Pathogenic T-cell clones in autoimmune diabetes: More lessons from the NOD mouse

Advances in Immunology

Volumn 87, Issue , 2005, Pages 123-162

  Haskins, Kathryn ^a  

^a UNIVERSITY OF COLORADO DENVER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; CHEMOKINE; CHEMOKINE RECEPTOR; CYTOKINE; CYTOKINE RECEPTOR; INSULIN; MAJOR HISTOCOMPATIBILITY ANTIGEN; PEPTIDE LIBRARY; T LYMPHOCYTE RECEPTOR; TETRAMER;

AMINO ACID SUBSTITUTION; ANTIGEN PRESENTATION; ANTIGEN SPECIFICITY; AUTOIMMUNE DISEASE; CELL CLONE; CELL CULTURE; CELL FUNCTION; CELL MIGRATION; CELL PROLIFERATION; DIABETES MELLITUS; EFFECTOR CELL; GENE EXPRESSION; GENE LOCUS; IMMUNOREGULATION; MOLECULAR CLONING; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEOMICS; REVIEW; SPLEEN CELL; T LYMPHOCYTE; TRANSGENE; TRANSGENIC MOUSE;

ANIMALS; AUTOANTIGENS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL MOVEMENT; CHEMOKINES; CLONE CELLS; CYTOKINES; DIABETES MELLITUS, TYPE 1; GENES, T-CELL RECEPTOR; HUMANS; MICE; MICE, INBRED NOD; MICE, TRANSGENIC; RECEPTORS, CHEMOKINE; RECEPTORS, CYTOKINE; RNA, MESSENGER; T-LYMPHOCYTES;

EID: 23644439438     PISSN: 00652776     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0065-2776(05)87004-X     Document Type: Review

References (152)

1. Abramson O., Qiu S., and Erle D.J. Preferential production of interferon-gamma by CD4+ T cells expressing the homing receptor integrin alpha4/beta7 Immunology 103 2001 155 163
2. Achenbach P., Kelemen K., Wegmann D.R., and Hutton J.C. Spontaneous peripheral T-cell responses to the IA-2beta (phogrin) autoantigen in young nonobese diabetic mice J. Autoimmun. 19 2002 111 116
3. Altman J.D., Moss P.A., Goulder P.J., Barouch D.H., McHeyzer-Williams M.G., Bell J.I., McMichael A.J., and Davis M.M. Phenotypic analysis of antigen-specific T lymphocytes Science 274 1996 94 96
4. Amrani A., Verdaguer J., Serra P., Tafuro S., Tan R., and Santamaria P. Progression of autoimmune diabetes driven by avidity maturation of a T-cell population Nature 406 2000 739 742
5. Amrani A., Verdaguer J., Thiessen S., Bou S., and Santamaria P. IL-1alpha, IL-1beta, and IFN-gamma mark beta cells for Fas-dependent destruction by diabetogenic CD4(+) T lymphocytes J. Clin. Invest. 105 2000 459 468
6. Anderson B., Park B.J., Verdaguer J., Amrani A., and Santamaria P. Prevalent CD8(+) T cell response against one peptide/MHC complex in autoimmune diabetes Proc. Natl. Acad. Sci. USA 96 1999 9311 9316
7. Andre-Schmutz I., Hindelang C., Benoist C., and Mathis D. Cellular and molecular changes accompanying the progression from insulitis to diabetes Eur. J. Immunol. 29 1999 245 255
8. Arden S.D., Zahn T., Steegers S., Webb S., Bergman B., O'Brien R.M., and Hutton J.C. Molecular cloning of a pancreatic islet-specific glucose-6-phosphatase catalytic subunit-related protein Diabetes 48 1999 531 542
9. Arnold P.Y., Burton A.R., and Vignali D.A. Diabetes incidence is unaltered in glutamate decarboxylase 65-specific TCR retrogenic nonobese diabetic mice: Generation by retroviral-mediated stem cell gene transfer J. Immunol. 173 2004 3103 3111
10. Bendelac A., Carnaud C., Boitard C., and Bach J.F. Syngeneic transfer of autoimmune diabetes from diabetic NOD mice to healthy neonates. Requirement for both L3T4+ and Lyt-2+ T cells J. Exp. Med. 166 1987 823 832
11. Bergman B., and Haskins K. Islet-specific T-cell clones from the NOD mouse respond to beta-granule antigen Diabetes 43 1994 197 203
12. Bergman B., and Haskins K. Autoreactive T-cell clones from the nonobese diabetic mouse Proc. Soc. Exp. Biol. Med. 214 1997 41 48
13. Bergman B., McManaman J.L., and Haskins K. Biochemical characterization of a beta cell membrane fraction antigenic for autoreactive T-cell clones J. Autoimmun. 14 2000 343 351
14. Bradley L.M., Asensio V.C., Schioetz L.K., Harbertson J., Krahl T., Patstone G., Woolf N., Campbell I.L., and Sarvetnick N. Islet-specific Th1, but not Th2, cells secrete multiple chemokines and promote rapid induction of autoimmune diabetes J. Immunol. 162 1999 2511 2520
