HLA-DR4-associated T and B cell responses to specific determinants on the IA-2 autoantigen in type 1 diabetes

Journal of Immunology

Volumn 193, Issue 9, 2014, Pages 4448-4456

  McLaughlin, Kerry A ^a   Gulati, Kavita ^a   Richardson, Carolyn C ^a   Morgan, Diana ^b   Bodansky, H Jonathan ^b   Feltbower, Richard G ^b   Christie, Michael R ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; AUTOANTIGEN; CD45RO ANTIGEN; EPITOPE; GAMMA INTERFERON; HLA DR4 ANTIGEN; IA 2 AUTOANTIBODY; INTERLEUKIN 10; PROTEIN IA 2; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR T BET; UNCLASSIFIED DRUG; PEPTIDE; PTPRN PROTEIN, HUMAN; RECEPTOR LIKE PROTEIN TYROSINE PHOSPHATASE;

ADOLESCENT; ADULT; ANTIGEN PRESENTATION; ARTICLE; B LYMPHOCYTE; CHILD; CONTROLLED STUDY; CYTOKINE RELEASE; FEMALE; HUMAN; HUMAN CELL; INSULIN DEPENDENT DIABETES MELLITUS; MAJOR CLINICAL STUDY; MALE; MEMORY T LYMPHOCYTE; PROTEIN EXPRESSION; T LYMPHOCYTE; TH1 CELL; TH2 CELL; ALLELE; BIOSYNTHESIS; CHEMISTRY; GENETICS; IMMUNOLOGY; IMMUNOPHENOTYPING; METABOLISM; PHENOTYPE; YOUNG ADULT;

ADOLESCENT; ADULT; ALLELES; AUTOANTIBODIES; AUTOANTIGENS; B-LYMPHOCYTES; CHILD; DIABETES MELLITUS, TYPE 1; EPITOPES; FEMALE; HLA-DR4 ANTIGEN; HUMANS; IMMUNOPHENOTYPING; INTERLEUKIN-10; MALE; PEPTIDES; PHENOTYPE; RECEPTOR-LIKE PROTEIN TYROSINE PHOSPHATASES, CLASS 8; T-LYMPHOCYTES; YOUNG ADULT;

EID: 84908124121     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1301902     Document Type: Article

References (49)

