Mucosal-associated invariant T cells in multiple sclerosis: The jury is still out

Frontiers in Immunology

Volumn 6, Issue SEP, 2015, Pages

  Treiner, Emmanuel ^a,b,c   Liblau, Roland S ^a,b,c  

^a University of Toulouse III   (France)

^b UNIVERSITÉ PAUL SABATIER   (France)

^c TOULOUSE UNIVERSITY HOSPITAL   (France)

Author keywords

Adaptive immunity; IFN gamma; Innate like T cells; MHC related 1; Multiple sclerosis

Indexed keywords

BIOLOGICAL MARKER; GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 18; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; T LYMPHOCYTE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA;

ADAPTIVE IMMUNITY; ANTIGEN RECOGNITION; CYTOTOXICITY; DEGRANULATION; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; HUMAN; IMMUNE SYSTEM; IMMUNIZATION; INFLAMMATION; MAJOR HISTOCOMPATIBILITY COMPLEX; MUCOSAL ASSOCIATED INVARIANT T CELL; MULTIPLE SCLEROSIS; NONHUMAN; REVIEW; T LYMPHOCYTE;

EID: 84946573239     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2015.00503     Document Type: Review

References (74)

1. Beecham AH, Patsopoulos NA, Xifara DK, Davis MF, Kemppinen A, Cotsapas C, et al. Analysis of immune-related loci identifies 48 new susceptibility variants for multiple sclerosis. Nat Genet (2013) 45(11):1353-60. doi:10.1038/ng.2770.
2. Hauser SL, Chan JR, Oksenberg JR. Multiple sclerosis: prospects and promise. Ann Neurol (2013) 74(3):317-27. doi:10.1002/ana.24009.
3. Housley WJ, Fernandez SD, Vera K, Murikinati SR, Grutzendler J, Cuerdon N, et al. Genetic variants associated with autoimmunity drive NFkappaB signaling and responses to inflammatory stimuli. Sci Transl Med (2015) 7(291):291ra93. doi:10.1126/scitranslmed.aaa9223.
4. Sawcer S, Hellenthal G, Pirinen M, Spencer CC, Patsopoulos NA, Moutsianas L, et al. Genetic risk and a primary role for cell-mediated immune mechanisms in multiple sclerosis. Nature (2011) 476(7359):214-9. doi:10.1038/nature10251.
5. Nylander A, Hafler DA. Multiple sclerosis. J Clin Invest (2012) 122(4):1180-8. doi:10.1172/JCI58649.
6. Ben-Nun A, Kaushansky N, Kawakami N, Krishnamoorthy G, Berer K, Liblau R, et al. From classic to spontaneous and humanized models of multiple sclerosis: impact on understanding pathogenesis and drug development. J Autoimmun (2014) 54:33-50. doi:10.1016/j.jaut.2014.06.004.
7. Rangachari M, Kuchroo VK. Using EAE to better understand principles of immune function and autoimmune pathology. J Autoimmun (2013) 45:31-9. doi:10.1016/j.jaut.2013.06.008.
8. Saxena A, Martin-Blondel G, Mars LT, Liblau RS. Role of CD8 T cell subsets in the pathogenesis of multiple sclerosis. FEBS Lett (2011) 585(23):3758-63. doi:10.1016/j.febslet.2011.08.047.
9. Bruck W, Gold R, Lund BT, Oreja-Guevara C, Prat A, Spencer CM, et al. Therapeutic decisions in multiple sclerosis: moving beyond efficacy. JAMA Neurol (2013) 70(10):1315-24. doi:10.1001/jamaneurol.2013.3510.
10. Treiner E, Duban L, Bahram S, Radosavljevic M, Wanner V, Tilloy F, et al. Selection of evolutionarily conserved mucosal-associated invariant T cells by MR1. Nature (2003) 422(6928):164-9. doi:10.1038/nature01433.
11. Huang S, Martin E, Kim S, Yu L, Soudais C, Fremont DH, et al. MR1 antigen presentation to mucosal-associated invariant T cells was highly conserved in evolution. Proc Natl Acad Sci U S A (2009) 106(20):8290-5. doi:10.1073/pnas.0903196106.
12. Goldfinch N, Reinink P, Connelley T, Koets A, Morrison I, Van Rhijn I. Conservation of mucosal associated invariant T (MAIT) cells and the MR1 restriction element in ruminants, and abundance of MAIT cells in spleen. Vet Res (2010) 41(5):62. doi:10.1051/vetres/2010034.
