MR1-restricted mucosal associated invariant T (MAIT) cells in the immune response to Mycobacterium tuberculosis

Immunological Reviews

Volumn 264, Issue 1, 2015, Pages 154-166

  Gold, Marielle C ^a,b,c   Napier, Ruth J ^a   Lewinsohn, David M ^a,b,c  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b PORTLAND VA MEDICAL CENTER   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

MR1; Mucosal associated invariant T cells (MAIT); Tuberculosis

Indexed keywords

GAMMA INTERFERON; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 18; INTERLEUKIN 22; T LYMPHOCYTE RECEPTOR; HLA ANTIGEN CLASS 1; LIGAND;

ANTIGEN PRESENTATION; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; HUMAN; INNATE IMMUNITY; LUNG ALVEOLUS MACROPHAGE; MACROPHAGE; MR1 RESTRICTED MUCOSAL ASSOCIATED INVARIANT T LYMPHOCYTE; MYCOBACTERIUM TUBERCULOSIS; NATURAL KILLER T CELL; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; TUBERCULOSIS; TUBERCULOSIS CONTROL; ANIMAL; CYTOLOGY; DISEASE PREDISPOSITION; EVOLUTION; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MUCOSA;

ANIMALS; BIOLOGICAL EVOLUTION; DISEASE SUSCEPTIBILITY; HISTOCOMPATIBILITY ANTIGENS CLASS I; HOST-PATHOGEN INTERACTIONS; HUMANS; LIGANDS; MUCOUS MEMBRANE; MYCOBACTERIUM TUBERCULOSIS; T-LYMPHOCYTE SUBSETS; TUBERCULOSIS;

EID: 84923165714     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/imr.12271     Document Type: Article

References (130)