1. van Belle, T. L., K. T. Coppieters, and M. G. von Herrath. 2011. Type 1 diabetes: etiology, immunology, and therapeutic strategies. Physiol. Rev. 91: 79-118.
2. Miller, B. J., M. C. Appel, J. J. O'Neil, and L. S. Wicker. 1988. Both the Lyt-2+ and L3T4+ T cell subsets are required for the transfer of diabetes in nonobese diabetic mice. J. Immunol. 140: 52-58.
3. Singal, D. P., and M. A. Blajchman. 1973. Histocompatibility (HL-A) antigens, lymphocytotoxic antibodies and tissue antibodies in patients with diabetes mellitus. Diabetes 22: 429-432.
4. Willcox, A., S. J. Richardson, A. J. Bone, A. K. Foulis, and N. G. Morgan. 2009. Analysis of islet inflammation in human type 1 diabetes. Clin. Exp. Immunol. 155: 173-181.
5. Nerup, J., P. Platz, O. O. Andersen, M. Christy, J. Lyngsoe, J. E. Poulsen, L. P. Ryder, L. S. Nielsen, M. Thomsen, and A. Svejgaard. 1974. HL-A antigens and diabetes mellitus. Lancet 2: 864-866.
6. Bingley, P. J., M. R. Christie, E. Bonifacio, R. Bonfanti, M. Shattock, M. T. Fonte, G. F. Bottazzo, and E. A. Gale. 1994. Combined analysis of autoantibodies improves prediction of IDDM in islet cell antibody-positive relatives. Diabetes 43: 1304-1310.
7. Pescovitz, M. D., C. J. Greenbaum, H. Krause-Steinrauf, D. J. Becker, S. E. Gitelman, R. Goland, P. A. Gottlieb, J. B. Marks, P. F. McGee, A. M. Moran, et al.; Type 1 Diabetes TrialNet Anti-CD20 Study Group. 2009. Rituximab, B-lymphocyte depletion, and preservation of beta-cell function. N. Engl. J. Med. 361: 2143-2152.
8. Serreze, D. V., H. D. Chapman, D. S. Varnum, M. S. Hanson, P. C. Reifsnyder, S. D. Richard, S. A. Fleming, E. H. Leiter, and L. D. Shultz. 1996. B lymphocytes are essential for the initiation of T cell-mediated autoimmune diabetes: analysis of a new "speed congenic" stock of NOD.Ig mu null mice. J. Exp. Med. 184: 2049-2053.
9. Noorchashm, H., N. Noorchashm, J. Kern, S. Y. Rostami, C. F. Barker, and A. Naji. 1997. B-cells are required for the initiation of insulitis and sialitis in nonobese diabetic mice. Diabetes 46: 941-946.
10. Akashi, T., S. Nagafuchi, K. Anzai, S. Kondo, D. Kitamura, S. Wakana, J. Ono, M. Kikuchi, Y. Niho, and T. Watanabe. 1997. Direct evidence for the contribution of B cells to the progression of insulitis and the development of diabetes in non-obese diabetic mice. Int. Immunol. 9: 1159-1164.
11. Noorchashm, H., Y. K. Lieu, N. Noorchashm, S. Y. Rostami, S. A. S. Greeley, A. Schlachterman, H. K. Song, L. E. Noto, A. M. Jevnikar, C. F. Barker, and A. Naji. 1999. I-Ag7-mediated antigen presentation by B lymphocytes is critical in overcoming a checkpoint in T cell tolerance to islet beta cells of nonobese diabetic mice. J. Immunol. 163: 743-750.
12. Ziegler, A. G., M. Hummel, M. Schenker, and E. Bonifacio. 1999. Autoantibody appearance and risk for development of childhood diabetes in offspring of parents with type 1 diabetes: the 2-year analysis of the German BABYDIAB Study. Diabetes 48: 460-468.
13. Gorus, F. K., P. Goubert, C. Semakula, C. L. Vandewalle, J. De Schepper, A. Scheen, M. R. Christie, and D. G. Pipeleers. 1997. IA-2-autoantibodies complement GAD65-autoantibodies in new-onset IDDM patients and help predict impending diabetes in their siblings. The Belgian Diabetes Registry. Diabetologia 40: 95-99.
14. Bingley, P. J., E. Bonifacio, and E. A. Gale. 1994. Antibodies to glutamic acid decarboxylase as predictors of insulin-dependent diabetes mellitus. Lancet 344: 266-267.
15. Christie, M. R., U. Roll, M. A. Payton, E. C. Hatfield, and A. G. Ziegler. 1997. Validity of screening for individuals at risk for type I diabetes by combined analysis of antibodies to recombinant proteins. Diabetes Care 20: 965-970.
16. Christie, M. R., S. Genovese, D. Cassidy, E. Bosi, T. J. Brown, M. Lai, E. Bonifacio, and G. F. Bottazzo. 1994. Antibodies to islet 37k antigen, but not to glutamate decarboxylase, discriminate rapid progression to IDDM in endocrine autoimmunity. Diabetes 43: 1254-1259.
