Identification of phenotypically and functionally heterogeneous mouse mucosal-associated invariant T cells using MR1 tetramers

Journal of Experimental Medicine

Volumn 212, Issue 7, 2015, Pages 1095-1108

  Rahimpour, Azad ^a   Koay, Hui Fern ^a   Enders, Anselm ^b   Clanchy, Rhiannon ^a   Eckle, Sidonia B G ^a   Meehan, Bronwyn ^a   Chen, Zhenjun ^a   Whittle, Belinda ^c   Liu, Ligong ^d   Fairlie, David P ^d   Goodnow, Chris C ^b   McCluskey, James ^a   Rossjohn, Jamie ^e,f   Uldrich, Adam P ^a   Pellicci, Daniel G ^a   Godfrey, Dale I ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^c Biology and Environment   (Australia)

^d UNIVERSITY OF QUEENSLAND   (Australia)

^e MONASH UNIVERSITY   (Australia)

^f CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 4; MR 1 ANTIGEN TETRAMER; PROMYELOCYTIC LEUKEMIA PROTEIN; RETINOID RELATED ORPHAN RECEPTOR GAMMA; T LYMPHOCYTE RECEPTOR; TETRAMER; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; CYTOKINE; HLA ANTIGEN CLASS 1; KRUPPEL LIKE FACTOR; LYMPHOCYTE ANTIGEN RECEPTOR; MR1 PROTEIN, MOUSE; ZBTB16 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN BINDING; ARTICLE; CD4 CD8 RATIO; CELL HETEROGENEITY; CELL SURFACE; CELLULAR DISTRIBUTION; CYTOKINE PRODUCTION; HUMAN; MOUSE; MUCOSAL ASSOCIATED INVARIANT T CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CELL PROLIFERATION; CYTOLOGY; HISTOLOGY; IMMUNOLOGY; METABOLISM; MUCOSA; NATURAL KILLER T CELL; SPECIES DIFFERENCE;

ANIMALS; CELL PROLIFERATION; CYTOKINES; HISTOCOMPATIBILITY ANTIGENS CLASS I; HISTOLOGICAL TECHNIQUES; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MUCOUS MEMBRANE; NATURAL KILLER T-CELLS; RECEPTORS, ANTIGEN, T-CELL; SPECIES SPECIFICITY;

EID: 84944872887     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20142110     Document Type: Article

References (42)

