Discovery of low-affinity preproinsulin epitopes and detection of autoreactive CD8 T-cells using combinatorial MHC multimers

Journal of Autoimmunity

Volumn 37, Issue 3, 2011, Pages 151-159

  Unger, Wendy W ^a,f   Velthuis, Jurjen ^a,f   Abreu, Joana R F ^a,f   Laban, Sandra ^a,f   Quinten, Edwin ^a,f   Kester, Michel G D ^a   Reker Hadrup, Sine ^b,g,h   Bakker, Arnold H ^b,g,h   Duinkerken, Gaby ^a,f   Mulder, Arend ^a,f   Franken, Kees L M C ^a,f   Hilbrands, Robert ^c   Keymeulen, Bart ^c   Peakman, Mark ^d,e   Ossendorp, Ferry ^a,f   Drijfhout, Jan Wouter ^a,f   Schumacher, Ton N ^a,b,f,g,h   Roep, Bart O ^a,f  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b NETHERLANDS CANCER INSTITUTE   (Netherlands)

^c FREE UNIVERSITY OF BRUSSELS   (Belgium)

^d GUY S HOSPITAL   (United Kingdom)

^e GUY'S AND ST THOMAS' NHS FOUNDATION TRUST   (United Kingdom)

^f VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^g GENTOFTE UNIVERSITY HOSPITAL   (Denmark)

^h UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Autoreactive; CD8 T cell; Immunotherapy; Preproinsulin; Type 1 diabetes

Indexed keywords

EPITOPE; FLUOROCHROME; HLA A1 ANTIGEN; HLA A2 ANTIGEN; HLA A3 ANTIGEN; HLA B7 ANTIGEN; PREPROINSULIN; PREPROINSULIN[29-38]; PREPROINSULIN[4-13]; PREPROINSULIN[76-84]; PREPROINSULIN[79-88]; PREPROINSULIN[9-18]; PROTEASOME; QUANTUM DOT; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; HUMAN; INSULIN DEPENDENT DIABETES MELLITUS; MAJOR CLINICAL STUDY; MAJOR HISTOCOMPATIBILITY COMPLEX; PANCREAS ISLET TRANSPLANTATION; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN MULTIMERIZATION; TREATMENT OUTCOME;

ALGORITHMS; AMINO ACID SEQUENCE; AUTOIMMUNITY; CD8-POSITIVE T-LYMPHOCYTES; COMBINATORIAL CHEMISTRY TECHNIQUES; DIABETES MELLITUS, TYPE 1; EPITOPES; EPITOPES, T-LYMPHOCYTE; GRAFT REJECTION; HLA-A ANTIGENS; HLA-B7 ANTIGEN; HUMANS; INSULIN; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS TRANSPLANTATION; MAJOR HISTOCOMPATIBILITY COMPLEX; MOLECULAR SEQUENCE DATA; PEPTIDES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; PROTEIN PRECURSORS; QUANTUM DOTS;

EID: 80755153651     PISSN: 08968411     EISSN: 10959157     Source Type: Journal    
DOI: 10.1016/j.jaut.2011.05.012     Document Type: Article

References (51)

