The molecular bases of δ/αβ T cell-mediated antigen recognition

Journal of Experimental Medicine

Volumn 211, Issue 13, 2014, Pages 2599-2615

  Pellicci, Daniel G ^a   Uldrich, Adam P ^a   Le Nours, Jérôme ^b   Ross, Fiona ^a   Chabrol, Eric ^b   Eckle, Sidonia B G ^a   de Boer, Renate ^c   Lim, Ricky T ^a   McPherson, Kirsty ^a   Besra, Gurdyal ^d   Howell, Amy R ^e   Moretta, Lorenzo ^f   McCluskey, James ^a   Heemskerk, Mirjam H M ^c   Gras, Stephanie ^b   Rossjohn, Jamie ^b,g   Godfrey, Dale I ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^d UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^e UNIVERSITY OF CONNECTICUT   (United States)

^f G GASLINI INSTITUTE   (Italy)

^g CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA GALACTOSYLCERAMIDE; GLUCOSYLCERAMIDE; HLA ANTIGEN; SILVER; ALPHA-GALACTOSYLCERAMIDE; CD1D ANTIGEN; GALACTOSYLCERAMIDE; LIPID; LYMPHOCYTE ANTIGEN RECEPTOR; PEPTIDE;

ANTIGEN RECOGNITION; ARTICLE; CELLS BY BODY ANATOMY; CONTROLLED STUDY; CROSS REACTION; CRYSTAL STRUCTURE; FLOW CYTOMETRY; GAMMA DELTA T LYMPHOCYTE; GENE EXPRESSION; GENE LOCUS; HUMAN; HUMAN CELL; IMMUNE SYSTEM; NATURAL KILLER T CELL; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; AMINO ACID SEQUENCE; CELL CLONE; CHEMICAL STRUCTURE; CHEMISTRY; IMMUNOLOGY; JURKAT CELL LINE; LYMPHOCYTE ACTIVATION; MOLECULAR GENETICS; T LYMPHOCYTE;

AMINO ACID SEQUENCE; ANTIGENS, CD1D; CLONE CELLS; GALACTOSYLCERAMIDES; HUMANS; JURKAT CELLS; LIPIDS; LYMPHOCYTE ACTIVATION; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDES; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; T-LYMPHOCYTES;

EID: 84930416297     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20141764     Document Type: Article

References (54)

