Another View of T Cell Antigen Recognition: Cooperative Engagement of Glycolipid Antigens by Va14Ja18 Natural TCR

Journal of Immunology

Volumn 171, Issue 9, 2003, Pages 4539-4551

  Stanic, Aleksandar K ^a   Shashidharamurthy, R ^a   Bezbradica, Jelena S ^a   Matsuki, Naoto ^a   Yoshimura, Yoshitaka ^a   Miyake, Sachiko ^b   Choi, Eun Young ^c   Schell, Todd D ^d   Van Kaer, Luc ^a   Tevethia, Satvir S ^d   Roopenian, Derry C ^c   Yamamura, Takashi ^b   Joyce, Sebastian ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTE OF NEUROSCIENCE   (Japan)

^c PENN STATE COLLEGE OF MEDICINE   (United States)

^d JACKSON LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA GALACTOSYLCERAMIDE; ANTIGEN; GALACTOSYLCERAMIDE; GLYCOLIPID; GLYCOLIPID ANTIGEN; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIGEN PRESENTATION; ANTIGEN RECOGNITION; ANTIGEN SPECIFICITY; ARTICLE; BETA CHAIN; CELL PROLIFERATION; CELLULAR IMMUNITY; COMPLEX FORMATION; CYTOKINE RELEASE; DRUG RECEPTOR BINDING; EFFECTOR CELL; IMMUNE RESPONSE; MOLECULAR RECOGNITION; MOUSE; NATURAL KILLER CELL; NATURAL KILLER CELL VA14JA18; NONHUMAN; PRIORITY JOURNAL; RECEPTOR DOWN REGULATION; T LYMPHOCYTE ACTIVATION;

EID: 10744225154     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.171.9.4539     Document Type: Article

References (82)

1. Joyce, S. 2001. CDld and natural T cells: how their properties jump start the immune system. Cell. Mol. Life Sci. 58:442.
2. + T lymphocytes. Science 268:863.
3. + targets. J. Immunol. 160:3681.
4. Chiu, Y. H., J. Jayawardena, A. Weiss, D. Lee, S. H. Park, A. Dautry-Varsat, and A. Bendelac. 1999. Distinct subsets of CD1d-restricted T cells recognize self-antigens loaded in different cellular compartments. J. Exp. Med. 189:103.
5. Molano, A., S. H. Park, Y. H. Chiu, S. Nosseir, A. Bendelac, and M. Tsuji. 2000. The IgG response to the circumsporozoite protein is MHC class II-dependent and CD1d-independent: exploring the role of GPIs in NK T cell activation and antimalarial responses. J. Immunol. 164:5005.
6. Park, S.-H., J. H. Roark, and A. Bendelac. 1998. Tissue-specific recognition of mouse CD1 molecules. J. Immunol. 160:3128.
7. Chiu, Y. H., S. H. Park, K. Benlagha, C. Forestier, J. Jayawardena-Wolf, P. B. Savage, L. Teyton, and A. Bendelac. 2002. Multiple defects in antigen presentation and T cell development by mice expressing cytoplasmic tail-truncated CD1d. Nat. Immunol. 3:55.
8. De Silva, A. D., J.-J. Park, N. Matsuki, A. K. Stanic, R. R. Brutkiewicz, M. E. Medof, and S. Joyce. 2002. Lipid protein interactions: the assembly of CD1d1 with cellular phospholipids occurs in the endoplasmic reticulum. J. Immunol. 168:723.
9. Roberts, T. J., V. Sriram, P. M. Spence, M. Gui, K. Hayakawa, I. Bacik, J. R. Bennink, J. W. Yewdell, and R. R. Brutkiewicz. 2002. Recycling CD1d1 molecules present endogenous antigens processed in an endocytic compartment to NKT cells. J. Immunol. 168:5409.
10. Brossay, L., M. Chioda, N. Burdin, Y. Koezuka, G. Casorati, P. Dellabona, and M. Kronenberg. 1998. CD1d-mediated recognition of an α -galactosylceramide by natural killer T cells is highly conserved through mammalian evolution. J. Exp. Med. 188:1521.
