CTL activation is induced by cross-linking of TCR/MHC-peptide-CD8/p56lck adducts in rafts

European Journal of Immunology

Volumn 31, Issue 5, 2001, Pages 1561-1570

  Doucey, Marie Agnès ^a   Legler, Daniel F ^a   Boucheron, Nicole ^a   Cerottini, Jean Charles ^a   Bron, Claude ^a   Luescher, Immanuel F ^a,b  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b LUDWIG INSTITUTE FOR CANCER RESEARCH   (Switzerland)

Author keywords

CD8; CTL; MHC peptide; Raft; TCR

Indexed keywords

CALCIUM; CD3 ANTIGEN; CD8 ANTIGEN; DIPALMITOYLPHOSPHATIDYLETHANOLAMINE; LIPID; METHYL BETA CYCLODEXTRIN; MONOMER; PEPTIDE; POLYMER; PROTEIN P56; PROTEIN TYROSINE KINASE; REAGENT; T LYMPHOCYTE RECEPTOR;

ANTIGEN BINDING; ARTICLE; CALCIUM MOBILIZATION; CELL SPECIFICITY; COMPLEX FORMATION; CONTROLLED STUDY; CROSS LINKING; CYTOTOXIC T LYMPHOCYTE; DIMERIZATION; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; LYMPHOCYTE CLONE; MAJOR HISTOCOMPATIBILITY COMPLEX; MOLECULE; PHOTOREACTIVITY; PLASMODIUM BERGHEI; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; SPOROZOITE; SUSPENSION; T LYMPHOCYTE ACTIVATION;

ANIMALS; ANTIGENS, CD3; ANTIGENS, CD8; ANTIGENS, PROTOZOAN; BETA-CYCLODEXTRINS; CALCIUM; CELLS, CULTURED; CROSS-LINKING REAGENTS; CYCLODEXTRINS; DETERGENTS; DIMERIZATION; ENZYME ACTIVATION; FLOW CYTOMETRY; HUMANS; LYMPHOCYTE ACTIVATION; LYMPHOCYTE SPECIFIC PROTEIN TYROSINE KINASE P56(LCK); MACROMOLECULAR SUBSTANCES; MEMBRANE MICRODOMAINS; PALMITIC ACID; PLASMODIUM BERGHEI; PROTEIN TRANSPORT; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; SOLUBILITY; T-LYMPHOCYTES, CYTOTOXIC;

EID: 0034998414     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/1521-4141(200105)31:5<1561::AID-IMMU1561>3.0.CO;2-W     Document Type: Article

References (48)