15. Brandtzaeg P., Farstad I.N., and Haraldsen G. Regional specialization in the mucosal immune system: Primed cells do not always home along the same track Immunol. Today 20 1999 267 277
16. Brimnes M.K., Jensen T., Jorgensen T.N., Michelsen B.K., Troelsen J., and Werdelin O. Low expression of insulin in the thymus of non-obese diabetic mice J. Autoimmun. 19 2002 203 213
17. Butcher E.C., Williams M., Youngman K., Rott L., and Briskin M. Lymphocyte trafficking and regional immunity Adv. Immunol. 72 1999 209 253
18. Candeias S., Katz J., Benoist C., Mathis D., and Haskins K. Islet-specific T-cell clones from nonobese diabetic mice express heterogeneous T-cell receptors Proc. Natl. Acad. Sci. USA 88 1991 6167 6170
19. Crawford F., Huseby E., White J., Marrack P., and Kappler J.W. Mimotopes for Alloreactive and Conventional T Cells in a Peptide-MHC Display Library PLoS Biol. 2 2004 E90
20. Cuff C.A., Schwartz J., Bergman C.M., Russell K.S., Bender J.R., and Ruddle N.H. Lymphotoxin alpha3 induces chemokines and adhesion molecules: Insight into the role of LT alpha in inflammation and lymphoid organ development J. Immunol. 161 1998 6853 6860
21. Dallas-Pedretti A., McDuffie M., and Haskins K. A diabetes-associated T-cell autoantigen maps to a telomeric locus on mouse chromosome 6 Proc. Natl. Acad. Sci. USA 92 1995 1386 1390
22. Daniel D., Gill R.G., Schloot N., and Wegmann D. Epitope specificity, cytokine production profile and diabetogenic activity of insulin-specific T-cell clones isolated from NOD mice Eur. J. Immunol. 25 1995 1056 1062
23. Daniel D., and Wegmann D.R. Intranasal administration of insulin peptide B: 9-23 protects NOD mice from diabetes Ann. N. Y. Acad. Sci. 778 1996 371 372
24. Daniel D., and Wegmann D.R. Protection of nonobese diabetic mice from diabetes by intranasal or subcutaneous administration of insulin peptide B-(9-23) Proc. Natl. Acad. Sci. USA 93 1996 956 960
25. Delovitch T.L., and Singh B. The nonobese diabetic mouse as a model of autoimmune diabetes: Immune dysregulation gets the NOD Immunity 7 1997 727 738
26. DiLorenzo T.P., Graser R.T., Ono T., Christianson G.J., Chapman H.D., Roopenian D.C., Nathenson S.G., and Serreze D.V. 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 95 1998 12538 12543
27. Dobbs C., and Haskins K. Comparison of a T-cell clone and of T cells from a TCR transgenic mouse: TCR transgenic T cells specific for self-antigen are atypical J. Immunol. 166 2001 2495 2504
28. Dorner B.G., Scheffold A., Rolph M.S., Huser M.B., Kaufmann S.H., Radbruch A., Flesch I.E., and Kroczek R.A. MIP-1alpha, MIP-1beta, RANTES, and ATAC/lymphotactin function together with IFN-gamma as type 1 cytokines Proc. Natl. Acad. Sci. USA 99 2002 6181 6186
29. Dorner B.G., Steinbach S., Huser M.B., Kroczek R.A., and Scheffold A. Single-cell analysis of the murine chemokines MIP-1alpha, MIP-1beta, RANTES and ATAC/lymphotactin by flow cytometry J. Immunol. Methods 274 2003 83 91
30. Ellerman K.E., and Like A.A. Islet cell membrane antigens activate diabetogenic CD4+ T-cells in the BB/Wor rat Diabetes 48 1999 975 982
31. Fleming T.J., and Malek T.R. Multiple glycosylphosphatidylinositol- anchored Ly-6 molecules and transmembrane Ly-6E mediate inhibition of IL-2 production J. Immunol. 153 1994 1955 1962
32. Gonzalez A., Andre-Schmutz I., Carnaud C., Mathis D., and Benoist C. Damage control, rather than unresponsiveness, effected by protective DX5+ T cells in autoimmune diabetes Nat. Immunol. 2 2001 1117 1125
33. Gonzalez A., Katz J.D., Mattei M.G., Kikutani H., Benoist C., and Mathis D. Genetic control of diabetes progression Immunity 7 1997 873 883
34. Graser R.T., DiLorenzo T.P., Wang F., Christianson G.J., Chapman H.D., Roopenian D.C., Nathenson S.G., and Serreze D.V. 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. 164 2000 3913 3918