13. Tilloy F, Treiner E, Park SH, Garcia C, Lemonnier F, de la Salle H, et al. An invariant T cell receptor alpha chain defines a novel TAP-independent major histocompatibility complex class Ib-restricted alpha/beta T cell subpopulation in mammals. J Exp Med (1999) 189(12):1907-21. doi:10.1084/jem.189.12.1907.
14. Tsukamoto K, Deakin JE, Graves JA, Hashimoto K. Exceptionally high conservation of the MHC class I-related gene, MR1, among mammals. Immunogenetics (2013) 65(2):115-24. doi:10.1007/s00251-012-0666-5.
15. Le Bourhis L, Guerri L, Dusseaux M, Martin E, Soudais C, Lantz O. Mucosal-associated invariant T cells: unconventional development and function. Trends Immunol (2011) 32(5):212-8. doi:10.1016/j.it.2011.02.005.
16. Reantragoon R, Corbett AJ, Sakala IG, Gherardin NA, Furness JB, Chen Z, et al. Antigen-loaded MR1 tetramers define T cell receptor heterogeneity in mucosal-associated invariant T cells. J Exp Med (2013) 210(11):2305-20. doi:10.1084/jem.20130958.
17. Martin E, Treiner E, Duban L, Guerri L, Laude H, Toly C, et al. Stepwise development of MAIT cells in mouse and human. PLoS Biol (2009) 7(3):e54. doi:10.1371/journal.pbio.1000054.
18. Walker LJ, Kang YH, Smith MO, Tharmalingham H, Ramamurthy N, Fleming VM, et al. Human MAIT and CD8alphaalpha cells develop from a pool of type-17 precommitted CD8+ T cells. Blood (2012) 119(2):422-33. doi:10.1182/blood-2011-05-353789.
19. Kjer-Nielsen L, Patel O, Corbett AJ, Le Nours J, Meehan B, Liu L, et al. MR1 presents microbial vitamin B metabolites to MAIT cells. Nature (2012) 491(7426):717-23. doi:10.1038/nature11605.
20. Corbett AJ, Eckle SB, Birkinshaw RW, Liu L, Patel O, Mahony J, et al. T-cell activation by transitory neo-antigens derived from distinct microbial pathways. Nature (2014) 509(7500):361-5. doi:10.1038/nature13160.
21. Birkinshaw RW, Kjer-Nielsen L, Eckle SB, McCluskey J, Rossjohn J. MAITs, MR1 and vitamin B metabolites. Curr Opin Immunol (2014) 26:7-13. doi:10.1016/j.coi.2013.09.007.
22. Leeansyah E, Loh L, Nixon DF, Sandberg JK. Acquisition of innate-like microbial reactivity in mucosal tissues during human fetal MAIT-cell development. Nat Commun (2014) 5:3143. doi:10.1038/ncomms4143.
23. Dusseaux M, Martin E, Serriari N, Peguillet I, Premel V, Louis D, et al. Human MAIT cells are xenobiotic-resistant, tissue-targeted, CD161hi IL-17-secreting T cells. Blood (2011) 117(4):1250-9. doi:10.1182/blood-2010-08-303339.
24. Le Bourhis L, Dusseaux M, Bohineust A, Bessoles S, Martin E, Premel V, et al. MAIT cells detect and efficiently lyse bacterially-infected epithelial cells. PLoS Pathog (2013) 9(10):e1003681. doi:10.1371/journal.ppat.1003681.
25. Lepore M, Kalinichenko A, Colone A, Paleja B, Singhal A, Tschumi A, et al. Parallel T-cell cloning and deep sequencing of human MAIT cells reveal stable oligoclonal TCRbeta repertoire. Nat Commun (2014) 5:3866. doi:10.1038/ncomms4866.
26. Tang XZ, Jo J, Tan AT, Sandalova E, Chia A, Tan KC, et al. IL-7 licenses activation of human liver intrasinusoidal mucosal-associated invariant T cells. J Immunol (2013) 190(7):3142-52. doi:10.4049/jimmunol.1203218.
27. Teunissen MB, Yeremenko NG, Baeten DL, Chielie S, Spuls PI, de Rie MA, et al. 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(12):2898-907. doi:10.1038/jid.2014.261.
28. Carolan E, Tobin LM, Mangan BA, Corrigan M, Gaoatswe G, Byrne G, et al. Altered distribution and increased IL-17 production by mucosal-associated invariant T cells in adult and childhood obesity. J Immunol (2015) 194(12):5775-80. doi:10.4049/jimmunol.1402945.
