CD8+ T cells in autoimmunity

Inmunologia

Volumn 27, Issue 1, 2008, Pages 11-21

  Tsai, S ^a   Shameli, A ^a   Santamaria, Pere ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

Autoimmunity; CD8+ suppressor T lymphocytes; CD8+ T lymphocytes

Indexed keywords

EPITOPE;

AUTOIMMUNE DISEASE; AUTOIMMUNITY; CD8+ T LYMPHOCYTE; CELL COMPARTMENTALIZATION; DIABETOGENESIS; LYMPHOCYTE ACTIVATION; NONHUMAN; PATHOGENESIS; REVIEW;

EID: 44649167001     PISSN: 02139626     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0213-9626(08)70045-3     Document Type: Review

References (113)

1. Palmer E. Negative selection-clearing out the bad apples from the T-cell repertoire. Nat Rev Immunol 2003; 3: 383-391.
2. Zehn D, Bevan MJ. T cells with low avidity for a tissue-restricted antigen routinely evade central and peripheral tolerance and cause autoimmunity. Immunity 2006; 25: 261-270.
3. Van Parijs L, Abbas AK. Homeostasis and self-tolerance in the immune system: turning lymphocytes off. Science 1998; 280: 243-248.
4. Redmond WL, Sherman LA. Peripheral tolerance of CD8 T lymphocytes. Immunity 2005; 22: 275-284.
5. Dyment DA, Sadovnick AD, Willer CJ, Armstrong H, Cader ZM, Wiltshire S, et al. An extended genome scan in 442 Canadian multiple sclerosis-affected sibships: A report from the Canadian Collaborative Study Group. Hum Mol Genet 2004; 13: 1005-1015.
6. Lincoln MR, Montpetit A, Cader MZ, Saarela J, Dyment DA, Tiislar M, et al. A predominant role for the HLA class II region in the association of the MHC region with multiple sclerosis. Nat Genet 2005; 37: 1108-1112.
7. Nepom GT, Kwok WW. Molecular basis for HLA-DQ associations with IDDM. Diabetes 1998; 47: 1177-1184.
8. Langholz B, Tuomilehto-Wolf E, Thomas D, Pitkaniemi J, Tuomilehto J. Variation in HLA-associated risks of childhood insulin-dependent diabetes in the Finnish population: I. Allele effects at A, B, and DR loci. DiMe Study Group. Childhood Diabetes in Finland. Genet Epidemiol 1995; 12: 441-453.
9. Noble JA, Valdes AM, Bugawan TL, Apple RJ, Thomson G, Erlich HA. The HLA class I A locus affects susceptibility to type 1 diabetes. Hum Immunol 2002; 63: 657-664.
10. Tait BD, Colman PG, Morahan G, Marchinovska L, Dore E, Gellert S, et al. HLA genes associated with autoimmunity and progression to disease in type 1 diabetes. Tissue Antigens 2003; 61: 146-153.
11. Itoh N, Hanafusa T, Miyazaki A, Miyagawa J, Yamagata K, Yamamoto K, et al. Mononuclear cell infiltration and its relation to the expression of major histocompatibility complex antigens and adhesion molecules in pancreas biopsy specimens from newly diagnosed insulin-dependent diabetes mellitus patients. J Clin Invest 1993; 92: 2313-2322.
12. Santamaria P, Nakhleh RE, Sutherland DE, Barbosa JJ. Characterization of T lymphocytes infiltrating human pancreas allograft affected by isletitis and recurrent diabetes. Diabetes 1992; 41: 53-61.
13. Somoza N, Vargas F, Roura-Mir C, Vives-Pi M, Fernandez-Figueras MT, Ariza A, et al. Pancreas in recent onset insulin-dependent diabetes mellitus. Changes in HLA, adhesion molecules and autoantigens, restricted T cell receptor V beta usage, and cytokine profile. J Immunol 1994; 153: 1360-1377.
14. + T cells in organ-specific autoimmune diseases: insight from transgenic mouse models. Immunol Rev 1999; 169: 81-92.
15. + cytotoxic T cells in the destruction of pancreatic beta-cells in nonobese diabetic mice. J Immunol 1994; 152: 2042-2050.