35. Groenen P., and Wieringa B. Expanding complexity in myotonic dystrophy Bioessays 20 1998 901 912
36. Gurlo T., Kawamura K., and von Grafenstein H. Role of inflammatory infiltrate in activation and effector function of cloned islet reactive nonobese diabetic CD8+ T cells: Involvement of a nitric oxide-dependent pathway J. Immunol. 163 1999 5770 5780
37. Hagopian W.A., Michelsen B., Karlsen A.E., Larsen F., Moody A., Grubin C.E., Rowe R., Petersen J., McEvoy R., and Lernmark A. Autoantibodies in IDDM primarily recognize the 65,000-M(r) rather than the 67,000-M(r) isoform of glutamic acid decarboxylase Diabetes 42 1993 631 636
38. Halbout P., Briand J.P., Becourt C., Muller S., and Boitard C. T cell response to preproinsulin I and II in the nonobese diabetic mouse J. Immunol. 169 2002 2436 2443
39. Hanninen A., Jaakkola I., and Jalkanen S. Mucosal addressin is required for the development of diabetes in nonobese diabetic mice J. Immunol. 160 1998 6018 6025
40. Hanninen A., Jaakkola I., Salmi M., Simell O., and Jalkanen S. Ly-6C regulates endothelial adhesion and homing of CD8(+) T cells by activating integrin-dependent adhesion pathways Proc. Natl. Acad. Sci. USA 94 1997 6898 6903
41. Haskins K. T-cell receptor transgenic (TCR-Tg) mice from two diabetogenic CD4+ islet-antigen-specific T-cell clones J. Autoimmun. 22 2004 107 109
42. Haskins K., and McDuffie M. Acceleration of diabetes in young NOD mice with a CD4+ islet-specific T cell clone Science 249 1990 1433 1436
43. Haskins K., Portas M., Bergman B., Lafferty K., and Bradley B. Pancreatic islet-specific T-cell clones from nonobese diabetic mice Proc. Natl. Acad. Sci. USA 86 1989 8000 8004
44. Haskins K., Portas M., Bradley B., Wegmann D., and Lafferty K. T-lymphocyte clone specific for pancreatic islet antigen Diabetes 37 1988 1444 1448
45. Haskins K., and Wegmann D. Diabetogenic T-cell clones Diabetes 45 1996 1299 1305
46. Herold K.C., Montag A.G., Meyer S.M., Wojcikowski C., and Fitch F.W. Expression of Ly-6C by T lymphocytes of NOD mice after CD3-complex stimulation. Identification of activated cells during insulitis of prediabetic mice Diabetes 39 1990 815 820
47. Hiemstra H.S., Duinkerken G., Benckhuijsen W.E., Amons R., de Vries R.R., Roep B.O., and Drijfhout J.W. The identification of CD4+ T-cell epitopes with dedicated synthetic peptide libraries Proc. Natl. Acad. Sci. USA 94 1997 10313 10318
48. Hoglund P., Mintern J., Waltzinger C., Heath W., Benoist C., and Mathis D. Initiation of autoimmune diabetes by developmentally regulated presentation of islet cell antigens in the pancreatic lymph nodes J. Exp. Med. 189 1999 331 339
49. Huang G.C., Tremble J., Bailyes E., Arden S.D., Kaye T., McGregor A.M., and Banga J.P. HLA-DR-restricted T-cell lines from newly diagnosed type 1 diabetic patients specific for insulinoma and normal islet beta cell proteins: Lack of reactivity to glutamic acid decarboxylase Clin. Exp. Immunol. 102 1995 152 158
50. Hutton J.C. The insulin secretory granule Diabetologia 32 1989 271 281
51. Hynes R.O. Integrins: Versatility, modulation, and signaling in cell adhesion Cell 69 1992 11 25
52. Hynes R.O. Integrins: Bidirectional, allosteric signaling machines Cell 110 2002 673 687
53. Jaakkola I., Merinen M., Jalkanen S., and Hanninen A. Ly6C induces clustering of LFA-1 (CD11a/CD18) and is involved in subtype-specific adhesion of CD8 T cells J. Immunol. 170 2003 1283 1290
54. Jang M.H., Seth N.P., and Wucherpfennig K.W. Ex vivo analysis of thymic CD4 T cells in nonobese diabetic mice with tetramers generated from I-A(g7)/class II-associated invariant chain peptide precursors J. Immunol. 171 2003 4175 4186
55. Jansen A., Homo-Delarche F., Hooijkaas H., Leenen P.J., Dardenne M., and Drexhage H.A. Immunohistochemical characterization of monocytes-macrophages and dendritic cells involved in the initiation of the insulitis and beta-cell destruction in NOD mice Diabetes 43 1994 667 675
