β-Cell-specific CD8 T cell phenotype in type 1 diabetes reflects chronic autoantigen exposure

Diabetes

Volumn 64, Issue 3, 2015, Pages 916-925

  Skowera, Ania ^a,g   Ladell, Kristin ^b   McLaren, James E ^b   Dolton, Garry ^b   Matthews, Katherine K ^b,c   Gostick, Emma ^b   Kronenberg Versteeg, Deborah ^a   Eichmann, Martin ^a   Knight, Robin R ^a   Heck, Susanne ^d   Powrie, Jake ^d   Bingley, Polly J ^e   Dayan, Colin M ^b   Miles, John J ^b,c,f   Sewell, Andrew K ^b   Price, David A ^b   Peakman, Mark ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b CARDIFF UNIVERSITY SCHOOL OF MEDICINE   (United Kingdom)

^c QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

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

^e UNIVERSITY OF BRISTOL   (United Kingdom)

^f UNIVERSITY OF QUEENSLAND   (Australia)

^g QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HLA ANTIGEN CLASS 1; T LYMPHOCYTE RECEPTOR; TETRAMER; AUTOANTIGEN; GLUTAMATE DECARBOXYLASE; GLUTAMATE DECARBOXYLASE 2; PTPRN PROTEIN, HUMAN; RECEPTOR LIKE PROTEIN TYROSINE PHOSPHATASE;

ADULT; ARTICLE; CD8+ T LYMPHOCYTE; CELL COMPARTMENTALIZATION; CELL EXPANSION; CONTROLLED STUDY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; INSULIN DEPENDENT DIABETES MELLITUS; MOLECULAR BIOLOGY; PANCREAS ISLET BETA CELL; PHENOTYPE; PRIORITY JOURNAL; T LYMPHOCYTE SUBPOPULATION; CELL DIFFERENTIATION; CYTOLOGY; FEMALE; IMMUNOLOGY; MALE; PHYSIOLOGY;

ADULT; AUTOANTIGENS; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; DIABETES MELLITUS, TYPE 1; FEMALE; FLOW CYTOMETRY; GLUTAMATE DECARBOXYLASE; HUMANS; INSULIN-SECRETING CELLS; MALE; RECEPTOR-LIKE PROTEIN TYROSINE PHOSPHATASES, CLASS 8;

EID: 84962052827     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db14-0332     Document Type: Article

References (47)