16. Serreze DV, Chapman HD, Varnum DS, Gerling I, Leiter EH, Shultz LD. Initiation of autoimmune diabetes in NOD/Lt mice is MHC class I-dependent. J Immunol 1995 158: 3978-3986.
17. Serreze DV, Leiter EH, Christianson GJ, Greiner D, Roopenian, DC. Major histocompatibility complex class I-deficient NOD-B2mnull mice are diabetes and insulitis resistant. Diabetes 1994; 43: 505-509.
18. + T cells in the initiation of insulin-dependent diabetes mellitus. Eur J Immunol 1996; 26: 1762-1769.
19. DiLorenzo TP, Graser RT, Ono T, Christianson GJ, Chapman HD, Roopenian DC, et al. Major histocompatibility complex class I-restricted T cells are required for all but the end stages of diabetes development in nonobese diabetic mice and use a prevalent T cell receptor alpha chain gene rearrangement. Proc Natl Acad Sci USA 1998; 95: 12538-12543.
20. Sumida T, Furukawa M, Sakamoto A, Namekawa T, Maeda T, Zijlstra M, et al. Prevention of insulitis and diabetes in beta 2-microglobulin-deficient non-obese diabetic mice. Int Immunol 1994; 6: 1445-1449.
21. Pearson T, Markees TG, Serreze DV, Pierce MA, Marron MP, Wicker LS, et al. Genetic disassociation of autoimmunity and resistance to costimulation blockade-induced transplantation tolerance in nonobese diabetic mice. J Immunol 2003; 171: 185-195.
22. + T-cells from diabetic versus prediabetic NOD.NON-Thy-1a donors. Diabetes 1993; 42: 44-55.
23. Wong FS, Karttunen J, Dumont C, Wen L, Visintin I, Pilip IM, et al. Identification of an MHC class I-restricted autoantigen in type 1 diabetes by screening an organ-specific cDNA library. Nat Med 1999; 5: 1026-1031.
24. + T cells from nonobese diabetic mice use highly homologous T cell receptor alpha-chain CDR3 sequences. J Immunol 1995; 154: 2494-2503.
25. + T cells expressing identical endogenous TCR-alpha chains. J Immunol 1996; 157: 4726-4735.
26. + T cells in autoimmune diabetes. Proc Natl Acad Sci USA 2003; 100: 8384-8388.
27. Verdaguer J, Schmidt D, Amrani A, Anderson B, Averill N, Santamaria P. Spontaneous autoimmune diabetes in monoclonal T cell nonobese diabetic mice. J Exp Med 1997; 186: 1663-1676.
28. Trudeau JD, Kelly-Smith C, Verchere CB, Elliott JF, Dutz JP, Finegood DT, et al. Prediction of spontaneous autoimmune diabetes in NOD mice by quantification of autoreactive T cells in peripheral blood. J Clin Invest 2003; 111: 217-223.
29. Amrani A, Verdaguer J, Serra P, Tafuro S, Tan R, Santamaria P. Progression of autoimmune diabetes driven by avidity maturation of a T-cell population. Nature 2000; 406: 739-742.
30. Han B, Serra P, Yamanouchi J, Amrani A, Elliott JF, Dickie P, et al. Developmental control of CD8 T cell-avidity maturation in autoimmune diabetes. J Clin Invest 2005; 115: 1879-1887.
31. Han B, Serra P, Amrani A, Yamanouchi J, Maree AF, Edelstein-Keshet L, Santamaria P. Prevention of diabetes by manipulation of anti-IGRP autoimmunity: high efficiency of a low-affinity peptide. Nat Med 2005; 11: 645-652.
32. Standifer NE, Ouyang Q, Panagiotopoulos C, Verchere CB, Tan R, Greenbaum CJ, et al. Identification of Novel HLA-A*0201-restricted epitopes in recent-onset type 1 diabetic subjects and antibody-positive relatives. Diabetes 2006; 55: 3061-3067.
33. Hassainya Y, Garcia-Pons F, Kratzer R, Lindo V, Greer F, Lemonnier FA, et al. Identification of naturally processed HLA-A2-restricted proinsulin epitopes by reverse immunology. Diabetes 2005; 54: 2053-2059.