11. + NK T lymphocytes. J. Immunol. 161:3271.
12. 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.
13. Nieda, M., A. Nicol, Y. Koezuka, A. Kikuchi, T. Takahashi, H. Nakamura, H. Furukawa, T. Yabe, Y. Ishikawa, K. Tadokoro, and T. Juji. 1999. Activation of human Vα24NKT cells by α-glycosylceramide in a CD1d-restricted and Vα24TCR-mediated manner. Hum. Immunol. 60:10.
14. Spada, F. M., Y. Koezuka, and S. A. Porcelli. 1998. CD1d-restricted recognition of synthetic glycolipid antigens by human natural killer T cells. J. Exp. Med. 188:1529.
15. Stanic, A. K., A. D. De Silva, J. J. Park, V. Sriram, S. Ichikawa, Y. Hirabyashi, K. Hayakawa, L. Van Kaer, R. R. Brutkiewicz, and S. Joyce. 2003. Defective presentation of the CD1d1-restricted natural Va14Ja18 NKT lymphocyte antigen caused by β-D-glucosylceramide synthase deficiency. Proc. Natl. Acad. Sci. USA 100:1849.
16. Bendelac, A., and R. Medzhitov. 2002. Adjuvants of immunity: harnessing innate immunity to promote adaptive immunity. J. Exp. Med. 195:F19.
17. Hong, S., M. T. Wilson, I. Serizawa, L. Wu, N. Singh, O. V. Naidenko, T. Miura, T. Haba, D. C. Scherer, J. Wei, et al. 2001. The natural killer T-cell ligand α-galactosylceramide prevents autoimmune diabetes in non-obese diabetic mice. Nat. Med. 7:1052.
18. Sharif, S., G. A. Arreaza, P. Zucker, Q. S. Mi, J. Sondhi, O. V. Naidenko, M. Kronenberg, Y. Koezuka, T. L. Delovitch, J. M. Gombert, et al. 2001. Activation of natural killer T cells by α-galactosylceramide treatment prevents the onset and recurrence of autoimmune type 1 diabetes. Nat. Med. 7:1057.
19. Miyamoto, K., S. Miyake, and T. Yamamura. 2001. A synthetic glycolipid prevents autoimmune encephalomyelitis by inducing Th2 bias of natural killer T cells. Nature 413:531.
20. Singh, A. K., M. T. Wilson, S. Hong, D. Olivares-Villagomez, C. Du, A. K. Stanic, S. Joyce, S. Sriram, Y. Koezuka, and L. Van Kaer. 2001. Natural killer T cell activation protects mice against experimental autoimmune encephalomyelitis. J. Exp. Med. 194:1801.
21. Wilson, M. T., A. K. Singh, and L. Van Kaer. 2002. Immunotherapy with ligands of natural killer T cells. Trends Mol. Med. 8:225.
22. Margulies, D. H. 1997. Interactions of TCRs with MHC-peptide complexes: a quantitative basis for mechanistic models. Curr. Opin. Immunol. 9:390.
23. Davis, M. M., J. J. Boniface, Z. Reich, D. Lyons, J. Hampl, B. Arden, and Y. Chien. 1998. Ligand recognition by αβ T cell receptors. Annu. Rev. Immunol. 16:523.
24. Germain, R. N., and I. Stefanova. 1999. The dynamics of T cell receptor signaling: complex orchestration and the key roles of tempo and cooperation. Annu. Rev. Immunol. 17:467.
25. Garcia, K. C., L. Teyton, and I. A. Wilson. 1999. Structural basis for T cell recognition. Annu. Rev. Immunol. 17:369.
26. 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.
27. Schumann, J., R. B. Voyle, B. Y. Wei, and H. R. MacDonald. 2003. Influence of the TCR Vβ domain on the avidity of CD1d:α -galactosylceramide binding by invariant Vα14 NKT cells. J. Immunol. 170:5815.
