ZnT8-reactive T cells are weakly pathogenic in NOD mice but can participate in diabetes under inflammatory conditions

Diabetes

Volumn 63, Issue 10, 2014, Pages 3438-3448

  Nayak, Deepak K ^a   Calderon, Boris ^a   Vomund, Anthony N ^a   Unanue, Emil R ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

UNCLASSIFIED DRUG; ZINC TRANSPORTER; ZINC TRANSPORTER 8; CATION TRANSPORT PROTEIN; ZINC TRANSPORTER ZNT8, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ANTIGEN PRESENTING CELL; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; DIABETES MELLITUS; INFLAMMATION; INSULINOMA; MOUSE; NONHUMAN; ADOPTIVE TRANSFER; ANIMAL; CELL LINE; IMMUNOLOGY; INSULIN DEPENDENT DIABETES MELLITUS; METABOLISM; NONOBESE DIABETIC MOUSE; PATHOLOGY;

ADOPTIVE TRANSFER; ANIMALS; CATION TRANSPORT PROTEINS; CD4-POSITIVE T-LYMPHOCYTES; CELL LINE; DIABETES MELLITUS, TYPE 1; INFLAMMATION; MICE; MICE, INBRED NOD;

EID: 84907486501     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db13-1882     Document Type: Article

References (50)

