CD8 T cell autoreactivity to preproinsulin epitopes with very low human leucocyte antigen class I binding affinity

Clinical and Experimental Immunology

Volumn 170, Issue 1, 2012, Pages 57-65

  Abreu, J R F ^a   Martina, S ^a   Verrijn Stuart, A A ^a,b   Fillie Y E ^a   Franken, K L M C ^a   Drijfhout, J W ^a   Roep, B O ^a,c  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c JDRF Center for Beta Cell Therapy in Diabetes in Europe   (Netherlands)

Author keywords

Affinity; Autoimmunity; CD8 T cell; Tolerance; Type 1 diabetes

Indexed keywords

HLA A2 ANTIGEN; HLA ANTIGEN CLASS 1; PREPROINSULIN; QUANTUM DOT;

ANTIGEN BINDING; ARTICLE; AUTOIMMUNITY; BINDING AFFINITY; CD8+ T LYMPHOCYTE; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; HUMAN; IMMUNOGENICITY; INSULIN DEPENDENT DIABETES MELLITUS; MALE; PRESCHOOL CHILD; PRIORITY JOURNAL; PROTEIN BINDING; SCHOOL CHILD; ULTRAVIOLET IRRADIATION;

ADOLESCENT; ALGORITHMS; AMINO ACID SEQUENCE; AUTOIMMUNITY; CD8-POSITIVE T-LYMPHOCYTES; CHILD; CHILD, PRESCHOOL; DIABETES MELLITUS, TYPE 1; EPITOPES, T-LYMPHOCYTE; FEMALE; HISTOCOMPATIBILITY ANTIGENS CLASS I; HLA-A2 ANTIGEN; HUMANS; INSULIN; INSULIN-SECRETING CELLS; MALE; PEPTIDES; PROTEIN BINDING; PROTEIN PRECURSORS;

EID: 84865631586     PISSN: 00099104     EISSN: 13652249     Source Type: Journal    
DOI: 10.1111/j.1365-2249.2012.04635.x     Document Type: Article

References (38)

