Syk and ZAP-70 mediate recruitment of p56lck/CD4 to the activated T cell receptor/CD3/zeta complex

doi:10.1084/jem.181.6.1997

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Syk and ZAP-70 mediate recruitment of p56lck/CD4 to the activated T cell receptor/CD3/zeta complex

M Thome, P Duplay, M Guttinger and O Acuto
Department of Immunology, Institut Pasteur, Paris, France.

During antigen recognition by T cells, CD4 and the T-cell receptor (TCR)/CD3/zeta complex are thought to interact with the same major histocompatibility complex II molecule in a stable ternary complex. Evidence has suggested that the association of CD4 with TCR/CD3/zeta requires the interaction of the protein tyrosine kinase p56lck with CD4. We have taken a biochemical approach to understand the mechanism by which p56lck and, in particular, its src homology (SH) 2 domain contributes to the association of CD4 with TCR/CD3/zeta during activation. We have previously shown that the p56lck SH2 domain binds directly to tyrosine-phosphorylated ZAP-70. Here we formally demonstrate the in vivo association of p56lck with the homologous protein tyrosine kinases Syk and ZAP-70 after CD3 stimulation of Jurkat cells. A tyrosine-phosphorylated peptide containing the sequence predicted to be optimal for binding to the SH2 domain of src family kinases specifically competes for this association, indicating that tyrosine-phosphorylated ZAP-70 and Syk bind to p56lck by an SH2- mediated interaction. We also show that the same peptide is able to compete for the activation-dependent TCR/CD4 association in Jurkat cells. Moreover, ZAP-70 and CD4 cocap only after CD3 stimulation in human T lymphoblasts. We propose that the interaction of the p56lck SH2 domain with zeta-associated tyrosine-phosphorylated ZAP-70 and/or Syk enables CD4 to associate with antigen-stimulated TCR/CD3/zeta complexes.
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Zeitlmann, L., Knorr, T., Knoll, M., Romeo, C., Sirim, P., Kolanus, W. (1998). T Cell Activation Induced by Novel Gain-of-function Mutants of Syk and ZAP-70. J. Biol. Chem. 273: 15445-15452 [Abstract] [Full Text]
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Farber, D. L. (1998). Cutting Edge Commentary: Differential TCR Signaling and the Generation of Memory T Cells. J. Immunol. 160: 535-539 [Abstract] [Full Text]
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Mege, D., Di Bartolo, V., Germain, V., Tuosto, L., Michel, F., Acuto, O. (1996). Mutation of Tyrosines 492/493 in the Kinase Domain of ZAP-70 Affects Multiple T-cell Receptor Signaling Pathways. J. Biol. Chem. 271: 32644-32652 [Abstract] [Full Text]
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Couture, C., Deckert, M., Williams, S., Russo, F. O., Altman, A., Mustelin, T. (1996). Identification of the Site in the Syk Protein Tyrosine Kinase That Binds the SH2 Domain of Lck. J. Biol. Chem. 271: 24294-24299 [Abstract] [Full Text]
Duplay, P., Alcover, A., Fargeas, C., Sekaly, R. P., Branton, P. E. (1996). An Activated Epidermal Growth Factor Receptor/Lck Chimera Restores Early T Cell Receptor-mediated Calcium Response in a CD45-deficient T Cell Line. J. Biol. Chem. 271: 17896-17902 [Abstract] [Full Text]
August, A., Dupont, B. (1996). Association between Mitogen-activated Protein Kinase and the [IMAGE] Chain of the T Cell Receptor (TcR) with the SH2,3 Domain of p56[IMAGE]. J. Biol. Chem. 271: 10054-10059 [Abstract] [Full Text]
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