Neuropathologic, phenotypic and functional analyses of Mucosal Associated Invariant T cells in Multiple Sclerosis

Clinical Immunology

Volumn 166-167, Issue , 2016, Pages 1-11

  Salou, Marion ^a,b   Nicol, Bryan ^a,b   Garcia, Alexandra ^a,c   Baron, Daniel ^a,b,c   Michel, Laure ^a,d   Elong Ngono, Annie ^a,b   Hulin, Philippe ^e   Nedellec, Steven ^e   Jacq Foucher, Marylène ^f   Le Frère, Fabienne ^f   Jousset, Natacha ^f   Bourreille, Arnaud ^f   Wiertlewski, Sandrine ^d,f   Soulillou, Jean Paul ^a   Brouard, Sophie ^a,c   Nicot, Arnaud B ^a,b,c   Degauque, Nicolas ^a,c   Laplaud, David Axel ^a,d,f  

^a Centre National de la Recherche Scientifique   (France)

^b UNIVERSITÉ DE NANTES   (France)

^c Department of Nephrology Transplantation   (France)

^d Nantes Hospital   (France)

^e Recombinant Protein Production Facility Federative Research Structure François Bonamy   (France)

^f INSERM   (France)

Author keywords

Central nervous system; Mucosal associated T cells; Multiple sclerosis; Neuroinflammation

Indexed keywords

IMMUNOMODULATING AGENT; IMMUNOSUPPRESSIVE AGENT; INTERLEUKIN 12; INTERLEUKIN 18; INTERLEUKIN 23; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; P SELECTIN GLYCOPROTEIN LIGAND 1; T LYMPHOCYTE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA INHIBITOR; HLA ANTIGEN CLASS 1; INTERLEUKIN 18 PROTEIN, HUMAN; LYMPHOCYTE ANTIGEN RECEPTOR; MINOR HISTOCOMPATIBILITY ANTIGEN; MR1 PROTEIN, HUMAN;

ADULT; AGED; ARTICLE; BLOOD BRAIN BARRIER; CENTRAL NERVOUS SYSTEM; COHORT ANALYSIS; FEMALE; FLOW CYTOMETRY; HUMAN; IMMUNOFLUORESCENCE TEST; IN VITRO STUDY; MAJOR CLINICAL STUDY; MALE; MICROENVIRONMENT; MUCOSAL ASSOCIATED INVARIANT T CELL; MULTIPLE SCLEROSIS; NEUROPATHOLOGY; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; T LYMPHOCYTE; VERY ELDERLY; BIOLOGICAL MODEL; BRAIN; CASE CONTROL STUDY; CELL MOTION; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; IMMUNOPHENOTYPING; METABOLISM; MIDDLE AGED; MUCOSAL IMMUNITY; MUCOSAL-ASSOCIATED INVARIANT T CELL; PATHOLOGY; VASCULARIZATION;

ADULT; BLOOD-BRAIN BARRIER; BRAIN; CASE-CONTROL STUDIES; CELL MOVEMENT; FEMALE; GENE EXPRESSION REGULATION; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; IMMUNITY, MUCOSAL; IMMUNOPHENOTYPING; INTERLEUKIN-18; INTERLEUKIN-23; MALE; MIDDLE AGED; MINOR HISTOCOMPATIBILITY ANTIGENS; MODELS, BIOLOGICAL; MUCOSAL-ASSOCIATED INVARIANT T CELLS; MULTIPLE SCLEROSIS, CHRONIC PROGRESSIVE; MULTIPLE SCLEROSIS, RELAPSING-REMITTING; RECEPTORS, ANTIGEN, T-CELL;

EID: 84963579542     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2016.03.014     Document Type: Article

References (56)