1. Birkinshaw, R.W., L. Kjer-Nielsen, S.B. Eckle, J. McCluskey, and J. Rossjohn. 2014. MAITs, MR1 and vitamin B metabolites. Curr. Opin. Immunol. 26:7-13. http://dx.doi.org/10.1016/j.coi.2013.09.007
2. Corbett, A.J., S.B. Eckle, R.W. Birkinshaw, L. Liu, O. Patel, J. Mahony, Z. Chen, R. Reantragoon, B. Meehan, H. Cao, et al. 2014. T-cell activation by transitory neo-antigens derived from distinct microbial pathways. Nature. 509:361-365. http://dx.doi.org/10.1038/nature13160
3. α19i T cells regulate autoimmune inflammation. Nat. Immunol. 7:987-994. http://dx.doi.org/10.1038/ni1370
4. Dash, P., J.L. McClaren, T.H. Oguin III, W. Rothwell, B. Todd, M.Y. Morris, J. Becksfort, C. Reynolds, S.A. Brown, P.C. Doherty, and P.G. Thomas. 2011. Paired analysis of TCRα and TCRβ chains at the singlecell level in mice. J. Clin. Invest. 121:288-295. http://dx.doi.org/10.1172/ JCI44752
5. Dusseaux, M., E. Martin, N. Serriari, I. Péguillet, V. Premel, D. Louis, M. Milder, L. Le Bourhis, C. Soudais, E. Treiner, and O. Lantz. 2011. Human MAIT cells are xenobiotic-resistant, tissue-targeted, CD161hi IL-17-secreting T cells. Blood. 117:1250-1259. http://dx.doi.org/10 .1182/blood-2010-08-303339
6. Eckle, S.B., R.W. Birkinshaw, L. Kostenko, A.J. Corbett, H.E. McWilliam, R. Reantragoon, Z. Chen, N.A. Gherardin, T. Beddoe, L. Liu, et al. 2014.A molecular basis underpinning the T cell receptor heterogeneity of mucosal-associated invariant T cells. J. Exp. Med. 211:1585-1600. http:// dx.doi.org/10.1084/jem.20140484
7. Geissmann, F., T.O. Cameron, S. Sidobre, N. Manlongat, M. Kronenberg, M.J. Briskin, M.L. Dustin, and D.R. Littman. 2005. Intravascular immune surveillance by CXCR6+ NKT cells patrolling liver sinusoids. PLoS Biol. 3:e113. http://dx.doi.org/10.1371/journal.pbio.0030113
8. Godfrey, D.I., S. Stankovic, and A.G. Baxter. 2010. Raising the NKT cell family. Nat. Immunol. 11:197-206. http://dx.doi.org/10.1038/ni.1841
9. Gold, M.C., S. Cerri, S. Smyk-Pearson, M.E. Cansler, T.M. Vogt, J. Delepine, E. Winata, G.M. Swarbrick, W.J. Chua, Y.Y. Yu, et al. 2010. Human mucosal associated invariant T cells detect bacterially infected cells. PLoS Biol. 8:e1000407. http://dx.doi.org/10.1371/journal.pbio.1000407
10. Gold, M.C., J.E. McLaren, J.A. Reistetter, S. Smyk-Pearson, K. Ladell, G.M. Swarbrick, Y.Y. Yu, T.H. Hansen, O. Lund, M. Nielsen, et al. 2014. MR1- restricted MAIT cells display ligand discrimination and pathogen selectivity through distinct T cell receptor usage. J. Exp. Med. 211:1601-1610. http://dx.doi.org/10.1084/jem.20140507
11. Kawachi, I., J. Maldonado, C. Strader, and S. Gilfillan. 2006. MR1-restricted Vα19i mucosal-associated invariant T cells are innate T cells in the gut lamina propria that provide a rapid and diverse cytokine response. J. Immunol. 176:1618-1627. http://dx.doi.org/10.4049/jimmunol.176.3.1618
12. Kjer-Nielsen, L., O. Patel, A.J. Corbett, J. Le Nours, B. Meehan, L. Liu, M. Bhati, Z. Chen, L. Kostenko, R. Reantragoon, et al. 2012. MR1 presents microbial vitamin B metabolites to MAIT cells. Nature. 491:717-723. http://dx.doi.org/10.1038/nature11605
13. Kovalovsky, D., O.U. Uche, S. Eladad, R.M. Hobbs, W. Yi, E. Alonzo, K. Chua, M. Eidson, H.J. Kim, J.S. Im, et al. 2008. The BTB-zinc finger transcriptional regulator PLZF controls the development of invariant natural killer T cell effector functions. Nat. Immunol. 9:1055-1064. http://dx.doi.org/10.1038/ni.1641
