Cytotoxic NKG2C+ CD4 T Cells target oligodendrocytes in multiple sclerosis

Journal of Immunology

Volumn 190, Issue 6, 2013, Pages 2510-2518

  Zaguia, Fatma ^a,b   Saikali, Philippe ^a,b,e   Ludwin, Samuel ^c   Newcombe, Jia ^d   Beauseigle, Diane ^a   McCrea, Ellie ^b   Duquette, Pierre ^a   Prat, Alexandre ^a   Antel, Jack P ^b   Arbour, Nathalie ^a  

^a NOTRE DAME HOSPITAL   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c QUEEN S UNIVERSITY   (Canada)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

^e CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD56 ANTIGEN; FAS LIGAND; GRANZYME B; HLA E ANTIGEN; LYMPHOCYTE RECEPTOR; MEMBRANE RECEPTOR; MYELIN; NATURAL KILLER CELL RECEPTOR NKG2C; NATURAL KILLER CELL RECEPTOR NKG2D; PERFORIN; PHYTOHEMAGGLUTININ; UNCLASSIFIED DRUG;

ADULT; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; EX VIVO STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MULTIPLE SCLEROSIS; NATURAL KILLER CELL; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE ACTIVATION; UPREGULATION;

ANTIGENS, CD56; CD4-POSITIVE T-LYMPHOCYTES; CELL LINE; CELL MOVEMENT; CYTOTOXICITY, IMMUNOLOGIC; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; INFLAMMATION; MULTIPLE SCLEROSIS; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY C; OLIGODENDROGLIA; UP-REGULATION;

EID: 84874826127     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1202725     Document Type: Article

References (41)

