Revisiting regulatory T cells in type 1 diabetes

Current Opinion in Endocrinology, Diabetes and Obesity

Volumn 19, Issue 4, 2012, Pages 271-278

  Zhang, Yuxia ^a,b   Bandala Sanchez, Esther ^a,b   Harrison, Leonard C ^a,b  

^a WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Antigen specificity; Inflammation; Regulatory T cells; Treg stability; Type 1 diabetes

Indexed keywords

CYTOKINE; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR FOXP3;

ANTIGEN SPECIFICITY; AUTOIMMUNE DISEASE; CD4+ CD25+ T LYMPHOCYTE; CELL DIFFERENTIATION; EFFECTOR CELL; GENE LOCUS; HOMEOSTASIS; HUMAN; INFLAMMATION; INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PROTEIN METHYLATION; REGULATORY T LYMPHOCYTE; REVIEW; TH1 CELL; TH17 CELL;

ANTIGENS, CD; CELL DIFFERENTIATION; CYTOKINES; DIABETES MELLITUS, TYPE 1; DNA METHYLATION; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; HUMANS; IMMUNOTHERAPY; INFLAMMATION; LYMPHOCYTE ACTIVATION; MALE; T-LYMPHOCYTES, REGULATORY; TH1 CELLS; TH17 CELLS;

EID: 84864631552     PISSN: 1752296X     EISSN: 17522978     Source Type: Journal    
DOI: 10.1097/MED.0b013e328355a2d5     Document Type: Review

References (89)

