Structure and binding kinetics of three different human CD1d-α-galactosylceramide-specific T cell receptors

Journal of Experimental Medicine

Volumn 203, Issue 3, 2006, Pages 699-710

  Gadola, Stephan D ^a,b   Koch, Michael ^c   Marles Wright, Jon ^c   Lissin, Nikolai M ^d   Shepherd, Dawn ^b   Matulis, Gediminas ^a   Harlos, Karl ^c   Villiger, Peter M ^a   Stuart, David I ^c   Jakobsen, Bent K ^d   Cerundolo, Vincenzo ^b   Jones, E Yvonne ^c  

^a UNIVERSITY OF BERN   (Switzerland)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^d Avidex Ltd   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

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

ALPHA HELIX; ANTIGEN RECOGNITION; ARTICLE; BINDING KINETICS; COMPLEMENTARITY DETERMINING REGION; CONTROLLED STUDY; CRYSTAL STRUCTURE; HUMAN; HUMAN CELL; MAJOR HISTOCOMPATIBILITY COMPLEX; NATURAL KILLER T CELL; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN STRUCTURE; RECEPTOR BINDING;

ANIMALS; ANTIGEN PRESENTATION; ANTIGENS, CD1; COMPLEMENTARITY DETERMINING REGIONS; CRYSTALLOGRAPHY, X-RAY; GALACTOSYLCERAMIDES; HUMANS; KILLER CELLS, NATURAL; MICE; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; STRUCTURE-ACTIVITY RELATIONSHIP; T-LYMPHOCYTES;

EID: 33645074941     PISSN: 00221007     EISSN: 00221007     Source Type: Journal    
DOI: 10.1084/jem.20052369     Document Type: Article

References (53)

