Single insulin-specific CD8 + T cells show characteristic gene expression profiles in human type 1 diabetes

Diabetes

Volumn 60, Issue 12, 2011, Pages 3289-3299

  Luce, Sandrine ^a,b   Lemonnier, François ^a,b   Briand, Jean Paul ^c   Coste, Joel ^d   Lahlou, Najiba ^c,d   Muller, Sylviane ^c   Larger, Etienne ^b,d   Rocha, Benedita ^b   Mallone, Roberto ^a,b   Boitard, Christian ^a,b,d  

^a INSERM   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c INSTITUT DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^d Hôpital Cochin ^*  (France)

Author keywords

[No Author keywords available]

Indexed keywords

HLA A1 ANTIGEN; INSULIN; INTERLEUKIN 10; PREPROINSULIN;

ADULT; ARTICLE; BETA CHAIN; CD8+ T LYMPHOCYTE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOMEGALOVIRUS; DISEASE DURATION; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; HUMAN; INSULIN DEPENDENT DIABETES MELLITUS; MALE; MEMBRANE MARKER; MEMORY T LYMPHOCYTE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL;

ADULT; CD8-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; DIABETES MELLITUS, TYPE 1; FEMALE; GENE EXPRESSION PROFILING; HUMANS; INSULIN; MALE; MIDDLE AGED; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 82255183367     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db11-0270     Document Type: Article

References (45)