1. Babbe H., Roers A., Waisman A., Lassmann H., Goebels N., Hohlfeld R., Friese M., Schröder R., Deckert M., Schmidt S., et al. Clonal expansions of CD8(+) T cells dominate the T cell infiltrate in active multiple sclerosis lesions as shown by micromanipulation and single cell polymerase chain reaction. J. Exp. Med. 2000, 192:393-404.
2. Booss J., Esiri M.M., Tourtellotte W.W., Mason D.Y. Immunohistological analysis of T lymphocyte subsets in the central nervous system in chronic progressive multiple sclerosis. J. Neurol. Sci. 1983, 62:219-232.
3. Salou M., Garcia A., Michel L., Gainche-Salmon A., Loussouarn D., Nicol B., Guillot F., Hulin P., Nedellec S., Baron D., et al. Expanded CD8 T-cell sharing between periphery and CNS in multiple sclerosis. Ann. Clin. Transl. Neurol. 2015, 2:609-622.
4. Junker A., Ivanidze J., Malotka J., Eiglmeier I., Lassmann H., Wekerle H., Meinl E., Hohlfeld R., Dornmair K. Multiple sclerosis: T-cell receptor expression in distinct brain regions. Brain J. Neurol. 2007, 130:2789-2799.
5. Montes M., Zhang X., Berthelot L., Laplaud D.-A., Brouard S., Jin J., Rogan S., Armao D., Jewells V., Soulillou J.-P., et al. Oligoclonal myelin-reactive T-cell infiltrates derived from multiple sclerosis lesions are enriched in Th17 cells. Clin. Immunol. 2009, 130:133-144. 10.1016/j.clim.2008.08.030.
6. Jilek S., Schluep M., Rossetti A.O., Guignard L., Le Goff G., Pantaleo G., Du Pasquier R.A. CSF enrichment of highly differentiated CD8+ T cells in early multiple sclerosis. Clin. Immunol. 2007, 123:105-113.
7. Tzartos J.S., Friese M.A., Craner M.J., Palace J., Newcombe J., Esiri M.M., Fugger L. Interleukin-17 production in central nervous system-infiltrating T cells and glial cells is associated with active disease in multiple sclerosis. Am. J. Pathol. 2008, 172:146-155. 10.2353/ajpath.2008.070690.
8. Maggi L., Santarlasci V., Capone M., Peired A., Frosali F., Crome S.Q., Querci V., Fambrini M., Liotta F., Levings M.K., et al. CD161 is a marker of all human IL-17-producing T-cell subsets and is induced by RORC. Eur. J. Immunol. 2010, 40:2174-2181. 10.1002/eji.200940257.
9. Martin E., Treiner E., Duban L., Guerri L., Laude H., Toly C., Premel V., Devys A., Moura I.C., Tilloy F., et al. Stepwise development of MAIT cells in mouse and human. PLoS Biol. 2009, 7:e54. 10.1371/journal.pbio.1000054.
10. Walker L.J., Kang Y.-H., Smith M.O., Tharmalingham H., Ramamurthy N., Fleming V.M., Sahgal N., Leslie A., Oo Y., Geremia A., et al. Human MAIT and CD8 cells develop from a pool of type-17 precommitted CD8+ T cells. Blood 2012, 119:422-433. 10.1182/blood-2011-05-353789.
11. Dusseaux M., Martin E., Serriari N., Péguillet I., Premel V., Louis D., Milder M., Le Bourhis L., Soudais C., Treiner E., et al. Human MAIT cells are xenobiotic-resistant, tissue-targeted, CD161hi IL-17-secreting T cells. Blood 2011, 117:1250-1259. 10.1182/blood-2010-08-303339.
12. Patel O., Kjer-Nielsen L., Le Nours J., Eckle S.B.G., Birkinshaw R., Beddoe T., Corbett A.J., Liu L., Miles J.J., Meehan B., et al. Recognition of vitamin B metabolites by mucosal-associated invariant T cells. Nat. Commun. 2013, 4:2142. 10.1038/ncomms3142.
13. Reantragoon R., Corbett A.J., Sakala I.G., Gherardin N.A., Furness J.B., Chen Z., Eckle S.B.G., Uldrich A.P., Birkinshaw R.W., Patel O., et al. Antigen-loaded MR1 tetramers define T cell receptor heterogeneity in mucosal-associated invariant T cells. J. Exp. Med. 2013, 210:2305-2320. 10.1084/jem.20130958.