1. WHO. WHO Report 2010 Global Tuberculosis Control. Geneva: WHO, 2010.
2. Verrall AJ, Netea MG, Alisjahbana B, Hill PC, van Crevel R. Early clearance of Mycobacterium tuberculosis: a new frontier in prevention. Immunology 2014;141:506-513.
3. Winslow GM, Cooper A, Reiley W, Chatterjee M, Woodland DL. Early T-cell responses in tuberculosis immunity. Immunol Rev 2008;225:284-299.
4. Nardell EA, Wallis RS. Here today-gone tomorrow: the case for transient acute tuberculosis infection. Am J Respir Crit Care Med 2006;174:734-735.
5. Lurie MB. Experimental epidemiology of tuberculosis: hereditary resistance to attack by tuberculosis and to the ensuing disease and the effect of the concentration of tubercle bacilli upon these two phases of resistance. J Exp Med 1944;79:573-589.
6. Zanetti C, Peracchi M, Zorzi D, Fiorio S, Fallico L, Palu G. Outbreak of transient conversions of the QuantiFERON-TB Gold In-Tube test in laboratory health care worker screenings. Clinical and vaccine immunology: CVI 2012;19:954-960.
7. Morrison J, Pai M, Hopewell PC. Tuberculosis and latent tuberculosis infection in close contacts of people with pulmonary tuberculosis in low-income and middle-income countries: a systematic review and meta-analysis. Lancet Infect Dis 2008;8:359-368.
8. Verver S, et al. Proportion of tuberculosis transmission that takes place in households in a high-incidence area. Lancet 2004;363:212-214.
9. Friedman LN, et al. High rate of negative results of tuberculin and QuantiFERON tests among individuals with a history of positive skin test results. Infection control and hospital epidemiology: the official journal of the Society of Hospital Epidemiologists of America 2006;27:436-441.
10. Ringshausen FC, Nienhaus A, Schablon A, Schlosser S, Schultze-Werninghaus G, Rohde G. Predictors of persistently positive Mycobacterium-tuberculosis-specific interferon-gamma responses in the serial testing of health care workers. BMC Infect Dis 2010;10:220.
11. Nunes-Alves C, Booty MG, Carpenter SM, Jayaraman P, Rothchild AC, Behar SM. In search of a new paradigm for protective immunity to TB. Nat Rev Microbiol 2014;12:289-299.
12. Barnes PF, Bloch AB, Davidson PT, Snider DE Jr. Tuberculosis in patients with human immunodeficiency virus infection. N Engl J Med 1991;324:1644-1650.
13. Geldmacher C, Zumla A, Hoelscher M. Interaction between HIV and Mycobacterium tuberculosis: HIV-1-induced CD4 T-cell depletion and the development of active tuberculosis. Current opinion in HIV and AIDS 2012;7:268-275.
14. Casanova JL, Abel L. Genetic dissection of immunity to mycobacteria: the human model. Annu Rev Immunol 2002;20:581-620.
15. Wallis RS. Tumour necrosis factor antagonists: structure, function, and tuberculosis risks. Lancet Infect Dis 2008;8:601-611.
16. Lewinsohn DA, Heinzel AS, Gardner JM, Zhu L, Alderson MR, Lewinsohn DM. Mycobacterium tuberculosis-specific CD8+ T cells preferentially recognize heavily infected cells. Am J Respir Crit Care Med 2003;168:1346-1352.
17. Porcelli S, Yockey CE, Brenner MB, Balk SP. Analysis of T cell antigen receptor (TCR) expression by human peripheral blood CD4-8- alpha/beta T cells demonstrates preferential use of several V beta genes and an invariant TCR alpha chain. J Exp Med 1993;178:1-16.
18. Treiner E, et al. Selection of evolutionarily conserved mucosal-associated invariant T cells by MR1. Nature 2003;422:164-169.
19. Gold MC, et al. Human Mucosal Associated Invariant T Cells Detect Bacterially Infected Cells. PLoS Biol 2010;8:e1000407.
20. Le Bourhis L, et al. Antimicrobial activity of mucosal-associated invariant T cells. Nat Immunol 2010;11:701-708.
21. Kjer-Nielsen L, et al. MR1 presents microbial vitamin B metabolites to MAIT cells. Nature 2012;491:717-723.
22. Gold MC, et al. Human thymic MR1-restricted MAIT cells are innate pathogen-reactive effectors that adapt following thymic egress. Mucosal Immunol 2013;6:35-44.
23. Le Bourhis L, et al. MAIT Cells Detect and Efficiently Lyse Bacterially-Infected Epithelial Cells. PLoS Pathog 2013;9:e1003681.
24. Brennan PJ, Brigl M, Brenner MB. Invariant natural killer T cells: an innate activation scheme linked to diverse effector functions. Nat Rev Immunol 2013;13:101-117.
