The Vα14 invariant natural killer T cell TCR forces microbial glycolipids and CD1d into a conserved binding mode

Journal of Experimental Medicine

Volumn 207, Issue 11, 2010, Pages 2383-2393

  Li, Yali ^a   Girardi, Enrico ^a   Wang, Jing ^a   Yu, Esther Dawen ^a   Painter, Gavin F ^b   Kronenberg, Mitchell ^a   Zajonc, Dirk M ^a  

^a LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^b CALLAGHAN INNOVATION   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA GALACTOSYLCERAMIDE; CD1D ANTIGEN; GLYCOLIPID; T LYMPHOCYTE RECEPTOR;

ARTICLE; BINDING AFFINITY; CELL STRUCTURE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION;

ANTIGENS, BACTERIAL; ANTIGENS, CD1D; BORRELIA BURGDORFERI; GALACTOSYLCERAMIDES; HUMANS; NATURAL KILLER T-CELLS; PROTEIN STRUCTURE, QUATERNARY; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 78149305888     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20101335     Document Type: Article

References (44)

1. + T cells. Curr. Opin. Immunol. 7:367-374. doi:10.1016/0952-7915(95)80112-X
2. Bendelac, A., P.B. Savage, and L. Teyton. 2007. The biology of NKT cells. Annu. Rev. Immunol. 25:297-336. doi:10.1146/annurev.immunol.25.022106.141711
3. 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. doi:10.1038/nature05907
4. Brigl, M., and M.B. Brenner. 2004. CD1: antigen presentation and T cell function. Annu. Rev. Immunol. 22:817-890. doi:10.1146/annurev.immunol.22.012703. 104608
5. Cantu, C. III, K. Benlagha, P.B. Savage, A. Bendelac, and L. Teyton. 2003. The paradox of immune molecular recognition of alpha-galactosylceramide: low affinity, low specificity for CD1d, high affinity for alpha beta TCRs. J. Immunol. 170:4673-4682.
6. Collaborative Computational Project Number 4. 1994. The CCP4 Suite: Programs for protein crystallography. Acta Crystallogr. 50:760-763.
7. Emsley, P., and K. Cowtan. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60:2126-2132. doi:10.1107/S0907444904019158
8. Florence, W.C., C. Xia, L.E. Gordy, W. Chen, Y. Zhang, J. Scott-Browne, Y. Kinjo, K.O. Yu, S. Keshipeddy, D.G. Pellicci, et al. 2009. Adaptability of the semi-invariant natural killer T-cell receptor towards structurally diverse CD1d-restricted ligands. EMBO J. 28:3781. doi:10.1038/emboj.2009.348
9. Fox, L.M., D.G. Cox, J.L. Lockridge, X. Wang, X. Chen, L. Scharf, D.L. Trott, R.M. Ndonye, N. Veerapen, G.S. Besra, et al. 2009. Recognition of lyso-phospholipids by human natural killer T lymphocytes. PLoS Biol. 7:e1000228. doi:10.1371/journal.pbio.1000228
10. Godfrey, D.I., D.G. Pellicci, O. Patel, L. Kjer-Nielsen, J. McCluskey, and J. Rossjohn. 2010. Antigen recognition by CD1d-restricted NKT T cell receptors. Semin. Immunol. 22:61-67. doi:10.1016/j.smim.2009.10.004
11. Kawano, T., J. Cui, Y. Koezuka, I. Toura, Y. Kaneko, K. Motoki, H. Ueno, R. Nakagawa, H. Sato, E. Kondo, et al. 1997. CD1d-restricted and TCR-mediated activation of valpha14 NKT cells by glycosylceramides. Science. 278:1626-1629. doi:10.1126/science.278.5343.1626
12. Kinjo, Y., D. Wu, G. Kim, G.W. Xing, M.A. Poles, D.D. Ho, M. Tsuji, K. Kawahara, C.H. Wong, and M. Kronenberg. 2005. Recognition of bacterial glycosphingolipids by natural killer T cells. Nature. 434:520-525. doi:10.1038/nature03407
13. Kinjo, Y., E. Tupin, D. Wu, M. Fujio, R. Garcia-Navarro, M.R. Benhnia, D.M. Zajonc, G. Ben-Menachem, G.D. Ainge, G.F. Painter, et al. 2006. Natural killer T cells recognize diacylglycerol antigens from pathogenic bacteria. Nat. Immunol. 7:978-986. doi:10.1038/ni1380