1. Sospedra, M., and R. Martin. 2005. Immunology of multiple sclerosis. Annu. Rev. Immunol. 23: 683-747
2. Höftberger, R., F. Aboul-Enein, W. Brueck, C. Lucchinetti, M. Rodriguez, M. Schmidbauer, K. Jellinger, and H. Lassmann. 2004. Expression of major histocompatibility complex class I molecules on the different cell types in multiple sclerosis lesions. Brain Pathol. 14: 43-50
3. Antel, J. P., E. McCrea, U. Ladiwala, Y. F. Qin, and B. Becher. 1998. Non-MHCrestricted cell-mediated lysis of human oligodendrocytes in vitro: relation with CD56 expression. J. Immunol. 160: 1606-1611
4. Vergelli, M., H. Le, J. M. van Noort, S. Dhib-Jalbut, H. McFarland, and R. Martin. 1996. A novel population of CD4+CD56+ myelin-reactive T cells lyses target cells expressing CD56/neural cell adhesion molecule. J. Immunol. 157: 679-688
5. Lanier, L. L. 2005. NK cell recognition. Annu. Rev. Immunol. 23: 225-274
6. Sáez-Borderías, A., N. Romo, G. Magri, M. Gumá, A. Angulo, and M. López-Botet. 2009. IL-12-dependent inducible expression of the CD94/NKG2A inhibitory receptor regulates CD94/NKG2C+ NK cell function. J. Immunol. 182: 829-836
7. van Bijnen, S. T., M. Withaar, F. Preijers, A. van der Meer, T. de Witte, P. Muus, and H. Dolstra. 2011. T cells expressing the activating NK-cell receptors KIR2DS4, NKG2C and NKG2D are elevated in paroxysmal nocturnal hemoglobinuria and cytotoxic toward hematopoietic progenitor cell lines. Exp. Hematol. 39: 751-762.e1-3
8. Gumá, M., A. Angulo, C. Vilches, N. Gómez-Lozano, N. Malats, and M. López-Botet. 2004. Imprint of human cytomegalovirus infection on the NK cell receptor repertoire. Blood 104: 3664-3671
9. Sáez-Borderías, A., N. Romo, F. Ruiz-Cabello, J. Cantón, D. Tielemans, A. W. Langerak, and M. López-Botet. 2011. Natural killer cell receptor expression reflects the role of human cytomegalovirus in the pathogenesis of a subset of CD4+ T-cell large granular lymphocytosis. Hum. Immunol. 72: 226- 228
10. Meresse, B., S. A. Curran, C. Ciszewski, G. Orbelyan, M. Setty, G. Bhagat, L. Lee, M. Tretiakova, C. Semrad, E. Kistner, et al. 2006. Reprogramming of CTLs into natural killer-like cells in celiac disease. J. Exp. Med. 203: 1343- 1355
11. Morel, E., S. Escamochero, R. Cabañas, R. Díaz, A. Fiandor, and T. Bellón. 2010. CD94/NKG2C is a killer effector molecule in patients with Stevens- Johnson syndrome and toxic epidermal necrolysis. J. Allergy Clin. Immunol. 125: 703-710, 710.e1-710.e8
12. McDonald, W. I., A. Compston, G. Edan, D. Goodkin, H. P. Hartung, F. D. Lublin, H. F. McFarland, D. W. Paty, C. H. Polman, S. C. Reingold, et al. 2001. Recommended diagnostic criteria for multiple sclerosis: guidelines from the International Panel on the diagnosis of multiple sclerosis. Ann. Neurol. 50: 121-127
13. Arbour, N., R. Lapointe, P. Saikali, E. McCrea, T. Regen, and J. P. Antel. 2006. A new clinically relevant approach to expand myelin specific T cells. J. Immunol. Methods 310: 53-61
14. D'Souza, S., K. Alinauskas, E. McCrea, C. Goodyer, and J. P. Antel. 1995. Differential susceptibility of human CNS-derived cell populations to TNFdependent and independent immune-mediated injury. J. Neurosci. 15: 7293- 7300
15. D'Souza, S. D., B. Bonetti, V. Balasingam, N. R. Cashman, P. A. Barker, A. B. Troutt, C. S. Raine, and J. P. Antel. 1996. Multiple sclerosis: Fas signaling in oligodendrocyte cell death. J. Exp. Med. 184: 2361-2370
16. Wosik, K., F. Ruffini, G. Almazan, A. Olivier, J. Nalbantoglu, and J. P. Antel. 2004. Resistance of human adult oligodendrocytes to AMPA/kainate receptormediated glutamate injury. Brain 127: 2636-2648
17. Saikali, P., J. P. Antel, C. L. Pittet, J. Newcombe, and N. Arbour. 2010. Contribution of astrocyte-derived IL-15 to CD8 T cell effector functions in multiple sclerosis. J. Immunol. 185: 5693-5703
18. Pittet, C. L., J. Newcombe, J. P. Antel, and N. Arbour. 2011. The majority of infiltrating CD8 T lymphocytes in multiple sclerosis lesions is insensitive to enhanced PD-L1 levels on CNS cells. Glia 59: 841-856
19. Saikali, P., J. P. Antel, J. Newcombe, Z. Chen, M. Freedman, M. Blain, R. Cayrol, A. Prat, J. A. Hall, and N. Arbour. 2007. NKG2D-mediated cytotoxicity toward oligodendrocytes suggests a mechanism for tissue injury in multiple sclerosis. J. Neurosci. 27: 1220-1228
20. Basu, A., J. K. Krady, and S. W. Levison. 2004. Interleukin-1: a master regulator of neuroinflammation. J. Neurosci. Res. 78: 151-156
21. Owens, T. 2002. Identification of new therapeutic targets for prevention of CNS inflammation. Expert Opin. Ther. Targets 6: 203-215
