MAIT cells are activated during human viral infections

Nature Communications

Volumn 7, Issue , 2016, Pages

  Van Wilgenburg, Bonnie ^a   Scherwitzl, Iris ^b   Hutchinson, Edward C ^c   Leng, Tianqi ^a   Kurioka, Ayako ^a   Kulicke, Corinna ^a   De Lara, Catherine ^a   Cole, Suzanne ^a   Vasanawathana, Sirijitt ^d   Limpitikul, Wannee ^e   Malasit, Prida ^f,g   Young, Duncan ^h   Denney, Laura ^a   Moore, Michael D ^c   Fabris, Paolo ⁱ   Giordani, Maria Teresa ⁱ   Oo, Ye Htun ^j   Laidlaw, Stephen M ^k   Dustin, Lynn B ^k   Ho, Ling Pei ^a   Thompson, Fiona M ^a   Ramamurthy, Narayan ^a   Mongkolsapaya, Juthathip ^b,g   Willberg, Christian B ^a,h   Screaton, Gavin R ^b   Klenerman, Paul ^a,h   Barnes, Eleanor ^a   Ball, Jonathan ^l   Burgess, Gary ^m   Cooke, Graham ^b   Dillon, John ⁿ   Gore, Charles ^o   Foster, Graham ^p   Guha, Neil ^l   Halford, Rachel ^o   Herath, Cham ^q   Holmes, Chris ^r   Howe, Anita ^s   Hudson, Emma ^a   Irving, William ^l   Khakoo, Salim ^t   Koletzki, Diana ^u   Martin, Natasha ^v   Mbisa, Tamyo ^w   McKeating, Jane ^j   McLauchlan, John ^x   Miners, Alec ^y   Murray, Andrea ^z   Shaw, Peter ^aa   Simmonds, Peter ^a   Spencer, Chris ^ab   Targett Adams, Paul ^ac   Thomson, Emma ^x   Vickerman, Peter ^ad   Zitzmann, Nicole ^r   more..

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d KHON KAEN HOSPITAL   (Thailand)

^e Songkhla Hospital   (Thailand)

^f NATIONAL SCIENCE AND TECHNOLOGY DEVELOPMENT AGENCY   (Thailand)

^g MAHIDOL UNIVERSITY   (Thailand)

^h JOHN RADCLIFFE HOSPITAL   (United Kingdom)

ⁱ SAN BORTOLO HOSPITAL   (Italy)

^j UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^k UNIVERSITY OF OXFORD   (United Kingdom)

^l UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^m Wright Fleming Institute ^*  (United States)

ⁿ UNIVERSITY OF DUNDEE   (United Kingdom)

^o Hepatitis C Trust   (United Kingdom)

^p QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^q Stockley Park   (United Kingdom)

^r UNIVERSITY OF OXFORD   (United Kingdom)

^s ST PAUL S HOSPITAL   (Canada)

^t UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^u JANSSEN RESEARCH FOUNDATION   (Belgium)

^v UNIVERSITY OF CALIFORNIA   (United States)

^w PUBLIC HEALTH ENGLAND   (United Kingdom)

^x UNIVERSITY OF GLASGOW   (United Kingdom)

^y LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^z NOTTINGHAM CITY HOSPITAL   (United Kingdom)

^aa MERCK RESEARCH LABORATORIES   (United States)

^ab UNIVERSITY OF OXFORD   (United Kingdom)

^ac MEDIVIR AB   (Sweden)

^ad UNIVERSITY OF BRISTOL   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; ANTIVIRUS AGENT; BETA INTERFERON; CD161 ANTIGEN; CD38 ANTIGEN; CD69 ANTIGEN; GAMMA INTERFERON; GRANZYME B; INTERLEUKIN 12; INTERLEUKIN 15; INTERLEUKIN 18; MESSENGER RNA; T LYMPHOCYTE RECEPTOR; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 8; CYTOKINE;

BACTERIUM; CELLS AND CELL COMPONENTS; DENGUE FEVER; DISEASE SEVERITY; HEPATITIS; IMMUNIZATION; INFECTIOUS DISEASE; INFLUENZA; LIGAND; VIRUS;