1. Amir, A.L., D.M. van der Steen, R.S. Hagedoorn, M.G. Kester, C.A. van Bergen, J.W. Drijfhout, A.H. de Ru, J.H. Falkenburg, P.A. van Veelen, and M.H. Heemskerk. 2011. Allo-HLA-reactive T cells inducing graftversus- host disease are single peptide specific. Blood. 118:6733-6742. http://dx.doi.org/10.1182/blood-2011-05-354787
2. Bhati, M., D.K. Cole, J. McCluskey, A.K. Sewell, and J. Rossjohn. 2014. The versatility of the αβ T-cell antigen receptor. Protein Sci. 23:260-272. http://dx.doi.org/10.1002/pro.2412
3. 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
4. Borg, N.A., L.K. Ely, T. Beddoe, W.A. Macdonald, H.H. Reid, C.S. Clements, A.W. Purcell, L. Kjer-Nielsen, J.J. Miles, S.R. Burrows, et al. 2005. The CDR3 regions of an immunodominant T cell receptor dictate the 'energetic landscape' of peptide-MHC recognition. Nat. Immunol. 6:171-180. http://dx.doi.org/10.1038/ni1155
5. Borg, N.A., K.S. Wun, L. Kjer-Nielsen, M.C. Wilce, D.G. Pellicci, R. Koh, G.S. Besra, M. Bharadwaj, D.I. Godfrey, J. McCluskey, and J. Rossjohn. 2007. CD1d-lipid-antigen recognition by the semi-invariant NKT T-cell receptor. Nature. 448:44-49. http://dx.doi.org/10.1038/nature05907
6. Born, W.K., M. Kemal Aydintug, and R.L. O'Brien. 2013. Diversity of γδ T-cell antigens. Cell. Mol. Immunol. 10:13-20. http://dx.doi.org/10.1038/cmi.2012.45
7. Bowen, S., P. Sun, F. Livak, S. Sharrow, and R.J. Hodes. 2014. A novel T cell subset with trans-rearranged Vγ-Cβ TCRs shows Vβ expression is dispensable for lineage choice and MHC restriction. J. Immunol. 192:169-177. http://dx.doi.org/10.4049/jimmunol.1302398
8. Bricogne, G., E. Blanc, M. Brandl, C. Flensburg, P. Keller, W. Paciorek, P. Roversi, A. Sharff, O.S. Smart, C. Vonrhein, and T.O. Womack. 2011. autoBUSTER, Version 1.6.0. Global Phasing Ltd, Cambridge, UK. Available at: https://www.globalphasing.com/buster/(accessed June 29, 2014).
9. Brigl, M., and M.B. Brenner. 2004. CD1: antigen presentation and T cell function. Annu. Rev. Immunol. 22:817-890. http://dx.doi.org/10.1146/annurev.immunol.22.012703.104608
10. Brossay, L., O. Naidenko, N. Burdin, J. Matsuda, T. Sakai, and M. Kronenberg. 1998. Structural requirements for galactosylceramide recognition by CD1-restricted NK T cells. J. Immunol. 161:5124-5128.
11. Burrows, S.R., Z. Chen, J.K. Archbold, F.E. Tynan, T. Beddoe, L. Kjer- Nielsen, J.J. Miles, R. Khanna, D.J. Moss, Y.C. Liu, et al. 2010. Hard wiring of T cell receptor specificity for the major histocompatibility complex is underpinned by TCR adaptability. Proc. Natl. Acad. Sci. USA. 107:10608-10613. http://dx.doi.org/10.1073/pnas.1004926107
12. Ciofani, M., and J.C. Zúñiga-Pflücker. 2010. Determining γδ versus αß T cell development. Nat. Rev. Immunol. 10:657-663.
13. Clements, C.S., L. Kjer-Nielsen, W.A. MacDonald, A.G. Brooks, A.W. Purcell, J. McCluskey, and J. Rossjohn. 2002. The production, purification and crystallization of a soluble heterodimeric form of a highly selected T-cell receptor in its unliganded and liganded state. Acta Crystallogr. D Biol. Crystallogr. 58:2131-2134. http://dx.doi.org/10.1107/S0907444902015482
14. 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
15. DeLano, W.L. 2002. The PyMOL Molecular Graphics System. Available at: http://www.pymol.org (accessed June 29, 2014).
16. 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
17. Emsley, P., B. Lohkamp, W.G. Scott, and K. Cowtan. 2010. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66:486-501. http://dx.doi.org/10.1107/S0907444910007493
18. Gapin, L. 2014. Check MAIT. J. Immunol. 192:4475-4480. http://dx.doi.org/10.4049/jimmunol.1400119
19. Girardi, E., and D.M. Zajonc. 2012. Molecular basis of lipid antigen presentation by CD1d and recognition by natural killer T cells. Immunol. Rev. 250:167-179. http://dx.doi.org/10.1111/j.1600-065X.2012.01166.x
20. Girardi, E., I. Maricic, J. Wang, T.T. Mac, P. Iyer, V. Kumar, and D.M. Zajonc. 2012. Type II natural killer T cells use features of both innatelike and conventional T cells to recognize sulfatide self antigens. Nat. Immunol. 13:851-856. http://dx.doi.org/10.1038/ni.2371
