Human β-cell killing by autoreactive preproinsulin-specific CD8 T cells is predominantly granule-mediated with the potency dependent upon T-cell receptor avidity

Diabetes

Volumn 62, Issue 1, 2013, Pages 205-213

  Knight, Robin R ^a   Kronenberg, Deborah ^a,b   Zhao, Min ^a   Huang, Guo Cai ^a   Eichmann, Martin ^a   Bulek, Anna ^c   Wooldridge, Linda ^c   Cole, David K ^c   Sewell, Andrew K ^c   Peakman, Mark ^a,b   Skowera, Ania ^a,b  

^a KING'S COLLEGE LONDON   (United Kingdom)

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

^c CARDIFF UNIVERSITY SCHOOL OF MEDICINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FAS ANTIGEN; FAS LIGAND; PREPROINSULIN; T LYMPHOCYTE RECEPTOR; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

APOPTOSIS; ARTICLE; CD8+ T LYMPHOCYTE; CELL CLONE; CELL DEATH; CELL KILLING; CYTOTOXICITY; DEGRANULATION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOPATHOLOGY; IMMUNOREACTIVITY; INSULIN DEPENDENT DIABETES MELLITUS; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN INTERACTION; TARGET CELL;

ANTIGENS, CD95; CD8-POSITIVE T-LYMPHOCYTES; CELL DEGRANULATION; CELL LINE; CYTOTOXICITY, IMMUNOLOGIC; FAS LIGAND PROTEIN; HUMANS; INSULIN; INSULIN-SECRETING CELLS; PROTEIN PRECURSORS; RECEPTORS, ANTIGEN, T-CELL; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84872051107     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db12-0315     Document Type: Article

References (30)

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;313:353-360 (Pubitemid 15046367)
2. 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
3. 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
4. Wicker LS, Leiter EH, Todd JA, et al. Beta 2-microglobulin-deficient NOD mice do not develop insulitis or diabetes. Diabetes 1994;43:500-504 (Pubitemid 24064260)
5. Liblau RS, Wong FS, Mars LT, Santamaria P. Autoreactive CD8 T cells in organ-specific autoimmunity: emerging targets for therapeutic intervention. Immunity 2002;17:1-6 (Pubitemid 34874613)
6. Coppieters K, Amirian N, von Herrath M. Intravital imaging of CTLs killing islet cells in diabetic mice. J Clin Invest 2012;122:119-131
7. Skowera A, Ellis RJ, Varela-Calviño R, et al. 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;118:3390-3402
8. 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
9. 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
10. Lieberman J. The ABCs of granule-mediated cytotoxicity: new weapons in the arsenal. Nat Rev Immunol 2003;3:361-370 (Pubitemid 37323196)
11. Itoh N, Imagawa A, Hanafusa T, et al. Requirement of Fas for the development of autoimmune diabetes in nonobese diabetic mice. J Exp Med 1997;186:613-618 (Pubitemid 27360805)
12. Kägi D, Ledermann B, Bürki K, Zinkernagel RM, Hengartner H. Molecular mechanisms of lymphocyte-mediated cytotoxicity and their role in immunological protection and pathogenesis in vivo. Annu Rev Immunol 1996;14:207-232 (Pubitemid 26130183)
13. Shrestha B, Diamond MS. Fas ligand interactions contribute to CD8+ T-cell-mediated control of West Nile virus infection in the central nervous system. J Virol 2007;81:11749-11757 (Pubitemid 47623807)
14. Campbell PD, Estella E, Dudek NL, et al. Cytotoxic T-lymphocyte-mediated killing of human pancreatic islet cells in vitro. Hum Immunol 2008;69:543-551
15. Thomas HE, Trapani JA, Kay TW. The role of perforin and granzymes in diabetes. Cell Death Differ 2010;17:577-585
16. Roep BO, Peakman M. Diabetogenic T lymphocytes in human Type 1 diabetes. Curr Opin Immunol 2011;23:746-753
17. Kronenberg D, Knight RR, Estorninho M, et al. Circulating Preproinsulin Signal Peptide-Specific CD8 T Cells Restricted by the Susceptibility Molecule HLA-A24 Are Expanded at Onset of Type 1 Diabetes and Kill β-Cells. Diabetes 2012;61:1752-1759
18. Huang GC, Zhao M, Jones P, et al. The development of new density gradient media for purifying human islets and islet-quality assessments. Transplantation 2004;77:143-145 (Pubitemid 38116889)
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. Blomberg K, Hautala R, Lövgren J, Mukkala VM, Lindqvist C, Akerman K. Time-resolved fluorometric assay for natural killer activity using target cells labelled with a fluorescence enhancing ligand. J Immunol Methods 1996;193:199-206 (Pubitemid 26227987)
21. Cole DK, Dunn SM, Sami M, Boulter JM, Jakobsen BK, Sewell AK. T cell receptor engagement of peptide-major histocompatibility complex class I does not modify CD8 binding. Mol Immunol 2008;45:2700-2709
22. Kuzushima K, Hayashi N, Kimura H, Tsurumi T. Efficient identification of HLA-A*2402-restricted cytomegalovirus-specific CD8(+) T-cell epitopes by a computer algorithm and an enzyme-linked immunospot assay. Blood 2001;98:1872-1881
23. Burrows SR, Elkington RA, Miles JJ, et al. Promiscuous CTL recognition of viral epitopes on multiple human leukocyte antigens: biological validation of the proposed HLA A24 supertype. J Immunol 2003;171:1407-1412 (Pubitemid 36900074)
24. Kataoka T, Takaku K, Magae J, et al. Acidification is essential for maintaining the structure and function of lytic granules of CTL. Effect of concanamycin A, an inhibitor of vacuolar type H(+)-ATPase, on CTL-mediated cytotoxicity. J Immunol 1994;153:3938-3947
25. 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
26. Kägi D, Odermatt B, Seiler P, Zinkernagel RM, Mak TW, Hengartner H. Reduced incidence and delayed onset of diabetes in perforin-deficient nonobese diabetic mice. J Exp Med 1997;186:989-997 (Pubitemid 27441144)
27. Mastrandrea L, Yu J, Behrens T, et al. Etanercept treatment in children with new-onset type 1 diabetes: pilot randomized, placebo-controlled, double-blind study. Diabetes Care 2009;32:1244-1249
28. Klempner MS, Styrt B. Alkalinizing the intralysosomal pH inhibits degranulation of human neutrophils. J Clin Invest 1983;72:1793-1800 (Pubitemid 14229059)
29. Zhang Y, Lee AS, Shameli A, et al. TLR9 blockade inhibits activation of diabetogenic CD8+ T cells and delays autoimmune diabetes. J Immunol 2010;184:5645-5653
30. Day EK, Carmichael AJ, ten Berge IJ, Waller EC, Sissons JG, Wills MR. Rapid CD8+ T cell repertoire focusing and selection of high-affinity clones into memory following primary infection with a persistent human virus: human cytomegalovirus. J Immunol 2007;179:3203-3213