Diabetogenic T cells recognize insulin bound to IAg7 in an unexpected, weakly binding register

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 24, 2010, Pages 10978-10983

  Stadinski, Brian D ^a,b,d   Zhang, Li ^c   Crawford, Frances ^a,b   Marrack, Philippa ^a,b   Eisenbarth, George S ^a,c   Kappler, John W ^a,b  

^a UNIVERSITY OF COLORADO   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c UNIVERSITY OF COLORADO DENVER   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Antigen presentation; Autoimmunity; Diabetes; Self antigens; Tolerance

Indexed keywords

AMINO ACID; INSULIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PROTEIN IAG7; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOIMMUNITY; BINDING AFFINITY; CONTROLLED STUDY; DIABETOGENESIS; DISEASE PREDISPOSITION; INSULIN DEPENDENT DIABETES MELLITUS; MAJOR HISTOCOMPATIBILITY COMPLEX; MOUSE; NONHUMAN; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; T LYMPHOCYTE;

AMINO ACID SEQUENCE; ANIMALS; ANTIGEN PRESENTATION; BINDING SITES; CD4-POSITIVE T-LYMPHOCYTES; CYSTEINE; DIABETES MELLITUS, TYPE 1; EPITOPES; HISTOCOMPATIBILITY ANTIGENS CLASS II; HYBRIDOMAS; INSULIN; MICE; MICE, INBRED NOD; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING;

EID: 77954643719     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1006545107     Document Type: Article

References (39)