1. Germain, R. N. and Stefanova, I., The dynamics of T cell receptor signaling: complex orchestration and the key roles of tempo and cooperation. Annu. Rev. Immunol. 1999. 17: 467-522.
2. + CTL. In Sitkovsky, M. V. and Henkart, P. A. (Eds.) Cytotoxic cells: basic mechanisms and medical applications. Lippincott Williams & Wilkins, Philadelphia 2000, pp 25-43.
3. Boniface, J. J., Rabinowitz, J. D., Wulfing, C., Hampl, J., Reich, Z., Altman, J. D., Kantor, R. M., Beeson, C., McConnell, H. M. and Davis, M. M., Initiation of signal transduction through the T cell receptor requires the multivalent engagement of peptide/MHC ligands. Immunity 1998. 9: 459-466.
4. Casares, S., Zong, C. S., Radu, D. L., Miller, A., Bona, C. A. and Brumeanu, T. D., Antigen-specific signaling by a soluble, dimeric peptide/major histocompatibility complex class II/Fc chimera leading to T helper cell type 2 differentiation. J. Exp. Med. 1999. 190: 543-553.
5. Hamad, A. R., O'Herrin, S. M., Lebowitz, M. S., Srikrishnan, A., Bieler, J., Schneck, J. and Pardoll, D., Potent T cell activation with dimeric peptide-major histocompatibility complex class II ligand: the role of CD4 coreceptor. J. Exp. Med. 1998. 188: 1633-1640.
6. Cochran, J. R., Cameron, T. O. and Stern, L. J., The relationship of MHC-peptide binding and T cell activation probed using chemically defined MHC class II oligomers. Immunity 2000. 12: 241-250.
7. Delon, J., Gregoire, C., Malissen, B., Darche, S., Lemaitre, F., Kourilsky, P., Abastado, J. P. and Trautmann, A., CD8 expression allows T cell signaling by monomeric peptide-MHC complexes. Immunity 1998. 9: 467-473.
8. Daniels, M. A. and Jameson, S. C., Critical role for CD8 in T cell receptor binding and activation by peptide/major histocompatibility complex multimers. J. Exp. Med. 2000. 191: 335-346.
9. Luescher, I. F., Vivier, E., Layer, A., Mahiou, J., Godeau, F., Malissen, B. and Romero, P., CD8 modulation of T cell antigen receptor-ligand interactions on living cytotoxic T lymphocytes. Nature 1995. 373: 353-356.
10. + CTL clones is determined by the frequency of serial TCR engagement. J. Immunol. 1998. 161: 553-562.
11. Irie, H. Y., Ravichandran, K. S. and Burakoff, S. J., CD8 beta chain influences CD8 alpha chain-associated Lck kinase activity. J. Exp. Med. 1995. 181: 1267-1273.
12. Zamoyska, R., The CD8 coreceptor revisited: one chain good, two chains better. Immunity 1994. 1: 243-246.
13. Bosselut, R., Zhang, W., Ashe, J. M., Kopacz, J. L., Samelson, L. E. and Singer, A., Association of the adaptor molecule LAT with CD4 and CD8 coreceptors identifies a new coreceptor function in T cell receptor signal transduction. J. Exp. Med. 1999. 190: 1517-1526.
14. + T cells in the thymus. Immunity 2000. 12: 409-418.
15. Arcaro, A., Gregoire, C., Boucheron, N., Stotz, S., Palmer, E., Malissen, B. and Luescher, I. F., Essential role of CD8 palmitoylation in CD8 coreceptor function. J. Immunol. 2000. 165: 2068-2076.
16. Irie, H. Y., Mong, M. S., Itano, A., Crooks, M. E., Littman, D. R., Burakoff, S. J. and Robey, E., The cytoplasmic domain of CD8 beta regulates Lck kinase activation and CD8T cell development. J. Immunol. 1998. 161: 183-191.
17. Melkonian, K. A., Ostermeyer, A. G., Chen, J. Z., Roth, M. G. and Brown, D. A., Role of lipid modifications in targeting proteins to detergent-resistant membrane rafts. Many raft proteins are acylated, while few are prenylated. J. Biol. Chem. 1999. 274: 3910-3917.
18. Simons, K. and Ikonen, E., Functional rafts in cell membranes. Nature 1997. 387: 569-572.
19. Friedrichson, T. and Kurzchalia, T. V., Microdomains of GPI-anchored proteins in living cells revealed by crosslinking. Nature 1998. 394: 802-805.
20. Varma, R. and Mayor, S., GPI-anchored proteins are organized in submicron domains at the cell surface. Nature 1998. 394: 798-801.
21. Crise, B. and Rose, J. K., Identification of palmitoylation sites on CD4, the human immunodeficiency virus receptor. J. Biol. Chem. 1992. 267: 13593-13597.
22. Zhang, W., Trible, R. P. and Samelson, L. E., LAT palmitoylation: its essential role in membrane microdomain targeting and tyrosine phosphorylation during T cell activation. Immunity 1998. 9: 239-246.
23. van't Hof, W. and Resh, M. D., Rapid plasma membrane anchoring of newly synthesized p59fyn: selective requirement for NH2-terminal myristoylation and palmitoylation at cysteine-3. J. Cell Biol. 1997. 136: 1023-1035.
24. Ashwell, J. D. and D'Oro, U., CD45 and Src-family kinases: and now for something completely different. Immunol. Today 1999. 20: 412-416.
25. Leitenberg, D., Boulin, Y., Lu, D. D. and Bottomly, K., Biochemical association of CD45 with the T cell receptor complex: regulation by CD45 isoform and during T cell activation. Immunity 1999. 10: 701-711.
