HLA-DQ2 and -DQ8 signatures of gluten T cell epitopes in celiac disease

Journal of Clinical Investigation

Volumn 116, Issue 8, 2006, Pages 2226-2236

  Tollefsen, Stig ^a   Arentz Hansen, Helene ^a   Fleckenstein, Burkhard ^a   Molberg, Øyvind ^a,b   Ráki, Melinda ^a   Kwok, William W ^c   Jung, Günther ^d   Lundin, Knut E A ^a,b   Sollid, Ludvig M ^a  

^a UNIVERSITY OF OSLO   (Norway)

^b OSLO UNIVERSITY HOSPITAL   (Norway)

^c BENAROYA RESEARCH INSTITUTE   (United States)

^d UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; GLIADIN; GLUTEN; HETERODIMER; HLA DQ2 ANTIGEN; HLA DQ8 ANTIGEN; PEPTIDE; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 2; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

ADULT; ARTICLE; CELIAC DISEASE; CELL ISOLATION; CLINICAL ARTICLE; CONTROLLED STUDY; DEAMINATION; GENE MAPPING; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; INSULIN DEPENDENT DIABETES MELLITUS; PRIORITY JOURNAL; PROTEIN BINDING; T LYMPHOCYTE;

AMINO ACID SEQUENCE; CELIAC DISEASE; DIABETES MELLITUS, TYPE 1; DIMERIZATION; EPITOPES; GLIADIN; HLA ANTIGENS; HLA-DQ ANTIGENS; HUMANS; IMMUNITY, MUCOSAL; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; T-LYMPHOCYTES;

EID: 33746694192     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI27620     Document Type: Article

References (48)

