CD161++CD8+ T cells, including the MAIT cell subset, are specifically activated by IL-12+IL-18 in a TCR-independent manner

European Journal of Immunology

Volumn 44, Issue 1, 2014, Pages 195-203

  Ussher, James E ^a   Bilton, Matthew ^a   Attwod, Emma ^a   Shadwell, Jonathan ^a   Richardson, Rachel ^a   de Lara, Catherine ^a   Mettke, Elisabeth ^a   Kurioka, Ayako ^a   Hansen, Ted H ^b   Klenerman, Paul ^a,c   Willberg, Christian B ^a,c  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c JOHN RADCLIFFE HOSPITAL   (United Kingdom)

Author keywords

CD161++ T cells; IL 12; IL 18; MAIT cells; T cells

Indexed keywords

CD161 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 18; T LYMPHOCYTE RECEPTOR; T LYMPHOCYTE RECEPTOR ALPHA CHAIN; CD8 ANTIGEN; INTERLEUKIN 18 RECEPTOR; LYMPHOCYTE ANTIGEN RECEPTOR; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY B;

ARTICLE; BACTERIUM; CD161++ CD8+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; IMMUNOPHENOTYPING; IMMUNOSTIMULATION; MUCOSAL ASSOCIATED INVARIANT T LYMPHOCYTE; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; CELL LINE; CELL SEPARATION; DRUG EFFECTS; FLOW CYTOMETRY; HUMAN; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; MUCOSA; NATURAL KILLER T CELL;

ANTIGENS, CD8; CELL LINE; CELL SEPARATION; FLOW CYTOMETRY; HUMANS; INTERFERON-GAMMA; INTERLEUKIN-12; INTERLEUKIN-18; LYMPHOCYTE ACTIVATION; MUCOUS MEMBRANE; NATURAL KILLER T-CELLS; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY B; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; RECEPTORS, INTERLEUKIN-18; T-LYMPHOCYTE SUBSETS;

EID: 84892453502     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201343509     Document Type: Article

References (43)