14. Treiner E., Duban L., Bahram S., Radosavljevic M., Wanner V., Tilloy F., Affaticati P., Gilfillan S., Lantz O. Selection of evolutionarily conserved mucosal-associated invariant T cells by MR1. Nature 2003, 422:164-169. 10.1038/nature01433.
15. Corbett A.J., Eckle S.B.G., Birkinshaw R.W., Liu L., Patel O., Mahony J., Chen Z., Reantragoon R., Meehan B., Cao H., et al. T-cell activation by transitory neo-antigens derived from distinct microbial pathways. Nature 2014, 509:361-365. 10.1038/nature13160.
16. Kjer-Nielsen L., Patel O., Corbett A.J., Le Nours J., Meehan B., Liu L., Bhati M., Chen Z., Kostenko L., Reantragoon R., et al. MR1 presents microbial vitamin B metabolites to MAIT cells. Nature 2012, 10.1038/nature11605.
17. Le Bourhis L., Martin E., Péguillet I., Guihot A., Froux N., Coré M., Lévy E., Dusseaux M., Meyssonnier V., Premel V., et al. Antimicrobial activity of mucosal-associated invariant T cells. Nat. Immunol. 2010, 11:701-708. 10.1038/ni.1890.
18. Chua W.-J., Truscott S.M., Eickhoff C.S., Blazevic A., Hoft D.F., Hansen T.H. Polyclonal mucosa-associated invariant T cells have unique innate functions in bacterial infection. Infect. Immun. 2012, 80:3256-3267. 10.1128/IAI.00279-12.
19. Gold M.C., Cerri S., Smyk-Pearson S., Cansler M.E., Vogt T.M., Delepine J., Winata E., Swarbrick G.M., Chua W.-J., Yu Y.Y.L., et al. Human mucosal associated invariant T cells detect bacterially infected cells. PLoS Biol. 2010, 8:e1000407. 10.1371/journal.pbio.1000407.
20. Meierovics A., Yankelevich W.-J.C., Cowley S.C. MAIT cells are critical for optimal mucosal immune responses during in vivo pulmonary bacterial infection. Proc. Natl. Acad. Sci. U. S. A. 2013, 10.1073/pnas.1302799110.
21. Salerno-Goncalves R., Rezwan T., Sztein M.B. B cells modulate mucosal associated invariant T cell immune responses. Front. Immunol. 2014, 4. 10.3389/fimmu.2013.00511.
22. Lepore M., Kalinicenko A., Colone A., Paleja B., Singhal A., Tschumi A., Lee B., Poidinger M., Zolezzi F., Quagliata L., et al. Parallel T-cell cloning and deep sequencing of human MAIT cells reveal stable oligoclonal TCRβ repertoire. Nat. Commun. 2014, 5. 10.1038/ncomms4866.
23. Le Bourhis L., Dusseaux M., Bohineust A., Bessoles S., Martin E., Premel V., Coré M., Sleurs D., Serriari N.-E., Treiner E., et al. MAIT cells detect and efficiently lyse bacterially-infected epithelial cells. PLoS Pathog. 2013, 9:e1003681. 10.1371/journal.ppat.1003681.
24. Kurioka A., Ussher J.E., Cosgrove C., Clough C., Fergusson J.R., Smith K., Kang Y.-H., Walker L.J., Hansen T.H., Willberg C.B., et al. MAIT cells are licensed through granzyme exchange to kill bacterially sensitized targets. Mucosal Immunol. 2015, 8:429-440. 10.1038/mi.2014.81.
25. Abrahamsson S.V., Angelini D.F., Dubinsky A.N., Morel E., Oh U., Jones J.L., Carassiti D., Reynolds R., Salvetti M., Calabresi P.A., et al. Non-myeloablative autologous haematopoietic stem cell transplantation expands regulatory cells and depletes IL-17 producing mucosal-associated invariant T cells in multiple sclerosis. Brain J. Neurol. 2013, 136:2888-2903.
26. Illés Z., Shimamura M., Newcombe J., Oka N., Yamamura T. Accumulation of Valpha7.2-Jalpha33 invariant T cells in human autoimmune inflammatory lesions in the nervous system. Int. Immunol. 2004, 16:223-230.
27. + MAIT cells infiltrate into the CNS and alterations in their blood frequencies correlate with IL-18 serum levels in multiple sclerosis. Eur. J. Immunol. 2014, 44:3119-3128. 10.1002/eji.201344160.
