Current approaches to measuring human islet-antigen specific T cell function in type 1 diabetes

Clinical and Experimental Immunology

Volumn 162, Issue 2, 2010, Pages 197-209

  Mannering, S I ^a   Wong, F S ^b   Durinovic Bello I ^c   Brooks Worrell, B ^d   Tree, T I ^e   Cilio, C M ^f   Schloot, N C ^g   Mallone, R ^h  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b CARDIFF UNIVERSITY   (United Kingdom)

^c KING'S COLLEGE LONDON   (United Kingdom)

^d BENAROYA RESEARCH INSTITUTE   (United States)

^e UNIVERSITY OF WASHINGTON   (United States)

^f LUND UNIVERSITY   (Sweden)

^g UNIVERSITY HOSPITAL DÜSSELDORF   (Germany)

^h HÔPITAL SAINT VINCENT DE PAUL   (France)

Author keywords

CFSE; ELISPOT; Immunoblot; T cell assays; Tetramer; Type 1 diabetes

Indexed keywords

AUTOANTIBODY; C PEPTIDE; CARBOXYFLUORESCEIN DIACETATE SUCCINIMIDYL ESTER; EPITOPE; GLUCOSE; HLA ANTIGEN CLASS 1; INSULIN; MONOCLONAL ANTIBODY CD3; PREPROINSULIN; PROINSULIN; T LYMPHOCYTE RECEPTOR; TETRAMER;

ADAPTIVE IMMUNITY; ANTIGEN PRESENTING CELL; ANTIGEN SPECIFICITY; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL ASSAY; CYTOKINE SECRETION ASSAY; ENZYME LINKED IMMUNOSPOT ASSAY; FLOW CYTOMETRY; GLUCOSE METABOLISM; HLA SYSTEM; HUMAN; IMMUNOASSAY; IMMUNOBLOTTING; IMMUNOREACTIVITY; IMMUNOTHERAPY; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN METABOLISM; LYMPHOCYTE PROLIFERATION; NONHUMAN; PANCREAS ISLET CELL FUNCTION; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN METABOLISM; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION;

EID: 78649358914     PISSN: 00099104     EISSN: 13652249     Source Type: Journal    
DOI: 10.1111/j.1365-2249.2010.04237.x     Document Type: Article

References (61)