1. Kantwerk G., Cobbold S., Waldmann H., Kolb H. L3T4 and Lyt-2 T cells are both involved in the generation of low-dose streptozotocin-induced diabetes in mice. Clin Exp Immunol 1987, 70:585-592.
2. Serreze D.V., Leiter E.H., Christianson G.J., Greiner D., Roopenian D.C. Major histocompatibility complex class I-deficient NOD-B2mnull mice are diabetes and insulitis resistant. Diabetes 1994, 43:505-509.
3. Wicker L.S., Leiter E.H., Todd J.A., Renjilian R.J., Peterson E., Fischer P.A., et al. Beta 2-microglobulin-deficient NOD mice do not develop insulitis or diabetes. Diabetes 1994, 43:500-504.
4. Santamaria P., Utsugi T., Park B.J., Averill N., Kawazu S., Yoon J.W. Beta-cell-cytotoxic CD8+ T cells from nonobese diabetic mice use highly homologous T cell receptor alpha-chain CDR3 sequences. J Immunol 1995, 154:2494-2503.
5. Wong F.S., Visintin I., Wen L., Flavell R.A., Janeway C.A. CD8 T cell clones from young nonobese diabetic (NOD) islets can transfer rapid onset of diabetes in NOD mice in the absence of CD4 cells. J Exp Med 1996, 183:67-76.
6. Graser R.T., DiLorenzo T.P., Wang F., Christianson G.J., Chapman H.D., Roopenian D.C., et al. Identification of a CD8 T cell that can independently mediate autoimmune diabetes development in the complete absence of CD4 T cell helper functions. J Immunol 2000, 164:3913-3918.
7. Hassainya Y., Garcia-Pons F., Kratzer R., Lindo V., Greer F., Lemonnier F.A., et al. Identification of naturally processed HLA-A2 - restricted proinsulin epitopes by reverse immunology. Diabetes 2005, 54:2053-2059.
8. Ouyang Q., Standifer N.E., Qin H., Gottlieb P., Verchere C.B., Nepom G.T., et al. Recognition of HLA class I-restricted {beta}-cell epitopes in type 1 diabetes. Diabetes 2006, 55:3068-3074.
9. Standifer N.E., Ouyang Q., Panagiotopoulos C., Verchere C.B., Tan R., Greenbaum C.J., et al. Identification of novel HLA-A*0201-restricted epitopes in recent-onset type 1 diabetic subjects and antibody-positive relatives. Diabetes 2006, 55:3061-3067.
10. Toma A., Haddouk S., Briand J.P., Camoin L., Gahery H., Connan F., et al. Recognition of a subregion of human proinsulin by class I-restricted T cells in type 1 diabetic patients. PNAS 2005, 102:10581-10586.
11. Pinkse G.G., Tysma O.H., Bergen C.A., Kester M.G., Ossendorp F., van Veelen P.A., et al. Autoreactive CD8 T cells associated with beta cell destruction in type 1 diabetes. PNAS 2005, 102:18425-18430.
12. Durinovic-Bello I., Wu R.P., Gersuk V.H., Sanda S., Shilling H.G., Nepom G.T. Insulin gene VNTR genotype associates with frequency and phenotype of the autoimmune response to proinsulin. Genes Immun 2010, 11:188-193.
13. Skowera A., Ellis R.J., Varela-Calvino R., Arif S., Huang G.C., Van-Krinks C., et al. Glucose-regulated cytotoxic T-cell epitope of preproinsulin targets killing of beta-cells in human type 1 diabetes. J Clin Invest 2008.
14. Levisetti M.G., Lewis D.M., Suri A., Unanue E.R. Weak proinsulin peptide-major histocompatibility complexes are targeted in autoimmune diabetes in mice. Diabetes 2008, 57:1852-1860.
15. Toebes M., Coccoris M., Bins A., Rodenko B., Gomez R., Nieuwkoop N.J., et al. Design and use of conditional MHC class I ligands. Nat Med 2006, 12:246-251.
16. Hadrup S.R., Bakker A.H., Shu C.J., Andersen R.S., van Veluw J., Hombrink P., et al. Parallel detection of antigen-specific T-cell responses by multidimensional encoding of MHC multimers. Nat Methods 2009, 6:520-526.
17. Keymeulen B., Gillard P., Mathieu C., Movahedi B., Maleux G., Delvaux G., et al. Correlation between beta cell mass and glycemic control in type 1 diabetic recipients of islet cell graft. PNAS 2006, 103:17444-17449.