56. Jansen G., Mahadevan M., Amemiya C., Wormskamp N., Segers B., Hendriks W., O'Hoy K., Baird S., Sabourin L., and Lennon G. Characterization of the myotonic dystrophy region predicts multiple protein isoform-encoding mRNAs Nat. Genet. 1 1992 261 266
57. Judkowski V., Krakowski M., Rodriguez E., Mocnick L., Santamaria P., and Sarvetnick N. Increased islet antigen presentation leads to type-1 diabetes in mice with autoimmune susceptibility Eur. J. Immunol. 34 2004 1031 1040
58. Judkowski V., Pinilla C., Schroder K., Tucker L., Sarvetnick N., and Wilson D.B. 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. 166 2001 908 917
59. Katz J.D., Benoist C., and Mathis D. T helper cell subsets in insulin-dependent diabetes Science 268 1995 1185 1188
60. Katz J.D., Wang B., Haskins K., Benoist C., and Mathis D. Following a diabetogenic T cell from genesis through pathogenesis Cell 74 1993 1089 1100
61. Kaufman D.L., Clare-Salzler M., Tian J., Forsthuber T., Ting G.S., Robinson P., Atkinson M.A., Sercarz E.E., Tobin A.J., and Lehmann P.V. Spontaneous loss of T-cell tolerance to glutamic acid decarboxylase in murine insulin-dependent diabetes Nature 366 1993 69 72
62. Kelemen K., Crawford M.L., Gill R.G., Hutton J.C., and Wegmann D. Cellular immune response to phogrin in the NOD mouse: Cloned T-cells cause destruction of islet transplants Diabetes 48 1999 1529 1534
63. Kelemen K., Gottlieb P.A., Putnam A.L., Davidson H.W., Wegmann D.R., and Hutton J.C. HLA-DQ8-associated T cell responses to the diabetes autoantigen phogrin (IA-2 beta) in human prediabetes J. Immunol. 172 2004 3955 3962
64. Kelemen K., Wegmann D.R., and Hutton J.C. T-cell epitope analysis on the autoantigen phogrin (IA-2beta) in the nonobese diabetic mouse Diabetes 50 2001 1729 1734
65. Klenerman P., Cerundolo V., and Dunbar P.R. Tracking T cells with tetramers: New tales from new tools Nat. Rev. Immunol. 2 2002 263 272
66. Kommajosyula S., Reddy S., Nitschke K., Kanwar J.R., Karanam M., and Krissansen G.W. Leukocytes infiltrating the pancreatic islets of nonobese diabetic mice are transformed into inactive exiles by combinational anti-cell adhesion therapy J. Leukoc. Biol. 70 2001 510 517
67. Kouskoff V., Korganow A.S., Duchatelle V., Degott C., Benoist C., and Mathis D. Organ-specific disease provoked by systemic autoimmunity Cell 87 1996 811 822
68. Krawczyk C., Bachmaier K., Sasaki T., Jones G.R., Snapper B.S., Bouchard D., Kozieradzki I., Ohashi S.P., Alt W.F., and Penninger M.J. Cbl-b is a negative regulator of receptor clustering and raft aggregation in T cells Immunity 13 2000 463 473
69. Kurrer M.O., Pakala S.V., Hanson H.L., and Katz J.D. Beta cell apoptosis in T cell-mediated autoimmune diabetes Proc. Natl. Acad. Sci. USA 94 1997 213 218
70. Lafaille J.J. T-cell receptor transgenic mice in the study of autoimmune diseases J. Autoimmun. 22 2004 95 106
71. Lan M.S., Wasserfall C., Maclaren N.K., and Notkins A.L. IA-2, a transmembrane protein of the protein tyrosine phosphatase family, is a major autoantigen in insulin-dependent diabetes mellitus Proc. Natl. Acad. Sci. USA 93 1996 6367 6370
72. Langmuir P.B., Bridgett M.M., Bothwell A.L., and Crispe I.N. Bone marrow abnormalities in the non-obese diabetic mouse Int. Immunol. 5 1993 169 177
73. Levisetti M.G., Suri A., Vidavsky I., Gross M.L., Kanagawa O., and Unanue E.R. Autoantibodies and CD4 T cells target a beta cell retroviral envelope protein in non-obese diabetic mice Int. Immunol. 15 2003 1473 1483
74. Liblau R.S., Wong F.S., Mars L.T., and Santamaria P. Autoreactive CD8 T cells in organ-specific autoimmunity: Emerging targets for therapeutic intervention Immunity 17 2002 1 6
75. Lieberman S.M., and DiLorenzo T.P. A comprehensive guide to antibody and T-cell responses in type 1 diabetes Tissue Antigens 62 2003 359 377