22. Vincent, T., P. Saikali, R. Cayrol, A. D. Roth, A. Bar-Or, A. Prat, and J. P. Antel. 2008. Functional consequences of neuromyelitis optica-IgG astrocyte interactions on blood-brain barrier permeability and granulocyte recruitment. J. Immunol. 181: 5730-5737
23. Wischhusen, J., M. A. Friese, M. Mittelbronn, R. Meyermann, and M. Weller. 2005. HLA-E protects glioma cells from NKG2D-mediated immune responses in vitro: implications for immune escape in vivo. J. Neuropathol. Exp. Neurol. 64: 523-528
24. Durrenberger, P. F., L. V. Webb, M. J. Sim, R. S. Nicholas, D. M. Altmann, and R. J. Boyton. 2012. Increased HLA-E expression in white matter lesions in multiple sclerosis. Immunology 137: 317-325
25. Stromnes, I. M., L. M. Cerretti, D. Liggitt, R. A. Harris, and J. M. Goverman. 2008. Differential regulation of central nervous system autoimmunity by T(H)1 and T(H)17 cells. Nat. Med. 14: 337-342
26. Stadelmann, C., C. Wegner, and W. Brück. 2011. Inflammation, demyelination, and degeneration - recent insights from MS pathology. Biochim. Biophys. Acta 1812: 275-282
27. Grenier, Y., T. C. Ruijs, Y. Robitaille, A. Olivier, and J. P. Antel. 1989. Immunohistochemical studies of adult human glial cells. J. Neuroimmunol. 21: 103- 115
28. Lee, S. C., and C. S. Raine. 1989. Multiple sclerosis: oligodendrocytes in active lesions do not express class II major histocompatibility complex molecules. J. Neuroimmunol. 25: 261-266
29. Antel, J. P., K. Williams, M. Blain, E. McRea, and J. McLaurin. 1994. Oligodendrocyte lysis by CD4+ T cells independent of tumor necrosis factor. Ann. Neurol. 35: 341-348
30. Gumá, M., L. K. Busch, L. I. Salazar-Fontana, B. Bellosillo, C. Morte, P. García, and M. López-Botet. 2005. The CD94/NKG2C killer lectin-like receptor constitutes an alternative activation pathway for a subset of CD8+ T cells. Eur. J. Immunol. 35: 2071-2080
31. Romo, N., M. Fitó, M. Gumá, J. Sala, C. García, R. Ramos, A. Muntasell, R. Masiá, J. Bruguera, I. Subirana, et al. 2011. Association of atherosclerosis with expression of the LILRB1 receptor by human NK and T-cells supports the infectious burden hypothesis. Arterioscler. Thromb. Vasc. Biol. 31: 2314-2321
32. Martínez-Rodríguez, J. E., M. López-Botet, E. Munteis, J. Rio, J. Roquer, X. Montalban, and M. Comabella. 2011. Natural killer cell phenotype and clinical response to interferon-beta therapy in multiple sclerosis. Clin. Immunol. 141: 348-356
33. Correale, J., and A. Villa. 2008. Isolation and characterization of CD8+ regulatory T cells in multiple sclerosis. J. Neuroimmunol. 195: 121-134
34. Lu, L., H. J. Kim, M. B. Werneck, and H. Cantor. 2008. Regulation of CD8+ regulatory T cells: Interruption of the NKG2A-Qa-1 interaction allows robust suppressive activity and resolution of autoimmune disease. Proc. Natl. Acad. Sci. USA 105: 19420-19425
35. Vergelli, M., B. Hemmer, P. A. Muraro, L. Tranquill, W. E. Biddison, A. Sarin, H. F. McFarland, and R. Martin. 1997. Human autoreactive CD4+ T cell clones use perforin- or Fas/Fas ligand-mediated pathways for target cell lysis. J. Immunol. 158: 2756-2761
36. Allez, M., V. Tieng, A. Nakazawa, X. Treton, V. Pacault, N. Dulphy, S. Caillat- Zucman, P. Paul, J.-M. Gornet, C. Douay, et al. 2007. CD4+NKG2D+ T cells in Crohn's disease mediate inflammatory and cytotoxic responses through MICA interactions. Gastroenterology 132: 2346-2358
37. Groh, V., A. Bruhl, H. El-Gabalawy, J. L. Nelson, and T. Spies. 2003. Stimulation of T cell autoreactivity by anomalous expression of NKG2D and its MIC ligands in rheumatoid arthritis. Proc. Natl. Acad. Sci. USA 100: 9452-9457
38. Durrenberger, P. F., A. Ettorre, F. Kamel, L. V. Webb, M. Sim, R. S. Nicholas, O. Malik, R. Reynolds, R. J. Boyton, and D. M. Altmann. 2012. Innate immunity in multiple sclerosis white matter lesions: expression of natural cytotoxicity triggering receptor 1 (NCR1). J. Neuroinflammation 9: 1
39. Suvas, S., A. K. Azkur, and B. T. Rouse. 2006. Qa-1b and CD94-NKG2a interaction regulate cytolytic activity of herpes simplex virus-specific memory CD8+ T cells in the latently infected trigeminal ganglia. J. Immunol. 176: 1703-1711
40. King, A., D. S. Allan, M. Bowen, S. J. Powis, S. Joseph, S. Verma, S. E. Hiby, A. J. McMichael, Y. W. Loke, and V. M. Braud. 2000. HLA-E is expressed on trophoblast and interacts with CD94/NKG2 receptors on decidual NK cells. Eur. J. Immunol. 30: 1623-1631
41. Kappos, L., D. Bates, G. Edan, M. Eraksoy, A. Garcia-Merino, N. Grigoriadis, H. P. Hartung, E. Havrdová, J. Hillert, R. Hohlfeld, et al. 2011. Natalizumab treatment for multiple sclerosis: updated recommendations for patient selection and monitoring. Lancet Neurol. 10: 745-758