29. Magalhaes I, Pingris K, Poitou C, Bessoles S, Venteclef N, Kiaf B, et al. Mucosal-associated invariant T cell alterations in obese and type 2 diabetic patients. J Clin Invest (2015) 125(4):1752-62. doi:10.1172/JCI78941.
30. Turtle CJ, Delrow J, Joslyn RC, Swanson HM, Basom R, Tabellini L, et al. Innate signals overcome acquired TCR signaling pathway regulation and govern the fate of human CD161(hi) CD8alpha(+) semi-invariant T cells. Blood (2011) 118(10):2752-62. doi:10.1182/blood-2011-02-334698.
31. Serriari NE, Eoche M, Lamotte L, Lion J, Fumery M, Marcelo P, et al. Innate mucosal-associated invariant T (MAIT) cells are activated in inflammatory bowel diseases. Clin Exp Immunol (2014) 176(2):266-74. doi:10.1111/cei.12277.
32. Rahimpour A, Koay HF, Enders A, Clanchy R, Eckle SB, Meehan B, et al. Identification of phenotypically and functionally heterogeneous mouse mucosal-associated invariant T cells using MR1 tetramers. J Exp Med (2015) 212(7):1095-108. doi:10.1084/jem.20142110.
33. Gold MC, Cerri S, Smyk-Pearson S, Cansler ME, Vogt TM, Delepine J, et al. Human mucosal associated invariant T cells detect bacterially infected cells. PLoS Biol (2010) 8(6):e1000407. doi:10.1371/journal.pbio.1000407.
34. Le Bourhis L, Martin E, Peguillet I, Guihot A, Froux N, Core M, et al. Antimicrobial activity of mucosal-associated invariant T cells. Nat Immunol (2010) 11(8):701-8. doi:10.1038/ni.1890.
35. Leung DT, Bhuiyan TR, Nishat NS, Hoq MR, Aktar A, Rahman MA, et al. Circulating mucosal associated invariant T cells are activated in Vibrio cholerae O1 infection and associated with lipopolysaccharide antibody responses. PLoS Negl Trop Dis (2014) 8(8):e3076. doi:10.1371/journal.pntd.0003076.
36. Salerno-Goncalves R, Rezwan T, Sztein MB. B cells modulate mucosal associated invariant T cell immune responses. Front Immunol (2014) 4:511. doi:10.3389/fimmu.2013.00511.
37. Ussher JE, Bilton M, Attwod E, Shadwell J, Richardson R, de Lara C, et al. CD161++ CD8+ T cells, including the MAIT cell subset, are specifically activated by IL-12+IL-18 in a TCR-independent manner. Eur J Immunol (2014) 44(1):195-203. doi:10.1002/eji.201343509.
38. Chua WJ, Truscott SM, EickhoffCS, Blazevic A, Hoft DF, Hansen TH. Polyclonal mucosa-associated invariant T cells have unique innate functions in bacterial infection. Infect Immun (2012) 80(9):3256-67. doi:10.1128/IAI.00279-12.
39. Gold MC, Napier RJ, Lewinsohn DM. MR1-restricted mucosal associated invariant T (MAIT) cells in the immune response to Mycobacterium tuberculosis. Immunol Rev (2015) 264(1):154-66. doi:10.1111/imr.12271.
40. Sharma PK, Wong EB, Napier RJ, Bishai WR, Ndung'u T, Kasprowicz VO, et al. High expression of CD26 accurately identifies human bacteria-reactive MR1-restricted MAIT cells. Immunology (2015) 145(3):443-53. doi:10.1111/imm.12461.
41. Grimaldi D, Le Bourhis L, Sauneuf B, Dechartres A, Rousseau C, Ouaaz F, et al. Specific MAIT cell behaviour among innate-like T lymphocytes in critically ill patients with severe infections. Intensive Care Med (2014) 40(2):192-201. doi:10.1007/s00134-013-3163-x.
42. Cosgrove C, Ussher JE, Rauch A, Gartner K, Kurioka A, Huhn MH, et al. Early and nonreversible decrease of CD161++/MAIT cells in HIV infection. Blood (2013) 121(6):951-61. doi:10.1182/blood-2012-06-436436.
43. Leeansyah E, Ganesh A, Quigley MF, Sonnerborg A, Andersson J, Hunt PW, et al. Activation, exhaustion, and persistent decline of the antimicrobial MR1-restricted MAIT-cell population in chronic HIV-1 infection. Blood (2013) 121(7):1124-35. doi:10.1182/blood-2012-07-445429.