1. Walker, L. J., Kang, Y.-H., Smith, M. O., Tharmalingham, H., Ramamurthy, N., Fleming, V., Sahgal, N. et al., Human MAIT and CD8αα cells develop from a pool of type-17 pre-committed CD8+ T cells. Blood 2011. 119: 422-433.
2. Treiner, E. and Lantz, O., CD1d- and MR1-restricted invariant T cells: of mice and men. Curr. Opin. Immunol. 2006. 18: 519-526.
3. Tilloy, F., Treiner, E., Park, S. H., Garcia, C., Lemonnier, F., la Salle de, H., Bendelac, A. 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.
4. Treiner, E., Duban, L., Bahram, S., Radosavljevic, M., Wanner, V., Tilloy, F., Affaticati, P. et al., Selection of evolutionarily conserved mucosal-associated invariant T cells by MR1. Nature 2003. 422: 164-169.
5. Huang, S., Gilfillan, S., Cella, M., Miley, M. J., Lantz, O., Lybarger, L., Fremont, D. H. et al., Evidence for MR1 antigen presentation to mucosal-associated invariant T cells. J. Biol. Chem. 2005. 280: 21183-21193.
6. Chua, W.-J., Kim, S., Myers, N., Huang, S., Yu, L., Fremont, D. H., Diamond, M. S. et al., Endogenous MHC-related protein 1 is transiently expressed on the plasma membrane in a conformation that activates mucosal-associated invariant T cells. J. Immunol. 2011. 186: 4744-4750.
7. Reantragoon, R., Kjer-Nielsen, L., Patel, O., Chen, Z., Illing, P. T., Bhati, M., Kostenko, L. et al., Structural insight into MR1-mediated recognition of the mucosal associated invariant T cell receptor. J. Exp. Med. 2012. 209: 761-774.
8. Le Bourhis, L., Martin, E., Péguillet, I., Guihot, A., Froux, N., Coré, M., Lévy, E. et al., Antimicrobial activity of mucosal-associated invariant T cells. Nat. Immunol. 2010. 11: 701-708.
9. Miley, M. J., Truscott, S. M., Yu, Y. Y. L., Gilfillan, S., Fremont, D. H., Hansen, T. H. and Lybarger, L., Biochemical features of the MHC-related protein 1 consistent with an immunological function. J. Immunol. 2003. 170: 6090-6098.
10. Kjer-Nielsen, L., Patel, O., Corbett, A. J., Le Nours, J., Meehan, B., Liu, L., Bhati, M. et al., MR1 presents microbial vitamin B metabolites to MAIT cells. Nature 2012. 491: 1-9.
11. Tang, X.-Z., Jo, J., Tan, A. T., Sandalova, E., Chia, A., Tan, K. C., Lee, K. H. et al., IL-7 licenses activation of human liver intrasinusoidal mucosal-associated invariant T cells. J. Immunol. 2013. 190: 3142-3152.
12. Billerbeck, E., Kang, Y.-H., Walker, L., Lockstone, H., Grafmueller, S., Fleming, V., Flint, J. et al., Analysis of CD161 expression on human CD8+ T cells defines a distinct functional subset with tissue-homing properties. Proc. Natl. Acad. Sci. 2010. 107: 3006-3011.
13. Georgel, P., Radosavljevic, M., Macquin, C. and Bahram, S., The non-conventional MHC class I MR1 molecule controls infection by Klebsiella pneumoniae in mice. Mol. Immunol. 2011. 48: 769-775.
14. Chua, W. J., Truscott, S. M., Eickhoff, C. S., Blazevic, A., Hoft, D. F. and Hansen, T. H., Polyclonal MAIT cells have unique innate functions in bacterial infection. Infect. Immun. 2012. 80: 3256-3267.
15. Gold, M. C., Cerri, S., Smyk-Pearson, S., Cansler, M. E., Vogt, T. M., Delepine, J., Winata, E. et al., Human mucosal associated invariant T cells detect bacterially infected cells. PLoS Biol. 2010. 8: e1000407.
16. Oo, Y. H., Banz, V., Kavanagh, D., Liaskou, E., Withers, D. R., Humphreys, E., Reynolds, G. M. et al., CXCR3-dependent recruitment and CCR6-mediated positioning of Th-17 cells in the inflamed liver. J. Hepatol. 2012. 57: 1044-1051.
17. Annibali, V., Ristori, G., Angelini, D. F., Serafini, B., Mechelli, R., Cannoni, S., Romano, S. et al., CD161highCD8+T cells bear pathogenetic potential in multiple sclerosis. Brain 2011. 134: 542-554.
18. Gunderson, A. J., Mohammed, J., Horvath, F. J., Podolsky, M. A., Anderson, C. R. and Glick, A. B., CD8(+) T cells mediate RAS-induced psoriasis-like skin inflammation through IFN-γ. J. Invest. Dermatol. 2013. 133: 955-963.
19. Gorski, K. S., Waller, E. L., Bjornton-Severson, J., Hanten, J. A., Riter, C. L., Kieper, W. C., Gorden, K. B. et al., Distinct indirect pathways govern human NK-cell activation by TLR-7 and TLR-8 agonists. Int. Immunol. 2006. 18: 1115-1126.
20. Micallef, M. J., Ohtsuki, T., Kohno, K., Tanabe, F., Ushio, S., Namba, M., Tanimoto, T. et al., Interferon-gamma-inducing factor enhances T helper 1 cytokine production by stimulated human T cells: synergism with interleukin-12 for interferon-gamma production. Eur. J. Immunol. 1996. 26: 1647-1651.
21. Kohno, K., Kataoka, J., Ohtsuki, T., Suemoto, Y., Okamoto, I., Usui, M., Ikeda, M. et al., IFN-gamma-inducing factor (IGIF) is a costimulatory factor on the activation of Th1 but not Th2 cells and exerts its effect independently of IL-12. J. Immunol. 1997. 158: 1541-1550.
