HLA-E restricted CD8+ T cell subsets are phenotypically altered in multiple sclerosis patients

Multiple Sclerosis Journal

Volumn 20, Issue 7, 2014, Pages 790-801

  Pannemans, Kim ^a   Broux, Bieke ^a   Goris, An ^b   Dubois, Bénédicte ^b   Broekmans, Tom ^a,c   Van Wijmeersch, Bart ^a   Geraghty, Daniel ^d   Stinissen, Piet ^a   Hellings, Niels ^a  

^a HASSELT UNIVERSITY   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c PHL University College   (Belgium)

^d Fred Hutchinson Cancer Research Center   (United States)

Author keywords

Autoreactive T cells; Cytotoxic T cells; HLA E; Multiple sclerosis; Polymorphisms; Regulatory T cells

Indexed keywords

CD28 ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; GAMMA INTERFERON; HLA DRB1 ANTIGEN; HLA E ANTIGEN; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 27; INTERLEUKIN 4; TRANSCRIPTION FACTOR FOXP3; AUTACOID; CYTOKINE; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, HUMAN; HLA ANTIGEN CLASS 1; HLA-E ANTIGEN; KLRC2 PROTEIN, HUMAN; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY C;

ADULT; AGED; ANTIGEN EXPRESSION; ARTICLE; B LYMPHOCYTE; BRAIN DAMAGE; CD8+ T LYMPHOCYTE; CELL ACTIVATION; CELLS; CENTRAL NERVOUS SYSTEM; CEREBROSPINAL FLUID CYTOLOGY; COHORT ANALYSIS; COMPARATIVE STUDY; CONTROLLED STUDY; DISEASE PREDISPOSITION; EX VIVO STUDY; FEMALE; FLOW CYTOMETRY; GENE MUTATION; GENETIC POLYMORPHISM; GENOTYPE; HAPLOTYPE; HUMAN; HUMAN TISSUE; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATORY CELL; KINETICS; MAJOR CLINICAL STUDY; MALE; MULTIPLE SCLEROSIS; NKG2C POSITIVE CD8 POSITIVE T LYMPHOCYTE; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; PROTEIN EXPRESSION; REGULATORY MECHANISM; SURFACE PROPERTY; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; UPREGULATION; ALLELE; AUTOIMMUNITY; CELL ISOLATION; HUMAN CELL; CASE CONTROL STUDY; CELL CULTURE; GENETIC PREDISPOSITION; GENETICS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; MIDDLE AGED; REGULATORY T LYMPHOCYTE; YOUNG ADULT;

ADULT; AGED; CASE-CONTROL STUDIES; CD8-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM; CYTOKINES; FEMALE; FLOW CYTOMETRY; FORKHEAD TRANSCRIPTION FACTORS; GENETIC PREDISPOSITION TO DISEASE; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; IMMUNOHISTOCHEMISTRY; INFLAMMATION MEDIATORS; LYMPHOCYTE ACTIVATION; MALE; MIDDLE AGED; MULTIPLE SCLEROSIS; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY C; PHENOTYPE; POLYMORPHISM, GENETIC; T-LYMPHOCYTES, REGULATORY; YOUNG ADULT;

EID: 84902145624     PISSN: 13524585     EISSN: 14770970     Source Type: Journal    
DOI: 10.1177/1352458513509703     Document Type: Article

References (36)

