Transgenically induced GAD tolerance curtails the development of early β-cell autoreactivities but causes the subsequent development of supernormal autoreactivities to other β-cell antigens

Diabetes

Volumn 58, Issue 12, 2009, Pages 2843-2850

  Tian, Jide ^a   Dang, Hoa ^a   Von Boehmer, Harald ^b   Jaeckel, Elmar ^c   Kaufman, Daniel L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIGEN; GLUTAMATE DECARBOXYLASE 65;

AGED; ANIMAL EXPERIMENT; ANTIGEN PRESENTING CELL; ARTICLE; AUTOIMMUNITY; CONTROLLED STUDY; ENZYME LINKED IMMUNOSPOT ASSAY; INSULIN DEPENDENT DIABETES MELLITUS; LYMPH NODE; MOUSE; NONHUMAN; NONOBESE DIABETIC MOUSE; PANCREAS; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; SPLEEN; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TH1 CELL;

AMINO ACID SEQUENCE; ANIMALS; AUTOANTIGENS; AUTOIMMUNITY; DIABETES MELLITUS, TYPE 1; GLUTAMATE DECARBOXYLASE; INSULIN-SECRETING CELLS; MICE; MICE, INBRED NOD; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; PANCREAS; SPLEEN; T-LYMPHOCYTES;

EID: 73249137408     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db08-0851     Document Type: Article

References (46)

