol 2001;167:5636-5644 (Pubitemid 33062753)
41. Zheng Y, Delgoffe GM, Meyer CF, Chan W, Powell JD. Anergic T cells are metabolically anergic. J Immunol 2009;183:6095-6101
42. Brogdon JL, Xu Y, Szabo SJ, et al. Histone deacetylase activities are required for innate immune cell control of Th1 but not Th2 effector cell function. Blood 2007;109:1123-1130 (Pubitemid 46220659)