Ins2 deficiency augments spontaneous HLA-A*0201-restricted T Cell responses to insulin

Journal of Immunology

Volumn 184, Issue 2, 2010, Pages 658-665

  Jarchum, Irene ^a   DiLorenzo, Teresa P ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; HLA A ANTIGEN; INSULIN; PREPROINSULIN; HLA A*0201 ANTIGEN; HLA-A*0201 ANTIGEN; PROTEIN PRECURSOR;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD8+ T LYMPHOCYTE; DISEASE ASSOCIATION; DISEASE PREDISPOSITION; FEMALE; INSULIN DEFICIENCY; INSULIN DEPENDENT DIABETES MELLITUS; LYMPHOCYTIC INFILTRATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN TARGETING; T LYMPHOCYTE; TARGET CELL; ANIMAL; CELL MOTION; DISEASE MODEL; GENETICS; HUMAN; IMMUNOLOGY; NONOBESE DIABETIC MOUSE; PANCREAS ISLET; THYMUS; TRANSGENIC MOUSE;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELL MOVEMENT; DIABETES MELLITUS, TYPE 1; DISEASE MODELS, ANIMAL; EPITOPES; HLA-A ANTIGENS; HUMANS; INSULIN; ISLETS OF LANGERHANS; MICE; MICE, INBRED NOD; MICE, TRANSGENIC; PROTEIN PRECURSORS; THYMUS GLAND;

EID: 76249103112     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0903414     Document Type: Article

References (49)

