Diversity of T Cells Restricted by the MHC Class I-Related Molecule MR1 Facilitates Differential Antigen Recognition

Immunity

Volumn 44, Issue 1, 2016, Pages 32-45

  Gherardin, Nicholas A ^a,b   Keller, Andrew N ^c   Woolley, Rachel E ^c   Le Nours, Jérôme ^c   Ritchie, David S ^a,b   Neeson, Paul J ^b   Birkinshaw, Richard W ^c   Eckle, Sidonia B G ^a   Waddington, John N ^a   Liu, Ligong ^d   Fairlie, David P ^d   Uldrich, Adam P ^a   Pellicci, Daniel G ^a   McCluskey, James ^a   Godfrey, Dale I ^a   Rossjohn, Jamie ^c,e  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b PETER MACCALLUM CANCER CENTRE   (Australia)

^c MONASH UNIVERSITY   (Australia)

^d UNIVERSITY OF QUEENSLAND   (Australia)

^e CARDIFF UNIVERSITY SCHOOL OF MEDICINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FOLIC ACID; MAJOR HISTOCOMPATIBILITY COMPLEX CLASS I RELATED MOLECULE; PEPTIDES AND PROTEINS; PROTEIN CDR3BETA; PROTEIN TRAVI1 2; RIBOFLAVIN DERIVATIVE; UNCLASSIFIED DRUG; HLA ANTIGEN CLASS 1; LYMPHOCYTE ANTIGEN RECEPTOR; MR1 PROTEIN, HUMAN;

ANTIGEN RECOGNITION; ARTICLE; BLOOD; HUMAN; HUMAN CELL; IMMUNOREACTIVITY; MUCOSAL ASSOCIATED INVARIANT T CELL; NORMAL HUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN STRUCTURE; T LYMPHOCYTE; ANTIGEN PRESENTATION; AUTOIMMUNITY; CHEMISTRY; FLOW CYTOMETRY; IMMUNOLOGY; JURKAT CELL LINE; LYMPHOCYTE ACTIVATION; MUCOSAL IMMUNITY; SURFACE PLASMON RESONANCE; T LYMPHOCYTE SUBPOPULATION; X RAY CRYSTALLOGRAPHY;

ANTIGEN PRESENTATION; AUTOIMMUNITY; CRYSTALLOGRAPHY, X-RAY; FLOW CYTOMETRY; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; IMMUNITY, MUCOSAL; JURKAT CELLS; LYMPHOCYTE ACTIVATION; RECEPTORS, ANTIGEN, T-CELL; SURFACE PLASMON RESONANCE; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES;

EID: 84958878687     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2015.12.005     Document Type: Article

References (35)