1. Wing K, Sakaguchi S. Regulatory T cells exert checks and balances on self tolerance and autoimmunity. Nat Immunol 2010; 11:7-13.
2. Curotto de Lafaille MA, Lafaille JJ. Natural and adaptive Foxp3 regulatory T cells: more of the same or a division of labor? Immunity 2009; 30:626-635.
3. Fontenot JD, Gavin MA, Rudensky AY. Foxp3 programs the development and function of CD4CD25 regulatory T cells. Nat Immunol 2003; 4:330-336.
4. Hori S, Nomura T, Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science 2003; 299:1057-1061.
5. Khattri R, Cox T, Yasayko SA, Ramsdell F. An essential role for Scurfin in CD4CD25 T regulatory cells. Nat Immunol 2003; 4:337-342.
6. Sakaguchi S, Yamaguchi T, Nomura T, Ono M. Regulatory T cells and immune tolerance. Cell 2008; 133:775-787.
7. Zheng Y, Rudensky AY. Foxp3 in control of the regulatory T cell lineage. Nat Immunol 2007; 8:457-462.
8. Spoerl S, Li XC. Regulatory T cells and the quest for transplant tolerance. Discov Med 2011; 11:25-34.
9. Bennett CL, Christie J, Ramsdell F, et al. The immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome (IPEX) is caused by mutations of FOXP3. Nat Genet 2001; 27:20-21.
10. Wildin RS, Ramsdell F, Peake J, et al. X-linked neonatal diabetes mellitus, enteropathy and endocrinopathy syndrome is the human equivalent of mouse scurfy. Nat Genet 2001; 27:18-20.
11. Jordan MS, Boesteanu A, Reed AJ, et al. Thymic selection of CD4CD25 regulatory T cells induced by an agonist self-peptide. Nat Immunol 2001; 2:301-306.
12. Kawahata K, Misaki Y, Yamauchi M, et al. Generation of CD4()CD25() regulatory T cells from autoreactive T cells simultaneously with their negative selection in the thymus and from nonautoreactive T cells by endogenous TCR expression. J Immunol 2002; 168:4399-4405.
13. Hsieh CS, Liang Y, Tyznik AJ, et al. Recognition of the peripheral self by naturally arising CD25 CD4 T cell receptors. Immunity 2004; 21:267-277.
14. Pacholczyk R, Ignatowicz H, Kraj P, Ignatowicz L. Origin and T cell receptor diversity of Foxp3CD4CD25 T cells. Immunity 2006; 25:249-259.
15. Wong J, Obst R, Correia-Neves M, et al. Adaptation of TCR repertoires to selfpeptides in regulatory and nonregulatory CD4 T cells. J Immunol 2007; 178:7032-7041.
16. Haribhai D, Williams JB, Jia S, et al. A requisite role for induced regulatory T cells in tolerance based on expanding antigen receptor diversity. Immunity 2011; 35:109-122.
17. Vignali DA, Collison LW, Workman CJ. How regulatory T cells work. Nat Rev Immunol 2008; 8:523-532.
18. Shevach EM. Mechanisms of Foxp3 T regulatory cell-mediated suppression. Immunity 2009; 30:636-645.
19. Roep BO, Atkinson M, von Herrath M. Satisfaction (not) guaranteed: re-evaluating the use of animal models of type 1 diabetes. Nat Rev Immunol 2004; 4:989-997.
20. Santamaria P. The long and winding road to understanding and conquering type 1 diabetes. Immunity 2010; 32:437-445.
21. Wang B, Andre I, Gonzalez A, et al. Interferon-gamma impacts at multiple points during the progression of autoimmune diabetes. Proc Natl Acad Sci USA 1997; 94:13844-13849.
22. Jain R, Tartar DM, Gregg RK, et al. Innocuous IFNgamma induced by adjuvantfree antigen restores normoglycemia in NOD mice through inhibition of IL-17 production. J Exp Med 2008; 205:207-218.
23. Emamaullee JA, Davis J, Merani S, et al. Inhibition of Th17 cells regulates autoimmune diabetes in NOD mice. Diabetes 2009; 58:1302-1311.
24. Ferraro A, Socci C, Stabilini A, et al. Expansion of Th17 cells and functional defects in T regulatory cells are key features of the pancreatic lymph nodes in patients with type 1 diabetes. Diabetes 2011; 60:2903-2913.