ANTIVIRAL THERAPY; ARTICLE; CD8+ T LYMPHOCYTE; DENGUE; DISEASE SEVERITY; FLOW CYTOMETRY; HEPATITIS C; HUMAN; HUMAN CELL; INFLUENZA; MUCOSAL ASSOCIATED INVARIANT T LYMPHOCYTE; NONHUMAN; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TREATMENT RESPONSE; UPREGULATION; VIRUS REPLICATION; ADULT; CELL CULTURE; COCULTURE; FEMALE; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; MALE; METABOLISM; MONONUCLEAR CELL; MUCOSAL-ASSOCIATED INVARIANT T CELL; PHYSIOLOGY; VIRUS INFECTION;

BACTERIA (MICROORGANISMS); DENGUE VIRUS; HEPATITIS C VIRUS; ORTHOMYXOVIRIDAE;

ADULT; CELLS, CULTURED; COCULTURE TECHNIQUES; CYTOKINES; FEMALE; HUMANS; LEUKOCYTES, MONONUCLEAR; LYMPHOCYTE ACTIVATION; MALE; MUCOSAL-ASSOCIATED INVARIANT T CELLS; VIRUS DISEASES;

EID: 84975705227     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms11653     Document Type: Article

References (65)

1. Porcelli, S., Yockey, C. E., Brenner, M. B. & Balk, S. P. 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. 178, 1-16 (1993).
2. 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. 189, 1907-1921 (1999).
3. Dusseaux, M. et al. Human MAIT cells are xenobiotic-resistant, tissue-targeted, CD161hi IL-17-secreting T cells. Blood 117, 1250-1259 (2011).
4. Treiner, E. et al. Selection of evolutionarily conserved mucosal-associated invariant T cells by MR1. Nature 422, 164-169 (2003).
5. Tang, X.-Z. et al. IL-7 licenses activation of human liver intrasinusoidal mucosal-associated invariant T cells. J. Immunol. 190, 3142-3152 (2013).
6. Martin, E. et al. Stepwise development of MAIT cells in mouse and human. PLoS Biol. 7, e54 (2009).
7. Kjer-Nielsen, L. et al. MR1 presents microbial Vitamin B metabolites to MAIT cells. Nature 491, 717-723 (2012).
8. Corbett, A. J. et al. T-cell activation by transitory neo-antigens derived from distinct microbial pathways. Nature 509, 361-365 (2014).
9. Georgel, P., Radosavljevic, M., Macquin, C. & Bahram, S. The nonconventional MHC class I MR1 molecule controls infection by Klebsiella pneumoniae in mice. Mol. Immunol. 48, 769-775 (2011).
10. Chua, W.-J. et al. Polyclonal MAIT Cells have unique innate functions in bacterial infection. Infect. Immun. 80, 3256-3267 (2012).
11. Rahimpour, A. et al. Identification of phenotypically and functionally heterogeneous mouse mucosal-associated invariant T cells using MR1 tetramers. J. Exp. Med. 212, 1095-1108 (2015).
12. + T cells, including the MAIT cell subset, are specifically activated by IL-12+IL-18 in a TCR-independent manner. Eur. J. Immunol. 44, 195-203 (2014).
13. Billerbeck, E. et al. Analysis of CD161 expression on human CD8+ T cells defines a distinct functional subset with tissue-homing properties. Proc. Natl Acad. Sci. USA 107, 3006-3011 (2010).
14. Takahashi, T., Dejbakhsh-Jones, S. & Strober, S. Expression of CD161 (NKR-P1A) defines subsets of human CD4 and CD8 T cells with different functional activities. J. Immunol. 176, 211-216 (2006).
15. Lanier, L. L., Chang, C. & Phillips, J. H. Human NKRP1A. A disulfide-linked homodimer of the C-type lectin superfamily expressed by a subset of NK and T lymphocytes. J. Immunol. 153, 2417-2428 (1994).
16. Fergusson, J. R. et al. CD161 defines a transcriptional and functional phenotype shared across distinct human T cell lineages. Cell Rep. 9, 1075-1088 (2014).
17. Ivanov, I. I. et al. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 126, 1121-1133 (2006).
18. Singh, S. P. et al. PLZF regulates CCR6 and is critical for the acquisition and maintenance of the Th17 phenotype in human cells. J. Immunol. 194, 4350-4361 (2015).
19. Savage, A. K. et al. The transcription factor PLZF directs the effector program of the NKT cell lineage. Immunity 29, 391-403 (2008).
20. Gleimer, M., von Boehmer, H. & Kreslavsky, T. PLZF controls the expression of a limited number of genes essential for NKT cell function. Front. Immunol. 3, 374 (2012).