1. Hellings N, Raus J and Stinissen P. Insights into the immunopathogenesis of multiple sclerosis. Immunol Res 2002; 25: 27-51 (Pubitemid 34155248)
2. Nylander A and Hafler DA. Multiple sclerosis. J Clin Invest 2012; 122: 1180-1188
3. Sawcer S, Hellenthal G, Pirinen M, et al. Genetic risk and a primary role for cell-mediated immune mechanisms in multiple sclerosis. Nature 2011; 476: 214-219
4. Broux B, Hellings N, Venken K, et al. Haplotype 4 of the multiple sclerosis-associated interleukin-7 receptor alpha gene influences the frequency of recent thymic emigrants. Genes Immun 2010; 11: 326-333
5. El Behi M, Rostami A and Ciric B. Current views on the roles of Th1 and Th17 cells in experimental autoimmune encephalomyelitis. J Neuroimmune Pharmacol 2010 Jun; 5(2): 189-197
6. Montes M, Zhang X, Berthelot L, et al. Oligoclonal myelin-reactive T-cell infiltrates derived from multiple sclerosis lesions are enriched in Th17 cells. Clin Immunol 2009; 130: 133-144
7. Viglietta V, Baecher-Allan C, Weiner HL, et al. Loss of functional suppression by CD4+CD25+ regulatory T cells in patients with multiple sclerosis. J Exp Med 2004; 199: 971-979 (Pubitemid 38481088)
8. Venken K, Hellings N, Hensen K, et al. Secondary progressive in contrast to relapsing-remitting multiple sclerosis patients show a normal CD4+CD25+ regulatory T-cell function and FOXP3 expression. J Neurosci Res 2006; 83: 1432-1446 (Pubitemid 43844989)
9. Abbas AK, Benoist C, Bluestone JA, et al. Regulatory T cells: Recommendations to simplify the nomenclature. Nat Immunol 2013; 14: 307-308
10. Pietra G, Romagnani C, Moretta L, et al. HLA-E and HLAE- bound peptides: Recognition by subsets of NK and T cells. Curr Pharm Des 2009; 15: 3336-3344
11. Zaguia F, Saikali P, Ludwin S, et al. Cytotoxic NKG2C+ CD4 T cells target oligodendrocytes in multiple sclerosis. J Immunol 2013; 190: 2510-2518
12. Lee N, Llano M, Carretero M, et al. HLA-E is a major ligand for the natural killer inhibitory receptor CD94/NKG2A. Proc Natl Acad Sci U S A 1998; 95: 5199-5204 (Pubitemid 28208575)
13. O'Callaghan CA. Natural killer cell surveillance of intracellular antigen processing pathways mediated by recognition of HLA-E and Qa-1b by CD94/NKG2 receptors. Microbes Infect 2000; 2: 371-380 (Pubitemid 30241039)
14. Chess L and Jiang H. Resurrecting CD8+ suppressor T cells. Nat Immunol 2004; 5: 469-471
15. Lu L, Werneck MB and Cantor H. The immunoregulatory effects of Qa-1. Immunol Rev 2006; 212: 51-59 (Pubitemid 44116699)
16. Hu D, Ikizawa K, Lu L, et al. Analysis of regulatory CD8 T cells in Qa-1-deficient mice. Nat Immunol 2004; 5: 516-523 (Pubitemid 38660464)
17. Strong RK, Holmes MA, Li P, et al. HLA-E allelic variants. Correlating differential expression, peptide affinities, crystal structures, and thermal stabilities. J Biol Chem 2003; 278: 5082-5090 (Pubitemid 36801018)
18. Matte C, Lacaille J, Zijenah L, et al. HLA-G and HLA-E polymorphisms in an indigenous African population. The ZVITAMBO Study Group. Hum Immunol 2000; 61: 1150-1156 (Pubitemid 32043893)
19. Goris A, Walton A, Ban M, et al. A Taqman assay for high-throughput genotyping of the multiple sclerosis-associated HLA-DRB1*1501 allele. Tissue Antigens 2008; 72: 401-403
20. Broux B, Pannemans K, Zhang X, et al. CX3CR1 drives cytotoxic CD4+CD28- T cells into the brain of multiple sclerosis patients. J Autoimmun 2012; 38: 10-19
21. Purcell S, Neale B, Todd-Brown K, et al. PLINK: A tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 2007; 81: 559-575 (Pubitemid 47330214)
22. Cassell D and Forman J. Two roles for CD4 cells in the control of the generation of cytotoxic T lymphocytes. J Immunol 1991; 146: 3-10
23. Koch S and Larbi A, Derhovanessian E, et al. Multiparameter flow cytometric analysis of CD4 and CD8 T cell subsets in young and old people. Immun Ageing 2008; 5: 5-6
24. Jiang H, Ware R, Stall A, et al. Murine CD8+ T cells that specifically delete autologous CD4+ T cells expressing V beta 8 TCR: A role of the Qa-1 molecule. Immunity 1995; 2: 185-194
25. Jiang H, Kashleva H, Xu LX, et al. T cell vaccination induces T cell receptor Vbeta-specific Qa-1-restricted regulatory CD8(+) T cells. Proc Natl Acad Sci U S A 1998; 95: 4533-457
26. Panoutsakopoulou V, Huster KM, McCarty N, et al. Suppression of autoimmune disease after vaccination with autoreactive T cells that express Qa-1 peptide complexes. J Clin Invest 2004; 113: 1218-1224 (Pubitemid 38544107)
27. Jagessar SA, Heijmans N, Blezer EL, et al. Unravelling the T-cell mediated autoimmune attack on CNS myelin in a new primate EAE model induced with MOG(34-56) peptide in incomplete adjuvant. Eur J Immunol 2012; Jan; 42(1): 217-227
28. Pietra G, Romagnani C, Mazzarino P, et al. HLA-E-restricted recognition of cytomegalovirus-derived peptides by human CD8+ cytolytic T lymphocytes. Proc Natl Acad Sci U S A 2003; 100: 10896-10901
29. Romagnani C, Pietra G, Falco M, et al. HLA-E-restricted recognition of human cytomegalovirus by a subset of cytolytic T lymphocytes. Hum Immunol 2004; 65: 437-445 (Pubitemid 38686768)
30. Jiang H, Canfield SM, Gallagher MP, et al. HLA-E-restricted regulatory CD8(+) T cells are involved in development and control of human autoimmune type 1 diabetes. J Clin Invest 2010; 120: 3641-3650
31. Morandi F, Venturi C, Rizzo R, et al. Intrathecal soluble HLA-E correlates with disease activity in patients with multiple sclerosis and may cooperate with soluble HLA-G in the resolution of neuroinflammation. J Neuroimmune Pharmacol 2013 Sep; 8(4): 944-955
32. Soper DM, Kasprowicz DJ and Ziegler SF. IL-2Rbeta links IL-2R signaling with Foxp3 expression. Eur J Immunol 2007; 37: 1817-1826 (Pubitemid 47071667)
33. Wood KJ and Sawitzki B. Interferon gamma: A crucial role in the function of induced regulatory T cells in vivo. Trends Immunol 2006; 27: 183-187
34. Hermans G, Denzer U, Lohse A, et al. Cellular and humoral immune responses against autoreactive T cells in multiple sclerosis patients after T cell vaccination. J Autoimmun 1999; 13: 233-246 (Pubitemid 29436138)
35. Correale J and Villa A. Isolation and characterization of CD8+ regulatory T cells in multiple sclerosis. J Neuroimmunol 2008; 195: 121-134
36. Yao Y, Han W, Liang J, et al. Glatiramer acetate ameliorates inflammatory bowel disease in mice through the induction of Qa-1-restricted CD8(+) regulatory cells. Eur J Immunol 2013; 43: 125-136.