14. 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 alpha-galactosylceramide. Nat. Immunol. 6:819-826. doi:10.1038/ni1225
15. Lovell, S.C., I.W. Davis, W.B. Arendall III, P.I. de Bakker, J.M. Word, M.G. Prisant, J.S. Richardson, and D.C. Richardson. 2003. Structure validation by Calpha geometry: phi,psi and Cbeta deviation. Proteins. 50:437-450. doi:10.1002/prot.10286
16. Mallevaey, T., J.P. Scott-Browne, J.L. Matsuda, M.H. Young, D.G. Pellicci, O. Patel, M. Thakur, L. Kjer-Nielsen, S.K. Richardson, V. Cerundolo, et al. 2009. T cell receptor CDR2 β and CDR3 β loops collaborate functionally to shape the iNKT cell repertoire. Immunity. 31:60-71. doi:10.1016/j.immuni.2009.05.010
17. Mattner, J., K.L. Debord, N. Ismail, R.D. Goff, C. Cantu III, D. Zhou, P. Saint-Mezard, V. Wang, Y. Gao, N. Yin, et al. 2005. Exogenous and endogenous glycolipid antigens activate NKT cells during microbial infections. Nature. 434:525-529. doi:10.1038/nature03408
18. McCarthy, C., D. Shepherd, S. Fleire, V.S. Stronge, M. Koch, P.A. Illarionov, G. Bossi, M. Salio, G. Denkberg, F. Reddington, et al. 2007. The length of lipids bound to human CD1d molecules modulates the affinity of NKT cell TCR and the threshold of NKT cell activation. J. Exp. Med. 204:1131-1144. doi:10.1084/jem.20062342
19. Moody, D.B., D.M. Zajonc, and I.A. Wilson. 2005. Anatomy of CD1-lipid antigen complexes. Nat. Rev. Immunol. 5:387-399. doi:10.1038/nri1605
20. Otwinowski, Z., and W. Minor. 1997. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:307-326. doi:10.1016/S0076-6879(97)76066-X
21. 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 V β 8.2 and V β 7 semi-invariant NKT T cell receptors. Immunity. 31:47-59. doi:10.1016/j.immuni.2009.04.018
22. Raju, R., B.F. Castillo, S.K. Richardson, M. Thakur, R. Severins, M. Kronenberg, and A.R. Howell. 2009. Synthesis and evaluation of 3″- and 4″-deoxy and -fluoro analogs of the immunostimulatory glycolipid, KRN7000. Bioorg. Med. Chem. Lett. 19:4122-4125. doi:10.1016/j.bmcl.2009.06.005
23. Rudolph, M.G., R.L. Stanfield, and I.A. Wilson. 2006. How TCRs bind MHCs, peptides, and coreceptors. Annu. Rev. Immunol. 24:419-466. doi:10.1146/annurev. immunol.23.021704.115658
24. Schiefner, A., M. Fujio, D. Wu, C.H. Wong, and I.A. Wilson. 2009. Structural evaluation of potent NKT cell agonists: implications for design of novel stimulatory ligands. J. Mol. Biol. 394:71-82. doi:10.1016/j.jmb.2009.08. 061
25. 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. doi:10.1038/ni1510
26. Sidobre, S., O.V. Naidenko, B.C. Sim, N.R. Gascoigne, K.C. Garcia, and M. Kronenberg. 2002. The V α 14 NKT cell TCR exhibits high-affinity binding to a glycolipid/CD1d complex. J. Immunol. 169:1340-1348.
27. Sidobre, S., K.J. Hammond, L. Bénazet-Sidobre, S.D. Maltsev, S.K. Richardson, R.M. Ndonye, A.R. Howell, T. Sakai, G.S. Besra, S.A. Porcelli, and M. Kronenberg. 2004. The T cell antigen receptor expressed by Valpha14i NKT cells has a unique mode of glycosphingolipid antigen recognition. Proc. Natl. Acad. Sci. USA. 101:12254-12259. doi:10.1073/pnas.0404632101
28. Silk, J.D., M. Salio, B.G. Reddy, D. Shepherd, U. Gileadi, J. Brown, S.H. Masri, P. Polzella, G. Ritter, G.S. Besra, et al. 2008. Cutting edge: nonglycosidic CD1d lipid ligands activate human and murine invariant NKT cells. J. Immunol. 180:6452-6456.
29. Sriram, V., W. Du, J. Gervay-Hague, and R.R. Brutkiewicz. 2005. Cell wall glycosphingolipids of Sphingomonas paucimobilis are CD1d-specific ligands for NKT cells. Eur. J. Immunol. 35:1692-1701. doi:10.1002/eji.200526157