1. Green, P.H., and Jabri, B. 2003. Coeliac disease. Lancet. 362:383-391.
2. Sollid, L.M. 2000. Molecular basis of celiac disease. Annu. Rev. Immunol. 18:53-81.
3. Sollid, L.M., and Lie, B.A. 2005. Celiac disease genetics: current concepts and practical applications. Clin. Gastroenterol. Hepatol. 3:843-851.
4. Lundin, K.E.A., et al. 1993. Gliadin-specific, HLA- DQ(α1*0501,β1*0201) restricted T cells isolated from the small intestinal mucosa of celiac disease patients. J. Exp. Med. 178:187-196.
5. Molberg, Ø., et al. 1997. Gliadin specific, HLA DQ2-restricted T cells are commonly found in small intestinal biopsies from coeliac disease patients, but not from controls. Scand. J. Immunol. 46:103-109.
6. Lundin, K.E.A., Scott, H., Fausa, O., Thorsby, E., and Sollid, L.M. 1994. T cells from the small intestinal mucosa of a DR4, DQ7/DR4, DQ8 celiac disease patient preferentially recognize gliadin when presented by DQ8. Hum. Immunol. 41:285-291.
7. Molberg, Ø., et al. 1998. Tissue transglutaminase selectively modifies gliadin peptides that are recognized by gut-derived T cells. Nat. Med. 4:713-717.
8. van de Wal, Y., et al. 1998. Selective deamidation by tissue transglutaminase strongly enhances gliadin-specific T cell reactivity. J. Immunol. 161:1585-1588.
9. Johansen, B.H., Vartdal, F., Eriksen, J.A., Thorsby, E., and Sollid, L.M. 1996. Identification of a putative motif for binding of peptides to HLA-DQ2. Int. Immunol. 8:177-182.
10. van de Wal, Y., Kooy, Y.M.C., Drijfhout, J.W., Amons, R., and Koning, F. 1996. Peptide binding characteristics of the coeliac disease-associated DQ(α1*0501, β1*0201) molecule. Immunogenetics. 44:246-253.
11. Kwok, W.W., Domeier, M.L., Raymond, F.C., Byers, P., and Nepom, G.T. 1996. Allele-specific motifs characterize HLA-DQ interactions with a diabetes-associated peptide derived from glutamic acid decarboxylase. J. Immunol. 156:2171-2177.
12. Godkin, A., et al. 1997. Use of eluted peptide sequence data to identify the binding characteristics of peptides to the insulin-dependent diabetes susceptibility allele HLA-DQ8 (DQ 3.2). Int. Immunol. 9:905-911.
13. Suri, A., Walters, J.J., Gross, M.L., and Unanue, E.R. 2005. Natural peptides selected by diabetogenic DQ8 and murine I-A(g7)molecules show common sequence specificity. J. Clin. Invest. 115:2268-2276. doi:10.1172/JCI25350.
14. Sjöström, H., et al. 1998. Identification of a gliadin T-cell epitope in coeliac disease: general importance of gliadin deamidation for intestinal T-cell recognition. Scand. J. Immunol. 48:111-115.
15. Arentz-Hansen, H., et al. 2000. The intestinal T cell response to α-gliadin in adult celiac disease is focused on a single deamidated glutamine targeted by tissue transglutaminase. J. Exp. Med. 191:603-612.
16. Anderson, R.P., Degano, P., Godkin, A.J., Jewell, D.P., and Hill, A.V. 2000. In vivo antigen challenge in celiac disease identifies a single transglutaminase-modified peptide as the dominant A-gliadin T-cell epitope. Nat. Med. 6:337-342.
17. Vader, W., et al. 2002. The gluten response in children with celiac disease is directed toward multiple gliadin and glutenin peptides. Gastroenterology. 122:1729-1737.
18. Arentz-Hansen, H., et al. 2002. Celiac lesion T cells recognize epitopes that cluster in regions of gliadins rich in proline residues. Gastroenterology. 123:803-809.
19. Qiao, S.W., et al. 2005. Refining the rules of gliadin T cell epitope binding to the disease-associated DQ2 molecule in celiac disease: importance of proline spacing and glutamine deamidation. J. Immunol. 175:254-261.
20. van de Wal, Y., et al. 1998. Small intestinal T cells of celiac disease patients recognize a natural pepsin fragment of gliadin. Proc. Natl. Acad. Sci. U. S. A. 95:10050-10054.
21. van de Wal, Y., et al. 1999. Glutenin is involved in the gluten-driven mucosal T cell response. Eur. J. Immunol. 29:3133-3139.
22. Svejgaard, A., and Ryder, L.P. 1981. HLA genotype distribution and genetic models of insulin-dependent diabetes mellitus. Ann. Hum. Genet. 45:293-298.
23. Todd, J.A., Bell, J.I., and McDevitt, H.O. 1987. HLA-DQb gene contributes to susceptibility and resistance to insulin-dependent diabetes mellitus. Nature. 329:599-604.
24. Thorsby, E. 1997. Invited anniversary review: HLA associated diseases. Hum. Immunol. 53:1-11.