25. Fuschiotti P, et al. Analysis of the TCR alpha-chain rearrangement profile in human T lymphocytes. Mol Immunol 2007;44:3380-3388.
26. Greenaway HY, Ng B, Price DA, Douek DC, Davenport MP, Venturi V. NKT and MAIT invariant TCRalpha sequences can be produced efficiently by VJ gene recombination. Immunobiology 2012;218:213-224.
27. Tilloy F, 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;189:1907-1921.
28. Coles MC, Raulet DH. NK1 1+ T cells in the liver arise in the thymus and are selected by interactions with class I molecules on CD4+CD8+ cells. J Immunol 2000;164:2412-2418.
29. Seach N, et al. Double positive thymocytes select mucosal-associated invariant T cells. J Immunol 2013;191:6002-6009.
30. Urdahl KB, Sun JC, Bevan MJ. Positive selection of MHC class Ib-restricted CD8(+) T cells on hematopoietic cells. Nat Immunol 2002;3:772-779.
31. Cho H, Bediako Y, Xu H, Choi HJ, Wang CR. Positive selecting cell type determines the phenotype of MHC class Ib-restricted CD8+ T cells. Proc Natl Acad Sci USA 2011;108:13241-13246.
32. Prince AL, Yin CC, Enos ME, Felices M, Berg LJ. The Tec kinases Itk and Rlk regulate conventional versus innate T-cell development. Immunol Rev 2009;228:115-131.
33. Martin E, et al. Stepwise Development of MAIT Cells in Mouse and Human. PLoS Biol 2009;7:e54.
34. Kovalovsky D, et al. The BTB-zinc finger transcriptional regulator PLZF controls the development of invariant natural killer T cell effector functions. Nat Immunol 2008;9:1055-1064.
35. Savage AK, et al. The transcription factor PLZF directs the effector program of the NKT cell lineage. Immunity 2008;29:391-403.
36. Kreslavsky T, et al. TCR-inducible PLZF transcription factor required for innate phenotype of a subset of gammadelta T cells with restricted TCR diversity. Proc Natl Acad Sci USA 2009;106:12453-12458.
37. 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.
38. Eidson M, et al. Altered development of NKT cells, gammadelta T cells, CD8 T cells and NK cells in a PLZF deficient patient. PLoS ONE 2011;6:e24441.
39. Thomas SY, et al. PLZF induces an intravascular surveillance program mediated by long-lived LFA-1-ICAM-1 interactions. J Exp Med 2011;208:1179-1188.
40. Reantragoon R, et al. Antigen-loaded MR1 tetramers define T cell receptor heterogeneity in mucosal-associated invariant T cells. J Exp Med 2013;210:2305-2320.
41. Dusseaux M, et al. Human MAIT cells are xenobiotic-resistant, tissue-targeted, CD161hi IL-17-secreting T cells. Blood 2011;117:1250-1259.
42. Jo J, et al. Toll-like receptor 8 agonist and bacteria trigger potent activation of innate immune cells in human liver. PLoS Pathog 2014;10:e1004210.
43. Hansen TH, Huang S, Arnold PL, Fremont DH. Patterns of nonclassical MHC antigen presentation. Nat Immunol 2007;8:563-568.
44. Gold MC, et al. MR1-restricted MAIT cells display ligand discrimination and pathogen selectivity through distinct T cell receptor usage. J Exp Med 2014;211:1601-1610.
45. Lepore M, et al. Parallel T-cell cloning and deep sequencing of human MAIT cells reveal stable oligoclonal TCRbeta repertoire. Nat Commun 2014;5:3866.
46. Riegert P, Wanner V, Bahram S. Genomics, isoforms, expression, and phylogeny of the MHC class I-related MR1 gene. J Immunol 1998;161:4066-4077.
47. Parra-Cuadrado JF, del Moral MG, Garcia-Pavia P, Setien F, Martinez-Naves E. Characterization of the MHC class I-related MR1 locus in nonhuman primates. Immunogenetics 2001;53:643-648.
48. 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;41:62.
49. Edholm ES, Grayfer L, Robert J. Evolution of nonclassical MHC-dependent invariant T cells. Cellular and molecular life sciences: CMLS 2014;71:4763-4780.
50. Miley MJ, et al. Biochemical Features of the MHC-Related Protein 1 Consistent with an Immunological Function. J Immunol 2003;170:6090-6098.
51. Huang S, et al. Evidence for MR1 antigen presentation to mucosal-associated invariant T cells. J Biol Chem 2005;280:21183-21193.
52. Huang S, et al. MR1 uses an endocytic pathway to activate mucosal-associated invariant T cells. J Exp Med 2008;205:1201-1211.
53. Huang S, et al. MR1 antigen presentation to mucosal-associated invariant T cells was highly conserved in evolution. Proc Natl Acad Sci USA 2009;106:8290-8295.