1. Roep BO, Peakman M. Antigen targets of type 1 diabetes autoimmunity. Cold Spring Harb Perspect Med 2012;2:a007781
2. Roep BO, Peakman M. Diabetogenic T lymphocytes in human Type 1 diabetes. Curr Opin Immunol 2011;23:746-753
3. Coppieters KT, Dotta F, Amirian N, et al. Demonstration of islet-autoreactive CD8 T cells in insulitic lesions from recent onset and long-term type 1 diabetes patients. J Exp Med 2012;209:51-60
4. Willcox A, Richardson SJ, Bone AJ, Foulis AK, Morgan NG. Analysis of islet inflammation in human type 1 diabetes. Clin Exp Immunol 2009;155:173-181
5. Skowera A, Ellis RJ, Varela-Calviño R, et al. CTLs are targeted to kill b cells in patients with type 1 diabetes through recognition of a glucose-regulated preproinsulin epitope [published correction appears in J Clin Invest 2009;119: 2844]. J Clin Invest 2008;118:3390-3402
6. Kronenberg D, Knight RR, Estorninho M, et al. Circulating preproinsulin signal peptide-specific CD8 T cells restricted by the susceptibility molecule HLAA24 are expanded at onset of type 1 diabetes and kill b-cells. Diabetes 2012;61: 1752-1759
7. Nejentsev S, Howson JM, Walker NM, et al; Wellcome Trust Case Control Consortium. Localization of type 1 diabetes susceptibility to the MHC class I genes HLA-B and HLA-A. Nature 2007;450:887-892
8. Scotto M, Afonso G, Larger E, et al. Zinc transporter (ZnT)8(186-194) is an immunodominant CD8+ T cell epitope in HLA-A2+ type 1 diabetic patients. Diabetologia 2012;55:2026-2031
9. Li S, Li H, Chen B, et al. Identification of novel HLA-A 0201-restricted cytotoxic T lymphocyte epitopes from Zinc Transporter 8. Vaccine 2013;31:1610-1615
10. Altman JD, Moss PA, Goulder PJ, et al. Phenotypic analysis of antigenspecific T lymphocytes. Science 1996;274:94-96
11. Wooldridge L, Lissina A, Cole DK, van den Berg HA, Price DA, Sewell AK. Tricks with tetramers: how to get the most from multimeric peptide-MHC. Immunology 2009;126:147-164
12. Chattopadhyay PK, Melenhorst JJ, Ladell K, et al. Techniques to improve the direct ex vivo detection of low frequency antigen-specific CD8+ T cells with peptide-major histocompatibility complex class I tetramers. Cytometry A 2008; 73:1001-1009
13. Mallone R, Scotto M, Janicki CN, et al.; T-Cell Workshop Committee, Immunology of Diabetes Society. Immunology of Diabetes Society T-Cell Workshop: HLA class I tetramer-directed epitope validation initiative. Diabetes Metab Res Rev 2011;27:720-726
14. Chattopadhyay PK, Price DA, Harper TF, et al. Quantum dot semiconductor nanocrystals for immunophenotyping by polychromatic flow cytometry. Nat Med 2006;12:972-977
15. Chattopadhyay PK, Gaylord B, Palmer A, et al. Brilliant violet fluorophores: a new class of ultrabright fluorescent compounds for immunofluorescence experiments. Cytometry A 2012;81:456-466
16. Gattinoni L, Lugli E, Ji Y, et al. A human memory T cell subset with stem cell-like properties. Nat Med 2011;17:1290-1297
17. Velthuis JH, Unger WW, Abreu JR, et al. Simultaneous detection of circulating autoreactive CD8+ T-cells specific for different islet cell-associated epitopes using combinatorial MHC multimers. Diabetes 2010;59:1721-1730
18. Bridgeman JS, Sewell AK, Miles JJ, Price DA, Cole DK. Structural and biophysical determinants of ab T-cell antigen recognition. Immunology 2012; 135:9-18
19. Bulek AM, Cole DK, Skowera A, et al. Structural basis for the killing of human beta cells by CD8(+) T cells in type 1 diabetes. Nat Immunol 2012;13: 283-289
20. Orban T, Bundy B, Becker DJ, et al.; Type 1 Diabetes TrialNet Abatacept Study Group. Co-stimulation modulation with abatacept in patients with recentonset type 1 diabetes: a randomised, double-blind, placebo-controlled trial. Lancet 2011;378:412-419
21. Coppieters KT, Harrison LC, von Herrath MG. Trials in type 1 diabetes: Antigen-specific therapies. Clin Immunol 2013;149:345-355
22. Moran A, Bundy B, Becker DJ, et al.; Type 1 Diabetes TrialNet Canakinumab Study Group; AIDA Study Group. Interleukin-1 antagonism in type 1 diabetes of recent onset: two multicentre, randomised, double-blind, placebo-controlled trials. Lancet 2013;381:1905-1915