25. Nepom, G.T., and Erlich, H. 1991. MHC class-II molecules and autoimmunity. Annu. Rev. Immunol. 9:493-525.
26. Redondo, M.J., and Eisenbarth, G.S. 2002. Genetic control of autoimmunity in type I diabetes and associated disorders. Diabetologia. 45:605-622.
27. Koeleman, B.P.C., et al. 2004. Genotype effects and epistasis in type 1 diabetes and HLA-DQ trans dimer associations with disease. Genes Immun. 5:381-388.
28. Lee, K.H., Wucherpfennig, K.W., and Wiley, D.C. 2001. Structure of a human insulin peptide-HLADQ8 complex and susceptibility to type 1 diabetes. Nat. Immunol. 2:501-507.
29. Kim, C.Y., Quarsten, H., Bergseng, E., Khosla, C., and Sollid, L.M. 2004. Structural basis for HLA-DQ2-mediated presentation of gluten epitopes in celiac disease. Proc. Natl. Acad. Sci. U. S. A. 101:4175-4179.
30. Jones, E.Y., Fugger, L., Strominger, J.L., and Siebold, C. 2006. MHC class II proteins and disease: a structural perspective. Nat. Rev. Immunol. 6:271-282.
31. Bergseng, E., Xia, J., Kim, C.Y., Khosla, C., and Sollid, L.M. 2005. Main chain hydrogen bond interactions in the binding of proline-rich gluten peptides to the Celiac disease-associated HLA-DQ2 molecule. J. Biol. Chem. 280:21791-21796.
32. Nelson, C.A., and Fremont, D.H. 1999. Structural principles of MHC class II antigen presentation. Rev. Immunogenet. 1:47-59.
33. Nepom, B.S., Schwarz, D., Palmer, J.P., and Nepom, G.T. 1987. Transcomplementation of HLA genes in IDDM. HLA-DQ α- and β-chains produce hybrid molecules in DR3/4 heterozygotes. Diabetes. 36:114-117.
34. Kwok, W.W., Kovats, S., Thurtle, P., and Nepom, G.T. 1993. HLA-DQ allelic polymorphisms constrain patterns of class II heterodimer formation. J. Immunol. 150:2263-2272.
35. Peakman, M., et al. 2001. Characterization of preparations of GAD65, proinsulin, and the islet tyrosine phosphatase IA-2 for use in detection of autoreactive T-cells in type 1 diabetes: report of phase II of the Second International Immunology of Diabetes Society Workshop for Standardization of T-cell assays in type 1 diabetes. Diabetes. 50:1749-1754.
36. Viglietta, V., Kent, S.C., Orban, T., and Hafler, D.A. 2002. GAD65-reactive T cells are activated in patients with autoimmune type 1a diabetes. J. Clin. Invest. 109:895-903. doi:10.1172/JCI200214114.
37. Kent, S.C., et al. 2005. Expanded T cells from pancreatic lymph nodes of type 1 diabetic subjects recognize an insulin epitope. Nature. 435:224-228.
38. Mannering, S.I., et al. 2005. The insulin A-chain epitope recognized by human T cells is posttranslationally modified. J. Exp. Med. 202:1191-1197.
39. Arentz-Hansen, E.H., McAdam, S.N., Molberg, Ø., Kristiansen, C., and Sollid, L.M. 2000. Production of a panel of recombinant gliadins for the characterisation of T cell reactivity in coeliac disease. Gut. 46:46-51.
40. Molberg, Ø., et al. 2003. Intestinal T-cell responses to high-molecular-weight glutenins in celiac disease. Gastroenterology. 125:337-344.
41. Piper, J.L., Gray, G.M., and Khosla, C. 2002. High selectivity of human tissue transglutaminase for immunoactive gliadin peptides: implications for celiac sprue. Biochemistry. 41:386-393.
42. Viken, H.D., et al. 1995. Characterization of an HLA-DQ2-specific monoclonal antibody. Influence of amino acid substitutions in DQβ1*0202. Hum. Immunol. 42:319-327.
43. Giles, R.C., et al. 1983. Structural analysis of a human I-A homologue using a monoclonal antibody that recognizes an MB3-like specificity. J. Exp. Med. 157:1461-1470.
44. + cytotoxic T lymphocyte clones directed at products of different class II major histocompatibility complex loci. J. Immunol. 131:678-683.
45. Amar, A., et al. 1987. Characterization of specific HLA-DQα allospecificities by genomic, biochemical, and serologic analysis. J. Immunol. 138:3986-3990.
46. Kwok, W.W., et al. 1988. HLA-DQ molecules form α-β heterodimers of mixed allotype. J. Immunol. 141:3123-3127.
47. Reichstetter, S., Kwok, W.W., and Nepom, G.T. 1999. Impaired binding of a DQ2 and DQ8-binding HSV VP16 peptide to a DQA1*0501/DQB1*0302 trans class II heterodimer. Tissue Antigens. 53:101-105.
48. Molberg, Ø., McAdam, S.N., Lundin, K.E.A., and Sollid, L.M. 2000. Studies of gliadin-specific T cells in celiac disease. In Celiac disease. Methods and protocols. M.N. Marsh, editor. Humana. Totowa, New Jersey, USA. 105-124.