21. Patel, O. et al. Recognition of Vitamin B metabolites by mucosal-associated invariant T cells. Nat. Commun. 4, 2142 (2013).
22. Kurioka, A. et al. MAIT cells are licensed through granzyme exchange to kill bacterially sensitized targets. Mucosal Immunol. 8, 429-440 (2015).
23. Le Bourhis, L., Dusseaux, M. & Bohineust, A. MAIT cells detect and efficiently lyse bacterially-infected epithelial cells. PLoS Pathog. 9, e1003681 (2013).
24. Jo, J. et al. Toll-like receptor 8 agonist and bacteria trigger potent activation of innate immune cells in human liver. PLoS Pathog. 10, e1004210 (2014).
25. Sattler, A., Dang-Heine, C., Reinke, P. & Babel, N. IL-15 dependent induction of IL-18 secretion as a feedback mechanism controlling human MAIT-cell effector functions. Eur. J. Immunol. 45, 2286-2298 (2015).
26. Chattergoon, M. A. et al. HIV and HCV activate the inflammasome in monocytes and macrophages via endosomal Toll-like receptors without induction of type 1 interferon. PLoS Pathog. 10, e1004082 (2014).
27. Hidmark, A. S. et al. Early alpha/beta interferon production by myeloid dendritic cells in response to UV-inactivated virus requires viral entry and interferon regulatory factor 3 but not MyD88. J. Virol. 79, 10376-10385 (2005).
28. Short, K. R., Brooks, A. G., Reading, P. C. & Londrigan, S. L. The fate of influenza A virus after infection of human macrophages and dendritic cells. J. Gen. Virol. 93, 2315-2325 (2012).
29. Marukian, S. et al. Cell culture-produced hepatitis C virus does not infect peripheral blood mononuclear cells. Hepatology 48, 1843-1850 (2008).
30. van Wilgenburg, B., Browne, C., Vowles, J. & Cowley, S. A. Efficient, long term production of monocyte-derived macrophages from human pluripotent stem cells under partly-defined and fully-defined conditions. PLoS ONE 8, e71098 (2013).
31. Stonier, S. W. & Schluns, K. S. Trans-presentation: a novel mechanism regulating IL-15 delivery and responses. Immunol. Lett. 127, 85-92 (2010).
32. Liang, Z. et al. Activation of Toll-like receptor 3 impairs the dengue virus serotype 2 replication through induction of IFN-b in cultured hepatoma cells. PLoS ONE 6, e23346 (2011).
33. García-Sastre, A. Induction and evasion of type I interferon responses by influenza viruses. Virus Res. 162, 12-18 (2011).
34. Castet, V. et al. Alpha interferon inhibits hepatitis C virus replication in primary human hepatocytes infected in vitro. J. Virol. 76, 8189-8199 (2002).
35. Symons, J. A., Alcamí, A. & Smith, G. L. Vaccinia virus encodes a soluble type I interferon receptor of novel structure and broad species specificity. Cell 81, 551-560 (1995).
36. Foster, G. R. et al. Efficacy of sofosbuvir plus ribavirin with or without peginterferon-alfa in patients with HCV genotype 3 infection and treatmentexperienced patients with cirrhosis and HCV genotype 2 infection. Gastroenterology 149, 1462-1470 (2015).
37. Le Bourhis, L. et al. Antimicrobial activity of mucosal-associated invariant T cells. Nat. Immunol. 11, 701-708 (2010).
38. Cosgrove, C. et al. Early and nonreversible decrease of CD161++/MAIT cells in HIV infection. Blood 121, 951-961 (2013).
39. Reilly, E. C., Wands, J. R. & Brossay, L. Cytokine dependent and independent iNKT cell activation. Cytokine 51, 227-231 (2010).
40. Paget, C. et al. Potential role of invariant NKT cells in the control of pulmonary inflammation and CD8+ T cell response during acute influenza A virus H3N2 pneumonia. J. Immunol. 186, 5590-5602 (2011).
41. Cui, Y. et al. Mucosal-associated invariant T cell-rich congenic mouse strain allows functional evaluation. J. Clin. Invest. 125, 4171-4185 (2015).
42. Reantragoon, R. et al. Antigen-loaded MR1 tetramers define T cell receptor heterogeneity in mucosal-associated invariant T cells. J. Exp. Med. 210, 2305-2320 (2013).
43. Leeansyah, E. et al. Activation, exhaustion, and persistent decline of the antimicrobial MR1-restricted MAIT-cell population in chronic HIV-1 infection. Blood 121, 1124-1135 (2013).