23. Buzzetti R. Diabetes: Immunotherapy for T1DM - still not there yet. Nat Rev Endocrinol 2013;9:697-698
24. Price DA, Brenchley JM, Ruff LE, et al. Avidity for antigen shapes clonal dominance in CD8+ T cell populations specific for persistent DNA viruses. J Exp Med 2005;202:1349-1361
25. Lissina A, Ladell K, Skowera A, et al. Protein kinase inhibitors substantially improve the physical detection of T-cells with peptide-MHC tetramers. J Immunol Methods 2009;340:11-24
26. Quigley MF, Almeida JR, Price DA, Douek DC. Unbiased molecular analysis of T cell receptor expression using template-switch anchored RT-PCR. Curr Protoc Immunol 2011;Chapter 10:Unit 10.33
27. Lefranc MP, Pommié C, Ruiz M, et al. IMGT unique numbering for immunoglobulin and T cell receptor variable domains and Ig superfamily V-like domains. Dev Comp Immunol 2003;27:55-77
28. Lugli E, Gattinoni L, Roberto A, et al. Identification, isolation and in vitro expansion of human and nonhuman primate T stem cell memory cells. Nat Protoc 2013;8:33-42
29. Brenchley JM, Karandikar NJ, Betts MR, et al. Expression of CD57 defines replicative senescence and antigen-induced apoptotic death of CD8+ T cells. Blood 2003;101:2711-2720
30. Appay V, van Lier RA, Sallusto F, Roederer M. Phenotype and function of human T lymphocyte subsets: consensus and issues. Cytometry A 2008;73:975-983
31. Sallusto F, Lenig D, Förster R, Lipp M, Lanzavecchia A. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 1999;401:708-712
32. Roederer M, Hardy RR. Frequency difference gating: a multivariate method for identifying subsets that differ between samples. Cytometry 2001;45:56-64
33. Roederer M, Moore W, Treister A, Hardy RR, Herzenberg LA. Probability binning comparison: a metric for quantitating multivariate distribution differences. Cytometry 2001;45:47-55
34. Miles JJ, Douek DC, Price DA. Bias in the ab T-cell repertoire: implications for disease pathogenesis and vaccination. Immunol Cell Biol 2011; 89:375-387
35. Crawford MP, Yan SX, Ortega SB, et al. High prevalence of autoreactive, neuroantigen-specific CD8+ T cells in multiple sclerosis revealed by novel flow cytometric assay. Blood 2004;103:4222-4231
36. Coppieters KT, von Herrath MG. Viruses and cytotoxic T lymphocytes in type 1 diabetes. Clin Rev Allergy Immunol 2011;41:169-178
37. Lugli E, Dominguez MH, Gattinoni L, et al. Superior T memory stem cell persistence supports long-lived T cell memory. J Clin Invest 2013;123:594-599
38. Takata H, Takiguchi M. Three memory subsets of human CD8+ T cells differently expressing three cytolytic effector molecules. J Immunol 2006;177: 4330-4340
39. Chattopadhyay PK, Betts MR, Price DA, et al. The cytolytic enzymes granyzme A, granzyme B, and perforin: expression patterns, cell distribution, and their relationship to cell maturity and bright CD57 expression. J Leukoc Biol 2009;85:88-97
40. Schirmer M, Goldberger C, Würzner R, et al. Circulating cytotoxic CD8(+) CD28(-) T cells in ankylosing spondylitis. Arthritis Res 2002;4:71-76
41. Sun Z, Zhong W, Lu X, et al. Association of Graves' disease and prevalence of circulating IFN-g-producing CD28(-) T cells. J Clin Immunol 2008;28: 464-472
42. Pedroza-Seres M, Linares M, Voorduin S, et al. Pars planitis is associated with an increased frequency of effector-memory CD57+ T cells. Br J Ophthalmol 2007;91:1393-1398
43. Chattopadhyay PK, Chelimo K, Embury PB, et al. Holoendemic malaria exposure is associated with altered Epstein-Barr virus-specific CD8(+) T-cell differentiation. J Virol 2013;87:1779-1788
44. Wooldridge L, Ekeruche-Makinde J, van den Berg HA, et al. A single autoimmune T cell receptor recognizes more than a million different peptides. J Biol Chem 2012;287:1168-1177
45. Price DA, Asher TE, Wilson NA, et al. Public clonotype usage identifies protective Gag-specific CD8+ T cell responses in SIV infection. J Exp Med 2009; 206:923-936
46. Chen H, Ndhlovu ZM, Liu D, et al. TCR clonotypes modulate the protective effect of HLA class I molecules in HIV-1 infection. Nat Immunol 2012;13:691-700
47. Ladell K, Hashimoto M, Iglesias MC, et al. A molecular basis for the control of preimmune escape variants by HIV-specific CD8+ T cells. Immunity 2013;38: 425-436