14. Kreslavsky, T., A.K. Savage, R. Hobbs, F. Gounari, R. Bronson, P. Pereira, P.P. Pandolfi, A. Bendelac, and H. von Boehmer. 2009. TCR-inducible PLZF transcription factor required for innate phenotype of a subset of γσ T cells with restricted TCR diversity. Proc. Natl. Acad. Sci. USA. 106:12453-12458. http://dx.doi.org/10.1073/pnas.0903895106
15. Le Bourhis, L., E. Martin, I. Péguillet, A. Guihot, N. Froux, M. Coré, E. Lévy, M. Dusseaux, V. Meyssonnier, V. Premel, et al. 2010. Antimicrobial activity of mucosal-associated invariant T cells. Nat. Immunol. 11:701-708. (published erratum appears in Nat. Immunol. 2010. 11:969) http://dx.doi .org/10.1038/ni.1890
16. Le Bourhis, L., Y.K. Mburu, and O. Lantz. 2013. MAIT cells, surveyors of a new class of antigen: development and functions. Curr. Opin. Immunol. 25:174-180. http://dx.doi.org/10.1016/j.coi.2013.01.005
17. Lee, Y.J., K.L. Holzapfel, J. Zhu, S.C. Jameson, and K.A. Hogquist. 2013. Steady-state production of IL-4 modulates immunity in mouse strains and is determined by lineage diversity of iNKT cells. Nat. Immunol. 14:1146-1154. http://dx.doi.org/10.1038/ni.2731
18. Leeansyah, E., L. Loh, D.F. Nixon, and J.K. Sandberg. 2014. Acquisition of innate-like microbial reactivity in mucosal tissues during human fetal MAIT-cell development. Nat. Commun. 5:3143. http://dx.doi.org/10 .1038/ncomms4143
19. Lepore, M., A. Kalinichenko, A. Colone, B. Paleja, A. Singhal, A. Tschumi, B. Lee, M. Poidinger, F. Zolezzi, L. Quagliata, et al. 2014. Parallel T-cell cloning and deep sequencing of human MAIT cells reveal stable oligoclonal TCRβ repertoire. Nat. Commun. 5:3866. (published erratum appears in Nat. Commun. 2014. 5:4493) http://dx.doi.org/10.1038/ncomms4866
20. Martin, E., E. Treiner, L. Duban, L. Guerri, H. Laude, C. Toly, V. Premel, A. Devys, I.C. Moura, F. Tilloy, et al. 2009. Stepwise development of MAIT cells in mouse and human. PLoS Biol. 7:e54. http://dx.doi.org/ 10.1371/journal.pbio.1000054
21. McWilliam, H.E., R.W. Birkinshaw, J.A. Villadangos, J. McCluskey, and J. Rossjohn. 2015. MR1 presentation of vitamin B-based metabolite ligands. Curr. Opin. Immunol. 34:28-34. http://dx.doi.org/10.1016/ j.coi.2014.12.004
22. Meierovics, A., W.J. Yankelevich, and S.C. Cowley. 2013. MAIT cells are critical for optimal mucosal immune responses during in vivo pulmonary bacterial infection. Proc. Natl. Acad. Sci. USA. 110:E3119-E3128. http://dx.doi.org/10.1073/pnas.1302799110
23. Miyazaki, Y., S. Miyake, A. Chiba, O. Lantz, and T. Yamamura. 2011. Mucosalassociated invariant T cells regulate Th1 response in multiple sclerosis. Int. Immunol. 23:529-535. http://dx.doi.org/10.1093/intimm/dxr047
24. Okamoto, N., O. Kanie, Y.Y. Huang, R. Fujii, H. Watanabe, and M. Shimamura. 2005. Synthetic α-mannosyl ceramide as a potent stimulant for an NKT cell repertoire bearing the invariant Vα19-Jα26 TCR α chain. Chem. Biol. 12:677-683. http://dx.doi.org/10.1016/ j.chembiol.2005.04.014
25. Patel, O., L. Kjer-Nielsen, J. Le Nours, S.B. Eckle, R. Birkinshaw, T. Beddoe, A.J. Corbett, L. Liu, J.J. Miles, B. Meehan, et al. 2013. Recognition of vitamin B metabolites by mucosal-associated invariant T cells. Nat. Commun. 4:2142. http://dx.doi.org/10.1038/ncomms3142
26. + CD1d-dependent precursor stage. J. Exp. Med. 195:835-844. http://dx.doi.org/10.1084/ jem.20011544
27. Pellicci, D.G., O. Patel, L. Kjer-Nielsen, S.S. Pang, L.C. Sullivan, K. Kyparissoudis, A.G. Brooks, H.H. Reid, S. Gras, I.S. Lucet, et al. 2009. Differential recognition of CD1d-α-galactosyl ceramide by the Vβ8.2 and Vβ7 semi-invariant NKT T cell receptors. Immunity. 31:47-59. http://dx.doi.org/10.1016/j.immuni.2009.04.018