1. Kaufman DL, Clare-Salzler M, Tian J, Forsthuber T, Ting GS, Robinson P, Atkinson MA, Sercarz EE, Tobin AJ, Lehmann PV. Spontaneous loss of T-cell tolerance to glutamic acid decarboxylase in murine insulin-dependent diabetes. Nature 1993;366:69-72
2. Tisch R, Yang XD, Singer SM, Liblau RS, Fugger L, McDevitt HO. Immune response to glutamic acid decarboxylase correlates with insulitis in non-obese diabetic mice. Nature 1993;366:72-75
3. Cetkovic-Cvrlje M, Gerling IC, Muir A, Atkinson MA, Elliott JF, Leiter EH. Retardation or acceleration of diabetes in NOD/Lt mice mediated by intrathymic administration of candidate beta-cell antigens. Diabetes 1997;46:1975-1982
4. Gerling IC, Atkinson MA, Leiter EH. The thymus as a site for evaluating the potency of candidate beta cell autoantigens in NOD mice. J Autoimmun 1994;7:851-858
5. Kash SF, Condie BG, Baekkeskov S. Glutamate decarboxylase and GABA in pancreatic islets: lessons from knock-out mice. Horm Metab Res 1999;31:340-344
6. Kim J, Richter W, Aanstoot HJ, Shi Y, Fu Q, Rajotte R, Warnock G, Baekkeskov S. Differential expression of GAD65 and GAD67 in human, rat, and mouse pancreatic islets. Diabetes 1993;42:1799-1808
7. Erlander MG, Tillakaratne NJ, Feldblum S, Patel N, Tobin AJ. Two genes encode distinct glutamate decarboxylases. Neuron 1991;7:91-100
8. Elliott JF, Qin HY, Bhatti S, Smith DK, Singh RK, Dillon T, Lauzon J, Singh B. Immunization with the larger isoform of mouse glutamic acid decarboxylase (GAD67) prevents autoimmune diabetes in NOD mice. Diabetes 1994;43:1494-1499
9. Zechel MA, Elliott JF, Atkinson MA, Singh B. Characterization of novel T-cell epitopes on 65 kDa and 67 kDa glutamic acid decarboxylase relevant in autoimmune responses in NOD mice. J Autoimmun 1998;11:83-95
10. Tian J, Chau C, Hales TG, Kaufman DL. GABA(A) receptors mediate inhibition of T cell responses. J Neuroimmunol 1999;96:21-28
11. Tian J, Lu Y, Zhang H, Chau CH, Dang HN, Kaufman DL. Gamma-aminobutyric acid inhibits T cell autoimmunity and the development of inflammatory responses in a mouse type 1 diabetes model. J Immunol 2004;173:5298-5304
12. Yoon JW, Yoon CS, Lim HW, Huang QQ, Kang Y, Pyun KH, Hirasawa K, Sherwin RS, Jun HS. Control of autoimmune diabetes in NOD mice by GAD expression or suppression in beta cells. Science 1999;284:1183-1187
13. Geng L, Solimena M, Flavell RA, Sherwin RS, Hayday AC. Widespread expression of an autoantigen-GAD65 transgene does not tolerize nonobese diabetic mice and can exacerbate disease. Proc Natl Acad Sci U S A 1998;95:10055-10060
14. Jaeckel E, Klein L, Martin-Orozco N, von Boehmer H. Normal incidence of diabetes in NOD mice tolerant to glutamic acid decarboxylase. J Exp Med 2003;197:1635-1644
15. Han B, Serra P, Amrani A, Yamanouchi J, Mare e 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
16. Harrington CJ, Paez A, Hunkapiller T, Mannikko V, Brabb T, Ahearn M, Beeson C, Goverman J. Differential tolerance is induced in T cells recognizing distinct epitopes of myelin basic protein. Immunity 1998;8:571-580
17. Targoni OS, Lehmann PV. Endogenous myelin basic protein inactivates the high avidity T cell repertoire. J Exp Med 1998;187:2055-2063
18. Sercarz EE, Lehmann PV, Ametani A, Benichou G, Miller A, Moudgil K. Dominance and crypticity of T cell antigenic determinants. Annu Rev Immunol 1993;11:729-766
19. Atkinson MA, Bowman MA, Campbell L, Darrow BL, Kaufman DL, Maclaren NK. Cellular immunity to a determinant common to glutamate decarboxylase and coxsackie virus in insulin-dependent diabetes. J Clin Invest 1994;94:2125-2129
20. Kaufman DL, Tisch R, Sarvetnick N, Chatenoud L, Harrison LC, Haskins K, Quinn A, Sercarz E, Singh B, von Herrath M, Wegmann D, Wen L, Zekzer D. Report from the 1st International NOD Mouse T-Cell Workshop and the follow-up mini-workshop. Diabetes 2001;50:2459-2463
21. Chao CC, McDevitt HO. Identification of immunogenic epitopes of GAD 65 presented by Ag7 in non-obese diabetic mice. Immunogenetics 1997;46:29-34
22. Olcott AP, Tian J, Walker V, Dang H, Middleton B, Adorini L, Washburn L, Kaufman DL. Antigen-based therapies using ignored determinants of beta cell antigens can more effectively inhibit late-stage autoimmune disease in diabetes-prone mice. J Immunol 2005;175:1991-1999