76. Lieberman S.M., Evans A.M., Han B., Takaki T., Vinnitskaya Y., Caldwell J.A., Serreze D.V., Shabanowitz J., Hunt D.F., Nathenson S.G., Santamaria P., and DiLorenzo T.P. Identification of the beta cell antigen targeted by a prevalent population of pathogenic CD8+ T cells in autoimmune diabetes Proc. Natl. Acad. Sci. USA 100 14 2003 8384 8388
77. Lieberman S.M., Takaki T., Han B., Santamaria P., Serreze D.V., and DiLorenzo T.P. Individual Nonobese Diabetic Mice Exhibit Unique Patterns of CD8+ T Cell reactivity to three islet antigens, including the newly identified widely expressed Dystrophia myotonica kinase J. Immunol. 173 2004 6727 6734
78. Luhder F., Hoglund P., Allison J.P., Benoist C., and Mathis D. Cytotoxic T lymphocyte-associated antigen 4 (CTLA-4) regulates the unfolding of autoimmune diabetes J. Exp. Med. 187 1998 427 432
79. McMurray R.W. Adhesion molecules in autoimmune disease Semin. Arthritis Rheum. 25 1996 215 233
80. Miller B.J., Appel M.C., O'Neil J.J., and Wicker L.S. Both the Lyt-2+ and L3T4+ T-cell subsets are required for the transfer of diabetes in nonobese diabetic mice J. Immunol. 140 1988 52 58
81. Moseley T.A., Haudenschild D.R., Rose L., and Reddi A.H. Interleukin-17 family and IL-17 receptors Cytokine. Growth Factor. Rev. 14 2003 155 174
82. Moser B., and Loetscher D.R. Lymphocyte traffic control by chemokines Nat. Immunol. 2 2001 123 128
83. Nagata M., Santamaria P., Kawamura T., Utsugi T., and Yoon J.W. Evidence for the role of CD8+ cytotoxic T cells in the destruction of pancreatic beta-cells in nonobese diabetic mice J. Immunol. 152 1994 2042 2050
84. Nagata M., and Yoon J.W. Studies on autoimmunity for T-cell-mediated b-cell destruction. Distinct difference in b-cell destruction between CD4+ and CD8+ T-cell clones derived from lymphocytes infiltrating the islets of NOD mice Diabetes 41 1992 998 1008
85. Nakano N., Kikutani H., Nishimoto H., and Kishimoto T. T cell receptor V gene usage of islet beta cell-reactive T cells is not restricted in non-obese diabetic mice J. Exp. Med. 173 1991 1091 1097
86. Nepom G.T. MHC multimers: Expanding the clinical toolkit Clin. Immunol. 106 2003 1 4
87. Nicolls M. The clinical and biological relationship between Type II Diabetes Mellitus and Alzheimer's Disease Curr. Alzheimer Res. 1 2004 47 54
88. Notkins A.L., and Lernmark A. Autoimmune type 1 diabetes: Resolved and unresolved issues J. Clin. Invest. 108 2001 1247 1252
89. O'Shea J.J., Ma A., Banatvala J.E., and Shepherd W.M. Cytokines and autoimmunity Nat. Rev. 2 2002 37 45
90. Pakala S.V., Chivetta M., Kelly C.B., and Katz J.D. In autoimmune diabetes the transition from benign to pernicious insulitis requires an islet cell response to tumor necrosis factor alpha J. Exp. Med. 189 1999 1053 1062
91. Panagiotopoulos C., Qin H., Tan R., and Verchere C.B. Identification of a beta-cell-specific HLA class I restricted epitope in type 1 diabetes Diabetes 52 2003 2647 2651
92. Pauza M.E., Dobbs C.M., He J., Patterson T., Wagner S., Anobile B.S., Bradley B.J., Lo D., and Haskins K. T-Cell Receptor Transgenic Response to an Endogenous Polymorphic Autoantigen Determines Susceptibility to Diabetes Diabetes 53 2004 978 988
93. Peterson J.D., and Haskins K. Transfer of diabetes in the NOD-scid mouse by CD4 T-cell clones. Differential requirement for CD8 T-cells Diabetes 45 1996 328 336
94. Peterson J.D., Pike B., Dallas-Pedretti A., and Haskins K. Induction of diabetes with islet-specific T-cell clones is age dependent Immunology 85 1995 455 460
95. Peterson J.D., Pike B., McDuffie M., and Haskins K. Islet-specific T-cell clones transfer diabetes to nonobese diabetic (NOD) F1 mice J. Immunol. 153 1994 2800 2806
96. Philbrick W.M., Maher S.E., Bridgett M.M., and Bothwell A.L. A recombination event in the 5′ flanking region of the Ly-6C gene correlates with impaired expression in the NOD, NZB and ST strains of mice EMBO J. 9 1990 2485 2492