17. Naserke, H. E., A. G. Ziegler, V. Lampasona, and E. Bonifacio. 1998. Early development and spreading of autoantibodies to epitopes of IA-2 and their association with progression to type 1 diabetes. J. Immunol. 161: 6963-6969.
18. Genovese, S., R. Bonfanti, E. Bazzigaluppi, V. Lampasona, E. Benazzi, E. Bosi, G. Chiumello, and E. Bonifacio. 1996. Association of IA-2 autoantibodies with HLA DR4 phenotypes in IDDM. Diabetologia 39: 1223-1226.
19. Howson, J. M., H. Stevens, D. J. Smyth, N. M. Walker, K. A. Chandler, P. J. Bingley, and J. A. Todd. 2011. Evidence that HLA class I and II associations with type 1 diabetes, autoantibodies to GAD and autoantibodies to IA-2, are distinct. Diabetes 60: 2635-2644.
20. Peakman, M., E. J. Stevens, T. Lohmann, P. Narendran, J. Dromey, A. Alexander, A. J. Tomlinson, M. Trucco, J. C. Gorga, and R. M. Chicz. 1999. Naturally processed and presented epitopes of the islet cell autoantigen IA-2 eluted from HLA-DR4. J. Clin. Invest. 104: 1449-1457.
21. Bunce, M., C. M. O'Neill, M. C. Barnardo, P. Krausa, M. J. Browning, P. J. Morris, and K. I. Welsh. 1995. Phototyping: comprehensive DNA typing for HLA-A, B, C, DRB1, DRB3, DRB4, DRB5 & DQB1 by PCR with 144 primer mixes utilizing sequence-specific primers (PCR-SSP). Tissue Antigens 46: 355-367.
22. ∗09 alleles by PCR amplification with sequence-specific primers (PCR-SSP) in 2 hours. Hum. Immunol. 34: 64-74.
23. Weenink, S. M., J. Lo, C. R. Stephenson, P. A. McKinney, R. Ananieva-Jordanova, B. Rees Smith, J. Furmaniak, J. M. Tremble, H. J. Bodansky, and M. R. Christie. 2009. Autoantibodies and associated T-cell responses to determinants within the 831-860 region of the autoantigen IA-2 in Type 1 diabetes. J. Autoimmun. 33: 147-154.
24. Wenzlau, J. M., K. Juhl, L. Yu, O. Moua, S. A. Sarkar, P. Gottlieb, M. Rewers, G. S. Eisenbarth, J. Jensen, H. W. Davidson, and J. C. Hutton. 2007. The cation efflux transporter ZnT8 (Slc30A8) is a major autoantigen in human type 1 diabetes. Proc. Natl. Acad. Sci. USA 104: 17040-17045.
25. Hatfield, E. C. I., C. J. Hawkes, M. A. Payton, and M. R. Christie. 1997. Cross reactivity between IA-2 and phogrin/IA-2beta in binding of autoantibodies in IDDM. Diabetologia 40: 1327-1333.
26. Dromey, J. A., S. M. Weenink, G. H. Peters, J. Endl, P. J. Tighe, I. Todd, and M. R. Christie. 2004. Mapping of epitopes for autoantibodies to the type 1 diabetes autoantigen IA-2 by peptide phage display and molecular modeling: overlap of antibody and T cell determinants. J. Immunol. 172: 4084-4090.
27. Hawkes, C. J., N. C. Schloot, J. Marks, S. J. Willemen, J. W. Drijfhout, E. K. Mayer, M. R. Christie, and B. O. Roep. 2000. T-cell lines reactive to an immunodominant epitope of the tyrosine phosphatase-like autoantigen IA-2 in type 1 diabetes. Diabetes 49: 356-366.
28. Arif, S., T. I. Tree, T. P. Astill, J. M. Tremble, A. J. Bishop, C. M. Dayan, B. O. Roep, and M. Peakman. 2004. Autoreactive T cell responses show proinflammatory polarization in diabetes but a regulatory phenotype in health. J. Clin. Invest. 113: 451-463.
29. Lighvani, A. A., D. M. Frucht, D. Jankovic, H. Yamane, J. Aliberti, B. D. Hissong, B. V. Nguyen, M. Gadina, A. Sher, W. E. Paul, and J. J. O'Shea. 2001. T-bet is rapidly induced by interferon-gamma in lymphoid and myeloid cells. Proc. Natl. Acad. Sci. USA 98: 15137-15142.
30. Yu, H. R., J. C. Chang, R. F. Chen, H. Chuang, K. C. Hong, L. Wang, and K. D. Yang. 2003. Different antigens trigger different Th1/Th2 reactions in neonatal mononuclear cells (MNCs) relating to T-bet/GATA-3 expression. J. Leukoc. Biol. 74: 952-958.
31. Ayyoub, M., F. Deknuydt, I. Raimbaud, C. Dousset, L. Leveque, G. Bioley, and D. Valmori. 2009. Human memory FOXP3+ Tregs secrete IL-17 ex vivo and constitutively express the T(H)17 lineage-specific transcription factor ROR-gamma t. Proc. Natl. Acad. Sci. USA 106: 8635-8640.
32. Yagi, H., T. Nomura, K. Nakamura, S. Yamazaki, T. Kitawaki, S. Hori, M. Maeda, M. Onodera, T. Uchiyama, S. Fujii, and S. Sakaguchi. 2004. Crucial role of FOXP3 in the development and function of human CD25+CD4+ regulatory T cells. Int. Immunol. 16: 1643-1656.