34. Toma A, Haddouk S, Briand JP, Camoin L, Gahery H, Connan F, et al. Recognition of a subregion of human proinsulin by class I-restricted T cells in type 1 diabetic patients. Proc Natl Acad Sci USA 2005; 102: 10581-10586.
35. Pinkse GG, Boitard C, Tree TI, Peakman M, Roep BO. HLA class I epitope discovery in type 1 diabetes: Independent and reproducible identification of proinsulin epitopes of CD8 T cells-report of the IDS T Cell Workshop Committee. Ann NY Acad Sci 2006; 1079: 19-23.
36. Serreze DV, Marron MP, Dilorenzo TP. "Humanized" HLA transgenic NOD mice to identify pancreatic beta cell autoantigens of potential clinical relevance to type 1 diabetes. Ann NY Acad Sci 2007; 1103: 103-111.
37. Takaki T, Marron MP, Mathews CE, Guttmann ST, Bottino R, Trucco M, et al. HLA-A*0201-restricted T cells from humanized NOD mice recognize autoantigens of potential clinical relevance to type 1 diabetes. J Immunol.2006; 176:3257-3265.
38. Blancou P, Mallone R, Martinuzzi E, Severe S, Pogu S, Novelli G, et al. Immunization of HLA class I transgenic mice identifies autoantigenic epitopes eliciting dominant responses in type 1 diabetes patients. J Immunol 2007; 178: 7458-7466.
39. Furuzawa-Carballeda J, Vargas-Rojas MI, Cabral RA. Autoimmune inflammation from the Th17 perspective. Autoimmun Rev 2007; 6:169-175.
40. Sospedra M, Martin R. Immunology of multiple sclerosis. Annu Rev Immunol 2005; 23: 683-747.
41. Huseby ES, Ohlen C, Goverman J. Cutting edge: myelin basic protein-specific cytotoxic T cell tolerance is maintained in vivo by a single dominant epitope in H-2k mice. J Immunol 1999; 163: 1115-1118.
42. + T cells are encephalitogenic and produce severe disease in C57BL/6 mice. J Immunol 2001; 166: 7579-7587.
43. + T cells in a model for multiple sclerosis. J Exp Med 2001; 194: 669-676.
44. + T cell responses during experimental autoimmune encephalomyelitis. Eur J Immunol 2005; 35: 76-85.
45. Fogdell-Hahn A, Ligers A, Gronning M, Hillert J, Olerup O. Multiple sclerosis: A modifying influence of HLA class I genes in an HLA class II associated autoimmune disease. Tissue Antigens 2000; 55: 140-148.
46. Yeo TW, De Jager PL, Gregory SG, Barcellos LF, Walton A, Goris A, et al. A second major histocompatibility complex susceptibility locus for multiple sclerosis. Ann Neurol 2007; 61: 228-236.
47. van Oosten BW, Lai M, Hodgkinson S, Barkhof F, Miller DH, Moseley IF, et al. Treatment of multiple sclerosis with the monoclonal anti-CD4 antibody cM-T412: results of a randomized, double-blind, placebo-controlled, MR-monitored phase II trial. Neurology 1997; 49: 351-357.
48. Hauser SL, Bhan AK, Gilles F, Kemp M, Kerr C, Weiner HL. Immunohistochemical analysis of the cellular infiltrate in multiple sclerosis lesions. Ann Neurol 1986; 19: 578-587.
49. Grenier Y, Ruijs TC, Robitaille Y, Olivier A, Antel JP. Immunohistochemical studies of adult human glial cells. J Neuroimmunol 1989; 21: 103-115.
50. Booss J, Esiri MM, Tourtellotte WW, Mason DY. Immunohistological analysis of T lymphocyte subsets in the central nervous system in chronic progressive multiple sclerosis. J Neurol Sci 1983; 62: 219-232.
51. + T cells in cerebrospinal fluid from multiple sclerosis patients. Brain 2002; 125: 538-550.
52. + T cells dominate the T cell infiltrate in active multiple sclerosis lesions as shown by micromanipulation and single cell polymerase chain reaction. J Exp Med 2000; 192: 393-404.