54. Reantragoon R, et al. Structural insight into MR1-mediated recognition of the mucosal associated invariant T cell receptor. J Exp Med 2012;209:761-774.
55. Patel O, et al. Recognition of vitamin B metabolites by mucosal-associated invariant T cells. Nat Commun 2013;4:2142.
56. Lopez-Sagaseta J, Dulberger CL, McFedries A, Cushman M, Saghatelian A, Adams EJ. MAIT recognition of a stimulatory bacterial antigen bound to MR1. J Immunol 2013;191:5268-5277.
57. Lopez-Sagaseta J, et al. The molecular basis for Mucosal-Associated Invariant T cell recognition of MR1 proteins. Proc Natl Acad Sci USA 2013;110:E1771-E1778.
58. Eckle SB, et al. A molecular basis underpinning the T cell receptor heterogeneity of mucosal-associated invariant T cells. J Exp Med 2014;211:1585-1600.
59. Corbett AJ, et al. T-cell activation by transitory neo-antigens derived from distinct microbial pathways. Nature 2014;509:361-365.
60. Young MH, et al. MAIT Cell Recognition of MR1 on Bacterially Infected and Uninfected Cells. PLoS ONE 2013;8:e53789.
61. Cooperman JM, Lopez R. Riboflavin. In: Machlin LJ ed. Handbook of Vitamins. New York and Basel: Marcel Dekker Inc, 1991:283-310.
62. Abbas CA, Sibirny AA. Genetic control of biosynthesis and transport of riboflavin and flavin nucleotides and construction of robust biotechnological producers. Microbiology and molecular biology reviews: MMBR 2011;75:321-360.
63. Blum JS, Wearsch PA, Cresswell P. Pathways of antigen processing. Annu Rev Immunol 2013;31:443-473.
64. Harriff MJ, Purdy GE, Lewinsohn DM. Escape from the phagosome: the explanation for MHC-I processing of mycobacterial antigens? Front Immunol 2012;3:40.
65. Beatty WL, Russell DG. Identification of mycobacterial surface proteins released into subcellular compartments of infected macrophages. Infect Immun 2000;68:6997-7002.
66. Beatty WL, Rhoades ER, Ullrich HJ, Chatterjee D, Heuser JE, Russell DG. Trafficking and release of mycobacterial lipids from infected macrophages. Traffic 2000;1:235-247.
67. Reichman LB, Hershfield ES. Tuberculosis: A Comprehensive International Approach. 2nd edn, rev. and expanded ed. New York: Dekker, 2000.
68. Hatch TF. Distribution and deposition of inhaled particles in respiratory tract. Microbiol Mol Biol Rev 1961;25:237-240.
69. Bermudez LE, Goodman J. Mycobacterium tuberculosis invades and replicates within type II alveolar cells. Infect Immun 1996;64:1400-1406.
70. Bermudez LE, Shelton K, Young LS. Comparison of the ability of Mycobacterium avium, M. smegmatis and M. tuberculosis to invade and replicate within HEp-2 epithelial cells. Tuber Lung Dis 1995;76:240-247.
71. Garcia-Perez BE, Hernandez-Gonzalez JC, Garcia-Nieto S, Luna-Herrera J. Internalization of a non-pathogenic mycobacteria by macropinocytosis in human alveolar epithelial A549 cells. Microb Pathog 2008;45:1-6.
72. Dam T, Danelishvili L, Wu M, Bermudez LE. The fadD2 gene is required for efficient Mycobacterium avium invasion of mucosal epithelial cells. J Infect Dis 2006;193:1135-1142.
73. Harriff MJ, et al. Mycobacterium avium genes MAV_5138 and MAV_3679 are transcriptional regulators that play a role in invasion of epithelial cells, in part by their regulation of CipA, a putative surface protein interacting with host cell signaling pathways. J Bacteriol 2009;191:1132-1142.
74. Miltner E, Daroogheh K, Mehta PK, Cirillo SL, Cirillo JD, Bermudez LE. Identification of Mycobacterium avium genes that affect invasion of the intestinal epithelium. Infect Immun 2005;73:4214-4221.
75. Sangari FJ, Goodman J, Bermudez LE. Mycobacterium avium enters intestinal epithelial cells through the apical membrane, but not by the basolateral surface, activates small GTPase Rho and, once within epithelial cells, expresses an invasive phenotype. Cell Microbiol 2000;2:561-568.
76. Sangari FJ, Goodman J, Petrofsky M, Kolonoski P, Bermudez LE. Mycobacterium avium invades the intestinal mucosa primarily by interacting with enterocytes. Infect Immun 2001;69:1515-1520.
77. Sangari FJ, Goodman JR, Bermudez LE. Ultrastructural study of Mycobacterium avium infection of HT-29 human intestinal epithelial cells. J Med Microbiol 2000;49:139-147.