22. Ariel, A., Novick, D., Rubinstein, M., Dinarello, C. A., Lider, O. and Hershkoviz, R., IL-12 and IL-18 induce MAP kinase-dependent adhesion of T cells to extracellular matrix components. J. Leukocyte Biol. 2002. 72: 192-198.
23. Fagundes, C. T., Costa, V. V., Cisalpino, D., Amaral, F. A., Souza, P. R. S., Souza, R. S., Ryffel, B. et al., IFN-γ production depends on IL-12 and IL-18 combined action and mediates host resistance to dengue virus infection in a nitric oxide-dependent manner. PLoS Negl. Trop. Dis. 2011. 5: e1449.
24. Pirhonen, J., Matikainen, S. and Julkunen, I., Regulation of virus-induced IL-12 and IL-23 expression in human macrophages. J. Immunol. 2002. 169: 5673-5678.
25. Rintahaka, J., Wiik, D., Kovanen, P. E., Alenius, H. and Matikainen, S., Cytosolic antiviral RNA recognition pathway activates caspases 1 and 3. J. Immunol. 2008. 180: 1749-1757.
26. Lee, M. S. and Kim, Y.-J., Signaling pathways downstream of pattern-recognition receptors and their cross talk. Annu. Rev. Biochem. 2007. 76: 447-480.
27. Takeda, K., Kaisho, T. and Akira, S., Toll-like receptors. Annu. Rev. Immunol. 2003. 21: 335-376.
28. Bachmann, M., Horn, K., Poleganov, M. A., Paulukat, J., Nold, M., Pfeilschifter, J. and Mühl, H., Interleukin-18 secretion and Th1-like cytokine responses in human peripheral blood mononuclear cells under the influence of the toll-like receptor-5 ligand flagellin. Cell. Microbiol. 2006. 8: 289-300.
29. Ghayur, T., Banerjee, S., Hugunin, M., Butler, D., Herzog, L., Carter, A., Quintal, L. et al., Caspase-1 processes IFN-gamma-inducing factor and regulates LPS-induced IFN-gamma production. Nature 1997. 386: 619-623.
30. Okamura, H., Tsutsi, H., Komatsu, T., Yutsudo, M., Hakura, A., Tanimoto, T., Torigoe, K. et al., Cloning of a new cytokine that induces IFN-gamma production by T cells. Nature 1995. 378: 88-91.
31. Otani, T., Nakamura, S., Toki, M., Motoda, R., Kurimoto, M. and Orita, K., Identification of IFN-gamma-producing cells in IL-12/IL-18-treated mice. Cell Immunol. 1999. 198: 111-119.
32. Cheung, H., Chen, N.-J., Cao, Z., Ono, N., Ohashi, P. S. and Yeh, W.-C., Accessory protein-like is essential for IL-18-mediated signaling. J. Immunol. 2005. 174: 5351-5357.
33. Cosgrove, C., Ussher, J. E., Rauch, A., Gärtner, K., Kurioka, A., Hühn, M. H., Adelmann, K. et al., Early and nonreversible decrease of CD161++/MAIT cells in HIV infection. Blood 2013. 121: 951-961.
34. Tada, H., Aiba, S., Shibata, K.-I., Ohteki, T. and Takada, H., Synergistic effect of Nod1 and Nod2 agonists with toll-like receptor agonists on human dendritic cells to generate interleukin-12 and T helper type 1 cells. Infect. Immun. 2005. 73: 7967-7976.
35. Seki, E., Tsutsui, H., Nakano, H., Tsuji, N., Hoshino, K., Adachi, O., Adachi, K. et al., Lipopolysaccharide-induced IL-18 secretion from murine Kupffer cells independently of myeloid differentiation factor 88 that is critically involved in induction of production of IL-12 and IL-1beta. J. Immunol. 2001. 166: 2651-2657.
36. Humann, J. and Lenz, L. L., Activation of naive NK cells in response to Listeria monocytogenes requires IL-18 and contact with infected dendritic cells. J. Immunol. 2010. 184: 5172-5178.
37. Kannan, Y., Yu, J., Raices, R. M., Seshadri, S., Wei, M., Caligiuri, M. A. and Wewers, M. D., IκBζ augments IL-12- and IL-18-mediated IFN-γ production in human NK cells. Blood 2011. 117: 2855-2863.
38. Nakahira, M., Tomura, M., Iwasaki, M., Ahn, H. J., Bian, Y., Hamaoka, T., Ohta, T. et al., An absolute requirement for STAT4 and a role for IFN-gamma as an amplifying factor in IL-12 induction of the functional IL-18 receptor complex. J. Immunol. 2001. 167: 1306-1312.
39. Barbulescu, K., Becker, C., Schlaak, J. F., Schmitt, E., Meyer zum Büschenfelde, K. H. and Neurath, M. F., IL-12 and IL-18 differentially regulate the transcriptional activity of the human IFN-gamma promoter in primary CD4+ T lymphocytes. J. Immunol. 1998. 160: 3642-3647.
40. Tyznik, A. J., Tupin, E., Nagarajan, N. A., Her, M. J., Benedict, C. A. and Kronenberg, M., Cutting edge: the mechanism of invariant NKT cell responses to viral danger signals. J. Immunol. 2008. 181: 4452-4456.
41. Szkaradkiewicz, A., Jopek, A. and Wysocki, J., Effects of IL-12 and IL-18 on HBcAg-specific cytokine production by CD4 T lymphocytes of children with chronic hepatitis B infection. Antiviral Res. 2005. 66: 23-27.
42. Schvoerer, E., Navas, M. C., Thumann, C., Fuchs, A., Meyer, N., Habersetzer, F. and Stoll-Keller, F., Production of interleukin-18 and interleukin-12 in patients suffering from chronic hepatitis C virus infection before antiviral therapy. J. Med. Virol. 2003. 70: 588-593.
43. Miyazaki, Y., Miyake, S., Chiba, A., Lantz, O. and Yamamura, T., Mucosal-associated invariant T cells regulate Th1 response in multiple sclerosis. Int. Immunol. 2011. 23: 529-535.