1. Atkinson MA, Maclaren NK. The pathogenesis of insulin-dependent diabetes mellitus. N Engl J Med 1994; 331:1428-36.
2. Anderson B, Park BJ, Verdaguer J, Amrani A, Santamaria P. Prevalent CD8(+) T cell response against one peptide/MHC complex in autoimmune diabetes. Proc Natl Acad Sci USA 1999; 96:9311-6.
3. Santamaria P, Utsugi T, Park BJ, Averill N, Kawazu S, Yoon JW. Beta-cell-cytotoxic CD8+ T cells from nonobese diabetic mice use highly homologous T cell receptor alpha-chain CDR3 sequences. J Immunol 1995; 154:2494-503.
4. Pinkse GG, Tysma OH, Bergen CA et al. Autoreactive CD8 T cells associated with beta cell destruction in type 1 diabetes. Proc Natl Acad Sci USA 2005; 102:18425-30.
5. Keymeulen B, Vandemeulebroucke E, Ziegler AG et al. Insulin needs after CD3-antibody therapy in new-onset type 1 diabetes. N Engl J Med 2005; 352:2598-608.
6. Willcox A, Richardson SJ, Bone AJ, Foulis AK, Morgan NG. Analysis of islet inflammation in human type 1 diabetes. Clin Exp Immunol 2009; 155:173-81.
7. Pugliese A, Eisenbarth GS. Human type 1 diabetes mellitus: genetic susceptiblity and resistance. In: Eisenbarth GS, Lafferty KJ, eds. Type 1 diabetes molecular, cellular, and clinical immunology. New York, Oxford: Oxford University Press, 1996:134-52.
8. Noble JA, Valdes AM, Cook M, Klitz W, Thomson G, Erlich HA. The role of HLA class II genes in insulin-dependent diabetes mellitus: molecular analysis of 180 Caucasian, multiplex families. Am J Hum Genet 1996; 59:1134-48.
9. Onengut-Gumuscu S, Concannon P. Mapping genes for autoimmunity in humans: type 1 diabetes as a model. Immunol Rev 2002; 190:182-94.
10. Palmer JP, Asplin CM, Clemons P et al. Insulin antibodies in insulin-dependent diabetics before insulin treatment. Science (NY) 1983; 222:1337-9.
11. Solimena M, Folli F, Denis-Donini S et al. Autoantibodies to glutamic acid decarboxylase in a patient with stiff-man syndrome, epilepsy, and type I diabetes mellitus. N Engl J Med 1988; 318:1012-20.
12. Rabin DU, Pleasic SM, Shapiro JA et al. Islet cell antigen 512 is a diabetes-specific islet autoantigen related to protein tyrosine phosphatases. J Immunol 1994; 152:3183-8.
13. Wenzlau JM, Juhl K, Yu L et al. The cation efflux transporter ZnT8 (Slc30A8) is a major autoantigen in human type 1 diabetes. Proc Natl Acad Sci USA 2007; 104:17040-5.
14. Bingley PJ, Christie M, Bonifacio E et al. Combined analysis of autoantibodies improves prediction of IDDM in islet cell antibody-positive relatives. Diabetes 1994; 43:1304-10.
15. Verge CF, Stenger D, Bonifacio E et al. Combined use of autoantibodies (IA-2 autoantibody, GAD autoantibody, insulin autoantibody, cytoplasmic islet cell antibodies) in type 1 diabetes: Combinatorial Islet Autoantibody Workshop. Diabetes 1998; 47:1857-66.
16. MacLeod MK, Clambey ET, Kappler JW, Marrack P. CD4 memory T cells: what are they and what can they do? Semin Immunol 2009; 21:53-61.
17. Mannering SI, Brodnicki TC. CD4+ T-cell specificity and function in type 1 diabetes. Expert Rev Clin Immunol 2007; 3:557-64.
18. 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.
19. Herold KC, Hagopian W, Auger JA et al. Anti-CD3 monoclonal antibody in new-onset type 1 diabetes mellitus.N Engl JMed 2002; 346:1692-8.
20. Ludvigsson J, Faresjo M, Hjorth M et al. GAD treatment and insulin secretion in recent-onset type 1 diabetes. N Engl J Med 2008; 359:1909-20.
21. Durinovic-Bello I, Rosinger S, Olson JA et al. DRB1*0401-restricted human T cell clone specific for the major proinsulin73-90 epitope expresses a down-regulatory T helper 2 phenotype. Proc Natl Acad Sci USA 2006; 103:11683-8.
22. Altman JD, Moss PA, Goulder PJ et al. Phenotypic analysis of antigen-specific T lymphocytes. Science (NY) 1996; 274:94-6.
23. Mallone R, Martinuzzi E, Blancou P et al. CD8+ T-cell responses identify {beta}-cell autoimmunity in human type 1 diabetes. Diabetes 2007; 56:613-21.
24. Martinuzzi E, Novelli G, Scotto M et al. The frequency and immunodominance of islet-specific CD8+ T-cell responses change after type 1 diabetes diagnosis and treatment. Diabetes 2008; 57:1312-20.
25. Martinuzzi E, Lemonnier FA, Boitard C, Mallone R. Measurement of CD8 T cell responses in human type 1 diabetes.Ann NY Acad Sci 2008; 1150:61-7.
26. Brooks-Worrell BM, Starkebaum GA, Greenbaum C, Palmer JP. Peripheral blood mononuclear cells of insulin-dependent diabetic patients respond to multiple islet cell proteins. J Immunol 1996; 157:5668-74.
27. Mannering SI, Morris JS, Jensen KP et al. A sensitive method for detecting proliferation of rare autoantigen-specific human T cells. J Immunol Methods 2003; 283:173-83.
28. Arif S, Tree TI, Astill TP et al. Autoreactive T cell responses show proinflammatory polarization in diabetes but a regulatory phenotype in health. J Clin Invest 2004; 113:451-63.
29. Di Lorenzo TP, Peakman M, Roep BO, Mini-Review T. Series on type 1 diabetes: systematic analysis of T cell epitopes in autoimmune diabetes. Clin Exp Immunol 2007; 148:1-16.
30. Mannering SI, Harrison LC, Williamson NA et al. The insulin A-chain epitope recognized by human T cells is posttranslationally modified. J Exp Med 2005; 202:1191-7.
31. Mannering SI, Pang SH, Williamson NA et al. The A-chain of insulin is a hot-spot for CD4+ T cell epitopes in human type 1 diabetes. Clin Exp Immunol 2009; 156:226-31.
32. Peakman M, Tree TI, Endl J, van Endert P, Atkinson MA, Roep BO. 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 2001; 50:1749-54.