26. Leupin, O., Zaru, R., Laroche, T., Muller, S. and Valitutti, S., Exclusion of CD45 from the T cell receptor signaling area in antigen-stimulated T lymphocytes. Curr. Biol. 2000. 10: 277-280.
27. Montixi, C., Langlet, C., Bernard, A. M., Thimonier, J., Dubois, C., Wurbel, M. A., Chauvin, J. P., Pierres, M. and He, H. T., Engagement of T cell receptor triggers its recruitment to low-density detergent-insoluble membrane domains. EMBO J. 1998. 17:5334-5348.
28. Xavier, R., Brennan, T., Li, Q., McCormack, C. and Seed, B., Membrane compartmentation is required for efficient T cell activation. Immunity 1998. 8: 723-732.
29. Lin, J., Weiss, A. and Finco, T. S., Localization of LAT in glycolipid-enriched microdomains is required for T cell activation. J. Biol. Chem. 1999. 274: 28861-28864.
30. Luescher, I. F., Anjuere, F., Peitsch, M. C., Jongeneel, C. V., Cerottini, J. C. and Romero, P., Structural analysis of TCR-ligand interactions studied on H-2Kd-restricted cloned CTL specific for a photoreactive peptide derivative. Immunity 1995. 3: 51-63.
31. Valitutti, S., Dessing, M., Aktories, K., Gallati, H. and Lanzavecchia, A., Sustained signaling leading to T cell activation results from prolonged occupancy. Role of T cell cytoskeleton. J. Exp. Med. 1995. 181: 577-584.
32. Kessler, B., Hudrisier, D., Cerottini, J. C. and Luescher, I. F., Role of CD8 in aberrant function of cytotoxic T lymphocytes. J. Exp. Med. 1997. 186: 2033-2038.
33. Kwong, J. and Lublin, D. M., Amino-terminal palmitate or polybasic domain can provide required second signal to myristate for membrane binding of p56lck. Biochem. Biophys. Res. Commun. 1995. 207: 868-876.
34. Wolven, A., Okamura, H., Rosenblatt, Y. and Resh, M. D., Palmitoylation of p59fyn is reversible and sufficient for plasma membrane association. Mol. Biol. Cell. 1997. 8: 1159-1173.
35. Shenoy-Scaria, A. M., Dietzen, D. J., Kwong, J., Link, D. C. and Lublin, D. M., Cysteine3 of Src family protein tyrosine kinase determines palmitoylation and localization in caveolae. J. Cell. Biol. 1994. 126: 353-363.
36. Janes, P. W., Ley, S. C. and Magee, A. I., Aggregation of lipid rafts accompanies signaling via the T cell antigen receptor. J. Cell Biol. 1999. 147: 447-461.
37. Resh, M. D., Fatty acylation of proteins: new insights into membrane targeting of myristoylated and palmitoylated proteins. Biochim. Biophys. Acta 1999. 1451: 1-16.
38. Legler, D. F., Doucey, M.-A., Cerottini, J.-C., Bron, C., Luescher, I., Selective inhibition of CTL activation by a dipalmitoyl-phospholipid that prevents recruitment of signaling molecules to lipid rafts. FASEB J. 2001, in press.
39. Webb, Y., Hermida-Matsumoto, L. and Resh, M. D., Inhibition of protein palmitoylation, raft localization, and T cell signaling by 2-bromopalmitate and polyunsaturated fatty acids. J. Biol. Chem. 2000. 275: 261-270.
40. Yamaguchi, H. and Hendrickson, W. A., Structural basis for activation of human lymphocyte kinase Lck upon tyrosine phosphorylation. Nature 1996. 384: 484-489.
41. Chan, A. C., Iwashima, M., Turck, C. W. and Weiss, A., ZAP-70: a 70 kDa protein-tyrosine kinase that associates with the TCRζ; chain. Cell 1992. 71: 649-662.
42. Thome, M., Germain, V., DiSanto, J. P. and Acuto, O., The p56lck SH2 domain mediates recruitment of CD8/p56lck to the activated T cell receptor/CDζ complex. Eur. J. Immunol. 1996. 26: 2093-2100.
43. Zhang, W., Sloan-Lancaster, J., Kitchen, J., Trible, R. P. and Samelson, L. E., LAT: the ZAP-70 tyrosine kinase substrate that links T cell receptor to cellular activation. Cell 1998. 92: 83-92.
44. Finco, T. S., Kadlecek, T., Zhang, W., Samelson, L. E. and Weiss, A., LAT is required for TCR-mediated activation of PLCgamma1 and the Ras pathway. Immunity 1998. 9: 617-626.
45. Stulnig, T.M., Berger, M., Sigmund, T., Raederstorff, D., Stockinger, H., and Waldhausl, W., Polyunsaturated fatty acids inhibit T cell signal transduction by modification of detergent-insoluble membrane domains. J. Cell Biol. 1998 143:637-644.
46. Altman, J. D., Moss, P. A. H., Goulder, P. J. R., Barouch, D. H., McHeyzer-Williams, M. G., Bell, J. I., McMichael, A. J. and Davis, M. M., Phenotypic analysis of antigen-specific T lymphocytes. Science 1996. 274: 94-96.
47. Hanke, T., Samuel, R. V., Blanchard, T. J., Neumann, V. C., Allen, T. M., Boyson, J. E., Sharpe, S. A., Cook, N., Smith, G. L., Watkins, D. I., Cranage, M. P. and McMichael, A. J., Effective induction of simian immunodeficiency virus-specific cytotoxic T lymphocytes in macaques by using a multiepitope gene and DNA prime-modified vaccinia virus Ankara boost vaccination regimen. J. Virol. 1999. 73: 7524-7532.
48. Anel, A., Martinez-Lorenzo, M. J., Schmitt-Verhulst, A. M. and Boyer, C., Influence on CD8 of TCR/CD3-generated signals in CTL clones and CTL precursor cells. J. Immunol. 1997. 158-19-28.