1. Faideau B, Larger E, Lepault F, Carel JC, Boitard C. Role of beta-cells in type 1 diabetes pathogenesis. Diabetes 2005;54(Suppl. 2):S87-S96 (Pubitemid 43343336)
2. Itoh N, Hanafusa T, Miyazaki A, et al. 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;92:2313-2322 (Pubitemid 23333537)
3. Somoza N, Vargas F, Roura-Mir C, et al. Pancreas in recent onset insulin-dependent diabetes mellitus. Changes in HLA, adhesion molecules and autoantigens, restricted T cell receptor V beta usage, and cytokine profile. J Immunol 1994;153:1360-1377 (Pubitemid 24228529)
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. Conrad B, Weidmann E, Trucco G, et al. Evidence for superantigen involvement in insulin-dependent diabetes mellitus aetiology. Nature 1994;371:351-355 (Pubitemid 24300620)
6. Martin S, Wolf-Eichbaum D, Duinkerken G, et al. Development of type 1 diabetes despite severe hereditary B-lymphocyte deficiency. N Engl J Med 2001;345:1036-1040
7. Sibley RK, Sutherland DE, Goetz F, Michael AF. Recurrent diabetes mellitus in the pancreas iso- and allograft. A light and electron microscopic and immunohistochemical analysis of four cases. Lab Invest 1985;53:132-144 (Pubitemid 15049005)
8. Thébault-Baumont K, Dubois-Laforgue D, Krief P, et al. Acceleration of type 1 diabetes mellitus in proinsulin 2-deficient NOD mice. J Clin Invest 2003;111:851-857 (Pubitemid 37074960)
9. Moriyama H, Abiru N, Paronen J, et al. Evidence for a primary islet autoantigen (preproinsulin 1) for insulitis and diabetes in the nonobese diabetic mouse. Proc Natl Acad Sci USA 2003;100:10376-10381 (Pubitemid 37071886)
10. Nakayama M, Abiru N, Moriyama H, et al. Prime role for an insulin epitope in the development of type 1 diabetes in NOD mice. Nature 2005; 435:220-223 (Pubitemid 40685949)
11. Ziegler AG, Hummel M, Schenker M, Bonifacio E. Autoantibody appearance and risk for development of childhood diabetes in offspring of parents with type 1 diabetes: the 2-year analysis of the German BABYDIAB Study. Diabetes 1999;48:460-468 (Pubitemid 29106857)
12. Toma A, Haddouk S, Briand JP, et al. Recognition of a subregion of human proinsulin by class I-restricted T cells in type 1 diabetic patients. Proc Natl Acad Sci USA 2005;102:10581-10586 (Pubitemid 41061597)
13. Toma A, Laïka T, Haddouk S, 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
14. Mallone R, Martinuzzi E, Blancou P, et al. CD8+ T-cell responses identify beta-cell autoimmunity in human type 1 diabetes. Diabetes 2007;56:613-621 (Pubitemid 46348452)
15. 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;57:1312-1320
16. Blancou P, Mallone R, Martinuzzi E, et al. Immunization of HLA class I transgenic mice identifies autoantigenic epitopes eliciting dominant responses in type 1 diabetes patients. J Immunol 2007;178:7458-7466 (Pubitemid 46847474)
17. 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 glucoseregulated preproinsulin epitope. J Clin Invest 2008;118:3390-3402
18. 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;102:18425-18430 (Pubitemid 43011242)
19. 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
20. 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
21. Gannagé M, Abel M, Michallet AS, et al. Ex vivo characterization of multi-epitopic tumor-specific CD8 T cells in patients with chronic myeloid leukemia: implications for vaccine development and adoptive cellular immunotherapy. J Immunol 2005;174:8210-8218 (Pubitemid 40806333)
22. Passoni L, Scardino A, Bertazzoli C, et al. ALK as a novel lymphoma-associated tumor antigen: identification of 2 HLA-A2.1-restricted CD8+ T-cell epitopes. Blood 2002;99:2100-2106 (Pubitemid 34525494)
23. Garboczi DN, Utz U, Ghosh P, et al. Assembly, specific binding, and crystallization of a human TCR-alphabeta with an antigenic Tax peptide from human T lymphotropic virus type 1 and the class I MHC molecule HLA-A2. J Immunol 1996;157:5403-5410 (Pubitemid 126448959)
24. Altman JD, Moss PA, Goulder PJ, et al. Phenotypic analysis of antigen-specific T lymphocytes. Science 1996;274:94-96 (Pubitemid 26332731)
25. Romero P, Zippelius A, Kurth I, et al. Four functionally distinct populations of human effector-memory CD8+ T lymphocytes. J Immunol 2007;178:4112-4119 (Pubitemid 46492360)
26. Monteiro M, Evaristo C, Legrand A, Nicoletti A, Rocha B. Cartography of gene expression in CD8 single cells: novel CCR7- subsets suggest differentiation independent of CD45RA expression. Blood 2007;109:2863-2870 (Pubitemid 46482082)
27. Peixoto A, Monteiro M, Rocha B, Veiga-Fernandes H. Quantification of multiple gene expression in individual cells. Genome Res 2004;14:1938-1947 (Pubitemid 39386508)
28. Peixoto A, Evaristo C, Munitic I, et al. CD8 single-cell gene coexpression reveals three different effector types present at distinct phases of the immune response. J Exp Med 2007;204:1193-1205 (Pubitemid 46798161)
29. Bland JM, Altman DG. Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1986;1:307-310 (Pubitemid 16134762)
30. 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
31. Appay V, Dunbar PR, Callan M, et al. Memory CD8+ T cells vary in differentiation phenotype in different persistent virus infections. Nat Med 2002;8: 379-385 (Pubitemid 34407033)
32. Jameson SC, Masopust D. Diversity in T cell memory: an embarrassment of riches. Immunity 2009;31:859-871
33. Weninger W, Manjunath N, von Andrian UH. Migration and differentiation of CD8+ T cells. Immunol Rev 2002;186:221-233
34. Ibegbu CC, Xu YX, Harris W, Maggio D, Miller JD, Kourtis AP. Expression of killer cell lectin-like receptor G1 on antigen-specific human CD8+ T lymphocytes during active, latent, and resolved infection and its relation with CD57. J Immunol 2005;174:6088-6094 (Pubitemid 40663797)
35. Rother KI, Harlan DM. Challenges facing islet transplantation for the treatment of type 1 diabetes mellitus. J Clin Invest 2004;114:877-883 (Pubitemid 39578711)
36. Liu EH, Digon BJ 3rd, Hirshberg B, et al. Pancreatic beta cell function persists in many patients with chronic type 1 diabetes, but is not dramatically improved by prolonged immunosuppression and euglycaemia from a beta cell allograft. Diabetologia 2009;52:1369-1380
37. Peakman M, Mahalingam M, Leslie RD, Vergani D. Co-expression of CD45RA (naive) and CD45R0 (memory) T-cell markers. Lancet 1994;343:424 (Pubitemid 24049578)
38. Cernea S, Herold KC. Monitoring of antigen-specific CD8 T cells in patients with type 1 diabetes treated with antiCD3 monoclonal antibodies. Clin Immunol 2010;134:121-129
39. 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;113:451-463 (Pubitemid 38544189)
40. Cui W, Kaech SM. Generation of effector CD8+ T cells and their conversion to memory T cells. Immunol Rev 2010;236:151-166
41. Champagne P, Dumont AR, Sékaly RP. Learning to remember: generation and maintenance of T-cell memory. DNA Cell Biol 2001;20:745-760
42. Gianani R, Campbell-Thompson M, Sarkar SA, et al. Dimorphic histopathology of long-standing childhood-onset diabetes. Diabetologia 2010;53: 690-698
43. Keenan HA, Sun JK, Levine J, et al. Residual insulin production and pancreatic β-cell turnover after 50 years of diabetes: Joslin Medalist Study. Diabetes 2010;59:2846-2853
44. Sherry NA, Kushner JA, Glandt M, Kitamura T, Brillantes AM, Herold KC. Effects of autoimmunity and immune therapy on beta-cell turnover in type 1 diabetes. Diabetes 2006;55:3238-3245 (Pubitemid 44923579)
45. Gras S, Saulquin X, Reiser JB, et al. Structural bases for the affinity-driven selection of a public TCR against a dominant human cytomegalovirus epitope. J Immunol 2009;183:430-437