1. Adams P.D., Afonine P.V., Bunkóczi G., Chen V.B., Davis I.W., Echols N., Headd J.J., Hung L.W., Kapral G.J., Grosse-Kunstleve R.W., et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 2010, 66:213-221.
2. Birkinshaw R.W., Kjer-Nielsen L., Eckle S.B., McCluskey J., Rossjohn J. MAITs, MR1 and vitamin B metabolites. Curr. Opin. Immunol. 2014, 26:7-13.
3. Chen V.B., Arendall W.B., Headd J.J., Keedy D.A., Immormino R.M., Kapral G.J., Murray L.W., Richardson J.S., Richardson D.C. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 2010, 66:12-21.
4. Corbett A.J., Eckle S.B., Birkinshaw R.W., Liu L., Patel O., Mahony J., Chen Z., Reantragoon R., Meehan B., Cao H., et al. T-cell activation by transitory neo-antigens derived from distinct microbial pathways. Nature 2014, 509:361-365.
5. Dash P., McClaren J.L., Oguin T.H., Rothwell W., Todd B., Morris M.Y., Becksfort J., Reynolds C., Brown S.A., Doherty P.C., Thomas P.G. Paired analysis of TCRα and TCRβ chains at the single-cell level in mice. J. Clin. Invest. 2011, 121:288-295.
6. Dusseaux M., Martin E., Serriari N., Péguillet I., Premel V., Louis D., Milder M., Le Bourhis L., Soudais C., Treiner E., Lantz O. Human MAIT cells are xenobiotic-resistant, tissue-targeted, CD161hi IL-17-secreting T cells. Blood 2011, 117:1250-1259.
7. Eckle S.B., Birkinshaw R.W., Kostenko L., Corbett A.J., McWilliam H.E., Reantragoon R., Chen Z., Gherardin N.A., Beddoe T., Liu L., et al. A molecular basis underpinning the T cell receptor heterogeneity of mucosal-associated invariant T cells. J. Exp. Med. 2014, 211:1585-1600.
8. Emsley P., Lohkamp B., Scott W.G., Cowtan K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 2010, 66:486-501.
9. Gold M.C., Cerri S., Smyk-Pearson S., Cansler M.E., Vogt T.M., Delepine J., Winata E., Swarbrick G.M., Chua W.J., Yu Y.Y., et al. Human mucosal associated invariant T cells detect bacterially infected cells. PLoS Biol. 2010, 8:e1000407.
10. Gold M.C., Eid T., Smyk-Pearson S., Eberling Y., Swarbrick G.M., Langley S.M., Streeter P.R., Lewinsohn D.A., Lewinsohn D.M. Human thymic MR1-restricted MAIT cells are innate pathogen-reactive effectors that adapt following thymic egress. Mucosal Immunol. 2013, 6:35-44.
11. Gold M.C., McLaren J.E., Reistetter J.A., Smyk-Pearson S., Ladell K., Swarbrick G.M., Yu Y.Y., Hansen T.H., Lund O., Nielsen M., 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.
12. Holst J., Szymczak-Workman A.L., Vignali K.M., Burton A.R., Workman C.J., Vignali D.A. Generation of T-cell receptor retrogenic mice. Nat. Protoc. 2006, 1:406-417.
13. Kabsch W. Xds. Acta Crystallogr. D Biol. Crystallogr. 2010, 66:125-132.
14. Kjer-Nielsen L., Clements C.S., Brooks A.G., Purcell A.W., McCluskey J., Rossjohn J. The 1.5 A crystal structure of a highly selected antiviral T cell receptor provides evidence for a structural basis of immunodominance. Structure 2002, 10:1521-1532.
15. Kjer-Nielsen L., Patel O., Corbett A.J., Le Nours J., Meehan B., Liu L., Bhati M., Chen Z., Kostenko L., Reantragoon R., et al. MR1 presents microbial vitamin B metabolites to MAIT cells. Nature 2012, 491:717-723.
16. Kurioka A., Ussher J.E., Cosgrove C., Clough C., Fergusson J.R., Smith K., Kang Y.H., Walker L.J., Hansen T.H., Willberg C.B., Klenerman P. MAIT cells are licensed through granzyme exchange to kill bacterially sensitized targets. Mucosal Immunol. 2015, 8:429-440.
17. Le Bourhis L., Martin E., Péguillet I., Guihot A., Froux N., Coré M., Lévy E., Dusseaux M., Meyssonnier V., Premel V., et al. Antimicrobial activity of mucosal-associated invariant T cells. Nat. Immunol. 2010, 11:701-708.
18. Lissina A., Ladell K., Skowera A., Clement M., Edwards E., Seggewiss R., van den Berg H.A., Gostick E., Gallagher K., Jones E., et al. Protein kinase inhibitors substantially improve the physical detection of T-cells with peptide-MHC tetramers. J. Immunol. Methods 2009, 340:11-24.