1. Erlich H, et al.; Type 1 Diabetes Genetics Consortium (2008) HLA DR-DQ haplotypes and genotypes and type 1 diabetes risk: Analysis of the type 1 diabetes genetics consortium families. Diabetes 57:1084-1092.
2. Prochazka M, Leiter EH, Serreze DV, Coleman DL (1987) Three recessive loci required for insulin-dependent diabetes in nonobese diabetic mice. Science 237:286-289. (Pubitemid 17095149)
3. Todd JA, Bell JI, McDevitt HO (1987) HLA-DQ beta gene contributes to susceptibility and resistance to insulin-dependent diabetes mellitus. Nature 329:599-604.
4. Suri A, Walters JJ, Gross ML, Unanue ER (2005) Natural peptides selected by diabetogenic DQ8 and murine I-A(g7) molecules show common sequence specificity. J Clin Invest 115: 2268-2276. (Pubitemid 41135930)
5. Reich EP, et al. (1994) Self peptides isolated from MHC glycoproteins of non-obese diabetic mice. J Immunol 152:2279-2288.
6. Suri A, et al. (2002) In APCs, the autologous peptides selected by the diabetogenic IAg7 molecule are unique and determined by the amino acid changes in the P9 pocket. J Immunol 168:1235-1243.
7. McFarland BJ, Beeson C (2002) Binding interactions between peptides and proteins of the class II major histocompatibility complex. Med Res Rev 22:168-203. (Pubitemid 34160584)
8. Hattori M, et al. (1986) The NOD mouse: Recessive diabetogenic gene in the major histocompatibility complex. Science 231:733-735. (Pubitemid 16104046)
9. Acha-Orbea H, McDevitt HO (1987) The first external domain of the nonobese diabetic mouse class II I-A beta chain is unique. Proc Natl Acad Sci USA 84:2435-2439. (Pubitemid 17075881)
10. Latek RR, et al. (2000) Structural basis of peptide binding and presentation by the type I diabetes-associated MHC class II molecule of NOD mice. Immunity 12:699-710.
11. Corper AL, et al. (2000) A structural framework for deciphering the link between IAg7 and autoimmune diabetes. Science 288:505-511.
12. Daniel D, Gill RG, Schloot N, Wegmann D (1995) Epitope specificity, cytokine production profile and diabetogenic activity of insulin-specific T cell clones isolated from NOD mice. Eur J Immunol 25:1056-1062.
13. Abiru N, et al. (2000) Dual overlapping peptides recognized by insulin peptide B:9-23 T cell receptor AV13S3 T cell clones of the NOD mouse. J Autoimmun 14:231-237.
14. Burton AR, et al. (2008) On the pathogenicity of autoantigen-specific T-cell receptors. Diabetes 57:1321-1330.
15. Levisetti MG, Suri A, Petzold SJ, Unanue ER (2007) The insulin-specific T cells of nonobese diabetic mice recognize a weak MHC-binding segment in more than one form. J Immunol 178:6051-6057. (Pubitemid 46717384)
16. Bankovich AJ, Girvin AT, Moesta AK, Garcia KC (2004) Peptide register shifting within the MHC groove: Theory becomes reality. Mol Immunol 40:1033-1039.
17. Anderton SM (2004) Post-translational modifications of self antigens: Implications for autoimmunity. Curr Opin Immunol 16:753-758.
18. Zhang L, Nakayama M, Eisenbarth GS (2008) Insulin as an autoantigen in NOD/human diabetes. Curr Opin Immunol 20:111-118.
19. Crawford F, et al. (2006) Use of baculovirus MHC/peptide display libraries to characterize T-cell receptor ligands. Immunol Rev 210:156-170.
20. Crawford F, Huseby E, White J, Marrack P, Kappler JW (2004) Mimotopes for alloreactive and conventional T cells in a peptide-MHC display library. PLoS Biol 2: 523-533.
21. Kubo RT, Born W, Kappler JW, Marrack P, Pigeon M (1989) Characterization of a monoclonal antibody which detects all murine alpha beta T cell receptors. J Immunol 142:2736-2742.
22. Lee KH, Wucherpfennig KW, Wiley DC (2001) Structure of a human insulin peptide-HLA-DQ8 complex and susceptibility to type 1 diabetes. Nat Immunol 2:501-507.
23. Truscott SM, et al. (2007) Disulfide bond engineering to trap peptides in the MHC class I binding groove. J Immunol 178:6280-6289.
24. Kersh GJ, et al. (2001) Structural and functional consequences of altering a peptide MHC anchor residue. J Immunol 166:3345-3354.
25. Carrasco-Marin E, Shimizu J, Kanagawa O, Unanue ER (1996) The class II MHC I-Ag7 molecules from non-obese diabetic mice are poor peptide binders. J Immunol 156: 450-458.
26. Stratmann T, et al. (2000) The I-Ag7 MHC class II molecule linked to murine diabetes is a promiscuous peptide binder. J Immunol 165:3214-3225.
27. Mathis D, Benoist C (2009) Aire. Annu Rev Immunol 27:287-312.
28. French MB, et al. (1997) Transgenic expression of mouse proinsulin II prevents diabetes in nonobese diabetic mice. Diabetes 46:34-39.
29. Pu Z, Lovitch SB, Bikoff EK, Unanue ER (2004) T cells distinguish MHC-peptide complexes formed in separate vesicles and edited by H2-DM. Immunity 20:467-476.
30. Mohan JF, et al. (2010) Unique autoreactive T cells recognize insulin peptides generated within the islets of Langerhans in autoimmune diabetes. Nat Immunol 11: 350-354.
31. Stadinski BD, et al. (2010) Chromogranin A is an autoantigen in type 1 diabetes. Nat Immunol 11:225-231.
32. He XL, et al. (2002) Structural snapshot of aberrant antigen presentation linked to autoimmunity: The immunodominant epitope of MBP complexed with I-Au. Immunity 17:83-94.
33. Li Y, et al. (2005) Structure of a human autoimmune TCR bound to a myelin basic protein self-peptide and a multiple sclerosis-associated MHC class II molecule. EMBO J 24:2968-2979. (Pubitemid 41486334)
34. Landais E, et al. (2009) New design of MHC class II tetramers to accommodate fundamental principles of antigen presentation. J Immunol 183:7949-7957.
35. Kappler JW, Skidmore B, White J, Marrack P (1981) Antigen-inducible, H-2-restricted, interleukin-2-producing T cell hybridomas. Lack of independent antigen and H-2 recognition. J Exp Med 153:1198-1214. (Pubitemid 11107588)
36. Kozono H, White J, Clements J, Marrack P, Kappler J (1994) Production of soluble MHC class II proteins with covalently bound single peptides. Nature 369:151-154. (Pubitemid 24153438)
37. O'Shea EK, Lumb KJ, Kim PS (1993) Peptide 'Velcro': Design of a heterodimeric coiled coil. Curr Biol 3:658-667.
38. Walker E, Warner NL, Chesnut R, Kappler J, Marrack P (1982) Antigen-specific. I region-restricted interactions in vitro between tumor cell lines and T cell hybridomas. J Immunol 128:2164-2169. (Pubitemid 12086504)
39. Guex N, Peitsch MC (1997) SWISS-MODEL and the Swiss-PdbViewer: An environment for comparative protein modeling. Electrophoresis 18:2714-2723. (Pubitemid 28059943)