97. Phillips J.M., Harach S.Z., Parish N.M., Fehervari Z., Haskins K., and Cooke A. Nondepleting anti-CD4 has an immediate action on diabetogenic effector cells, halting their destruction of pancreatic beta cells J. Immunol. 165 2000 1949 1955
98. Picarella D.E., Kratz A., Li C.B., Ruddle N.H., and Flavell R.A. Insulitis in transgenic mice expressing tumor necrosis factor beta (lymphotoxin) in the pancreas Proc. Natl. Acad. Sci. USA 89 1992 10036 10040
99. Poulin M., and Haskins K. Induction of diabetes in nonobese diabetic mice by Th2 T-cell clones from a TCR transgenic mouse J. Immunol. 164 2000 3072 3078
100. Pribila J.T., Quale A.C., Mueller K.L., and Shimizu Y. Integrins and T cell-mediated immunity Annu. Rev. Immunol. 22 2004 157 180
101. Quinn A. Antigen-induced T1D in NOD mice J. Autoimmun. 20 2003 207 210
102. Quinn A., McInerney B., Reich E.P., Kim O., Jensen K.P., and Sercarz E.E. Regulatory and effector CD4 T cells in nonobese diabetic mice recognize overlapping determinants on glutamic acid decarboxylase and use distinct V beta genes J. Immunol. 166 2001 2982 2991
103. Quinn A., McInerney M.F., and Sercarz E.E. MHC class I-restricted determinants on the glutamic acid decarboxylase 65 molecule induce spontaneous CTL activity J. Immunol. 167 2001 1748 1757
104. Quinn A., and Sercarz E.E. T cells with multiple fine specificities are used by non-obese diabetic (NOD) mice in the response to GAD(524-543) J. Autoimmun. 9 1996 365 370
105. Reijonen H., Mallone R., Heninger A.K., Laughlin E.M., Kochik S.A., Falk B., Kwok W.W., Greenbaum C., and Nepom G.T. GAD65-specific CD4+ T-cells with high antigen avidity are prevalent in peripheral blood of patients with type 1 diabetes Diabetes 53 2004 1987 1994
106. Roep B.O. Autoreactive T cells in endocrine/organ-specific autoimmunity: Why has progress been so slow? Springer Semin. Immunopathol. 24 2002 261 271
107. Roep B.O., Arden S.D., de Vries R.R., and Hutton J.C. T-cell clones from a type-1 diabetes patient respond to insulin secretory granule proteins Nature 345 1990 632 634
108. Rosmalen J.G., Martin T., Dobbs C., Voerman J.S., Drexhage H.A., Haskins K., and Leenen P.J. Subsets of macrophages and dendritic cells in nonobese diabetic mouse pancreatic inflammatory infiltrates: Correlation with the development of diabetes Lab. Invest. 80 2000 23 30
109. Rossini A.A. Autoimmune diabetes and the circle of tolerance Diabetes 53 2004 267 275
110. Sacca R., Cuff C.A., Lesslauer W., and Ruddle N.H. Differential activities of secreted lymphotoxin-alpha3 and membrane lymphotoxin-alpha1beta2 in lymphotoxin-induced inflammation: Critical role of TNF receptor 1 signaling J. Immunol. 160 1998 485 491
111. Savinov A.Y., Wong F.S., Stonebraker A.C., and Chervonsky A.V. Presentation of antigen by endothelial cells and chemoattraction are required for homing of insulin-specific CD8+ T cells J. Exp. Med. 197 2003 643 656
112. Schloot N.C., Daniel D., Norbury-Glaser M., and Wegmann D.R. Peripheral T-cell clones from NOD mice specific for GAD65 peptides: Lack of islet responsiveness or diabetogenicity J. Autoimmun. 9 1996 357 363
113. Schmidt D., Amrani A., Verdaguer J., Bou S., and Santamaria P. Autoantigen-independent deletion of diabetogenic CD4+ thymocytes by protective MHC class II molecules J. Immunol. 162 1999 4627 4636
114. Schmidt D., Verdaguer J., Averill N., and Santamaria P. A mechanism for the major histocompatibility complex-linked resistance to autoimmunity J. Exp. Med. 186 1997 1059 1075
115. Serreze D.V., and Leiter E.H. Tracking autoimmune T cells in diabetes J. Clin. Invest. 112 2003 826 828
116. Serreze D.V., Leiter E.H., Christianson G.J., Greiner D., and Roopenian D.C. Major histocompatibility complex class I-deficient NOD-B2mnull mice are diabetes and insulitis resistant Diabetes 43 1994 505 509