1. Brigl, M., and M.B. Brenner. 2004. CD1: antigen presentation and T cell function. Annu. Rev. Immunol. 22:817-890.
2. Porcelli, S.A., and R.L. Modlin. 1999. The CD1 system: antigenpresenting molecules for T cell recognition of lipids and glycolipids. Annu. Rev. Immunol. 17:297-329.
3. Porcelli, S., C.E. Yockey, M.B. Brenner, and S.P. Balk. 1993. Analysis of T cell antigen receptor (TCR) expression by human peripheral blood CD4-8- α/β T cells demonstrates preferential use of several V β genes and an invariant TCR α chain. J. Exp. Med. 178:1-16.
4. Lantz, O., and A. Bendelac. 1994. An invariant T cell receptor α chain is used by a unique subset of major histocompatibility complex class I-specific CD4+ and CD4-8- T cells in mice and humans. J. Exp. Med. 180:1097-1106.
5. Behar, S.M., and S. Cardell. 2000. Diverse CD1d-restricted T cells: diverse phenotypes, and diverse functions. Semin. Immunol. 12:551-560.
6. Van Rhijn, I., D.C. Young, J.S. Im, S.B. Levery, P.A. Illarionov, G.S. Besra, S.A. Porcelli, J. Gumperz, T.Y. Cheng, and D.B. Moody. 2004. CD1d-restricted T cell activation by nonlipidic small molecules. Proc. Natl. Acad. Sci. USA. 101:13578-13583.
7. 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 vα14 NKT cells by glycosylceramides. Science. 278:1626-1629.
8. Gadola, S.D., N. Dulphy, M. Salio, and V. Cerundolo. 2002. Vα24-JαQ-independent, CD1d-restricted recognition of α-galactosylceramide by human CD4(+) and CD8αβ(+) T lymphocytes. J. Immunol. 168:5514-5520.
9. Chang, D.H., K. Osman, J. Connolly, A. Kukreja, J. Krasovsky, M. Pack, A. Hutchinson, M. Geller, N. Liu, R. Annable, et al. 2005. Sustained expansion of NKT cells and antigen-specific T cells after injection of α-galactosyl- ceramide loaded mature dendritic cells in cancer patients. J. Exp. Med. 201:1503-1517.
10. Gapin, L., J.L. Matsuda, C.D. Surh, and M. Kronenberg. 2001. NKT cells derive from double-positive thymocytes that are positively selected by CD1d. Nat. Immunol. 2:971-978.
11. Benlagha, K., D.G. Wei, J. Veiga, L. Teyton, and A. Bendelac. 2005. Characterization of the early stages of thymic NKT cell development. J. Exp. Med. 202:485-492.
12. Chen, J.L., G. Stewart-Jones, G. Bossi, N.M. Lissin, L. Wooldridge, E.M. Choi, G. Held, P.R. Dunbar, R.M. Esnouf, M. Sami, et al. 2005. Structural and kinetic basis for heightened immunogenicity of T cell vaccines. J. Exp. Med. 201:1243-1255.
13. Garcia, K.C., L. Teyton, and I.A. Wilson. 1999. Structural basis of T cell recognition. Annu. Rev. Immunol. 17:369-397.
14. Al-Lazikani, B., A.M. Lesk, and C. Chothia. 2000. Canonical structures for the hypervariable regions of T cell αβ receptors. J. Mol. Biol. 295:979-995.
15. Rudolph, M.G., and I.A. Wilson. 2002. The specificity of TCR/pMHC interaction. Curr. Opin. Immunol. 14:52-65.
16. 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.
17. Bradbury, A., K.T. Belt, T.M. Neri, C. Milstein, and F. Calabi. 1988. Mouse CD1 is distinct from and co-exists with TL in the same thymus. EMBO J. 7:3081-3086.
18. Balk, S.P., P.A. Bleicher, and C. Terhorst. 1991. Isolation and expression of cDNA encoding the murine homologues of CD 1. J. Immunol. 146:768-774.
19. Zeng, Z., A.R. Castano, B.W. Segelke, E.A. Stura, P.A. Peterson, and I.A. Wilson. 1997. Crystal structure of mouse CD1: An MHC-like fold with a large hydrophobic binding groove. Science. 277:339-345.
20. Zajonc, D.M., C. Cantu III, J. Mattner, D. Zhou, P.B. Savage, A. Bendelac, I.A. Wilson, and L. Teyton. 2005. Structure and function of a potent agonist for the semi-invariant natural killer T cell receptor. Nat. Immunol. 6:810-818.
21. Giabbai, B., S. Sidobre, M.D. Crispin, Y. Sanchez-Ruiz, A. Bachi, M. Kronenberg, I.A. Wilson, and M. Degano. 2005. Crystal structure of mouse CD1d bound to the self ligand phosphatidylcholine: a molecular basis for NKT cell activation. J. Immunol. 175:977-984.
22. Grant, E.P., M. Degano, J.P. Rosat, S. Stenger, R.L. Modlin, I.A. Wilson, S.A. Porcelli, and M.B. Brenner. 1999. Molecular recognition of lipid antigens by T cell receptors. J. Exp. Med. 189:195-205.
23. Grant, E.P., E.M. Beckman, S.M. Behar, M. Degano, D. Frederique, G.S. Besra, I.A. Wilson, S.A. Porcelli, S.T. Furlong, and M.B. Brenner. 2002. Fine specificity of TCR complementarity-determining region residues and lipid antigen hydrophilic moieties in the recognition of a CD1-lipid complex. J. Immunol. 168:3933-3940.
24. Burdin, N., L. Brossay, M. Degano, H. Iijima, M. Gui, I.A. Wilson, and M. Kronenberg. 2000. Structural requirements for antigen presentation by mouse CD 1. Proc. Natl. Acad. Sci. USA. 97:10156-10161.
25. Zajonc, D.M., M.D. Crispin, T.A. Bowden, D.C. Young, T.Y. Cheng, J. Hu, C.E. Costello, P.M. Rudd, R.A. Dwek, M.J. Miller, et al. 2005. Molecular mechanism of lipopeptide presentation by CD1a. Immunity. 22:209-219.
26. Havran, W.L., and J.P. Allison. 1988. Developmentally ordered appearance of thymocytes expressing different T-cell antigen receptors. Nature. 335:443-445.
27. Matsuda, J.L., L. Gapin, N. Fazilleau, K. Warren, O.V. Naidenko, and M. Kronenberg. 2001. Natural killer T cells reactive to a single glycolipid exhibit a highly diverse T cell receptor β repertoire and small clone size. Proc. Natl. Acad. Sci. USA. 98:12636-12641.