78. Harriff MJ, et al. Human lung epithelial cells contain mycobacterium tuberculosis in a late endosomal vacuole and are efficiently recognized by CD8+ T cells. PLoS ONE 2014;9:e97515.
79. Chackerian A, Alt J, Perera V, Behar SM. Activation of NKT cells protects mice from tuberculosis. Infect Immun 2002;70:6302-6309.
80. Chua WJ, Truscott SM, Eickhoff CS, Blazevic A, Hoft DF, Hansen TH. Polyclonal mucosa-associated invariant T cells have unique innate functions in bacterial infection. Infect Immun 2012;80:3256-3267.
81. 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 USA 2013;110:E3119-3128.
82. Stenger S, et al. An antimicrobial activity of cytolytic T cells mediated by granulysin. Science 1998;282:121-125.
83. Cooper AM, Mayer-Barber KD, Sher A. Role of innate cytokines in mycobacterial infection. Mucosal Immunol 2011;4:252-260.
84. Cooper AM, Dalton DK, Stewart TA, Griffin JP, Russell DG, Orme IM. Disseminated tuberculosis in interferon gamma gene-disrupted mice. J Exp Med 1993;178:2243-2247.
85. Bonecini-Almeida MG, et al. Induction of in vitro human macrophage anti-mycobacterium tuberculosis activity: requirement for IFN-{gamma} and primed lymphocytes. J Immunol 1998;160:4490-4499.
86. Casanova JL, Abel L. The human model: a genetic dissection of immunity to infection in natural conditions. Nat Rev Immunol 2004;4:55-66.
87. Chan J, Xing Y, Magliozzo RS, Bloom BR. Killing of virulent Mycobacterium tuberculosis by reactive nitrogen intermediates produced by activated murine macrophages. J Exp Med 1992;175:1111-1122.
88. MacMicking JD, Taylor GA, McKinney JD. Immune control of tuberculosis by IFN-gamma-inducible LRG-47. Science 2003;302:654-659.
89. Deretic V. Autophagy as an immune defense mechanism. Curr Opin Immunol 2006;18:375-382.
90. Gutierrez MG, Master SS, Singh SB, Taylor GA, Colombo MI, Deretic V. Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 2004;119:753-766.
91. Chan ED, Chan J, Schluger NW. What is the role of nitric oxide in murine and human host defense against tuberculosis?Current knowledge. Am J Respir Cell Mol Biol 2001;25:606-612.
92. Liu PT, et al. Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response. Science 2006;311:1770-1773.
93. Fabri M, et al. Vitamin D is required for IFN-gamma-mediated antimicrobial activity of human macrophages. Sci Transl Med 2011;3:104ra102.
94. Singh SB, Davis AS, Taylor GA, Deretic V. Human IRGM induces autophagy to eliminate intracellular mycobacteria. Science 2006;313:1438-1441.
95. Moller M, Nebel A, Valentonyte R, van Helden PD, Schreiber S, Hoal EG. Investigation of chromosome 17 candidate genes in susceptibility to TB in a South African population. Tuberculosis 2009;89:189-194.
96. Gomez LM, et al. A polymorphism in the inducible nitric oxide synthase gene is associated with tuberculosis. Tuberculosis 2007;87:288-294.
97. Schon T, Elmberger G, Negesse Y, Pando RH, Sundqvist T, Britton S. Local production of nitric oxide in patients with tuberculosis. Int J Tuberc Lung Dis 2004;8:1134-1137.
98. Nicholson S, et al. Inducible nitric oxide synthase in pulmonary alveolar macrophages from patients with tuberculosis. J Exp Med 1996;183:2293-2302.
99. Facchetti F, et al. Expression of inducible nitric oxide synthase in human granulomas and histiocytic reactions. Am J Pathol 1999;154:145-152.
100. Choi HS, Rai PR, Chu HW, Cool C, Chan ED. Analysis of nitric oxide synthase and nitrotyrosine expression in human pulmonary tuberculosis. Am J Respir Crit Care Med 2002;166:178-186.
101. Guo FH, De Raeve HR, Rice TW, Stuehr DJ, Thunnissen FB, Erzurum SC. Continuous nitric oxide synthesis by inducible nitric oxide synthase in normal human airway epithelium in vivo. Proc Natl Acad Sci USA 1995;92:7809-7813.
102. Lane C, et al. Epithelial inducible nitric oxide synthase activity is the major determinant of nitric oxide concentration in exhaled breath. Thorax 2004;59:757-760.
103. Pechkovsky DV, et al. Human alveolar epithelial cells induce nitric oxide synthase-2 expression in alveolar macrophages. Eur Respir J 2002;19:672-683.
104. Guo FH, Erzurum SC. Characterization of inducible nitric oxide synthase expression in human airway epithelium. Environ Health Perspect 1998;106(Suppl 5):1119-1124.