25. Gambineri E, Torgerson TR, Ochs HD. Immune dysregulation, polyendocrinopathy, enteropathy, and X-linked inheritance (IPEX), a syndrome of systemic autoimmunity caused by mutations of FOXP3, a critical regulator of T-cell homeostasis. Curr Opin Rheumatol 2003; 15:430-435.
26. Gambineri E, Perroni L, Passerini L, et al. Clinical and molecular profile of a new series of patients with immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome: inconsistent correlation between forkhead box protein 3 expression and disease severity. J Allergy Clin Immunol 2008; 122:1105-1112; e1101.
27. Wildin RS, Smyk-Pearson S, Filipovich AH. Clinical and molecular features of the immunodysregulation, polyendocrinopathy, enteropathy, X linked (IPEX) syndrome. J Med Genet 2002; 39:537-545.
28. Sakaguchi S, Ono M, Setoguchi R, et al. Foxp3 CD25 CD4 natural regulatory T cells in dominant self-tolerance and autoimmune disease. Immunol Rev 2006; 212:8-27.
29. Chen Y, Kuchroo VK, Inobe J, et al. Regulatory T cell clones induced by oral tolerance: suppression of autoimmune encephalomyelitis. Science 1994; 265:1237-1240.
30. Mucida D, Kutchukhidze N, Erazo A, et al. Oral tolerance in the absence of naturally occurring Tregs. J Clin Invest 2005; 115:1923-1933.
31. Harrison LC. Vaccination against self to prevent autoimmune disease: the type 1 diabetes model. Immunol Cell Biol 2008; 86:139-145.
32. Leslie M. Immunology. Regulatory T cells get their chance to shine. Science 2011; 332:1020-1021.
33. Atkinson MA. Evaluating preclinical efficacy. Sci Transl Med 2011; 3:96cm22.
34. Lee JH, Kang SG, Kim CH. Foxp3 T cells undergo conventional first switch to lymphoid tissue homing receptors in thymus but accelerated second switch to nonlymphoid tissue homing receptors in secondary lymphoid tissues. J Immunol 2007; 178:301-311.
35. Huehn J, Siegmund K, Lehmann JC, et al. Developmental stage, phenotype, and migration distinguish naive-and effector/memory-like CD4 regulatory T cells. J Exp Med 2004; 199:303-313.
36. Cretney E, Xin A, Shi W, Minnich M, et al. The transcription factors Blimp-1 and IRF4 jointly control the differentiation and function of effector regulatory T cells. Nat Immunol 2011; 12:304-311.
37. Miyara M, Yoshioka Y, Kitoh A, et al. Functional delineation and differentiation dynamics of human CD4 T cells expressing the FoxP3 transcription factor. Immunity 2009; 30:899-911.
38. Sakaguchi S, Miyara M, Costantino CM, Hafler DA. Foxp3 regulatory T cells in the human immune system. Nat Rev Immunol 2010; 10:490-500.
39. Liu W, Putnam AL, Xu-Yu Z, et al. CD127 expression inversely correlates with Foxp3 and suppressive function of human CD4 T reg cells. J Exp Med 2006; 203:1701-1711.
40. Seddiki N, Santner-Nanan B, Martinson J, et al. Expression of interleukin (IL)-2 and IL-7 receptors discriminates between human regulatory and activated T cells. J Exp Med 2006; 203:1693-1700.
41. Thornton AM, Korty PE, Tran DQ, et al. Expression of Helios, an Ikaros transcription factor family member, differentiates thymic-derived from peripherally induced Foxp3 T regulatory cells. J Immunol 2010; 184:3433-3441.
42. Akimova T, Beier UH, Wang L, et al. Helios expression is a marker of T cell activation and proliferation. PLoS One 2011; 6:e24226.
43. Kanno Y, Vahedi G, Hirahara K, et al. Transcriptional and epigenetic control of T helper cell specification: molecular mechanisms underlying commitment and plasticity. Annu Rev Immunol 2012; 30:707-731.
44. Baron U, Floess S, Wieczorek G, et al. DNA demethylation in the human FOXP3 locus discriminates regulatory T cells from activated FOXP3() conventional T cells. Eur J Immunol 2007; 37:2378-2389.
45. Floess S, Freyer J, Siewert C, et al. Epigenetic control of the Foxp3 locus in regulatory T cells. PLoS Biol 2007; 5:e38.