23. Elias D, Reshef T, Birk OS, van der Zee R, Walker MD, Cohen IR. Vaccination against autoimmune mouse diabetes with a T-cell epitope of the human 65-kDa heat shock protein. Proc Natl Acad Sci U S A 1991;88:3088-3091
24. Muir A, Peck A, Clare-Salzler M, Song YH, Cornelius J, Luchetta R, Krischer J, Maclaren N. Insulin immunization of nonobese diabetic mice induces a protective insulitis characterized by diminished intraislet interferongamma transcription. J Clin Invest 1995;95:628-634
25. Tisch R, Wang B, Serreze DV. Induction of glutamic acid decarboxylase 65-specific Th2 cells and suppression of autoimmune diabetes at late stages of disease is epitope dependent. J Immunol 1999;163:1178-1187
26. Tian J, Atkinson MA, Clare-Salzler M, Herschenfeld A, Forsthuber T, Lehmann PV, Kaufman DL. Nasal administration of glutamate decarboxylase (GAD65) peptides induces Th2 responses and prevents murine insulin-dependent diabetes. J Exp Med 1996;183:1561-1567
27. Deng H, Apple R, Clare-Salzler M, Trembleau S, Mathis D, Adorini L, Sercarz E. Determinant capture as a possible mechanism of protection afforded by major histocompatibility complex class II molecules in autoimmune disease. J Exp Med 1993;178:1675-1680
28. Tian J, Lehmann PV, Kaufman DL. Determinant spreading of T helper 2 (Th2) responses to pancreatic islet autoantigens. J Exp Med 1997;186:2039-2043
29. Tian J, Gregori S, Adorini L, Kaufman DL. The frequency of high avidity T cells determines the hierarchy of determinant spreading. J Immunol 2001;166:7144-7150
30. Clare-Salzler M, Mullen Y. Marked dendritic cell-T cell cluster formation in the pancreatic lymph node of the non-obese diabetic mouse. Immunology 1992;76:478-484
31. Hill NJ, Van Gunst K, Sarvetnick N. Th1 and Th2 pancreatic inflammation differentially affects homing of islet-reactive CD4 cells in nonobese diabetic mice. J Immunol 2003;170:1649-1658
32. Forsthuber T, Yip HC, Lehmann PV. Induction of TH1 and TH2 immunity in neonatal mice. Science 1996;271:1728-1730
33. Tian J, Clare-Salzler M, Herschenfeld A, Middleton B, Newman D, Mueller R, Arita S, Evans C, Atkinson MA, Mullen Y, Sarvetnick N, Tobin AJ, Lehmann PV, Kaufman DL. Modulating autoimmune responses to GAD inhibits disease progression and prolongs islet graft survival in diabetesprone mice. Nat Med 1996;2:1348-1353
34. Quinn A, McInerney B, Reich EP, Kim O, Jensen KP, Sercarz EE. 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 2001;166:2982-2991
35. Han B, Serra P, Yamanouchi J, Amrani A, Elliott JF, Dickie P, Dilorenzo TP, Santamaria P. Developmental control of CD8 T cell-avidity maturation in autoimmune diabetes. J Clin Invest 2005;115:1879-1887
36. Ashton-Rickardt PG, Tonegawa S. A differential-avidity model for T-cell selection. Immunol Today 1994;15:362-366
37. Lehmann PV, Targoni OS, Forsthuber TG. Shifting T-cell activation thresholds in autoimmunity and determinant spreading. Immunol Rev 1998;164:53-61
38. Höglund P, Mintern J, Waltzinger C, Heath W, Benoist C, Mathis D. Initiation of autoimmune diabetes by developmentally regulated presentation of islet cell antigens in the pancreatic lymph nodes. J Exp Med 1999;189:331-339
39. 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
40. Nakayama M, Abiru N, Moriyama H, Babaya N, Liu E, Miao D, Yu L, Wegmann DR, Hutton JC, Elliott JF, Eisenbarth GS. Prime role for an insulin epitope in the development of type 1 diabetes in NOD mice. Nature 2005;435:220-223
41. King C, Ilic A, Koelsch K, Sarvetnick N. Homeostatic expansion of T cells during immune insufficiency generates autoimmunity. Cell 2004;117:265-277
42. Tian J, Kaufman DL. Antigen-based therapy for the treatment of type 1 diabetes. Diabetes 2009;58, 1939-1946
43. Tisch R, McDevitt HO. Antigen-specific immunotherapy: is it a real possibility to combat T-cell-mediated autoimmunity? Proc Natl Acad Sci U S A 1994;91:437-438
44. Steinman L. A few autoreactive cells in an autoimmune infiltrate control a vast population of nonspecific cells: a tale of smart bombs and the infantry. Proc Natl Acad Sci U S A 1996;93:2253-2256
45. Tian J, Olcott A, Hanssen L, Zekzer D, Kaufman DL. Antigen-based immunotherapy for autoimmune disease: from animal models to humans? Immunol Today 1999;20:190-195
46. Tian J, Kaufman DL. Attenuation of inducible Th2 immunity with autoimmune disease progression. J Immunol 1998;161:5399-5403