28. Kalergis, A. M., N. Boucheron, M. A. Doucey, E. Palmieri, E. C. Goyarts, Z. Vegh, I. F. Luescher, and S. G. Nathenson. 2001. Efficient T cell activation requires an optimal dwell-time of interaction between the TCR and the pMHC complex. Nat. Immunol. 2:229.
29. Holler, P. D., and D. M. Kranz. 2003. Quantitative analysis of the contribution of TCR/pepMHC affinity and CD8 to T cell activation. Immunity 18:255.
30. Garcia, K. C., C. A. Scott, A. Brunmark, F. R. Carbone, P. A. Peterson, I. A. Wilson, and L. Teyton. 1996. CD8 enhances formation of stable T-cell receptor/MHC class I molecule complexes. Nature 384:577.
31. Luescher, I. F., E. Vivier, A. Layer, J. Mahiou, F. Godeau, B. Malissen, and P. Romero. 1995. CD8 modulation of T-cell antigen receptor-ligand interactions on living cytotoxic T lymphocytes. Nature 373:353.
32. d to CD8: interaction with the amino terminus of a mature cell surface protein. J. Immunol. 160:2809.
33. Germain, R. N. 2001. The art of the probable: system control in the adaptive immune system. Science 293:240.
34. Fersht, A. 1999. Structure and Mechanism in Protein Science. Freeman. New York.
35. Benlagha, K., A. Weiss, A. Beavis, L. Teyton, and A. Bendelac. 2000. In vivo identification of glycolipid antigen-specific T cells using fluorescent CD1d tetramers. J. Exp. Med. 191:1895.
36. Cui, J., S. Tahiro, T. Kawano, H. Sato, E. Kondo, I. Toura, Y. Kaneko, H. Koseki, M. Kanno, and M. Taniguchi. 1997. Requirement for Vα14 NKT cells in IL-12-mediated rejection of tumors. Science 278:1623.
37. Mendiratta, S. K., W. D. Martin, S. Hong, A. Boesteanu, S. Joyce, and L. Van Kaer. 1997. CDIdI mutant mice are deficient in natural T cells that promptly produce IL-4. Immunity 6:469.
38. Choi, E. Y., Y. Yoshimura, G. J. Christianson, T. J. Sproule, S. Malarkannan, N. Shastri, S. Joyce, and D. C. Roopenian. 2001. Quantitative analysis of the immune response to mouse non-MHC transplantation antigens in vivo: the H60 histocompatibility antigen dominates over all others. J. Immunol. 166:4370.
39. + T-lymphocyte responses to multiple epitopes from Simian virus 40 (SV40) large T antigen in C57BL/6 mice immunized with SV40, SV40 T-antigen-transformed cells, or vaccinia virus recombinants expressing full-length T antigen or epitope minigenes. J. Virol. 74:6922.
40. Gui, M., J. Li, L. J. Wen, R. R. Hardy, and K. Hayakawa. 2001. TCRβ chain influences but does not solely control autoreactivity of Vα14Jα281 T cells. J. Immunol. 167:6239.
41. - T cells in mice and humans. J. Exp. Med. 180:1097.
42. Limbird, L. E. 1996. Cell Surface Receptors: A Short Course on Theory and Methods. Kluwer, Boston.
43. Matsuki, N., A. K. Stanic, M. E. Embers, L. Van Kaer, L. Morel, and S. Joyce. 2003. Genetic dissection of Val4Ja18 natural T cell number and function in autoimmune-prone mice. J. Immunol. 170:5429.
44. Joyce, S., A. S. Woods, J. W. Yewdell, J. R. Bennink, A. D. De Silva, A. Boesteanu, S. P. Balk, R. J. Cotter, and R. R. Brutkiewciz. 1998. Natural ligand of mouse CD1d1: cellular glycosylphosphatidylinositol. Science 279:1541.
45. 2-microglobulin. Proc. Natl. Acad. Sci. USA 89:2242.
46. Corr, M., A. E. Slanetz, L. F. Boyd, M. T. Jelonek, S. Khilko, B. K. AlRamadi, Y. S. Kim, S. E. Maher, A. L. M. Bothwell, and D. H. Margulies. 1994. T cell receptor-MHC class I peptide interactions: affinity, kinetics and specificity. Science 265:946.