21. Godfrey, D.I., J. McCluskey, and J. Rossjohn. 2005. CD1d antigen presentation: treats for NKT cells. Nat. Immunol. 6:754-756. http://dx.doi.org/10.1038/ni0805-754
22. Godfrey, D.I., J. Rossjohn, and J. McCluskey. 2008. The fidelity, occasional promiscuity, and versatility of T cell receptor recognition. Immunity. 28:304-314. http://dx.doi.org/10.1016/j.immuni.2008.02.004
23. Gras, S., S.R. Burrows, L. Kjer-Nielsen, C.S. Clements, Y.C. Liu, L.C. Sullivan, M.J. Bell, A.G. Brooks, A.W. Purcell, J. McCluskey, and J. Rossjohn. 2009. The shaping of T cell receptor recognition by selftolerance. Immunity. 30:193-203. http://dx.doi.org/10.1016/j.immuni.2008.11.011
24. Gras, S., Z. Chen, J.J. Miles, Y.C. Liu, M.J. Bell, L.C. Sullivan, L. Kjer- Nielsen, R.M. Brennan, J.M. Burrows, M.A. Neller, et al. 2010. Allelic polymorphism in the T cell receptor and its impact on immune responses. J. Exp. Med. 207:1555-1567. http://dx.doi.org/10.1084/jem.20100603
25. Gras, S., S.R. Burrows, S.J. Turner, A.K. Sewell, J. McCluskey, and J. Rossjohn. 2012. A structural voyage toward an understanding of the MHC-I-restricted immune response: lessons learned and much to be learned. Immunol. Rev. 250:61-81. http://dx.doi.org/10.1111/j.1600-065X.2012.01159.x
26. Hedrick, S.M., D.I. Cohen, E.A. Nielsen, and M.M. Davis. 1984. Isolation of cDNA clones encoding T cell-specific membrane-associated proteins. Nature. 308:149-153. http://dx.doi.org/10.1038/308149a0
27. Hochstenbach, F., and M.B. Brenner. 1989. T-cell receptor δ-chain can substitute for α to form a βα heterodimer. Nature. 340:562-565. http://dx.doi.org/10.1038/340562a0
28. Kabsch, W. 2010. Xds. Acta Crystallogr. D Biol. Crystallogr. 66:125-132. http://dx.doi.org/10.1107/S0907444909047337
29. Kjer-Nielsen, L., N.A. Borg, D.G. Pellicci, T. Beddoe, L. Kostenko, C.S. Clements, N.A. Williamson, M.J. Smyth, G.S. Besra, H.H. Reid, et al. 2006. A structural basis for selection and cross-species reactivity of the semi-invariant NKT cell receptor in CD1d/glycolipid recognition. J. Exp. Med. 203:661-673. http://dx.doi.org/10.1084/jem.20051777
30. 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.
31. Koch, M., V.S. Stronge, D. Shepherd, S.D. Gadola, B. Mathew, G. Ritter, A.R. Fersht, G.S. Besra, R.R. Schmidt, E.Y. Jones, and V. Cerundolo. 2005. The crystal structure of human CD1d with and without α-galactosylceramide. Nat. Immunol. 6:819-826. http://dx.doi.org/10.1038/ni1225
32. Lefranc, M.P., and T.H. Rabbitts. 1990. Genetic organization of the human T-cell receptor γ and δ loci. Res. Immunol. 141:565-577. http://dx.doi.org/10.1016/0923-2494(90)90058-7
33. Luoma, A.M., C.D. Castro, T. Mayassi, L.A. Bembinster, L. Bai, D. Picard, B. Anderson, L. Scharf, J.E. Kung, L.V. Sibener, et al. 2013. Crystal structure of Vδ1 T cell receptor in complex with CD1d-sulfatide shows MHC-like recognition of a self-lipid by human γδ T cells. Immunity. 39:1032-1042. http://dx.doi.org/10.1016/j.immuni.2013.11.001
34. Mangan, B.A., M.R. Dunne, V.P. O'Reilly, P.J. Dunne, M.A. Exley, D. O'Shea, E. Scotet, A.E. Hogan, and D.G. Doherty. 2013. Cutting edge: CD1d restriction and Th1/Th2/Th17 cytokine secretion by human Vδ3 T cells. J. Immunol. 191:30-34. http://dx.doi.org/10.4049/jimmunol.1300121
35. Matulis, G., J.P. Sanderson, N.M. Lissin, M.B. Asparuhova, G.R. Bommineni, D. Schümperli, R.R. Schmidt, P.M. Villiger, B.K. Jakobsen, and S.D. Gadola. 2010. Innate-like control of human iNKT cell autoreactivity via the hypervariable CDR3β loop. PLoS Biol. 8:e1000402. http://dx.doi.org/10.1371/journal.pbio.1000402
36. Miossec, C., F. Faure, L. Ferradini, S. Roman-Roman, S. Jitsukawa, S. Ferrini, A. Moretta, F. Triebel, and T. Hercend. 1990. Further analysis of the T cell receptor gamma/delta+ peripheral lymphocyte subset. The V delta 1 gene segment is expressed with either C alpha or C delta. J. Exp. Med. 171:1171-1188. http://dx.doi.org/10.1084/jem.171.4.1171
37. Miossec, C., A. Caignard, L. Ferradini, S. Roman-Roman, F. Faure, H. Michalaki, F. Triebel, and T. Hercend. 1991. Molecular characterization of human T cell receptor γδ chains including a Vδ1-encoded variable segment. Eur. J. Immunol. 21:1061-1064. http://dx.doi.org/10.1002/eji.1830210430