1. Anderson MS, Bluestone JA. The NOD mouse: A model of immune dysregulation. Annu Rev Immunol 2005;23:447-485
2. Arvan P, Pietropaolo M, Ostrov D, Rhodes CJ. Islet autoantigens: Structure, function, localization, and regulation. Cold Spring Harb Perspect Med 2012;2
3. Wegmann DR, Norbury-Glaser M, Daniel D. Insulin-specific T cells are a predominant component of islet infiltrates in pre-diabetic NOD mice. Eur J Immunol 1994;24:1853-1857
4. Daniel D, Gill RG, Schloot N, Wegmann D. Epitope specificity, cytokine production profile and diabetogenic activity of insulin-specific T cell clones isolated from NOD mice. Eur J Immunol 1995;25:1056-1062
5. Halbout P, Briand J-P, Bécourt C, Muller S, Boitard C. T cell response to preproinsulin I and II in the nonobese diabetic mouse. J Immunol 2002;169: 2436-2443
6. French MB, Allison J, Cram DS, et al. Transgenic expression of mouse proinsulin II prevents diabetes in nonobese diabetic mice. Diabetes 1997;46:34 -39
7. Jaeckel E, Lipes MA, von Boehmer H. Recessive tolerance to preproinsulin 2 reduces but does not abolish type 1 diabetes. Nat Immunol 2004;5:1028-1035
8. Nakayama M, Abiru N, Moriyama H, et al. Prime role for an insulin epitope in the development of type 1 diabetes in NOD mice. Nature 2005;435: 220-223
9. Mohan JF, Levisetti MG, Calderon B, Herzog JW, Petzold SJ, Unanue ER. Unique autoreactive T cells recognize insulin peptides generated within the islets of Langerhans in autoimmune diabetes. Nat Immunol 2010;11:350-354
10. Mohan JF, Calderon B, Anderson MS, Unanue ER. Pathogenic CD4+ T cells recognizing an unstable peptide of insulin are directly recruited into islets bypassing local lymph nodes. J Exp Med 2013;210:2403-2414
11. Muir A, Peck A, Clare-Salzler M, et al. Insulin immunization of nonobese diabetic mice induces a protective insulitis characterized by diminished intraislet interferon-gamma transcription. J Clin Invest 1995;95:628-634
12. Daniel C, Weigmann B, Bronson R, von Boehmer H. Prevention of type 1 diabetes in mice by tolerogenic vaccination with a strong agonist insulin mimetope. J Exp Med 2011;208:1501-1510
13. Lieberman SM, DiLorenzo TP. A comprehensive guide to antibody and T-cell responses in type 1 diabetes. Tissue Antigens 2003;62:359-377
14. Roep BO, Peakman M. Antigen targets of type 1 diabetes autoimmunity. Cold Spring Harb Perspect Med 2012;2:a007781
15. Haskins K. Pathogenic T-cell clones in autoimmune diabetes: More lessons from the NOD mouse. Adv Immunol 2005;87:123-162
16. Unanue ER. Antigen presentation in the autoimmune diabetes of the NOD mouse. Annu Rev Immunol 2014;32:579-608
17. Foster MC, Leapman RD, Li MX, Atwater I. Elemental composition of secretory granules in pancreatic islets of Langerhans. Biophys J 1993;64:525-532
18. Chimienti F, Devergnas S, Favier A, Seve M. Identification and cloning of a beta-cell-specific zinc transporter, ZnT-8, localized into insulin secretory granules. Diabetes 2004;53:2330-2337
19. Lemaire K, Ravier MA, Schraenen A, et al. Insulin crystallization depends on zinc transporter ZnT8 expression, but is not required for normal glucose homeostasis in mice. Proc Natl Acad Sci U S A 2009;106:14872-14877
20. Nicolson TJ, Bellomo EA, Wijesekara N, et al. Insulin storage and glucose homeostasis in mice null for the granule zinc transporter ZnT8 and studies of the type 2 diabetes-associated variants. Diabetes 2009;58:2070-2083
21. Wenzlau JM, Juhl K, Yu L, et al. The cation efflux transporter ZnT8 (Slc30A8) is a major autoantigen in human type 1 diabetes. Proc Natl Acad Sci USA 2007;104:17040-17045
22. Wenzlau JM, Liu Y, Yu L, et al. A common nonsynonymous single nucleotide polymorphism in the SLC30A8 gene determines ZnT8 autoantibody specificity in type 1 diabetes. Diabetes 2008;57:2693-2697
23. Skärstrand H, Lernmark A, Vaziri-Sani F. Antigenicity and epitope specificity of ZnT8 autoantibodies in type 1 diabetes. Scand J Immunol 2013;77: 21-29
24. Ingemansson S, Vaziri-Sani F, Lindblad U, Gudbjornsdottir S, Törn C; Diss-Study Group. Long-term sustained autoimmune response to beta cell specific zinc transporter (ZnT8, W, R, Q) in young adult patients with preserved beta cell function at diagnosis of diabetes. Autoimmunity 2013;46:50-61
25. Tiberti C, Yu L, Lucantoni F, et al. Detection of four diabetes specific autoantibodies in a single radioimmunoassay: An innovative high-throughput approach for autoimmune diabetes screening. Clin Exp Immunol 2011;166: 317-324
26. Andersen MK, Härkönen T, Forsblom C, Groop PH, Knip M, Tuomi T. Zinc transporter type 8 autoantibodies (ZnT8A): Prevalence and phenotypic associations in latent autoimmune diabetes patients and patients with adult onset type 1 diabetes. Autoimmunity 2013;46:251-258