28. Annibali V., Ristori G., Angelini D.F., Serafini B., Mechelli R., Cannoni S., Romano S., Paolillo A., Abderrahim H., Diamantini A., et al. CD161(high)CD8+ T cells bear pathogenetic potential in multiple sclerosis. Brain J. Neurol. 2011, 134:542-554. 10.1093/brain/awq354.
29. Miyazaki Y., Miyake S., Chiba A., Lantz O., Yamamura T. Mucosal-associated invariant T cells regulate Th1 response in multiple sclerosis. Int. Immunol. 2011, 23:529-535. 10.1093/intimm/dxr047.
30. McDonald W.I., Compston A., Edan G., Goodkin D., Hartung H.P., Lublin F.D., McFarland H.F., Paty D.W., Polman C.H., Reingold S.C., et al. Recommended diagnostic criteria for multiple sclerosis: guidelines from the International Panel on the Diagnosis of Multiple Sclerosis. Ann. Neurol. 2001, 50:121-127.
31. Polman C.H., Reingold S.C., Edan G., Filippi M., Hartung H.-P., Kappos L., Lublin F.D., Metz L.M., McFarland H.F., O'Connor P.W., et al. Diagnostic criteria for multiple sclerosis: 2005 revisions to the "McDonald criteria". Ann. Neurol. 2005, 58:840-846. 10.1002/ana.20703.
32. Weksler B.B. Blood-brain barrier-specific properties of a human adult brain endothelial cell line. FASEB J. 2005, 10.1096/fj.04-3458fje.
33. Prat A., Biernacki K., Lavoie J.-F., Poirier J., Duquette P., Antel J.P. Migration of multiple sclerosis lymphocytes through brain endothelium. Arch. Neurol. 2002, 59:391.
34. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods San Diego Calif. 2001, 25:402-408. 10.1006/meth.2001.1262.
35. Berthelot L., Laplaud D.-A., Pettré S., Ballet C., Michel L., Hillion S., Braudeau C., Connan F., Lefrère F., Wiertlewski S., et al. Blood CD8+ T cell responses against myelin determinants in multiple sclerosis and healthy individuals. Eur. J. Immunol. 2008, 38:1889-1899. 10.1002/eji.200838023.
36. Lee O.-J., Cho Y.-N., Kee S.-J., Kim M.-J., Jin H.-M., Lee S.-J., Park K.-J., Kim T.-J., Lee S.-S., Kwon Y.-S., et al. Circulating mucosal-associated invariant T cell levels and their cytokine levels in healthy adults. Exp. Gerontol. 2014, 49:47-54. 10.1016/j.exger.2013.11.003.
37. Novak J., Dobrovolny J., Novakova L., Kozak T. The decrease in number and change in phenotype of mucosal-associated invariant T cells in the elderly and differences in males and females of reproductive age. Scand. J. Immunol. 2014, (n/a-n/a). 10.1111/sji.12193.
38. Chattopadhyay P.K., Betts M.R., Price D.A., Gostick E., Horton H., Roederer M., Rosa S.C.D. 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. 10.1189/jlb.0208107.
39. Chen L., Flies D.B. Molecular mechanisms of T cell co-stimulation and co-inhibition. Nat. Rev. Immunol. 2013, 13:227-242. 10.1038/nri3405.
40. De Jager P.L., Baecher-Allan C., Maier L.M., Arthur A.T., Ottoboni L., Barcellos L., McCauley J.L., Sawcer S., Goris A., Saarela J., et al. The role of the CD58 locus in multiple sclerosis. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:5264-5269. 10.1073/pnas.0813310106.
41. Engelhardt B., Ransohoff R.M. Capture, crawl, cross: the T cell code to breach the blood-brain barriers. Trends Immunol. 2012, 33:579-589. 10.1016/j.it.2012.07.004.
42. Serriari N.-E., Eoche M., Lamotte L., Fumery M., Marcelo P., Chatelain D., Barre A., Nguyen-Khac E., Lantz O., Dupas J.-L., et al. Innate Mucosal-associated Invariant T (MAIT) cells are activated in inflammatory bowel diseases. Clin. Exp. Immunol. 2014, 10.1111/cei.12277.