44. Wong EB, Akilimali NA, Govender P, Sullivan ZA, Cosgrove C, Pillay M, et al. Low levels of peripheral CD161++CD8+ mucosal associated invariant T (MAIT) cells are found in HIV and HIV/TB co-infection. PLoS One (2013) 8(12):e83474. doi:10.1371/journal.pone.0083474.
45. Eberhard JM, Hartjen P, Kummer S, Schmidt RE, Bockhorn M, Lehmann C, et al. CD161+ MAIT cells are severely reduced in peripheral blood and lymph nodes of HIV-infected individuals independently of disease progression. PLoS One (2014) 9(11):e111323. doi:10.1371/journal.pone.0111323.
46. Greathead L, Metcalf R, Gazzard B, Gotch F, Steel A, Kelleher P. CD8+/CD161++ mucosal-associated invariant T-cell levels in the colon are restored on long-term antiretroviral therapy and correlate with CD8+ T-cell immune activation. AIDS (2014) 28(11):1690-2. doi:10.1097/QAD.0000000000000351.
47. Fernandez CS, Amarasena T, Kelleher AD, Rossjohn J, McCluskey J, Godfrey DI, et al. MAIT cells are depleted early but retain functional cytokine expression in HIV infection. Immunol Cell Biol (2015) 93(2):177-88. doi:10.1038/icb.2014.91.
48. Saeidi A, Tien Tien VL, Al-Batran R, Al-Darraji HA, Tan HY, Yong YK, et al. Attrition of TCR Valpha7.2+ CD161++ MAIT cells in HIV-tuberculosis co-infection is associated with elevated levels of PD-1 expression. PLoS One (2015) 10(4):e0124659. doi:10.1371/journal.pone.0124659.
49. Illes 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(2):223-30. doi:10.1093/intimm/dxh018.
50. Peterfalvi A, Gomori E, Magyarlaki T, Pal J, Banati M, Javorhazy A, et al. Invariant Valpha7.2-Jalpha33 TCR is expressed in human kidney and brain tumors indicating infiltration by mucosal-associated invariant T (MAIT) cells. Int Immunol (2008) 20(12):1517-25. doi:10.1093/intimm/dxn111.
51. Annibali V, Ristori G, Angelini DF, Serafini B, Mechelli R, Cannoni S, et al. CD161(high)CD8+T cells bear pathogenetic potential in multiple sclerosis. Brain (2011) 134(Pt 2):542-54. doi:10.1093/brain/awq354.
52. Cho YN, Kee SJ, Kim TJ, Jin HM, Kim MJ, Jung HJ, et al. Mucosal-associated invariant T cell deficiency in systemic lupus erythematosus. J Immunol (2014) 193(8):3891-901. doi:10.4049/jimmunol.1302701.
53. Kim JC, Jin HM, Cho YN, Kwon YS, Kee SJ, Park YW. Deficiencies of circulating mucosal-associated invariant T cells and natural killer T cells in patients with acute cholecystitis. J Korean Med Sci (2015) 30(5):606-11. doi:10.3346/jkms.2015.30.5.606.
54. Sugimoto C, Konno T, Wakao R, Fujita H, Fujita H, Wakao H. Mucosal-associated invariant T cell is a potential marker to distinguish fibromyalgia syndrome from arthritis. PLoS One (2015) 10(4):e0121124. doi:10.1371/journal.pone.0121124.
55. Hinks TS, Zhou X, Staples KJ, Dimitrov BD, Manta A, Petrossian T, et al. Innate and adaptive T cells in asthmatic patients: relationship to severity and disease mechanisms. J Allergy Clin Immunol (2015) 136(2):323-33. doi:10.1016/j.jaci.2015.01.014.
56. Dunne MR, Elliott L, Hussey S, Mahmud N, Kelly J, Doherty DG, et al. Persistent changes in circulating and intestinal gammadelta T cell subsets, invariant natural killer T cells and mucosal-associated invariant T cells in children and adults with coeliac disease. PLoS One (2013) 8(10):e76008. doi:10.1371/journal.pone.0076008.
57. Croxford JL, Miyake S, Huang YY, Shimamura M, Yamamura T. Invariant V(alpha)19i T cells regulate autoimmune inflammation. Nat Immunol (2006) 7(9):987-94. doi:10.1038/ni1370.
58. 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(9):529-35. doi:10.1093/intimm/dxr047.