117. Serreze D.V., Pierce M.A., Post C.M., Chapman H.D., Savage H., Bronson R.T., Rothman P.B., and Cox G.A. Paralytic autoimmune myositis develops in nonobese diabetic mice made Th1 cytokine-deficient by expression of an IFN-gamma receptor beta-chain transgene J. Immunol. 170 2003 2742 2749
118. Sharma P., Varma R., Sarasij R.C., Ira, Gousset K., Krishnamoorthy G., Rao M., and Mayor S. Nanoscale organization of multiple GPI-anchored proteins in living cell membranes Cell 116 2004 577 589
119. Shimizu J., Kanagawa O., and Unanue E.R. Presentation of beta-cell antigens to CD4+ and CD8+ T cells of non-obese diabetic mice J. Immunol. 151 1993 1723 1730
120. Simone E., Daniel D., Schloot N., Gottlieb P., Babu S., Kawasaki E., Wegmann D., and Eisenbarth G.S. T-cell receptor restriction of diabetogenic autoimmune NOD T cells Proc. Natl. Acad. Sci. USA 94 1997 2518 2521
121. Simone E.A., Yu L., Wegmann D.R., and Eisenbarth G.S. T cell receptor gene polymorphisms associated with anti-insulin, autoimmune T cells in diabetes-prone NOD mice J. Autoimmun. 10 1997 317 321
122. Stamp L.K., James M.J., and Cleland L.G. Interleukin-17: The missing link between T-cell accumulation and effector cell actions in rheumatoid arthritis? Immunol. Cell. Biol. 82 2004 1 9
123. Stratmann T., Martin-Orozco N., Mallet-Designe V., Poirot L., McGavern D., Losyev G., Dobbs C.M., Oldstone M.B., Yoshida K., Kikutani H., Mathis D., Benoist C., Haskins K., and Teyton L. Susceptible MHC alleles, not background genes, select an autoimmune T cell reactivity J. Clin. Invest. 112 2003 902 914
124. Supon P., Stecha P., and Haskins K. Anti-islet cell antibodies from NOD mice Diabetes 39 1990 1366 1372
125. Suri A., and Katz J.D. Dissecting the role of CD4+ T cells in autoimmune diabetes through the use of TCR transgenic mice Immunol. Rev. 169 1999 55 65
126. Tisch R., Wang B., Atkinson M.A., Serreze D.V., and Friedline R. A glutamic acid decarboxylase 65-specific Th2 cell clone immunoregulates autoimmune diabetes in nonobese diabetic mice J. Immunol. 166 2001 6925 6936
127. Tisch R., Yang X.D., Singer S.M., Liblau R.S., Fugger L., and McDevitt H.O. Immune response to glutamic acid decarboxylase correlates with insulitis in non-obese diabetic mice Nature 366 1993 72 75
128. Trudeau J.D., Kelly-Smith C., Verchere C.B., Elliott J.F., Dutz J.P., Finegood D.T., Santamaria P., and Tan R. Prediction of spontaneous autoimmune diabetes in NOD mice by quantification of autoreactive T cells in peripheral blood J. Clin. Invest. 111 2003 217 223
129. Tseng S.Y., and Dustin M.L. T-cell activation: A multidimensional signaling network Curr. Opin. Cell. Biol. 14 2002 575 580
130. Verdaguer J., Schmidt D., Amrani A., Anderson B., Averill N., and Santamaria P. Spontaneous autoimmune diabetes in monoclonal T cell nonobese diabetic mice J. Exp. Med. 186 1997 1663 1676
131. Verdaguer J., Yoon J.W., Anderson B., Averill N., Utsugi T., Park B.J., and Santamaria P. Acceleration of spontaneous diabetes in TCR-beta-transgenic nonobese diabetic mice by beta-cell cytotoxic CD8+ T cells expressing identical endogenous TCR-alpha chains J. Immunol. 157 1996 4726 4735
132. Verge C.F., Gianani R., Kawasaki E., Yu L., Pietropaolo M., Jackson R.A., Chase H.P., and Eisenbarth G.S. Prediction of type I diabetes in first-degree relatives using a combination of insulin, GAD, and ICA512bdc/IA-2 autoantibodies Diabetes 45 1996 926 933
133. Videbaek N., Harach S., Phillips J., Hutchings P., Ozegbe P., Michelsen B.K., and Cooke A. An islet-homing NOD CD8+ cytotoxic T cell clone recognizes GAD65 and causes insulitis J. Autoimmun. 20 2003 97 109
134. Wang Y., Hao L., Gill R.G., and Lafferty K.J. Autoimmune diabetes in NOD mouse is L3T4 T-lymphocyte dependent Diabetes 36 1987 535 538
135. Wansink D.G., van Herpen R.E., Coerwinkel-Driessen M.M., Groenen P.J., Hemmings B.A., and Wieringa B. Alternative splicing controls myotonic dystrophy protein kinase structure, enzymatic activity, and subcellular localization Mol. Cell. Biol. 23 2003 5489 5501