46. Curotto de Lafaille MA, Lino AC, Kutchukhidze N, Lafaille JJ. CD25-T cells generate CD25Foxp3 regulatory T cells by peripheral expansion. J Immunol 2004; 173:7259-7268.
47. Apostolou I, von Boehmer H. In vivo instruction of suppressor commitment in naive T cells. J Exp Med 2004; 199:1401-1408.
48. Chen W, Jin W, Hardegen N, et al. Conversion of peripheral CD4CD25-naive T cells to CD4CD25 regulatory T cells by TGF-beta induction of transcription factor Foxp3. J Exp Med 2003; 198:1875-1886.
49. Schallenberg S, Tsai PY, Riewaldt J, Kretschmer K. Identification of an immediate Foxp3(-) precursor to Foxp3() regulatory T cells in peripheral lymphoid organs of nonmanipulated mice. J Exp Med 2010; 207:1393-1407.
50. Francisco LM, Salinas VH, Brown KE. PD-L1 regulates the development, maintenance, and function of induced regulatory T cells. J Exp Med 2009; 206:3015-3029.
51. Coombes JL, Siddiqui KR, Arancibia-Carcamo CV, et al. A functionally specialized population of mucosal CD103 DCs induces Foxp3 regulatory T cells via a TGF-beta and retinoic acid-dependent mechanism. J Exp Med 2007; 204:1757-1764.
52. Quintana FJ, Basso AS, Iglesias AH, et al. Control of T(reg) and T(H)17 cell differentiation by the aryl hydrocarbon receptor. Nature 2008; 453:65-71.
53. Hill JA, Feuerer M, Tash K, et al. Foxp3 transcription-factor-dependent and-independent regulation of the regulatory T cell transcriptional signature. Immunity 2007; 27:786-800.
54. Zhou X, Bailey-Bucktrout SL, Jeker LT, et al. Instability of the transcription factor Foxp3 leads to the generation of pathogenic memory T cells in vivo. Nat Immunol 2009; 10:1000-1007.
55. McClymont SA, Putnam AL, Lee MR, et al. Plasticity of human regulatory T cells in healthy subjects and patients with type 1 diabetes. J Immunol 2011; 186:3918-3926.
56. Kukreja A, Cost G, Marker J, et al. Multiple immuno-regulatory defects in type-1 diabetes. J Clin Invest 2002; 109:131-140.
57. Lindley S, Dayan CM, Bishop A, et al. Defective suppressor function in CD4()CD25() T-cells from patients with type 1 diabetes. Diabetes 2005; 54:92-99.
58. Putnam AL, Vendrame F, Dotta F, Gottlieb PA. CD4CD25high regulatory T cells in human autoimmune diabetes. J Autoimmun 2005; 24:55-62.
59. Brusko T, Wasserfall C, McGrail K, et al. No alterations in the frequency of Foxp3 regulatory T-cells in type 1 diabetes. Diabetes 2007; 56:604-612.
60. Marwaha AK, Crome SQ, Panagiotopoulos C, et al. Cutting edge: increased IL-17-secreting T cells in children with new-onset type 1 diabetes. J Immunol 2010; 185:3814-3818.
61. Hughson A, Bromberg I, Johnson B, et al. Uncoupling of proliferation and cytokines from suppression within the CD4CD25Foxp3 T-cell compartment in the 1st year of human type 1 diabetes. Diabetes 2011; 60:2125-2133.
62. Badami E, Sorini C, Coccia M, et al. Defective differentiation of regulatory Foxp3 T cells by small-intestinal dendritic cells in patients with type 1 diabetes. Diabetes 2011; 60:2120-2124.
63. Schneider A, Rieck M, Sanda S, et al. The effector T cells of diabetic subjects are resistant to regulation via CD4 FOXP3 regulatory T cells. J Immunol 2008; 181:7350-7355.
64. Campbell DJ, Koch MA. Phenotypical and functional specialization of Foxp3 regulatory T cells. Nat Rev Immunol 2011; 11:119-130.
65. Sagoo P, Ali N, Garg G, et al. Human regulatory T cells with alloantigen specificity are more potent inhibitors of alloimmune skin graft damage than polyclonal regulatory T cells. Sci Transl Med 2011; 3:83ra42.
66. Tang Q, Adams JY, Penaranda C, et al. Central role of defective interleukin-2 production in the triggering of islet autoimmune destruction. Immunity 2008; 28:687-697.
67. Feuerer M, Jiang W, Holler PD, et al. Enhanced thymic selection of Foxp3 regulatory T cells in the NOD mouse model of autoimmune diabetes. Proc Natl Acad Sci USA 2007; 104:18181-18186.