27. Dang M, Rockell J, Wagner R, et al. Human type 1 diabetes is associated with T cell autoimmunity to zinc transporter 8. J Immunol 2011;186:6056-6063
28. Wu X, Xu X, Gu R, et al. Prediction of HLA class I-restricted T-cell epitopes of islet autoantigen combined with binding and dissociation assays. Autoimmunity 2012;45:176-185
29. Scotto M, Afonso G, Larger E, et al. Zinc transporter (ZnT)8(186-194) is an immunodominant CD8+ T cell epitope in HLA-A2+ type 1 diabetic patients. Diabetologia 2012;55:2026-2031
30. Énée É, Kratzer R, Arnoux JB, et al. ZnT8 is a major CD8+ T cell-recognized autoantigen in pediatric type 1 diabetes. Diabetes 2012;61:1779-1784
31. Chujo D, Foucat E, Nguyen TS, Chaussabel D, Banchereau J, Ueno H. ZnT8-Specific CD4+ T cells display distinct cytokine expression profiles between type 1 diabetes patients and healthy adults. PLoS ONE 2013;8:e55595
32. Katz JD, Wang B, Haskins K, Benoist C, Mathis D. Following a diabetogenic T cell from genesis through pathogenesis. Cell 1993;74:1089-1100
33. Chang KY, Suri A, Unanue ER. Predicting peptides bound to I-Ag7 class II histocompatibility molecules using a novel expectation-maximization alignment algorithm. Proteomics 2007;7:367-377
34. Mohan JF, Petzold SJ, Unanue ER. Register shifting of an insulin peptide-MHC complex allows diabetogenic T cells to escape thymic deletion. J Exp Med 2011;208:2375-2383
35. Calderon B, Suri A, Miller MJ, Unanue ER. Dendritic cells in islets of Langerhans constitutively present beta cell-derived peptides bound to their class II MHC molecules. Proc Natl Acad Sci U S A 2008;105:6121-6126
36. Suri A, Walters JJ, Gross ML, Unanue ER. Natural peptides selected by diabetogenic DQ8 and murine I-A(g7) molecules show common sequence specificity. J Clin Invest 2005;115:2268-2276
37. Suri A, Vidavsky I, van der Drift K, Kanagawa O, Gross ML, Unanue ER. In APCs, the autologous peptides selected by the diabetogenic I-Ag7 molecule are unique and determined by the amino acid changes in the P9 pocket. J Immunol 2002;168:1235-1243
38. Mohan JF, Unanue ER. Unconventional recognition of peptides by T cells and the implications for autoimmunity. Nat Rev Immunol 2012;12:721-728
39. Levisetti MG, Lewis DM, Suri A, Unanue ER. Weak proinsulin peptide-major histocompatibility complexes are targeted in autoimmune diabetes in mice. Diabetes 2008;57:1852-1860
40. Calderon B, Carrero JA, Unanue ER. The central role of antigen presentation in islets of Langerhans in autoimmune diabetes. Curr Opin Immunol 2014;26:32-40
41. Petyuk VA, Qian WJ, Hinault C, et al. Characterization of the mouse pancreatic islet proteome and comparative analysis with other mouse tissues. J Proteome Res 2008;7:3114-3126
42. Woanders LF, Chwalek K, Monetti M, Kumar C, Lammert E, Mann M. Quantitative proteomic analysis of single pancreatic islets. Proc Natl Acad Sci U S A 2009;106:18902-18907
43. Lieberman SM, Evans AM, Han B, et al. Identification of the ß cell antigen targeted by a prevalent population of pathogenic CD8+ T cells in autoimmune diabetes. Proc Natl Acad Sci U S A 2003;100:8384-8388
44. Gurr W, Yavari R, Wen L, et al. A Reg family protein is overexpressed in islets from a patient with new-onset type 1 diabetes and acts as T-cell autoantigen in NOD mice. Diabetes 2002;51:339-346
45. Baker RL, Delong T, Barbour G, Bradley B, Nakayama M, Haskins K. Cutting edge: CD4 T cells reactive to an islet amyloid polypeptide peptide accumulate in the pancreas and contribute to disease pathogenesis in nonobese diabetic mice. J Immunol 2013;191:3990-3994
46. Hallahan DE, Virudachalam S. Intercellular adhesion molecule 1 knockout abrogates radiation induced pulmonary inflammation. Proc Natl Acad Sci U S A 1997;94:6432-6437
47. Hallahan DE, Virudachalam S. Ionizing radiation mediates expression of cell adhesion molecules in distinct histological patterns within the lung. Cancer Res 1997;57:2096-2099
48. Heckmann M, Douwes K, Peter R, Degitz K. Vascular activation of adhesion molecule mRNA and cell surface expression by ionizing radiation. Exp Cell Res 1998;238:148-154
49. Calderon B, Carrero JA, Miller MJ, Unanue ER. Entry of diabetogenic T cells into islets induces changes that lead to amplification of the cellular response. Proc Natl Acad Sci U S A 2011;108:1567-1572
50. Carrero JA, Calderon B, Towfic F, Artyomov MN, Unanue ER. Defining the transcriptional and cellular landscape of type 1 diabetes in the NOD mouse. PLoS ONE 2013;8:e59701