38. O'Brien, R.L., C.L. Roark, N. Jin, M.K. Aydintug, J.D. French, J.L. Chain, J.M. Wands, M. Johnston, and W.K. Born. 2007. γδ T-cell receptors: functional correlations. Immunol. Rev. 215:77-88. http://dx.doi.org/10.1111/j.1600-065X.2006.00477.x
39. Patel, O., D.G. Pellicci, S. Gras, M.L. Sandoval-Romero, A.P. Uldrich, T. Mallevaey, A.J. Clarke, J. Le Nours, A. Theodossis, S.L. Cardell, et al. 2012. Recognition of CD1d-sulfatide mediated by a type II natural killer T cell antigen receptor. Nat. Immunol. 13:857-863. http://dx.doi.org/10.1038/ni.2372
40. 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
41. 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
42. Peyrat, M.A., F. Davodeau, I. Houde, F. Romagné, A. Necker, C. Leget, J.P. Cervoni, N. Cerf-Bensussan, H. Vié, M. Bonneville, et al. 1995. Repertoire analysis of human peripheral blood lymphocytes using a human V delta 3 region-specific monoclonal antibody. Characterization of dual T cell receptor (TCR) delta-chain expressors and alpha beta T cells expressing V delta 3J alpha C alpha-encoded TCR chains. J. Immunol. 155:3060-3067.
43. 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
44. Rossjohn, J., D.G. Pellicci, O. Patel, L. Gapin, and D.I. Godfrey. 2012. Recognition of CD1d-restricted antigens by natural killer T cells. Nat. Rev. Immunol. 12:845-857. http://dx.doi.org/10.1038/nri3328
45. Sandstrom, A., C.M. Peigné, A. Léger, J.E. Crooks, F. Konczak, M.C. Gesnel, R. Breathnach, M. Bonneville, E. Scotet, and E.J. Adams. 2014. The intracellular B30.2 domain of butyrophilin 3A1 binds phosphoantigens to mediate activation of human Vγ9Vδ2 T cells. Immunity. 40:490-500. http://dx.doi.org/10.1016/j.immuni.2014.03.003
46. Scott-Browne, J.P., J.L. Matsuda, T. Mallevaey, J. White, N.A. Borg, J. McCluskey, J. Rossjohn, J. Kappler, P. Marrack, and L. Gapin. 2007. Germline-encoded recognition of diverse glycolipids by natural killer T cells. Nat. Immunol. 8:1105-1113. http://dx.doi.org/10.1038/ni1510
47. Turner, S.J., P.C. Doherty, J. McCluskey, and J. Rossjohn. 2006. Structural determinants of T-cell receptor bias in immunity. Nat. Rev. Immunol. 6:883-894. http://dx.doi.org/10.1038/nri1977
48. Uldrich, A.P., J. Le Nours, D.G. Pellicci, N.A. Gherardin, K.G. McPherson, R.T. Lim, O. Patel, T. Beddoe, S. Gras, J. Rossjohn, and D.I. Godfrey. 2013. CD1d-lipid antigen recognition by the γδ TCR. Nat. Immunol. 14:1137-1145. http://dx.doi.org/10.1038/ni.2713
49. Vantourout, P., and A. Hayday. 2013. Six-of-the-best: unique contributions of γδ T cells to immunology. Nat. Rev. Immunol. 13:88-100. http://dx.doi.org/10.1038/nri3384
50. Vavassori, S., A. Kumar, G.S. Wan, G.S. Ramanjaneyulu, M. Cavallari, S. El Daker, T. Beddoe, A. Theodossis, N.K. Williams, E. Gostick, et al. 2013. Butyrophilin 3A1 binds phosphorylated antigens and stimulates human γδ T cells. Nat. Immunol. 14:908-916. http://dx.doi.org/10.1038/ni.2665
51. Wang, G.C., P. Dash, J.A. McCullers, P.C. Doherty, and P.G. Thomas. 2012. T cell receptor αβ diversity inversely correlates with pathogenspecific antibody levels in human cytomegalovirus infection. Sci. Transl. Med. 4:128ra42. http://dx.doi.org/10.1126/scitranslmed.3003647
52. Wun, K.S., G. Cameron, O. Patel, S.S. Pang, D.G. Pellicci, L.C. Sullivan, S. Keshipeddy, M.H. Young, A.P. Uldrich, M.S. Thakur, et al. 2011. A molecular basis for the exquisite CD1d-restricted antigen specificity and functional responses of natural killer T cells. Immunity. 34:327-339. http://dx.doi.org/10.1016/j.immuni.2011.02.001
53. Wun, K.S., F. Ross, O. Patel, G.S. Besra, S.A. Porcelli, S.K. Richardson, S. Keshipeddy, A.R. Howell, D.I. Godfrey, and J. Rossjohn. 2012. Human and mouse type I natural killer T cell antigen receptors exhibit different fine specificities for CD1d-antigen complex. J. Biol. Chem. 287:39139-39148. http://dx.doi.org/10.1074/jbc. M112.412320
54. Xiong, N., and D.H. Raulet. 2007. Development and selection of γδ T cells. Immunol. Rev. 215:15-31. http://dx.doi.org/10.1111/j.1600-065X.2006.00478.x