30. Sullivan, B.A., N.A. Nagarajan, G. Wingender, J. Wang, I. Scott, M. Tsuji, R.W. Franck, S.A. Porcelli, D.M. Zajonc, and M. Kronenberg. 2010. Mechanisms for glycolipid antigen-driven cytokine polarization by Valpha14i NKT cells. J. Immunol. 184:141-153. doi:10.4049/jimmunol.0902880
31. Tupin, E., M.R. Benhnia, Y. Kinjo, R. Patsey, C.J. Lena, M.C. Haller, M.J. Caimano, M. Imamura, C.H. Wong, S. Crotty, et al. 2008. NKT cells prevent chronic joint inflammation after infection with Borrelia burgdorferi. Proc. Natl. Acad. Sci. USA. 105:19863-19868. doi:10.1073/pnas.0810519105
32. Vagin, A., and A. Teplyakov. 1997. MOLREP: an automated program for molecular replacement. J. Appl. Cryst. 30:1022-1025. doi:10.1107/ S0021889897006766
33. Wang, J., Y. Li, Y. Kinjo, T.T. Mac, D. Gibson, G.F. Painter, M. Kronenberg, and D.M. Zajonc. 2010. Lipid binding orientation within CD1d affects recognition of Borrelia burgorferi antigens by NKT cells. Proc. Natl. Acad. Sci. USA. 107:1535-1540. doi:10.1073/pnas.0909479107
34. Winn, M.D., M.N. Isupov, and G.N. Murshudov. 2001. Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta Crystallogr. D Biol. Crystallogr. 57:122-133. doi:10.1107/S0907444900014736
35. Wu, D., G.W. Xing, M.A. Poles, A. Horowitz, Y. Kinjo, B. Sullivan, V. Bodmer-Narkevitch, O. Plettenburg, M. Kronenberg, M. Tsuji, et al. 2005. Bacterial glycolipids and analogs as antigens for CD1d-restricted NKT cells. Proc. Natl. Acad. Sci. USA. 102:1351-1356. doi:10.1073/pnas.0408696102
36. Wu, D., D.M. Zajonc, M. Fujio, B.A. Sullivan, Y. Kinjo, M. Kronenberg, I.A. Wilson, and C.H. Wong. 2006. Design of natural killer T cell activators: structure and function of a microbial glycosphingolipid bound to mouse CD1d. Proc. Natl. Acad. Sci. USA. 103:3972-3977. doi:10.1073/pnas.0600285103
37. Wu, L.C., D.S. Tuot, D.S. Lyons, K.C. Garcia, and M.M. Davis. 2002. Two-step binding mechanism for T-cell receptor recognition of peptide MHC. Nature. 418:552-556. doi:10.1038/nature00920
38. Yin, N., X. Long, R.D. Goff, D. Zhou, C. Cantu III, J. Mattner, P.S. Mezard, L. Teyton, A. Bendelac, and P.B. Savage. 2009. Alpha anomers of iGb3 and Gb3 stimulate cytokine production by natural killer T cells. ACS Chem. Biol. 4:199-208. doi:10.1021/cb800277n
39. Zajonc, D.M., and M. Kronenberg. 2007. CD1 mediated T cell recognition of glycolipids. Curr. Opin. Struct. Biol. 17:521-529. doi:10.1016/j.sbi.2007.09. 010
40. Zajonc, D.M., and M. Kronenberg. 2009. Carbohydrate specificity of the recognition of diverse glycolipids by natural killer T cells. Immunol. Rev. 230:188-200. doi:10.1111/j.1600-065X.2009.00802.x
41. Zajonc, D.M., and I.A. Wilson. 2007. Architecture of CD1 proteins. Curr. Top. Microbiol. Immunol. 314:27-50. doi:10.1007/978-3-540-69511-0-2
42. Zajonc, D.M., C. Cantu III, J. Mattner, D. Zhou, P.B. Savage, A. Bendelac, I.A. Wilson, and L. Teyton. 2005a. Structure and function of a potent agonist for the semi-invariant natural killer T cell receptor. Nat. Immunol. 6:810-818. doi:10.1038/ni1224
43. Zajonc, D.M., I. Maricic, D. Wu, R. Halder, K. Roy, C.H. Wong, V. Kumar, and I.A. Wilson. 2005b. Structural basis for CD1d presentation of a sulfatide derived from myelin and its implications for autoimmunity. J. Exp. Med. 202:1517-1526. doi:10.1084/jem.20051625
44. Zajonc, D.M., P.B. Savage, A. Bendelac, I.A. Wilson, and L. Teyton. 2008. Crystal structures of mouse CD1d-iGb3 complex and its cognate Valpha14 T cell receptor suggest a model for dual recognition of foreign and self glycolipids. J. Mol. Biol. 377:1104-1116. doi:10.1016/j.jmb.2008.01.061