136. Ward S.G., Bacon K., and Westwick J. Chemokines and T lymphocytes: More than an attraction Immunity 9 1998 1 11
137. Wasmeier C., and Hutton J.C. Molecular cloning of phogrin, a protein-tyrosine phosphatase homologue localized to insulin secretory granule membranes J. Biol. Chem. 271 1996 18161 18170
138. Wegmann D.R., and Eisenbarth G.S. It's insulin J. Autoimmun. 15 2000 286 291
139. Wegmann D.R., Norbury-Glaser M., and Daniel D. Insulin-specific T cells are a predominant component of islet infiltrates in prediabetic NOD mice Eur. J. Immunol. 24 1994 1853 1857
140. Wen L., Wong F.S., Burkly L., Altieri M., Mamalaki C., Kioussis D., Flavell R.A., and Sherwin R.S. Induction of insulitis by glutamic acid decarboxylase peptide-specific and HLA-DQ8-restricted CD4(+) T cells from human DQ transgenic mice J. Clin. Invest. 102 1998 947 957
141. Wilson D.B. GAD-about BDC2.5: peptides that stimulate BDC2.5 T cells and inhibit IDDM J. Autoimmun. 20 2003 199 201
142. Wilson D.B., Pinilla C., Wilson D.H., Schroder K., Boggiano C., Judkowski V., Kaye J., Hemmer B., Martin R., and Houghten R.A. Immunogenicity. I. Use of peptide libraries to identify epitopes that activate clonotypic CD4+ T cells and induce T cell responses to native peptide ligands J. Immunol. 163 1999 6424 6434
143. Wong F.S., Karttunen J., Dumont C., Wen L., Visintin I., Pilip I.M., Shastri N., Pamer E.G., and Janeway C.A. Jr. Identification of an MHC class I-restricted autoantigen in type 1 diabetes by screening an organ-specific cDNA library Nat. Med. 5 1999 1026 1031
144. Wong F.S., Moustakas A.K., Wen L., Papadopoulos G.K., and Janeway C.A. Jr. Analysis of structure and function relationships of an autoantigenic peptide of insulin bound to H-2K(d) that stimulates CD8 T cells in insulin-dependent diabetes mellitus Proc. Natl. Acad. Sci. USA 99 2002 5551 5556
145. Wong F.S., Visintin I., Wen L., Flavell R.A., and Janeway C.A. Jr. CD8 T-cell clones from young nonobese diabetic (NOD) islets can transfer rapid onset of diabetes in NOD mice in the absence of CD4 cells J. Exp. Med. 183 1996 67 76
146. Yang X.D., Sytwu H.K., McDevitt H.O., and Michie S.A. Involvement of beta 7 integrin and mucosal addressin cell adhesion molecule-1 (MAdCAM-1) in the development of diabetes in obese diabetic mice Diabetes 46 1997 1542 1547
147. Yang Y., and Santamaria P. T-cell receptor-transgenic NOD mice: A reductionist approach to understand autoimmune diabetes J. Autoimmun. 22 2004 121 129
148. Yoneda R., Yokono K., Nagata M., Tominaga Y., Moriyama H., Tsukamoto K., Miki M., Okamoto N., Yasuda H., Amano K., and Kasuga M. CD8 cytotoxic T-cell clone rapidly transfers autoimmune diabetes in very young NOD and MHC class I-compatible scid mice Diabetologia 40 1997 1044 1052
149. Yoshida K., Martin T., Yamamoto K., Dobbs C., Munz C., Kamikawaji N., Nakano N., Rammensee H.G., Sasazuki T., Haskins K., and Kikutani H. Evidence for shared recognition of a peptide ligand by a diverse panel of non-obese diabetic mice-derived, islet-specific, diabetogenic T-cell clones Int. Immunol. 14 2002 1439 1447
150. You S., Chen C., Lee W.H., Wu C.H., Judkowski V., Pinilla C., Wilson D.B., and Liu C.P. Detection and characterization of T cells specific for BDC2.5 T cell-stimulating peptides J. Immunol. 170 2003 4011 4020
151. Yu L., Robles D.T., Abiru N., Kaur P., Rewers M., Kelemen K., and Eisenbarth G.S. Early expression of antiinsulin autoantibodies of humans and the NOD mouse: Evidence for early determination of subsequent diabetes Proc. Natl. Acad. Sci. USA 97 2000 1701 1706
152. Zekzer D., Wong F.S., Ayalon O., Millet I., Altieri M., Shintani S., Solimena M., and Sherwin R.S. GAD-reactive CD4+ Th1 cells induce diabetes in NOD/SCID mice J. Clin. Invest. 101 1998 68 73