53. Neumann H, Medana IM, Bauer J, Lassmann H. Cytotoxic T lymphocytes in autoimmune and degenerative CNS diseases. Trends Neurosci 2002; 25: 313-319.
54. Jurewicz A, Biddison WE, Antel JP. MHC class I-restricted lysis of human oligodendrocytes by myelin basic protein peptide-specific CD8 T lymphocytes. J Immunol 1998; 160: 3056-3059.
55. + T-cell responses to human myelin protein-derived peptides. Proc Natl Acad Sci USA 1994; 91: 10859-10863.
56. Dressel A, Chin JL, Sette A, Gausling R, Hollsberg P, Hafler DA. Autoantigen recognition by human CD8 T cell clones: Enhanced agonist response induced by altered peptide ligands. J Immunol 1997; 159: 4943-4951.
57. + T lymphocytes from beta2 microglobulin (,2m) HLA-A2.1 monochain transgenic H-2Db ,2m double knockout mice. J Exp Med 1997; 185: 2043-2051.
58. Mars LT, Bauer J, Gross DA, Bucciarelli F, Firat H, Hudrisier D, et al. CD8 T cell responses to myelin oligodendrocyte glycoprotein-derived peptides in humanized HLA-A*0201-transgenic mice. J Immunol 2007; 179: 5090-5098.
59. de Jersey J, Snelgrove SL, Palmer SE, Teteris SA, Mullbacher A, Miller JF, Slattery RM. Beta cells cannot directly prime diabetogenic CD8 T cells in nonobese diabetic mice. Proc Natl Acad Sci USA 2007; 104: 1295-1300.
60. Gagnerault MC, Luan JJ, Lotton C, Lepault F. Pancreatic lymph nodes are required for priming of beta cell reactive T cells in NOD mice. J Exp Med 2002; 196: 369-377.
61. Turley S, Poirot L, Hattori M, Benoist C, Mathis D. Physiological beta cell death triggers priming of self-reactive T cells by dendritic cells in a type-1 diabetes model. J Exp Med 2003; 198: 1527-1537.
62. Yamanouchi J, Verdaguer J, Han B, Amrani A, Serra P, Santamaria P. Cross-priming of diabetogenic T cells dissociated from CTL-induced shedding of beta cell autoantigens. J Immunol 2003; 171: 6900-6909.
63. Trudeau JD, Dutz JP, Arany E, Hill DJ, Fieldus WE, Finegood DT. Neonatal beta-cell apoptosis: A trigger for autoimmune diabetes? Diabetes 2000; 49: 1-7.
64. Zhang Y, O'Brien B, Trudeau J, Tan R, Santamaria P, Dutz JP. In situ beta cell death promotes priming of diabetogenic CD8 T lymphocytes. J Immunol 2002; 168: 1466-1472.
65. Kurts C, Sutherland RM, Davey G, Li M, Lew AM, Blanas E, et al. CD8 T cell ignorance or tolerance to islet antigens depends on antigen dose. Proc Natl Acad Sci USA 1999; 96: 12703-12707.
66. Harbers SO, Crocker A, Catalano G, D'Agati V, Jung S, Desai DD, Clynes R. Antibody-enhanced cross-presentation of self antigen breaks T cell tolerance. J Clin Invest 2007; 117: 1361-1369.
67. Rock KL Shen L. Cross-presentation: Underlying mechanisms and role in immune surveillance. Immunol Rev 2005; 207: 166-183.
68. Frigerio S, Junt T, Lu B, Gerard C, Zumsteg U, Hollander GA, Piali L. Beta cells are responsible for CXCR3-mediated T-cell infiltration in insulitis. Nat Med 2002; 8: 1414-1420.
69. Lang KS, Recher M, Junt T, Navarini AA, Harris NL, Freigang S, et al. Toll-like receptor engagement converts T-cell autoreactivity into overt autoimmune disease. Nat Med 2005; 11: 138-145.
70. Baccala R, Hoebe K, Kono DH, Beutler B, Theofilopoulos AN. TLR-dependent and TLR-independent pathways of type I interferon induction in systemic autoimmunity. Nat Med 2007; 13: 543-551.