1. Zhang, L., M. Nakayama, and G. S. Eisenbarth. 2008. Insulin as an autoantigen in NOD/human diabetes. Curr. Opin. Immunol. 20: 111-118.
2. Pociot, F., and M. F. McDermott. 2002. Genetics of type 1 diabetes mellitus. Genes Immun. 3: 235-249.
3. Lucassen, A. M., C. Julier, J. P. Beressi, C. Boitard, P. Froguel, M. Lathrop, and J. I. Bell. 1993. Susceptibility to insulin dependent diabetes mellitus maps to a 4.1 kb segment of DNA spanning the insulin gene and associated VNTR. Nat. Genet. 4: 305-310.
4. Bennett, S. T., A. J. Wilson, F. Cucca, J. Nerup, F. Pociot, P. A. McKinney, A. H. Barnett, S. C. Bain, and J. A. Todd. 1996. IDDM2-VNTR-encoded susceptibility to type 1 diabetes: dominant protection and parental transmission of alleles of the insulin gene-linked minisatellite locus. J. Autoimmun. 9: 415-421.
5. Pérez De Nanclares, G., J. R. Bilbao, B. Calvo, J. C. Vitoria, F. Vázquez, and L. Castaño. 2003. 5′-Insulin gene VNTR polymorphism is specific for type 1 diabetes: no association with celiac or Addison's disease. Ann. N. Y. Acad. Sci. 1005: 319-323.
6. Pugliese, A., M. Zeller, A. Fernandez, Jr., L. J. Zalcberg, R. J. Bartlett, C. Ricordi, M. Pietropaolo, G. S. Eisenbarth, S. T. Bennett, and D. D. Patel. 1997. The insulin gene is transcribed in the human thymus and transcription levels correlated with allelic variation at the INS VNTR-IDDM2 susceptibility locus for type 1 diabetes. Nat. Genet. 15: 293-297.
7. Vafiadis, P., S. T. Bennett, J. A. Todd, J. Nadeau, R. Grabs, C. G. Goodyer, S. Wickramasinghe, E. Colle, and C. Polychronakos. 1997. Insulin expression in human thymus is modulated by INS VNTR alleles at the IDDM2 locus. Nat. Genet. 15: 289-292.
8. Deltour, L., P. Leduque, N. Blume, O. Madsen, P. Dubois, J. Jami, and D. Bucchini. 1993. Differential expression of the two nonallelic proinsulin genes in the developing mouse embryo. Proc. Natl. Acad. Sci. USA 90: 527-531.
9. Heath, V. L., N. C. Moore, S. M. Parnell, and D. W. Mason. 1998. Intrathymic expression of genes involved in organ specific autoimmune disease. J. Autoimmun. 11: 309-318.
10. Chentoufi, A. A., and C. Polychronakos. 2002. Insulin expression levels in the thymus modulate insulin-specific autoreactive T-cell tolerance: the mechanism by which the IDDM2 locus may predispose to diabetes. Diabetes 51: 1383-1390.
11. Faideau, B., J. P. Briand, C. Lotton, I. Tardivel, P. Halbout, J. Jami, J. F. Elliott, P. Krief, S. Muller, C. Boitard, and J. C. Carel. 2004. Expression of preproinsulin-2 gene shapes the immune response to preproinsulin in normal mice. J. Immunol. 172: 25-33. (Pubitemid 38020451)
12. Faideau, B., C. Lotton, B. Lucas, I. Tardivel, J. F. Elliott, C. Boitard, and J. C. Carel. 2006. Tolerance to proinsulin-2 is due to radioresistant thymic cells. J. Immunol. 177: 53-60. (Pubitemid 43939115)
13. Fan, Y., W. A. Rudert, M. Grupillo, J. He, G. Sisino, and M. Trucco. 2009. Thymus-specific deletion of insulin induces autoimmune diabetes. EMBO J. 28: 2812-2824.
14. Moriyama, H., N. Abiru, J. Paronen, K. Sikora, E. Liu, D. Miao, D. Devendra, J. Beilke, R. Gianani, R. G. Gill, and G. S. Eisenbarth. 2003. Evidence for a primary islet autoantigen (preproinsulin 1) for insulitis and diabetes in the nonobese diabetic mouse. Proc. Natl. Acad. Sci. USA 100: 10376-10381.
15. Thébault-Baumont, K., D. Dubois-Laforgue, P. Krief, J. P. Briand, P. Halbout, K. Vallon-Geoffroy, J. Morin, V. Laloux, A. Lehuen, J. C. Carel, et al. 2003. Acceleration of type 1 diabetes mellitus in proinsulin 2-deficient NOD mice. J. Clin. Invest. 111: 851-857.
16. DiLorenzo, T. P., R. T. Graser, T. Ono, G. J. Christianson, H. D. Chapman, D. C. Roopenian, S. G. Nathenson, and D. V. Serreze. 1998. 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 a chain gene rearrangement. Proc. Natl. Acad. Sci. USA 95: 12538-12543.
17. Katz, J., C. Benoist, and D. Mathis. 1993. Major histocompatibility complex class I molecules are required for the development of insulitis in non-obese diabetic mice. Eur. J. Immunol. 23: 3358-3360.
18. null mice are diabetes and insulitis resistant. Diabetes 43: 505-509.
19. 2-microglobulin- deficient non-obese diabetic mice. Int. Immunol. 6: 1445-1449.
20. + T cells in the initiation of insulin-dependent diabetes mellitus. Eur. J. Immunol. 26: 1762-1769.
21. Wicker, L. S., E. H. Leiter, J. A. Todd, R. J. Renjilian, E. Peterson, P. A. Fischer, P. L. Podolin, M. Zijlstra, R. Jaenisch, and L. B. Peterson. 1994. β 2-microglobulin-deficient NOD mice do not develop insulitis or diabetes. Diabetes 43: 500-504. (Pubitemid 24064260)
22. + T cell reactivity to three islet antigens, including the newly identified widely expressed dystrophia myotonica kinase. J. Immunol. 173: 6727-6734.
23. Wong, F. S., J. Karttunen, C. Dumont, L. Wen, I. Visintin, I. M. Pilip, N. Shastri, E. G. Pamer, and C. A. Janeway, Jr. 1999. Identification of an MHC class I-restricted autoantigen in type 1 diabetes by screening an organ-specific cDNA library. Nat. Med. 5: 1026-1031.
24. + T lymphocytes in spontaneously diabetic HLA-A2 transgenic NOD mice. J. Immunol. 180: 5430-5438.
25. + T-cell responses identify β-cell autoimmunity in human type 1 diabetes. Diabetes 56: 613-621.
26. Ouyang, Q., N. E. Standifer, H. Qin, P. Gottlieb, C. B. Verchere, G. T. Nepom, R. Tan, and C. Panagiotopoulos. 2006. Recognition of HLA class I-restricted β-cell epitopes in type 1 diabetes. Diabetes 55: 3068-3074.