47. Matsui, K., J. J. Boniface, P. A. Reay, H. Schild, B. Fazekas de St. Groth, and M. M. Davis. 1991. Low affinity interaction of peptide-MHC complexes with T cell receptors. Science 254:1788.
48. Crawford, F., H. Kozono, J. White, P. Marrack, and J. Kappler. 1998. Detection of antigen-specific T cells with multivalent soluble class II MHC covalent peptide complexes. Immunity 8:675.
49. Savage, P. A., J. J. Boniface, and M. M. Davis. 1999. A kinetic basis for T cell receptor repertoire selection during an immune response. Immunity 10:485.
50. Fahmy, T. M., J. G. Bieler, M. Edidin, and J. P. Schneck. 2001. Increased TCR avidity after T cell activation: a mechanism for sensing low-density antigen. Immunity 14:135.
51. Rosette, C., G. Werlen, M. A. Daniels, P. O. Holman, S. M. Alam, P. J. Travers, N. R. Gascoigne, E. Palmer, and S. C. Jameson. 2001. The impact of duration versus extent of TCR occupancy on T cell activation: a revision of the kinetic proofreading model. Immunity 15:59.
52. Savage, P. A., and M. M. Davis. 2001. A kinetic window constricts the T cell receptor repertoire in the thymus. Immunity 14:243.
53. Busch, D. H., and E. G. Pamer. 1999. T cell affinity maturation by selective expansion during infection. J. Exp. Med. 189:701.
54. + T cells. J. Exp. Med. 182:1591.
55. Hemmer, B., I. Stefanova, M. Vergelli, R. N. Germain, and R. Martin. 1998. Relationships among TCR ligand potency, thresholds for effector function elicitation, and the quality of early signaling events in human T cells. J. Immunol. 160:5807.
56. + T cells. J. Exp. Med. 186:757.
57. Itoh, Y., B. Hemmer, R. Martin, and R. N. Germain. 1999. Serial TCR engagement and down-modulation by peptide:MHC molecule ligands: relationship to the quality of individual TCR signaling events. J. Immunol. 162:2073.
58. + T cells differentiation. J. Immunol. 159:5956.
59. Carnaud, C., D. Lee, O. Donnars, S.-H. Park, A. Beavis, Y. Koezuka, and A. Bendelac. 1999. Cross-talk between cells of the innate immune system: NKT cells rapidly activate NK cells. J. Immunol. 163:4647.
60. Liu, H., M. Rhodes, D. L. Wiest, and D. A. Vignali. 2000. On the dynamics of TCR:CD3 complex cell surface expression and downmodulation. Immunity 13:665.
61. San Jose, E., A. Borroto, F. Niedergang, A. Alcover, and B. Alarcon. 2000. Triggering the TCR complex causes the downregulation of nonengaged receptors by a signal transduction-dependent mechanism. Immunity 12:161.
62. Valitutti, S., S. Muller, M. Salio, and A. Lanzavecchia. 1997. Degradation of T cell receptor (TCR)-CD3-ζ complexes after antigenic stimulation. J. Exp. Med. 185:1859.
63. Royer, W. E., Jr., J. E. Knapp, K. Strand, and H. A. Heaslet. 2001. Cooperative hemoglobins: conserved fold, diverse quaternary assemblies and allosteric mechanisms. Trends Biochem. Sci. 26:297.
64. Joyce, S., P. Tabaczewski, R. H. Angeletti, S. G. Nathenson, and I. Stroynowski. 1994. A non-polymorphic MHC class Ib molecule binds a large array of diverse self peptides. J. Exp. Med. 179:579.
65. Hartel, S., H. A. Diehl, and F. Ojeda. 1998. Methyl-β-cyclodextrins and liposomes as water-soluble carriers for cholesterol incorporation into membranes and its evaluation by a microenzymatic fluorescence assay and membrane fluidity-sensitive dyes. Anal. Biochem. 258:277.