43. Havenith S.H.C., Yong S.L., Henson S.M., Piet B., Idu M.M., Koch S.D., Jonkers R.E., Kragten N.A.M., Akbar A.N., van Lier R.A.W., et al. Analysis of stem-cell-like properties of human CD161++IL-18Rα+ memory CD8+ T cells. Int. Immunol. 2012, 24:625-636. 10.1093/intimm/dxs069.
44. + semi-invariant T cells. Blood 2011, 118:2752-2762. 10.1182/blood-2011-02-334698.
45. Losy J., Niezgoda A. IL-18 in patients with multiple sclerosis. Acta Neurol. Scand. 2001, 104:171-173.
46. Nicoletti F., Di Marco R., Mangano K., Patti F., Reggio E., Nicoletti A., Bendtzen K., Reggio A. Increased serum levels of interleukin-18 in patients with multiple sclerosis. Neurology 2001, 57:342-344.
47. Balashov K.E., Rottman J.B., Weiner H.L., Hancock W.W. CCR5(+) and CXCR3(+) T cells are increased in multiple sclerosis and their ligands MIP-1alpha and IP-10 are expressed in demyelinating brain lesions. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:6873-6878.
48. Windhagen A., Newcombe J., Dangond F., Strand C., Woodroofe M.N., Cuzner M.L., Hafler D.A. Expression of costimulatory molecules B7-1 (CD80), B7-2 (CD86), and interleukin 12 cytokine in multiple sclerosis lesions. J. Exp. Med. 1995, 182:1985-1996.
49. Battistini L., Piccio L., Rossi B., Bach S., Galgani S., Gasperini C., Ottoboni L., Ciabini D., Caramia M.D., Bernardi G., et al. CD8+ T cells from patients with acute multiple sclerosis display selective increase of adhesiveness in brain venules: a critical role for P-selectin glycoprotein ligand-1. Blood 2003, 101:4775-4782. 10.1182/blood-2002-10-3309.
50. Bill R., Döring A., Deutsch U., Engelhardt B. PSGL-1 is dispensible for the development of active experimental autoimmune encephalomyelitis in SJL/J mice. J. Neuroimmunol. 2011, 232:207-208. 10.1016/j.jneuroim.2010.10.008.
51. Engelhardt B., Kempe B., Merfeld-Clauss S., Laschinger M., Furie B., Wild M.K., Vestweber D. P-selectin glycoprotein ligand 1 is not required for the development of experimental autoimmune encephalomyelitis in SJL and C57BL/6 mice. J. Immunol. 2005, 175:1267-1275.
52. Osmers I., Bullard D.C., Barnum S.R. PSGL-1 is not required for development of experimental autoimmune encephalomyelitis. J. Neuroimmunol. 2005, 166:193-196. 10.1016/j.jneuroim.2005.06.001.
53. Piccio L., Rossi B., Scarpini E., Laudanna C., Giagulli C., Issekutz A.C., Vestweber D., Butcher E.C., Constantin G. Molecular mechanisms involved in lymphocyte recruitment in inflamed brain microvessels: critical roles for P-selectin glycoprotein ligand-1 and heterotrimeric G(i)-linked receptors. J. Immunol. 2002, 168:1940-1949.
54. Ifergan I., Kebir H., Alvarez J.I., Marceau G., Bernard M., Bourbonnière L., Poirier J., Duquette P., Talbot P.J., Arbour N., et al. Central nervous system recruitment of effector memory CD8+ T lymphocytes during neuroinflammation is dependent on α4 integrin. Brain J. Neurol. 2011, 134:3560-3577. 10.1093/brain/awr268.
55. Wang H.H., Dai Y.Q., Qiu W., Lu Z.Q., Peng F.H., Wang Y.G., Bao J., Li Y., Hu X.Q. Interleukin-17-secreting T cells in neuromyelitis optica and multiple sclerosis during relapse. J. Clin. Neurosci. Off. J. Neurosurg. Soc. Aust. 2011, 18:1313-1317. 10.1016/j.jocn.2011.01.031.
56. Teunissen M.B.M., Yeremenko N.G., Baeten D.L.P., Chielie S., Spuls P.I., de Rie M.A., Lantz O., Res P.C.M. The IL-17A-producing CD8+ T-cell population in psoriatic lesional skin comprises mucosa-associated invariant T cells and conventional T cells. J. Invest. Dermatol. 2014, 134:2898-2907. 10.1038/jid.2014.261.