33. Lachenbruch, P. A. 2002. Analysis of data with excess zeros. Stat. Methods Med. Res. 11: 297-302.
34. Hersperger, A. R., F. Pereyra, M. Nason, K. Demers, P. Sheth, L. Y. Shin, C. M. Kovacs, B. Rodriguez, S. F. Sieg, L. Teixeira-Johnson, et al. 2010. Perforin expression directly ex vivo by HIV-specific CD8 T-cells is a correlate of HIV elite control. PLoS Pathog. 6: e1000917.
35. Ziegler, A. G., E. Bonifacio, BABYDIAB-BABYDIET Study Group. 2012. Age-related islet autoantibody incidence in offspring of patients with type 1 diabetes. Diabetologia 55: 1937-1943.
36. Ziegler, R., C. A. Alper, Z. L. Awdeh, L. Castano, S. J. Brink, J. S. Soeldner, R. A. Jackson, and G. S. Eisenbarth. 1991. Specific association of HLA-DR4 with increased prevalence and level of insulin autoantibodies in first-degree relatives of patients with type I diabetes. Diabetes 40: 709-714.
37. Serjeantson, S. W., M. R. Kohonen-Corish, M. J. Rowley, I. R. Mackay, W. Knowles, and P. Zimmet. 1992. Antibodies to glutamic acid decarbox-ylase are associated with HLA-DR genotypes in both Australians and Asians with type 1 (insulin-dependent) diabetes mellitus. Diabetologia 35: 996-1001.
38. 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.
39. Barker, J. M., K. J. Barriga, L. Yu, D. Miao, H. A. Erlich, J. M. Norris, G. S. Eisenbarth, and M. Rewers, Diabetes Autoimmunity Study in the Young. 2004. Prediction of autoantibody positivity and progression to type 1 diabetes: Diabetes Autoimmunity Study in the Young (DAISY). J. Clin. Endocrinol. Metab. 89: 3896-3902.
40. Kulmala, P., K. Savola, J. S. Petersen, P. Vähäsalo, J. Karjalainen, T. Löppönen, T. Dyrberg, H. K. Akerblom, and M. Knip, The Childhood Diabetes in Finland Study Group. 1998. Prediction of insulin-dependent diabetes mellitus in siblings of children with diabetes. A population-based study. J. Clin. Invest. 101: 327-336.
41. Bearzatto, M., H. Naserke, S. Piquer, K. Koczwara, V. Lampasona, A. Williams, M. R. Christie, P. J. Bingley, A. G. Ziegler, and E. Bonifacio. 2002. Two distinctly HLA-associated contiguous linear epitopes uniquely expressed within the islet antigen 2 molecule are major autoantibody epitopes of the diabetes-specific tyrosine phosphatase-like protein autoantigens. J. Immunol. 168: 4202-4208.
42. Ananieva-Jordanova, R., M. Evans, T. Nakamatsu, L. D. Premawardhana, J. Sanders, M. Powell, S. Chen, V. McGrath, C. Belton, C. Arnold, et al. 2005. Isolation and characterisation of a human monoclonal autoantibody to the islet cell autoantigen IA-2. J. Autoimmun. 24: 337-345.
43. ∗04, DQ8 Type 1 diabetes. Diabetologia 47: 439-450.
44. Ott, P. A., B. A. Herzog, S. Quast, H. H. Hofstetter, B. O. Boehm, M. Tary-Lehmann, I. Durinovic-Bello, B. R. Berner, and P. V. Lehmann. 2005. Islet-cell antigen-reactive T cells show different expansion rates and Th1/Th2 differentiation in type 1 diabetic patients and healthy controls. Clin. Immunol. 115: 102-114.
45. Chujo, D., E. Foucat, T. S. Nguyen, D. Chaussabel, J. Banchereau, and H. Ueno. 2013. ZnT8-Specific CD4+ T cells display distinct cytokine expression profiles between type 1 diabetes patients and healthy adults. PLoS ONE 8: e55595.
46. Saraiva, M., and A. O'Garra. 2010. The regulation of IL-10 production by immune cells. Nat. Rev. Immunol. 10: 170-181.
47. Zielinski, C. E., F. Mele, D. Aschenbrenner, D. Jarrossay, F. Ronchi, M. Gattorno, S. Monticelli, A. Lanzavecchia, and F. Sallusto. 2012. Pathogen-induced human TH17 cells produce IFN-γ or IL-10 and are regulated by IL-1β. Nature 484: 514-518.
48. Di Lorenzo, T. P., M. Peakman, and B. O. Roep. 2007. Translational mini-review series on type 1 diabetes: Systematic analysis of T cell epitopes in autoimmune diabetes. Clin. Exp. Immunol. 148: 1-16.
49. Monti, P., M. Scirpoli, A. Rigamonti, A. Mayr, A. Jaeger, R. Bonfanti, G. Chiumello, A. G. Ziegler, and E. Bonifacio. 2007. Evidence for in vivo primed and expanded autoreactive T cells as a specific feature of patients with type 1 diabetes. J. Immunol. 179: 5785-5792.