105. Pechkovsky DV, et al. Pattern of NOS2 and NOS3 mRNA expression in human A549 cells and primary cultured AEC II. Am J Physiol Lung Cell Mol Physiol 2002;282:L684-692.
106. Uetani K, Arroliga ME, Erzurum SC. Double-stranded rna dependence of nitric oxide synthase 2 expression in human bronchial epithelial cell lines BET-1A and BEAS-2B. Am J Respir Cell Mol Biol 2001;24:720-726.
107. Asano K, et al. Constitutive and inducible nitric oxide synthase gene expression, regulation, and activity in human lung epithelial cells. Proc Natl Acad Sci USA 1994;91:10089-10093.
108. Roy S, Sharma S, Sharma M, Aggarwal R, Bose M. Induction of nitric oxide release from the human alveolar epithelial cell line A549: an in vitro correlate of innate immune response to Mycobacterium tuberculosis. Immunology 2004;112:471-480.
109. Desvignes L, Ernst JD. Interferon-gamma-responsive nonhematopoietic cells regulate the immune response to Mycobacterium tuberculosis. Immunity 2009;31:974-985.
110. Lambrecht BN, Salomon B, Klatzmann D, Pauwels RA. Dendritic cells are required for the development of chronic eosinophilic airway inflammation in response to inhaled antigen in sensitized mice. J Immunol 1998;160:4090-4097.
111. Schon-Hegrad MA, Oliver J, McMenamin PG, Holt PG. Studies on the density, distribution, and surface phenotype of intraepithelial class II major histocompatibility complex antigen (Ia)-bearing dendritic cells (DC) in the conducting airways. J Exp Med 1991;173:1345-1356.
112. Heath WR, et al. Cross-presentation, dendritic cell subsets, and the generation of immunity to cellular antigens. Immunol Rev 2004;199:9-26.
113. Reiley WW, et al. ESAT-6-specific CD4 T cell responses to aerosol Mycobacterium tuberculosis infection are initiated in the mediastinal lymph nodes. Proc Natl Acad Sci USA 2008;105:10961-10966.
114. Wolf AJ, et al. Initiation of the adaptive immune response to Mycobacterium tuberculosis depends on antigen production in the local lymph node, not the lungs. J Exp Med 2008;205:105-115.
115. Chackerian AA, Alt JM, Perera TV, Dascher CC, Behar SM. Dissemination of Mycobacterium tuberculosis is influenced by host factors and precedes the initiation of T-cell immunity. Infect Immun 2002;70:4501-4509.
116. Shortman K, Liu YJ. Mouse and human dendritic cell subtypes. Nat Rev Immunol 2002;2:151-161.
117. Kapsenberg ML. Dendritic-cell control of pathogen-driven T-cell polarization. Nat Rev Immunol 2003;3:984-993.
118. Das G, Sheridan S, Janeway CA Jr. The source of early IFN-gamma that plays a role in Th1 priming. J Immunol 2001;167:2004-2010.
119. Edwards AD, et al. Microbial recognition via Toll-like receptor-dependent and -independent pathways determines the cytokine response of murine dendritic cell subsets to CD40 triggering. J Immunol 2002;169:3652-3660.
120. Hilkens CM, Kalinski P, de Boer M, Kapsenberg ML. Human dendritic cells require exogenous interleukin-12-inducing factors to direct the development of naive T-helper cells toward the Th1 phenotype. Blood 1997;90:1920-1926.
121. Ussher JE, 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 2013;44:195-203.
122. Annibali V, et al. CD161(high)CD8+T cells bear pathogenetic potential in multiple sclerosis. Brain 2011;134:542-554.
123. 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 2011;64:153-161.
124. Croxford JL, Miyake S, Huang YY, Shimamura M, Yamamura T. Invariant V(alpha)19i T cells regulate autoimmune inflammation. Nat Immunol 2006;7:987-994.
125. 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;16:223-230.
126. 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.
127. Willing A, 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;44:3119-3128.
128. Serriari NE, et al. Innate mucosal-associated invariant T (MAIT) cells are activated in inflammatory bowel diseases. Clin Exp Immunol 2014;176:266-274.
129. Roca FJ, Ramakrishnan L. TNF dually mediates resistance and susceptibility to mycobacteria via mitochondrial reactive oxygen species. Cell 2013;153:521-534.
130. Abu-Raddad LJ, et al. Epidemiological benefits of more-effective tuberculosis vaccines, drugs, and diagnostics. Proc Natl Acad Sci USA 2009;106:13980-13985.