28. + αβ T cells develop and expand in the absence of Itk. J. Immunol. 193:673-687. http://dx.doi.org/ 10.4049/jimmunol.1302058
29. Reantragoon, R., L. Kjer-Nielsen, O. Patel, Z. Chen, P.T. Illing, M. Bhati, L. Kostenko, M. Bharadwaj, B. Meehan, T.H. Hansen, et al. 2012. Structural insight into MR1-mediated recognition of the mucosal associated invariant T cell receptor. J. Exp. Med. 209:761-774. http:// dx.doi.org/10.1084/jem.20112095
30. Reantragoon, R., A.J. Corbett, I.G. Sakala, N.A. Gherardin, J.B. Furness, Z. Chen, S.B. Eckle, A.P. Uldrich, R.W. Birkinshaw, O. Patel, et al.
31. Antigen-loaded MR1 tetramers define T cell receptor heterogeneity in mucosal-associated invariant T cells. J. Exp. Med. 210:2305- 2320. http://dx.doi.org/10.1084/jem.20130958
32. Rossjohn, J., S. Gras, J.J. Miles, S.J. Turner, D.I. Godfrey, and J. McCluskey.
33. T cell antigen receptor recognition of antigen-presenting molecules. Annu. Rev. Immunol. 33:169-200. http://dx.doi.org/10.1146/annurevimmunol- 032414-112334
34. Savage, A.K., M.G. Constantinides, J. Han, D. Picard, E. Martin, B. Li, O. Lantz, and A. Bendelac. 2008. The transcription factor PLZF directs the effector program of the NKT cell lineage. Immunity. 29:391-403. http://dx.doi.org/10.1016/j.immuni.2008.07.011
35. Seach, N., L. Guerri, L. Le Bourhis, Y. Mburu, Y. Cui, S. Bessoles, C. Soudais, and O. Lantz. 2013. Double-positive thymocytes select mucosal-associated invariant T cells. J. Immunol. 191:6002-6009. http://dx.doi.org/10.4049/ jimmunol.1301212
36. Tang, X.Z., J. Jo, A.T. Tan, E. Sandalova, A. Chia, K.C. Tan, K.H. Lee, A.J. Gehring, G. De Libero, and A. Bertoletti. 2013. IL-7 licenses activation of human liver intrasinusoidal mucosal-associated invariant T cells. J. Immunol. 190:3142-3152. http://dx.doi.org/10.4049/jimmunol .1203218
37. Teunissen, M.B., N.G. Yeremenko, D.L. Baeten, S. Chielie, P.I. Spuls, M.A. de Rie, O. Lantz, and P.C. Res. 2014. The IL-17A-producing CD8+ T-cell population in psoriatic lesional skin comprises mucosaassociated invariant T cells and conventional T cells. J. Invest. Dermatol. 134:2898-2907. http://dx.doi.org/10.1038/jid.2014.261
38. Tilloy, F., E. Treiner, S.H. Park, C. Garcia, F. Lemonnier, H. de la Salle, A. Bendelac, M. Bonneville, and O. Lantz. 1999. An invariant T cell receptor α chain defines a novel TAP-independent major histocompatibility complex class Ib-restricted α/β T cell subpopulation in mammals. J. Exp. Med. 189:1907-1921. http://dx.doi.org/10.1084/jem.189 .12.1907
39. Treiner, E., L. Duban, S. Bahram, M. Radosavljevic, V. Wanner, F. Tilloy, P. Affaticati, S. Gilfillan, and O. Lantz. 2003. Selection of evolutionarily conserved mucosal-associated invariant T cells by MR1. Nature. 422:164-169. http://dx.doi.org/10.1038/nature01433
40. Ussher, J.E., P. Klenerman, and C.B. Willberg. 2014. Mucosal-associated invariant T-cells: new players in anti-bacterial immunity. Front. Immunol. 5:450. http://dx.doi.org/10.3389/fimmu.2014.00450
41. + T cells. Blood. 119:422-433. http://dx.doi.org/10.1182/ blood-2011-05-353789
42. Weigmann, B., I. Tubbe, D. Seidel, A. Nicolaev, C. Becker, and M.F. Neurath. 2007. Isolation and subsequent analysis of murine lamina propria mononuclear cells from colonic tissue. Nat. Protoc. 2:2307-2311. http://dx.doi.org/10.1038/nprot.2007.315