44. Fernandez, C. S. et al. MAIT cells are depleted early but retain functional cytokine expression in HIV infection. Immunol. Cell Biol. 93, 177-188 (2015).
45. Gherardin, N. A. et al. Diversity of T cells restricted by the MHC class i-related molecule MR1 facilitates differential antigen recognition. Immunity 44, 32-45 (2016).
46. Fergusson, J. R. et al. CD161 defines a transcriptional and functional phenotype across distinct human T cell lineages. Cell Rep. 9, 1075-1088 (2014).
47. Matikainen, S. et al. IFN-alpha and IL-18 synergistically enhance IFN-gamma production in human NK cells: differential regulation of Stat4 activation and IFN-gamma gene expression by IFN-alpha and IL-12. Eur. J. Immunol. 31, 2236-2245 (2001).
48. Jian, Y.-R., Chang, S.-Y., Lin, P.-Y., Yang, Y.-H. & Chuang, Y.-H. Inactivated influenza virus vaccine is efficient and reduces IL-4 and IL-6 in allergic asthma mice. Influenza Other Respi. Viruses 7, 1210-1217 (2013).
49. Thimme, R. Determinants of viral clearance and persistence during acute hepatitis C virus infection. J. Exp. Med. 194, 1395-1406 (2001).
50. Guidotti, L. G. Viral clearance without destruction of infected cells during acute HBV infection. Science 284, 825-829 (1999).
51. Pang, T., Cardosa, M. J. & Guzman, M. G. Of cascades and perfect storms: the immunopathogenesis of dengue haemorrhagic fever-dengue shock syndrome (DHF/DSS). Immunol. Cell Biol. 85, 43-45 (2007).
52. Wang, S. et al. Influenza virus-cytokine-protease cycle in the pathogenesis of vascular hyperpermeability in severe influenza. J. Infect. Dis. 202, 991-1001 (2010).
53. Murray, R. J. et al. Community-acquired pneumonia due to pandemic A(H1N1)2009 influenzavirus and methicillin resistant Staphylococcus aureus co-infection. PLoS ONE 5, e8705 (2010).
54. Morens, D. M., Taubenberger, J. K. & Fauci, A. S. Predominant role of bacterial pneumonia as a cause of death in pandemic influenza: implications for pandemic influenza preparedness. J. Infect. Dis. 198, 962-970 (2008).
55. Gérart, S. et al. Human iNKT and MAIT cells exhibit a PLZF-dependent proapoptotic propensity that is counterbalanced by XIAP. Blood 121, 614-623 (2013).
56. Fergusson, J. R., Fleming, V. M. & Klenerman, P. CD161-expressing human T cells. Front. Immunol. 2, 36 (2011).
57. Tsai, C.-Y. et al. Type I IFNs and IL-18 regulate the antiviral response of primary human γδ T cells against dendritic cells infected with Dengue virus. J. Immunol. 194, 3890-3900 (2015).
58. Fergusson, J. R. et al. CD161(int)CD8+ T cells: a novel population of highly functional, memory CD8+ T cells enriched within the gut. Mucosal Immunol. 9, 401-413 (2015).
59. Denney, L. et al. Reduction of natural killer but not effector CD8 T lymphocytes in three consecutive cases of severe/lethal H1N1/09 influenza A virus infection. PLoS ONE 5, e10675 (2010).
60. Zhao, Y. et al. High levels of virus-specific CD4+ T cells predict severe pandemic influenza A virus infection. Am. J. Respir. Crit. Care Med. 186, 1292-1297 (2012).
61. Foster, G. et al. Treatment of decompensated HCV cirrhosis in patients with diverse genotypes: 12 weeks sofosbuvir and NS5A inhibitors with/without ribavirin is effective in HCV genotypes 1 and 3. J. Hepatol. 62 (2015).
62. Pietschmann, T. et al. Construction and characterization of infectious intragenotypic and intergenotypic hepatitis C virus chimeras. Proc. Natl Acad. Sci. USA 103, 7408-7413 (2006).
63. Lindenbach, B. D. et al. Complete replication of hepatitis C virus in cell culture. Science 309, 623-626 (2005).
64. Hutchinson, E. C. et al. Conserved and host-specific features of influenza virion architecture. Nat. Commun. 5, 4816 (2014).
65. Hutchinson, E. C. et al. Mapping the phosphoproteome of influenza A and B viruses by mass spectrometry. PLoS Pathog. 8, e1002993 (2012).