68. Jailwala P, Waukau J, Glisic S, et al. Apoptosis of CD4 CD25(high) T cells in type 1 diabetes may be partially mediated by IL-2 deprivation. PLoS One 2009; 4:e6527.
69. Koch MA, Tucker-Heard G, Perdue NR, et al. The transcription factor T-bet controls regulatory T cell homeostasis and function during type 1 inflammation. Nat Immunol 2009; 10:595-602.
70. 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.
71. Dominguez-Villar M, Baecher-Allan CM, Hafler DA. Identification of T helper type 1-like, Foxp3 regulatory T cells in human autoimmune disease. Nat Med 2011; 17:673-675.
72. Yang XO, Nurieva R,Martinez GJ, et al. Molecular antagonism and plasticity of regulatory and inflammatory T cell programs. Immunity 2008; 29:44-56.
73. Oldenhove G, Bouladoux N, Wohlfert EA, et al. Decrease of Foxp3 Treg number and acquisition of effector cell phenotype during lethal infection. Immunity 2009; 31:772-786.
74. Sharma MD, Hou DY, Baban B, et al. Reprogrammed Foxp3() regulatory T cells provide essential help to support cross-presentation and CD8() T cell priming in naive mice. Immunity 2010; 33:942-954.
75. Snell-Bergeon JK, West NA, Mayer-Davis EJ, et al. Inflammatory markers are increased in youth with type 1 diabetes: the SEARCH Case-Control study. J Clin Endocrinol Metab 2010; 95:2868-2876.
76. Aribi M, Moulessehoul S, Kendouci-Tani M, et al. Relationship between interleukin-1beta and lipids in type 1 diabetic patients. Med Sci Monit 2007; 13:CR372-CR378.
77. Rachmiel M, Bloch O, Shaul AA, et al. Young patients with both type 1 diabetes mellitus and asthma have a unique IL-12 and IL-18 secretory pattern. Pediatr Diabetes 2011; 12:596-603.
78. Chen X, Baumel M, Mannel DN, et al. Interaction of TNF with TNF receptor type 2 promotes expansion and function of mouse CD4CD25 T regulatory cells. J Immunol 2007; 179:154-161.
79. Chen X, Oppenheim JJ. TNF-alpha: an activator of CD4Foxp3TNFR2 regulatory T cells. Curr Dir Autoimmun 2010; 11:119-134.
80. Ma HL, Napierata L, Stedman N, et al. Tumor necrosis factor alpha blockade exacerbates murine psoriasis-like disease by enhancing Th17 function and decreasing expansion of Treg cells. Arthritis Rheum 2010; 62:430-440.
81. Zheng Y, Josefowicz S, Chaudhry A, et al. Role of conserved noncoding DNA elements in the Foxp3 gene in regulatory T-cell fate. Nature 2010; 463:808-812.
82. Polansky JK, Schreiber L, Thelemann C, et al. Methylation matters: binding of Ets-1 to the demethylated Foxp3 gene contributes to the stabilization of Foxp3 expression in regulatory T cells. J Mol Med (Berl) 2010; 88:1029-1040.
83. Kim HP, Leonard WJ. CREB/ATF-dependent T cell receptor-induced FoxP3 gene expression: a role for DNA methylation. J Exp Med 2007; 204:1543-1551.
84. Burchill MA, Yang J, Vogtenhuber C, et al. IL-2 receptor beta-dependent STAT5 activation is required for the development of Foxp3 regulatory T cells. J Immunol 2007; 178:280-290.
85. Wang L, de Zoeten EF, Greene MI, Hancock WW. Immunomodulatory effects of deacetylase inhibitors: therapeutic targeting of Foxp3 regulatory T cells. Nat Rev Drug Discov 2009; 8:969-981.
86. Xiao Y, Li B, Zhou Z, et al. Histone acetyltransferase mediated regulation of Foxp3 acetylation and Treg function. Curr Opin Immunol 2010; 22:583-591.
87. Van Loosdregt J, Brunen D, Fleskens V, et al. Rapid temporal control of Foxp3 protein degradation by sirtuin-1. PLoS One 2011; 6:e19047.
88. Chong MM, Rasmussen JP, Rudensky AY, Littman DR. The RNAseIII enzyme Drosha is critical in T cells for preventing lethal inflammatory disease. J Exp Med 2008; 205:2005-2017.
89. Lu LF, Boldin MP, Chaudhry A, et al. Function of miR-146a in controlling Treg cell-mediated regulation of Th1 responses. Cell 2010; 142:914-929.