71. Graser RT, DiLorenzo TP, Wang F, Christianson GJ, Chapman HD, Roopenian DC, et al. Identification of a CD8 T cell that can independently mediate autoimmune diabetes development in the complete absence of CD4 T cell helper functions. J Immunol 2000; 164: 3913-3918.
72. Heath WR, Carbone FR. Cross-presentation, dendritic cells, tolerance and immunity. Annu Rev Immunol 2001; 19: 47-64.
73. + T cell tolerance through PD-1 and CTLA-4. Nat Immunol 2005; 6: 280-286.
74. Perez VL, Van Parijs L, Biuckians A, Zheng XX, Strom TB, Abbas AK. Induction of peripheral T cell tolerance in vivo requires CTLA-4 engagement. Immunity 1997; 6: 411-417.
75. Tivol EA, Borriello F, Schweitzer AN, Lynch WP, Bluestone JA, Sharpe AH. Loss of CTLA-4 leads to massive lymphoproliferation and fatal multiorgan tissue destruction, revealing a critical negative regulatory role of CTLA-4. Immunity 1995; 3: 541-547.
76. Waterhouse P, Penninger JM, Timms E, Wakeham A, Shahinian A, Lee KP, et al. Lymphoproliferative disorders with early lethality in mice deficient in Ctla-4. Science 1995; 270: 985-988.
77. Perrin PJ, Maldonado JH, Davis TA, June CH, Racke MK. CTLA-4 blockade enhances clinical disease and cytokine production during experimental allergic encephalomyelitis. J. Immunol. 1996; 157: 1333-1336.
78. + T cell responses to antigen in lymph nodes and tissues. J Immunol 2007; 179: 5064-5070.
79. Wang J, Yoshida T, Nakaki F, Hiai H, Okazaki T, Honjo T. Establishment of NOD-Pdcd1-/- mice as an efficient animal model of type I diabetes. Proc Natl Acad Sci USA 2005; 102: 11823-11828.
80. Nishimura H, Nose M, Hiai H, Minato N, Honjo T. Development of lupus-like autoimmune diseases by disruption of the PD-1 gene encoding an ITIM motif-carrying immunoreceptor. Immunity 1999; 11: 141-151.
81. Salama AD, Chitnis T, Imitola J, Ansari MJ, Akiba H, Tushima F, et al. Critical role of the programmed death-1 (PD-1) pathway in regulation of experimental autoimmune encephalomyelitis. J Exp Med 2003; 198: 71-78.
82. Latchman YE, Liang SC, Wu Y, Chernova T, Sobel RA, Klemm M, et al. PD-L1-deficient mice show that PD-L1 on T cells, antigen-presenting cells, and host tissues negatively regulates T cells. Proc Natl Acad Sci USA 2004; 101: 10691-10696.
83. Keir ME, Liang SC, Guleria I, Latchman YE, Qipo A, Albacker LA, et al. Tissue expression of PD-L1 mediates peripheral T cell tolerance. J Exp Med 2006; 203: 883-895.
84. Ansari MJ, Salama AD, Chitnis T, Smith RN, Yagita H, Akiba H, et al. The programmed death-1 (PD-1) pathway regulates autoimmune diabetes in nonobese diabetic (NOD) mice. J Exp Med 2003; 198: 63-69.
85. Guleria I, Gubbels Bupp M, Dada S, Fife B, Tang Q, Ansari MJ, et al. Mechanisms of PDL1-mediated regulation of autoimmune diabetes. Clin Immunol 2007; 125: 16-25.
86. Fife BT, Guleria I, Gubbels Bupp M, Eagar TN, Tang Q, Bour-Jordan H, et al. Insulin-induced remission in new-onset NOD mice is maintained by the PD-1-PD-L1 pathway. J Exp Med 2006; 203: 2737-2747.
87. Gao W, Demirci G, Strom TB, Li XC. Stimulating PD-1-negative signals concurrent with blocking CD154 co-stimulation induces long-term islet allograft survival. Transplantation 2003; 76: 994-999.