18. Beekman N.J., van Veelen P.A., van Hall T., Neisig A., Sijts A., Camps M., et al. Abrogation of CTL epitope processing by single amino acid substitution flanking the C-terminal proteasome cleavage site. J Immunol 2000, 164:1898-1905.
19. Eggers M., Boes-Fabian B., Ruppert T., Kloetzel P.M., Koszinowski U.H. The cleavage preference of the proteasome governs the yield of antigenic peptides. J Exp Med 1995, 182:1865-1870.
20. Kessler J.H., Beekman N.J., Bres-Vloemans S.A., Verdijk P., van Veelen P.A., Kloosterman-Joosten A.M., et al. Efficient identification of novel HLA-A*0201-presented cytotoxic T lymphocyte epitopes in the widely expressed tumor antigen PRAME by proteasome-mediated digestion analysis. J Exp Med 2001, 193:73-88.
21. Ottenhoff T., Geluk A., Toebes M., Benckhuijsen W.E., van Meijgaarden K.E., Drijfhout J.W. A sensitive fluorometric assay for quantitatively measuring specific peptide binding to HLA class I and class II molecules. J Immunol Methods 1997, 200:89-97.
22. Altman J.D., Moss P.A.H., Goulder P.J.R., Barouch D.H., Heyzer-Williams M.G., Bell J.I., et al. Phenotypic analysis of antigen-specific T lymphocytes. Science 1996, 274:94-96.
23. Rodenko B., Toebes M., Hadrup S.R., van Esch W.J.E., Molenaar A.M., Schumacher T.N.M., et al. Generation of peptide-MHC class I complexes through UV-mediated ligand exchange. Nat Protoc 2006, 1:1120-1132.
24. Bakker A.H., Hoppes R., Linnemann C., Toebes M., Rodenko B., Berkers C.R., et al. Conditional MHC class I ligands and peptide exchange technology for the human MHC gene products HLA-A1, -A3, -A11, and -B7. PNAS 2008, 105:3825-3830.
25. Parker K.C., Bednarek M.A., Coligan J.E. Scheme for ranking potential HLA-A2 binding peptides based on independent binding of individual peptide side-chains. J Immunol 1994, 152:163-175.
26. Rammensee H., Bachmann J., Emmerich N.P., Bachor O.A., Stevanovic S. SYFPEITHI: database for MHC ligands and peptide motifs. Immunogenetics 1997, 50:213-219.
27. Lundegaard C., Lamberth K., Harndahl M., Buus S., Lund O., Nielsen M. NetMHC-3.0: accurate web accessible predictions of human, mouse and monkey MHC class I affinities for peptides of length 8-11. Nucleic Acids Res 2008, 36:W509-W512.
28. Rammensee H., Bachmann J., Stevanovic S. MHC Ligands and Peptide Motifs 1997, New York. Chapman, Hall (Eds.).
29. Mallone R., Martinuzzi E., Blancou P., Novelli G., Afonso G., Dolz M., et al. CD8+ T-Cell responses identify {beta}-cell autoimmunity in human type 1 diabetes. Diabetes 2007, 56:613-621.
30. Reijonen H., Novak E.J., Kochik S., Heninger A., Liu A.W., Kwok W.W., et al. Detection of GAD65-specific T-cells by major histocompatibility complex class II tetramers in type 1 diabetic patients and at-risk subjects. Diabetes 2002, 51:1375-1382.
31. Zhang J., Markovic-Plese S., Lacet B., Raus J., Weiner H.L., Hafler D.A. Increased frequency of interleukin 2-responsive T cells specific for myelin basic protein and proteolipid protein in peripheral blood and cerebrospinal fluid of patients with multiple sclerosis. J Exp Med 1994, 179:973-984.
32. Takahashi K., Honeyman M.C., Harrison L.C. Cytotoxic T cells to an epitope in the islet autoantigen IA-2 are not disease-specific. Clin Immunol 2001, 99:360-364.
33. Velthuis J.H., Unger W.W., Abreu J.R., Duinkerken G., Franken K., Peakman M., et al. Simultaneous detection of circulating autoreactive CD8+ T-cells specific for different islet cell-associated epitopes using combinatorial MHC-multimers. Diabetes 2010.