59. Abrahamsson SV, Angelini DF, Dubinsky AN, Morel E, Oh U, Jones JL, 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 (2013) 136(Pt 9):2888-903. doi:10.1093/brain/awt182.
60. Willing A, Leach OA, Ufer F, Attfield KE, Steinbach K, Kursawe N, et al. CD8(+) 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(10):3119-28. doi:10.1002/eji.201344160.
61. Held K, Bhonsle-Deeng L, Siewert K, Sato W, Beltran E, Schmidt S, et al. alphabeta T-cell receptors from multiple sclerosis brain lesions show MAIT cell-related features. Neurol Neuroimmunol Neuroinflamm (2015) 2(4):e107. doi:10.1212/NXI.0000000000000107.
62. Chiba A, Tajima R, Tomi C, Miyazaki Y, Yamamura T, Miyake S. Mucosal-associated invariant T cells promote inflammation and exacerbate disease in murine models of arthritis. Arthritis Rheum (2012) 64(1):153-61. doi:10.1002/art.33314.
63. Gold MC, McLaren JE, Reistetter JA, Smyk-Pearson S, Ladell K, Swarbrick GM, et al. MR1-restricted MAIT cells display ligand discrimination and pathogen selectivity through distinct T cell receptor usage. J Exp Med (2014) 211(8):1601-10. doi:10.1084/jem.20140507.
64. Kurioka A, Ussher JE, Cosgrove C, Clough C, Fergusson JR, Smith K, et al. MAIT cells are licensed through granzyme exchange to kill bacterially sensitized targets. Mucosal Immunol (2015) 8(2):429-40. doi:10.1038/mi.2014.81.
65. Soudais C, Samassa F, Sarkis M, Le Bourhis L, Bessoles S, Blanot D, et al. In vitro and in vivo analysis of the gram-negative bacteria-derived riboflavin precursor derivatives activating mouse MAIT cells. J Immunol (2015) 194(10):4641-9. doi:10.4049/jimmunol.1403224.
66. Meierovics A, Yankelevich WJ, Cowley SC. MAIT cells are critical for optimal mucosal immune responses during in vivo pulmonary bacterial infection. Proc Natl Acad Sci U S A (2013) 110(33):E3119-28. doi:10.1073/pnas.1302799110.
67. Berer K, Krishnamoorthy G. Microbial view of central nervous system autoimmunity. FEBS Lett (2014) 588(22):4207-13. doi:10.1016/j.febslet.2014.04.007.
68. Nouri M, Bredberg A, Westrom B, Lavasani S. Intestinal barrier dysfunction develops at the onset of experimental autoimmune encephalomyelitis, and can be induced by adoptive transfer of auto-reactive T cells. PLoS One (2014) 9(9):e106335. doi:10.1371/journal.pone.0106335.
69. Seach N, Guerri L, Le Bourhis L, Mburu Y, Cui Y, Bessoles S, et al. Double-positive thymocytes select mucosal-associated invariant T cells. J Immunol (2013) 191(12):6002-9. doi:10.4049/jimmunol.1301212.
70. Jo J, Tan AT, Ussher JE, Sandalova E, Tang XZ, Tan-Garcia A, et al. Toll-like receptor 8 agonist and bacteria trigger potent activation of innate immune cells in human liver. PLoS Pathog (2014) 10(6):e1004210. doi:10.1371/journal.ppat.1004210.
71. Novick D, Kim S, Kaplanski G, Dinarello CA. Interleukin-18, more than a Th1 cytokine. Semin Immunol (2013) 25(6):439-48. doi:10.1016/j.smim.2013.10.014.
72. Axtell RC, de Jong BA, Boniface K, van der Voort LF, Bhat R, De Sarno P, et al. T helper type 1 and 17 cells determine efficacy of interferon-beta in multiple sclerosis and experimental encephalomyelitis. Nat Med (2010) 16(4):406-12. doi:10.1038/nm.2110.
73. Malhotra S, Rio J, Urcelay E, Nurtdinov R, Bustamante MF, Fernandez O, et al. NLRP3 inflammasome is associated with the response to IFN-beta in patients with multiple sclerosis. Brain (2015) 138(Pt 3):644-52. doi:10.1093/brain/awu388.
74. Inoue M, Williams KL, Oliver T, Vandenabeele P, Rajan JV, Miao EA, et al. Interferon-beta therapy against EAE is effective only when development of the disease depends on the NLRP3 inflammasome. Sci Signal (2012) 5(225):ra38. doi:10.1126/scisignal.2002767.