1. Bottazzo GF, Dean BM, McNally JM, MacKay EH, Swift PG, Gamble DR. In situ characterization of autoimmune phenomena and expression of HLA molecules in the pancreas in diabetic insulitis. N Engl J Med 1985; 313:353-60.
2. Itoh N, Hanafusa T, Miyazaki A etal. Mononuclear cell infiltration and its relation to the expression of major histocompatibility complex antigens and adhesion molecules in pancreas biopsy specimens from newly diagnosed insulin-dependent diabetes mellitus patients. J Clin Invest 1993; 92:2313-22.
3. Nejentsev S, Howson JM, Walker NM etal. Localization of type 1 diabetes susceptibility to the MHC class I genes HLA-B and HLA-A. Nature 2007; 450:887-92.
4. Pinkse GG, Tysma OH, Bergen CA etal. Autoreactive CD8 T cells associated with beta cell destruction in type 1 diabetes. Proc Natl Acad Sci USA 2005; 102:18425-30.
5. Serreze DV, Leiter EH, Christianson GJ, Greiner D, Roopenian DC. Major histocompatibility complex class I-deficient NOD-B2mnull mice are diabetes and insulitis resistant. Diabetes 1994; 43:505-9.
6. Takaki T, Marron MP, Mathews CE etal. HLA-A*0201-restricted T cells from humanized NOD mice recognize autoantigens of potential clinical relevance to type 1 diabetes. J Immunol 2006; 176:3257-65.
7. Velthuis JH, Unger WW, Abreu JR etal. Simultaneous detection of circulating autoreactive CD8+ T-cells specific for different islet cell-associated epitopes using combinatorial MHC multimers. Diabetes 2010; 59:1721-30.
8. Abreu JR, Roep BO. Autoreactive CD8 T cells in Type 1 diabetes: implications for pathogenesis, diagnosis, disease progression and therapeutic intervention. Diabetes Manag 2011; 1:99-108.
9. Roep BO, Peakman M. Surrogate end points in the design of immunotherapy trials: emerging lessons from type 1 diabetes. Nat Rev Immunol 2010; 10:145-52.
10. Buus S, Lauemoller SL, Worning P etal. Sensitive quantitative predictions of peptide-MHC binding by a 'Query by Committee' artificial neural network approach. Tissue Antigens 2003; 62:378-84.
11. D'Amaro J, Houbiers JG, Drijfhout JW etal. A computer program for predicting possible cytotoxic T lymphocyte epitopes based on HLA class I peptide-binding motifs. Hum Immunol 1995; 43:13-8.
12. Dick TP, Stevanovic S, Keilholz W etal. The making of the dominant MHC class I ligand SYFPEITHI. Eur J Immunol 1998; 28:2478-86.
13. Parker KC, Bednarek MA, Coligan JE. Scheme for ranking potential HLA-A2 binding peptides based on independent binding of individual peptide side-chains. J Immunol 1994; 152:163-75.
14. Rammensee H, Bachmann J, Emmerich NP, Bachor OA, Stevanovic S. SYFPEITHI: database for MHC ligands and peptide motifs. Immunogenetics 1999; 50:213-9.
15. Chen W, Khilko S, Fecondo J, Margulies DH, McCluskey J. Determinant selection of major histocompatibility complex class I-restricted antigenic peptides is explained by class I-peptide affinity and is strongly influenced by nondominant anchor residues. J Exp Med 1994; 180:1471-83.
16. Levisetti MG, Lewis DM, Suri A, Unanue ER. Weak proinsulin peptide-major histocompatibility complexes are targeted in autoimmune diabetes in mice. Diabetes 2008; 57:1852-60.
17. Levisetti MG, Suri A, Petzold SJ, Unanue ER. The insulin-specific T cells of nonobese diabetic mice recognize a weak MHC-binding segment in more than one form. J Immunol 2007; 178:6051-7.
18. Ouyang Q, Standifer NE, Qin H etal. Recognition of HLA class I-restricted beta-cell epitopes in type 1 diabetes. Diabetes 2006; 55:3068-74.
19. Unger WW, Velthuis J, Abreu JR etal. Discovery of low-affinity preproinsulin epitopes and detection of autoreactive CD8 T-cells using combinatorial MHC multimers. J Autoimmun 2011; 37:151-9.
20. Pugliese A, Zeller M, Fernandez A, Jr etal. 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 1997; 15:293-7.
21. Vafiadis P, Bennett ST, Todd JA etal. Insulin expression in human thymus is modulated by INS VNTR alleles at the IDDM2 locus. Nat Genet 1997; 15:289-92.
22. Durinovic-Bello I, Wu RP, Gersuk VH, Sanda S, Shilling HG, Nepom GT. Insulin gene VNTR genotype associates with frequency and phenotype of the autoimmune response to proinsulin. Genes Immun 2010; 11:188-93.
23. Skowera A, Ellis RJ, Varela-Calvino R etal. CTLs are targeted to kill beta cells in patients with type 1 diabetes through recognition of a glucose-regulated preproinsulin epitope. J Clin Invest 2008; 118:3390-402.
24. Craig ME, Hattersley A, Donaghue K. ISPAD Clinical Practice Consensus Guidelines 2006-2007. Definition, epidemiology and classification. Pediatr Diabetes 2006; 7:343-51.
25. Tan TL, Geluk A, Toebes M, Ottenhoff TH, Drijfhout JW. A novel, highly efficient peptide-HLA class I binding assay using unfolded heavy chain molecules: identification of HIV-1 derived peptides that bind to HLA-A*0201 and HLA-A*0301. J Immunol Methods 1997; 205:201-9.
26. Hadrup SR, Bakker AH, Shu CJ etal. Parallel detection of antigen-specific T-cell responses by multidimensional encoding of MHC multimers. Nat Methods 2009; 6:520-6.
27. Toebes M, Coccoris M, Bins A etal. Design and use of conditional MHC class I ligands. Nat Med 2006; 12:246-51.
28. Han B, Serra P, Amrani A etal. Prevention of diabetes by manipulation of anti-IGRP autoimmunity: high efficiency of a low-affinity peptide. Nat Med 2005; 11:645-52.
29. Deng L, Mariuzza RA. Recognition of self-peptide-MHC complexes by autoimmune T-cell receptors. Trends Biochem Sci 2007; 32:500-8.
30. Gebe JA, Falk BA, Rock KA etal. Low-avidity recognition by CD4+ T cells directed to self-antigens. Eur J Immunol 2003; 33:1409-17.
31. Mallone R, Kochik SA, Reijonen H etal. Functional avidity directs T-cell fate in autoreactive CD4+ T cells. Blood 2005; 106:2798-805.
32. Reijonen H, Mallone R, Heninger AK etal. GAD65-specific CD4+ T-cells with high antigen avidity are prevalent in peripheral blood of patients with type 1 diabetes. Diabetes 2004; 53:1987-94.
33. Anderton SM, Radu CG, Lowrey PA, Ward ES, Wraith DC. Negative selection during the peripheral immune response to antigen. J Exp Med 2001; 193:1-11.
34. Liu GY, Fairchild PJ, Smith RM, Prowle JR, Kioussis D, Wraith DC. Low avidity recognition of self-antigen by T cells permits escape from central tolerance. Immunity 1995; 3:407-15.
35. Baker C, Petrich de Marquesini LG, Bishop AJ, Hedges AJ, Dayan CM, Wong FS. Human CD8 responses to a complete epitope set from preproinsulin: implications for approaches to epitope discovery. J Clin Immunol 2008; 28:350-60.
36. Muraro PA, Vergelli M, Kalbus M etal. Immunodominance of a low-affinity major histocompatibility complex-binding myelin basic protein epitope (residues 111-129) in HLA-DR4 (B1*0401) subjects is associated with a restricted T cell receptor repertoire. J Clin Invest 1997; 100:339-49.
37. Standifer NE, Ouyang Q, Panagiotopoulos C etal. Identification of novel HLA-A*0201-restricted epitopes in recent-onset type 1 diabetic subjects and antibody-positive relatives. Diabetes 2006; 55:3061-7.
38. Klein L, Hinterberger M, Wirnsberger G, Kyewski B. Antigen presentation in the thymus for positive selection and central tolerance induction. Nat Rev Immunol 2009; 9:833-44.