19. Martin E., Treiner E., Duban L., Guerri L., Laude H., Toly C., Premel V., Devys A., Moura I.C., Tilloy F., et al. Stepwise development of MAIT cells in mouse and human. PLoS Biol. 2009, 7:e54.
20. Matulis G., Sanderson J.P., Lissin N.M., Asparuhova M.B., Bommineni G.R., Schümperli D., Schmidt R.R., Villiger P.M., Jakobsen B.K., Gadola S.D. Innate-like control of human iNKT cell autoreactivity via the hypervariable CDR3beta loop. PLoS Biol. 2010, 8:e1000402.
21. McCoy A.J., Grosse-Kunstleve R.W., Adams P.D., Winn M.D., Storoni L.C., Read R.J. Phaser crystallographic software. J. Appl. Cryst. 2007, 40:658-674.
22. Patel O., Kjer-Nielsen L., Le Nours J., Eckle S.B., Birkinshaw R., Beddoe T., Corbett A.J., Liu L., Miles J.J., Meehan B., et al. Recognition of vitamin B metabolites by mucosal-associated invariant T cells. Nat. Commun. 2013, 4:2142.
23. Rahimpour A., Koay H.F., Enders A., Clanchy R., Eckle S.B.G., Meehan B., Chen Z., Whittle B., Liu L., Fairlie D.P., et al. Identification of phenotypically and functionally heterogeneous mouse mucosal-associated invariant T cells using MR1 tetramers. J. Exp. Med. 2015, 212:1095-1108.
24. Reantragoon R., Kjer-Nielsen L., Patel O., Chen Z., Illing P.T., Bhati M., Kostenko L., Bharadwaj M., Meehan B., Hansen T.H., et al. Structural insight into MR1-mediated recognition of the mucosal associated invariant T cell receptor. J. Exp. Med. 2012, 209:761-774.
25. Reantragoon R., Corbett A.J., Sakala I.G., Gherardin N.A., Furness J.B., Chen Z., Eckle S.B., Uldrich A.P., Birkinshaw R.W., Patel O., et al. Antigen-loaded MR1 tetramers define T cell receptor heterogeneity in mucosal-associated invariant T cells. J. Exp. Med. 2013, 210:2305-2320.
26. Rossjohn J., Gras S., Miles J.J., Turner S.J., Godfrey D.I., McCluskey J. T cell antigen receptor recognition of antigen-presenting molecules. Annu. Rev. Immunol. 2015, 33:169-200.
27. Salio M., Silk J.D., Jones E.Y., Cerundolo V. Biology of CD1- and MR1-restricted T cells. Annu. Rev. Immunol. 2014, 32:323-366.
28. Tang X.Z., Jo J., Tan A.T., Sandalova E., Chia A., Tan K.C., Lee K.H., Gehring A.J., De Libero G., Bertoletti A. IL-7 licenses activation of human liver intrasinusoidal mucosal-associated invariant T cells. J. Immunol. 2013, 190:3142-3152.
29. Tilloy F., Treiner E., Park S.H., Garcia C., Lemonnier F., de la Salle H., Bendelac A., Bonneville M., Lantz O. 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.
30. Treiner E., Duban L., Bahram S., Radosavljevic M., Wanner V., Tilloy F., Affaticati P., Gilfillan S., Lantz O. Selection of evolutionarily conserved mucosal-associated invariant T cells by MR1. Nature 2003, 422:164-169.
31. Uldrich A.P., Le Nours J., Pellicci D.G., Gherardin N.A., McPherson K.G., Lim R.T., Patel O., Beddoe T., Gras S., Rossjohn J., Godfrey D.I. CD1d-lipid antigen recognition by the γδ TCR. Nat. Immunol. 2013, 14:1137-1145.
32. Ussher J.E., Bilton M., Attwod E., Shadwell J., Richardson R., de Lara C., Mettke E., Kurioka A., Hansen T.H., Klenerman P., Willberg C.B. 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, 44:195-203.
33. Ussher J.E., Klenerman P., Willberg C.B. Mucosal-associated invariant T-cells: new players in anti-bacterial immunity. Front. Immunol. 2014, 5:450.
34. Wang G.C., Dash P., McCullers J.A., Doherty P.C., Thomas P.G. T cell receptor αβ diversity inversely correlates with pathogen-specific antibody levels in human cytomegalovirus infection. Sci. Transl. Med. 2012, 4:128ra42.
35. Winn M.D., Ballard C.C., Cowtan K.D., Dodson E.J., Emsley P., Evans P.R., Keegan R.M., Krissinel E.B., Leslie A.G., McCoy A., et al. Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 2011, 67:235-242.