34. Naftanel M.A., Harlan D.M. Pancreatic islet transplantation. PLoS Med 2004, 1:198-201.
35. Keymeulen B., Ling Z., Gorus F.K., Delvaux G., Bouwens L., Grupping A., et al. Implantation of standardized beta-cell grafts in a liver segment of IDDM patients: graft and recipient characteristics in two cases of insulin-independence under maintenance immunosuppression for prior kidney graft. Diabetologia 1998, 41:452-459.
36. Hering B.J., Kandaswami R., Harmon J.V., Ansite J.D., Clemmings S.M., Sakai T., et al. Transplantation of cultured islets from two-layer preserved pancreases in type 1 diabetes with anti-CD3 antibody. Am J Transplant 2004, 4:390-401.
37. Ryan E.A., Paty B.W., Senior P.A., Bigam D., Alfadhli E., Kneteman N.M., et al. Five-year follow-up after clinical islet transplantation. Diabetes 2005, 54:2060-2069.
38. Elvin J., Cerundolo V., Elliott T., Townsend A. A quantitative assay of peptide-dependent class I assembly. Eur J Immunol 1991, 21:2025-2031.
39. Eijsink C., Kester M.G.D., Franke M.E.I., Franken K.L.M.C., Heemskerk M.H.M., Claas F.H.J., et al. Rapid assessment of the antigenic integrity of tetrameric HLA complexes by human monoclonal HLA antibodies. J Immunol Methods 2006, 315:153-161.
40. DiBrino M., Parker K.C., Shiloach J., Knierman M., Lukszo J., Turner R.V., et al. Endogenous peptides bound to HLA-A3 possess a specific combination of anchor residues that permit identification of potential antigenic peptides. PNAS 1993, 90:1508-1512.
41. Kubo R.T., Sette A., Grey H.M., Appella E., Sakaguchi K., Zhu N.Z., et al. Definition of specific peptide motifs for four major HLA-A alleles. J Immunol 1994, 152:3913-3924.
42. Sidney J., Grey H.M., Southwood S., Celis E., Wentworth P.A., del Guercio M.F., et al. Definition of an HLA-A3-like supermotif demonstrates the overlapping peptide-binding repertoires of common HLA molecules. Hum Immunol 1996, 45:79-93.
43. Baker C., Petrich de Marquesini L.G., Bishop A.J., Hedges A.J., Dayan C.M., Wong F.S. Human CD8 responses to a complete epitope set from preproinsulin: implications for approaches to epitope discovery. J Clin Invest 2008, 28:350-360.
44. Martinuzzi E., Novelli G., Scotto M., Blancou P., Bach J.M., Chaillous L., et al. The frequency and immunodominance of islet-specific CD8+ T-cell responses change after type 1 diabetes diagnosis and treatment. Diabetes 2008, 57:1312-1320.
45. Toma A., Lashka T., Haddouk S., Luce S., Briand J.P., Camoin L., et al. 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 2009, 58:394-402.
46. Naquet P., Ellis J., Tibensky D., Kenshole A., Singh B., Hodges R., et al. T cell autoreactivity to insulin in diabetic and related non-diabetic individuals. J Immunol 1988, 140:2569-2578.
47. Naik R.G., Beckers C., Wentwoord R., Frenken A., Duinkerken G., Brooks-Worrell B., et al. Precursor frequencies of T-cells reactive to insulin in recent onset type 1 diabetes mellitus. J Autoimmun 2004, 23:55-61.
48. Spielman R.S., Baker L., Zmijewski C.M. Gene dosage and susceptibility to insulin-dependent diabetes. Ann Hum Genet 1980, 44:135-150.
49. Harjutsalo V., Podar T., Tuomilehto J. Cumulative Incidence of type 1 diabetes in 10,168 siblings of Finnish young-onset type 1 diabetic patients. Diabetes 2005, 54:563-569.
50. Tsai S., Shameli A., Santamaria P. CD8+ T cells in type 1 diabetes. Advances in immunology. Immunopathogenesis of type 1 diabetes mellitus 2008, 79-124. Academic Press, Chapter 4. E. RUaH (Ed.).
51. Panagiotopoulos C., Qin H., Tan R., Verchere C.B. Identification of a beta-cell-specific HLA class I restricted epitope in type 1 diabetes. Diabetes 2003, 52:2647-2651.