28. van der Merwe, P.A., and S.J. Davis. 2003. Molecular interactions mediating T cell antigen recognition. Annu. Rev. Immunol. 21:659-684.
29. Sidobre, S., O.V. Naidenko, B.C. Sim, N.R. Gascoigne, K.C. Garcia, and M. Kronenberg. 2002. The Vα14 NKT cell TCR exhibits high-affinity binding to a glycolipid/CD1d complex. J. Immunol. 169:1340-1348.
30. Sidobre, S., K.J. Hammond, L. Benazet-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 Vα14i NKT cells has a unique mode of glycosphingolipid antigen recognition. Proc. Natl. Acad. Sci. USA. 101:12254-12259.
31. Cantu, C., III, K. Benlagha, P.B. Savage, A. Bendelac, and L. Teyton. 2003. The paradox of immune molecular recognition of α-galactosylceramide: low affinity, low specificity for CD1d, high affinity for αβTCRs. J. Immunol. 170:4673-4682.
32. Jorgensen, J.L., U. Esser, B. Fazekas de St Groth, P.A. Reay, and M.M. Davis. 1992. Mapping T-cell receptor-peptide contacts by variant peptide immunization of single-chain transgenics. Nature. 355:224-230.
33. Garboczi, D.N., P. Ghosh, U. Utz, Q.R. Fan, W.E. Biddison, and D.C. Wiley. 1996. Structure of the complex between human T-cell receptor, viral peptide and HLA-A 2. Nature. 384:134-141.
34. Garcia, K.C., M. Degano, L.R. Pease, M. Huang, P.A. Peterson, L. Teyton, and I.A. Wilson. 1998. Structural basis of plasticity in T cell receptor recognition of a self peptide-MHC antigen. Science. 279:1166-1172.
35. Fischer, K., E. Scotet, M. Niemeyer, H. Koebernick, J. Zerrahn, S. Maillet, R. Hurwitz, M. Kursar, M. Bonneville, S.H. Kaufmann, and U.E. Schaible. 2004. Mycobacterial phosphatidylinositol mannoside is a natural antigen for CD1d-restricted T cells. Proc. Natl. Acad. Sci. USA. 101:10685-10690.
36. Zhou, D., J. Mattner, C. Cantu III, N. Schrantz, N. Yin, Y. Gao, Y. Sagiv, K. Hudspeth, Y.P. Wu, T. Yamashita, et al. 2004. Lysosomal glycosphingolipid recognition by NKT cells. Science. 306:1786-1789.
37. Bendelac, A., M.N. Rivera, S.H. Park, and J.H. Roark. 1997. Mouse CD1-specific NK1 T cells: development, specificity, and function. Annu. Rev. Immunol. 15:535-562.
38. Schumann, J., R.B. Voyle, B.Y. Wei, and H.R. MacDonald. 2003. Cutting edge: influence of the TCR Vβ domain on the avidity of CD1d:α- galactosylceramide binding by invariant Vα14 NKT cells. J. Immunol. 170:5815-5819.
39. Stanic, A.K., R. Shashidharamurthy, J.S. Bezbradica, N. Matsuki, Y. Yoshimura, S. Miyake, E.Y. Choi, T.D. Schell, L. Van Kaer, S.S. Tevethia, et al. 2003. Another view of T cell antigen recognition: cooperative engagement of glycolipid antigens by Vα14Jα18 natural T(iNKT) cell receptor. J. Immunol. 171:4539-4551.
40. Stewart-Jones, G.B., A.J. McMichael, J.I. Bell, D.I. Stuart, and E.Y. Jones. 2003. A structural basis for immunodominant human T cell receptor recognition. Nat. Immunol. 4:657-663.
41. Karadimitris, A., S. Gadola, M. Altamirano, D. Brown, A. Woolfson, P. Klenerman, J.L. Chen, Y. Koezuka, I.A. Roberts, D.A. Price, et al. 2001. Human CD1d-glycolipid tetramers generated by in vitro oxidative refolding chromatography. Proc. Natl. Acad. Sci. USA. 98:3294-3298.
42. Boulter, J.M., M. Glick, P.T. Todorov, E. Baston, M. Sami, P. Rizkallah, and B.K. Jakobsen. 2003. Stable, soluble T-cell receptor molecules for crystallization and therapeutics. Protein Eng. 16:707-711.
43. Willcox, B.E., G.F. Gao, J.R. Wyer, C.A. O'Callaghan, J.M. Boulter, E.Y. Jones, P.A. van der Merwe, J.I. Bell, and B.K. Jakobsen. 1999. Production of soluble αβT-cell receptor heterodimers suitable for biophysical analysis of ligand binding. Protein Sci. 8:2418-2423.
44. Mieza, M.A., T. Itoh, J.Q. Cui, Y. Makino, T. Kawano, K. Tsuchida, T. Koike, T. Shirai, H. Yagita, A. Matsuzawa, et al. 1996. Selective reduction of Vα14+ NK T cells associated with disease development in autoimmune-prone mice. J. Immunol. 156:4035-4040.
45. Brunger, A.T., P.D. Adams, G.M. Clore, W.L. DeLano, P. Gros, R.W. Grosse-Kunstleve, J.S. Jiang, J. Kuszewski, M. Nilges, N.S. Pannu, et al. 1998. Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54(Pt 5):905-921.
46. Collaborative Computational Project, Number 4. 1994. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50:760-763.
47. Emsley, P., and K. Cowtan. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60:2126-2132.
48. Morris, R.J., A. Perrakis, and V.S. Lamzin. 2003. ARP/wARP and automatic interpretation of protein electron density maps. Methods Enzymol. 374:229-244.
49. Murshudov, G.N., A.A. Vagin, and E.J. Dodson. 1997. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53:240-255.
50. 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.
51. Stuart, D.I., M. Levine, H. Muirhead, and D.K. Stammers. 1979. Crystal structure of cat muscle pyruvate kinase at a resolution of 2.6 A. J. Mol. Biol. 134:109-142.
52. Esnouf, R.M. 1997. Polyalanine reconstruction from Calpha positions using the program CALPHA can aid initial phasing of data by molecular replacement procedures. Acta Crystallogr. D. Biol. Crystallogr. 53(Pt6):665-672.
53. Batuwangala, T., D. Shepherd, S.D. Gadola, K.J. Gibson, N.R. Zaccai, A.R. Fersht, G.S. Besra, V. Cerundolo, and E.Y. Jones. 2004. The crystal structure of human CD1b with a bound bacterial glycolipid. J. Immunol. 172:2382-2388.