66. Brown, D. A., and E. London. 2000. Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J. Biol. Chem. 275:17221.
67. Fujii, S., K. Shimizu, M. Kronenberg, and R. M. Steinman. 2002. Prolonged IFN-γ-producing NKT response induced with α -galactosylceramide-loaded DCs. Nat. Immunol. 3:867.
68. Leitenberg, D., and K. Bottomly. 1999. Regulation of naive T cell differentiation by varying the potency of TCR signal transduction. Semin. Immunol. 11:283.
69. - T-cell deficiency and IDDM in NOD/Lt mice. Diabetes 46:572.
70. - thymocytes. J. Autoimmun. 10:279.
71. - (NKT) thymocytes prevent insulin-dependent diabetes mellitus in non-obese diabetic (NOD)/Lt mice by the influence of interleukin (IL)-4 and/or IL-10. J. Exp. Med. 187:1047.
72. Beaudoin, L., V. Laloux, J. Novak, B. Lucas, and A. Lehuen. 2002. NKT cells inhibit the onset of diabetes by impairing the development of pathogenic T cells specific for pancreatic β cells. Immunity 17:725.
73. Lehuen, A., O. Lantz, L. Beaudoin, V. Laloux, C. Carnaud, A. Bendelac, J. F. Bach, and R. C. Monteiro. 1998. Overexpression of natural killer T cells protects Vα14Jα281 transgenic nonobese diabetic mice against diabetes. J. Exp. Med. 188:1831.
74. Naumov, Y. N., K. S. Bahjat, R. Gausling, R. Abraham, M. A. Exley, Y. Koezuka, S. B. Balk, J. L. Strominger, M. Clare-Salzer, and S. B. Wilson. 2001. Activation of CD1d-restricted T cells protects NOD mice from developing diabetes by regulating dendritic cell subsets. Proc. Natl. Acad. Sci. USA 98:13838.
75. Chun, T., M. J. Page, L. Gapin, J. L. Matsuda, H. Xu, H. Nguyen, H. S. Kang, A. K. Stanic, S. Joyce, W. A. Koltun, et al. 2003. CD1d-expressing dendritic cells but not thymic epithelial cells can mediate negative selection of NKT Cells. J. Exp. Med. 197:907.
76. Call, M. E., J. Pyrdol, M. Wiedmann, and K. W. Wucherpfennig. 2002. The organizing principle in the formation of the T cell receptor-CD3 complex. Cell 111:967.
77. Wang, J., K. Lim, A. Smolyar, M. Teng, J. Liu, A. G. Tse, R. E. Hussey, Y. Chishti, C. T. Thomson, R. M. Sweet, et al. 1998. Atomic structure of an αβ T cell receptor (TCR) heterodimer in complex with an anti-TCR Fab fragment derived from a mitogenic antibody. EMBO J. 17:10.
78. Ghendler, Y., A. Smolyar, H. C. Chang, and E. L. Reinherz. 1998. One of the CD3ε subunits within a T cell receptor complex lies in close proximity to the Cβ FG loop. J. Exp. Med. 187:1529.
79. Degermann, S., G. Sollami, and K. Karjalainen. 1999. T cell receptor β chain lacking the large solvent-exposed Cβ FG loop supports normal α/β T cell development and function in transgenic mice. J. Exp. Med. 189:1679.
80. Sasada, T., M. Touma, H. C. Chang, L. K. Clayton, J. H. Wang, and E. L. Reinherz. 2002. Involvement of the TCR Cβ FG loop in thymic selection and T cell function. J. Exp. Med. 195:1419.
81. Degermann, S., G. Sollami, and K. Karjalainen. 1999. Impaired NKI.I T cell development in mice transgenic for a T cell receptor β chain lacking the large, solvent-exposed Cβ FG loop. J. Exp. Med. 190:1357.
82. Block, M. S., A. J. Johnson, Y. Mendez-Fernandez, and L. R. Pease. 2001. Monomeric class I molecules mediate TCR/CD3ε/CD8 interaction on the surface of T cells. J. Immunol. 167:821.