33. Mannering SI, Purcell AW, Honeyman MC, McCluskey J, Harrison LC. Human T-cells recognise N-terminally Fmoc-modified peptide. Vaccine 2003; 21:3638-46.
34. Matsuo H, Batocchi AP, Hawke S et al. Peptide-selected T cell lines from myasthenia gravis patients and controls recognize epitopes that are not processed from whole acetylcholine receptor. J Immunol 1995; 155:3683-92.
35. Herold KC, Brooks-Worrell B, Palmer J et al. Validity and reproducibility of measurement of islet autoreactivity by T-cell assays in subjects with early type 1 diabetes. Diabetes 2009; 58:2588-95.
36. Martinuzzi E, Scotto M, Enee E et al. Serum-free culture medium and IL-7 costimulation increase the sensitivity of ELISpot detection. J Immunol Methods 2008; 333:61-70.
37. Meierhoff G, Ott PA, Lehmann PV, Schloot NC. Cytokine detection by ELISPOT: relevance for immunological studies in type 1 diabetes. Diabetes Metab Res Rev 2002; 18:367-80.
38. Schloot NC, Meierhoff G, Karlsson Faresjo M et al. Comparison of cytokine ELISpot assay formats for the detection of islet antigen autoreactive T cells. Report of the third Immunology of Diabetes Society T-Cell Workshop. J Autoimmun 2003; 21:365-76.
39. Manz R, Assenmacher M, Pfluger E, Miltenyi S, Radbruch A. Analysis and sorting of live cells according to secreted molecules, relocated to a cell-surface affinity matrix. Proc Natl Acad Sci USA 1995; 92:1921-5.
40. Seyfert-Margolis V, Gisler TD, Asare AL et al. Analysis of T-cell assays to measure autoimmune responses in subjects with type 1 diabetes: results of a blinded controlled study. Diabetes 2006; 55:2588-94.
41. Goel A, Chiu H, Felton J, Palmer JP, Brooks-Worrell B. T-cell responses to islet antigens improves detection of autoimmune diabetes and identifies patients with more severe beta-cell lesions in phenotypic type 2 diabetes. Diabetes 2007; 56:2110-5.
42. Brooks-Worrell B, Gersuk VH, Greenbaum C, Palmer JP. Intermolecular antigen spreading occurs during the preclinical period of human type 1 diabetes. J Immunol 2001; 166:5265-70.
43. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227:680-5.
44. Lyons AB, Parish CR. Determination of lymphocyte division by flow cytometry. J Immunol Methods 1994; 171:131-7.
45. Mannering SI, Dromey JA, Morris JS, Thearle DJ, Jensen KP, Harrison LC. An efficient method for cloning human autoantigenspecific T cells. J Immunol Methods 2005; 298:83-92.
46. Davis MM, Boniface JJ, Reich Z et al. Ligand recognition by alpha beta T cell receptors. Annu Rev Immunol 1998; 16:523-44.
47. Nepom GT, Buckner JH, Novak EJ et al. HLA class II tetramers: tools for direct analysis of antigen-specific CD4+ T cells. Arthritis Rheum 2002; 46:5-12.
48. Denkberg G, Cohen CJ, Segal D, Kirkin AF, Reiter Y. Recombinant human single-chain MHC-peptide complexes made from E. coli by in vitro refolding: functional single-chain MHC-peptide complexes and tetramers with tumor associated antigens. Eur J Immunol 2000; 30:3522-32.
49. Garboczi DN, Hung DT, Wiley DC. HLA-A2-peptide complexes: refolding and crystallization of molecules expressed in Escherichia coli and complexed with single antigenic peptides. Proc Natl Acad Sci USA 1992; 89:3429-33.
50. Novak EJ, Liu AW, Nepom GT, Kwok WW.MHC class II tetramers identify peptide-specific human CD4(+) T cells proliferating in response to influenza A antigen. J Clin Invest 1999; 104:R63-7.
51. James EA, LaFond R, Durinovic-Bello I, Kwok W. Visualizing antigen specific CD4+ T cells using MHC class II tetramers. J Vis Exp 2009; pii: 1167. doi: 10.3791/1167.
52. Yang J, Danke N, Roti M et al. CD4+ T cells from type 1 diabetic and healthy subjects exhibit different thresholds of activation to a naturally processed proinsulin epitope. J Autoimmun 2008; 31:30-41.
53. Casalegno-Garduno R, Schmitt A, Yao J et al. Multimer technologies for detection and adoptive transfer of antigen-specific T cells. Cancer Immunol Immunother 2009; 59:195-202.
54. Durinovic-Bello I, Wu RP, Gersuk VH, Sanda S, Shilling HG, Nepom GT. Insulin geneVNTR genotype associates with frequency and phenotype of the autoimmune response to proinsulin. Genes Immun 2010; 11:188-93.
55. Anikeeva N, Lebedeva T, Clapp AR et al. Quantum dot/peptide-MHC biosensors reveal strong CD8-dependent cooperation between self and viral antigens that augment the T cell response. Proc Natl Acad Sci USA 2006; 103:16846-51.
56. Scriba TJ, Purbhoo M, Day CL et al. Ultrasensitive detection and phenotyping of CD4+ T cells with optimized HLA class II tetramer staining. J Immunol 2005; 175:6334-43.
57. Mallone R, Kochik SA, Reijonen H et al. Functional avidity directs T-cell fate in autoreactive CD4+ T cells. Blood 2005; 106:2798-805.
58. Pfleger C, Meierhoff G, Kolb H, Schloot NC. Association of T-cell reactivity with beta-cell function in recent onset type 1 diabetes patients. J Autoimmun 2010; 34:127-35.
59. Jonuleit H, Schmitt E, Schuler G, Knop J, Enk AH. Induction of interleukin 10-producing, nonproliferating CD4(+) T cells with regulatory properties by repetitive stimulation with allogeneic immature human dendritic cells. J Exp Med 2000; 192:1213-22.
60. Tree TI, Lawson J, Edwards H et al. Naturally arising human CD4 T cells that recognize islet autoantigens and secrete IL-10 regulate pro-inflammatory T cell responses via linked suppression. Diabetes 2010; 59:1451-60.
61. Levings MK, Sangregorio R, Sartirana C et al. Human CD25+CD4+ T suppressor cell clones produce transforming growth factor beta, but not interleukin 10, and are distinct from type 1 T regulatory cells. J Exp Med 2002; 196:1335-46.