88. Rodgers JR, Cook RG. MHC class Ib molecules bridge innate and acquired immunity. Nat Rev Immunol 2005; 5: 459-471.
89. Hu D, Ikizawa K, Lu L, Sanchirico ME, Shinohara ML, Cantor H. Analysis of regulatory CD8 T cells in Qa-1-deficient mice. Nat Immunol 2004; 5: 516-523.
90. + cells in T cell receptor peptide-induced clonal unresponsiveness. Science 1993; 259: 91-94.
91. + T cells. Proc Natl Acad Sci USA 1998; 95: 4533-4537.
92. Madakamutil LT, Maricic I, Sercarz E, Kumar V. Regulatory T cells control autoimmunity in vivo by inducing apoptotic depletion of activated pathogenic lymphocytes. J Immunol 2003; 170: 2985-2992.
93. + T cells. J Immunol 2006; 177: 7645-7655.
94. Panoutsakopoulou V, Huster KM, McCarty N, Feinberg E, Wang R, Wucherpfennig KW, Cantor H. Suppression of autoimmune disease after vaccination with autoreactive T cells that express Qa-1 peptide complexes. J Clin Invest 2004; 113: 1218-1224.
95. Jiang H, Wu Y, Liang B, Zheng Z, Tang G, Kanellopoulos J, et al. 2005. An affinity/avidity model of peripheral T cell regulation. J Clin Invest 115: 302-312.
96. Shmidt TE, Zhuchenko TD, Iakhno NN. Glatiramer acetate (Copaxone) influence on different stages of multiple sclerosis pathogenesis. Zh Nevrol Psikhiatr Im S S Korsakova 2003; (Spec No 2): 79-82.
97. + T-cell repertoire in multiple sclerosis. J Neuroimmunol 2006; 180: 159-171.
98. + T cells in multiple sclerosis. J Immunol 2006; 176: 7119-7129.
99. Suzuki H, Kundig TM, Furlonger C, Wakeham A, Timms E, Matsuyama T, et al. Deregulated T cell activation and autoimmunity in mice lacking interleukin-2 receptor beta. Science 1995; 268: 1472-1476.
100. +CD122 regulatory T cells in the maintenance of T cell homeostasis. J Exp Med 2004; 200: 1123-1134.
101. + T cells. J Immunol 2005; 175: 7093-7097.
102. + T cells, a newly identified regulatory T subset, negatively regulate Graves' hyperthyroidism in a murine model. Endocrinology 2007; 148: 6040-6046.
103. + regulatory T cells in the recovery from experimental autoimmune Encephalomyelitis. J Immunol 2008; 180: 825-832.
104. - regulatory T cells. J Immunol 1998; 161: 5193-5202.
105. - T cells. Transplantation 2000; 69: 1304-1310.
106. - T cells in an autoimmune disease model. J Clin Invest 2003; 112: 1037-1048.
107. +CD28 regulatory cells in suppressing myasthenia gravis-associated responses by a dual altered peptide ligand. Proc Natl Acad Sci USA 2007; 104: 17459-17464.
108. Paas-Rozner M, Sela M, Mozes E. The nature of the active suppression of responses associated with experimental autoimmune myasthenia gravis by a dual altered peptide ligand administered by different routes. Proc Natl Acad Sci USA 2001; 98: 12642-12647.
109. Chang CC, Ciubotariu R, Manavalan JS, Yuan J, Colovai AI, Piazza F, et al. Tolerization of dendritic cells by T(S) cells: the crucial role of inhibitory receptors ILT3 and ILT4. Nat Immunol 2002; 3: 237-243.
110. + tolerogenic endothelial cells, inhibiting alloreactivity. Int Immunol 2004; 16: 1055-1068.
111. + T cell-mediated suppression of autoimmunity in a murine lupus model of peptide-induced immune tolerance depends on Foxp3 expression. J Immunol 2007; 178: 7649-7657.
112. Kang HK, Michaels MA, Berner BR, Datta SK. Very low-dose tolerance with nucleosomal peptides controls lupus and induces potent regulatory T cell subsets. J Immunol 2005; 174: 3247-3255.
113. Seo SK, Choi JH, Kim YH, Kang WJ, Park HY, Suh JH, et al. 4-1BB-mediated immunotherapy of rheumatoid arthritis. Nat Med 2004; 0: 1088-1094.