27. Pinkse, G. G., O. H. Tysma, C. A. Bergen, M. G. Kester, F. Ossendorp, P. A. van Veelen, B. Keymeulen, D. Pipeleers, J. W. Drijfhout, and B. O. Roep. 2005. Autoreactive CD8 T cells associated with β cell destruction in type 1 diabetes. Proc. Natl. Acad. Sci. USA 102: 18425-18430.
28. Skowera, A., R. J. Ellis, R. Varela-Calviño, S. Arif, G. C. Huang, C. Van-Krinks, A. Zaremba, C. Rackham, J. S. Allen, T. I. M. Tree, et al. 2008. CTLs are targeted to kill β cells in patients with type 1 diabetes through recognition of a glucose-regulated preproinsulin epitope. J. Clin. Invest. 118: 3390-3402.
29. Toma, A., S. Haddouk, J. P. Briand, L. Camoin, H. Gahery, F. Connan, D. Dubois-Laforgue, S. Caillat-Zucman, J. G. Guillet, J. C. Carel, et al. 2005. Recognition of a subregion of human proinsulin by class I-restricted T cells in type 1 diabetic patients. Proc. Natl. Acad. Sci. USA 102: 10581-10586.
30. Toma, A., T. Laïka, S. Haddouk, S. Luce, J. P. Briand, L. Camoin, F. Connan, M. Lambert, S. Caillat-Zucman, J. C. Carel, et al. 2009. Recognition of human proinsulin leader sequence by class I-restricted T-cells in HLA-A*0201 transgenic mice and in human type 1 diabetes. Diabetes 58: 394-402.
31. Fennessy, M., K. Metcalfe, G. A. Hitman, M. Niven, P. A. Biro, J. Tuomilehto, and E. Tuomilehto-Wolf. 1994. A gene in the HLA class I region contributes to susceptibility to IDDM in the Finnish population. Childhood Diabetes in Finland (DiMe) Study Group. Diabetologia 37: 937-944.
32. Nejentsev, S., J. M. Howson, N. M. Walker, J. Szeszko, S. F. Field, H. E. Stevens, P. Reynolds, M. Hardy, E. King, J. Masters, et al; Wellcome Trust Case Control Consortium. 2007. Localization of type 1 diabetes susceptibility to the MHC class I genes HLA-B and HLA-A. Nature 450: 887-892.
33. Robles, D. T., G. S. Eisenbarth, T. Wang, H. A. Erlich, T. L. Bugawan, S. R. Babu, K. Barriga, J. M. Norris, M. Hoffman, G. Klingensmith, et al; Diabetes Autoimmunity Study in the Young. 2002. Millennium award recipient contribution. Identification of children with early onset and high incidence of anti-islet autoantibodies. Clin. Immunol. 102: 217-224.
34. + T-cells in HLA-A*0201 transgenic NOD mice. Diabetes 56: 2551-2560.
35. Takaki, T., M. P. Marron, C. E. Mathews, S. T. Guttmann, R. Bottino, M. Trucco, T. P. DiLorenzo, and D. V. Serreze. 2006. HLA-A*0201-restricted T cells from humanized NOD mice recognize autoantigens of potential clinical relevance to type 1 diabetes. J. Immunol. 176: 3257-3265. (Pubitemid 43306990)
36. Jarchum, I., L. Nichol, M. Trucco, P. Santamaria, and T. P. DiLorenzo. 2008. Identification of novel IGRP epitopes targeted in type 1 diabetes patients. Clin. Immunol. 127: 359-365.
37. + T-cell responses change after type 1 diabetes diagnosis and treatment. Diabetes 57: 1312-1320.
38. Forestier, C., T. Takaki, A. Molano, J. S. Im, I. Baine, E. S. Jerud, P. Illarionov, R. Ndonye, A. R. Howell, P. Santamaria, et al. 2007. Improved outcomes in NOD mice treated with a novel Th2 cytokine-biasing NKT cell activator. J. Immunol. 178: 1415-1425.
39. +) T cells from the islets of NOD mice and their use for the study of autoreactive specificities. J. Immunol. Methods 339: 66-73.
40. Regner, M., M. H. Claësson, S. Bregenholt, and M. Röpke. 1996. An improved method for the detection of peptide-induced upregulation of HLA-A2 molecules on TAP-deficient T2 cells. Exp. Clin. Immunogenet. 13: 30-35.
41. Rammensee, H. G., J. Bachmann, and S. Stevanovic. 1997. MHC Ligands and Peptide Motifs. Landes Bioscience, Austin, TX.
42. + T cells in autoimmune diabetes. Proc. Natl. Acad. Sci. USA 100: 8384-8388.
43. Anderson, M. S., E. S. Venanzi, L. Klein, Z. Chen, S. P. Berzins, S. J. Turley, H. von Boehmer, R. Bronson, A. Dierich, C. Benoist, and D. Mathis. 2002. Projection of an immunological self shadow within the thymus by the aire protein. Science 298: 1395-1401.
44. Klein, L., M. Klugmann, K. A. Nave, V. K. Tuohy, and B. Kyewski. 2000. Shaping of the autoreactive T-cell repertoire by a splice variant of self protein expressed in thymic epithelial cells. Nat. Med. 6: 56-61.
45. Cetkovic-Cvrlje, M., I. C. Gerling, A. Muir, M. A. Atkinson, J. F. Elliott, and E. H. Leiter. 1997. Retardation or acceleration of diabetes in NOD/Lt mice mediated by intrathymic administration of candidate β-cell antigens. Diabetes 46: 1975-1982. (Pubitemid 27512083)
46. Marodon, G., S. Fisson, B. Levacher, M. Fabre, B. L. Salomon, and D. Klatzmann. 2006. Induction of antigen-specific tolerance by intrathymic injection of lentiviral vectors. Blood 108: 2972-2978.
47. Hassainya, Y., F. Garcia-Pons, R. Kratzer, V. Lindo, F. Greer, F. A. Lemonnier, G. Niedermann, and P. M. van Endert. 2005. Identification of naturally processed HLA-A2 - restricted proinsulin epitopes by reverse immunology. Diabetes 54: 2053-2059.
48. Karges, W., T. Rajasalu, A. Spyrantis, A. Wieland, B. Boehm, and R. Schirmbeck. 2007. The diabetogenic, insulin-specific CD8 T cell response primed in the experimental autoimmune diabetes model in RIP-B7.1 mice. Eur. J. Immunol. 37: 2097-2103.
49. Bresson, D., L. Togher, E. Rodrigo, Y. Chen, J. A. Bluestone, K. C. Herold, and M. von Herrath. 2006. Anti-CD3 and nasal proinsulin combination therapy enhances remission from recent-onset autoimmune diabetes by inducing Tregs. J. Clin. Invest. 116: 1371-1381.