Hypophosphorylated TCR/CD3ζ signals through a Grb2-SOS1-Ras pathway in Lck knockdown cells

European Journal of Immunology

Volumn 37, Issue 9, 2007, Pages 2539-2548

  Methi, Trond ^a   Ngai, Jacob ^a   Vang, Torkel ^a   Torgersen, Knut M ^a   Taskén, Kjetil ^a  

^a UNIVERSITY OF OSLO   (Norway)

Author keywords

CD3 ; Lck; Ras; Signal Transduction; T cell receptors

Indexed keywords

CD3 ANTIGEN; CD3ZETA ANTIGEN; CELL PROTEIN; GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; INTERLEUKIN 2; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; OKT 3; PROTEIN KINASE LCK; RAS PROTEIN; SOS PROTEIN; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR NFAT; TYROSINE BASED ACTIVATION MOTIF 1; UNCLASSIFIED DRUG; CD3 ANTIGEN, ZETA CHAIN; LYMPHOCYTE ANTIGEN RECEPTOR; PHOSPHOTYROSINE; SMALL INTERFERING RNA;

ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; NEGATIVE FEEDBACK; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; AMINO ACID SEQUENCE; CELL LINE; CHEMISTRY; ENZYME ACTIVATION; GENETICS; METABOLISM; MOLECULAR GENETICS; PHOSPHORYLATION;

AMINO ACID SEQUENCE; ANTIGENS, CD3; CELL LINE; ENZYME ACTIVATION; GRB2 ADAPTOR PROTEIN; HUMANS; LYMPHOCYTE SPECIFIC PROTEIN TYROSINE KINASE P56(LCK); MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PHOSPHOTYROSINE; PROTEIN BINDING; RAS PROTEINS; RECEPTORS, ANTIGEN, T-CELL; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SOS1 PROTEIN;

EID: 34548809782     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200636973     Document Type: Article

References (36)

1. Mustelin, T., Abraham, R. T., Rudd, C. E., Alonso, A. and Merlo, J. J., Protein tyrosine phosphorylation in T cell signaling. Front. Biosci. 2002. 7: 918-969.
2. Latour, S. and Veillette, A., Proximal protein tyrosine kinases in immunoreceptor signaling. Curr. Opin. Immunol. 2001. 13: 299-306.
3. Pitcher, L. A. and van Oers, N. S., T-cell receptor signal transmission: Who gives an ITAM? Trends Immunol. 2003. 24: 554-560.
4. Chan, A. C., Irving, B. A., Fraser, J. D. and Weiss, A., The zeta chain is associated with a tyrosine kinase and upon T-cell antigen receptor stimulation associates with ZAP-70, a 70-kDa tyrosine phosphoprotein. Proc. Natl. Acad. Sci. USA 1991. 88: 9166-9170.
5. Di Bartolo, V., Mege, D., Germain, V., Pelosi, M., Dufour, E., Michel, F., Magistrelli, G. et al., Tyrosine 319, a newly identified phosphorylation site of ZAP-70, plays a critical role in T cell antigen receptor signaling. J. Biol. Chem. 1999. 274: 6285-6294.
6. 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.
7. Jordan, M. S., Singer, A. L. and Koretzky, G. A., Adaptors as central mediators of signal transduction in immune cells. Nat. Immunol. 2003. 4: 110-116.
8. Su, B. and Karin, M., Mitogen-activated protein kinase cascades and regulation of gene expression. Curr. Opin. Immunol. 1996. 8: 402-411.
9. Ravichandran, K. S., Lee, K. K., Songyang, Z., Cantley, L. C., Burn, P. and Burakoff, S. J., Interaction of Shc with the zeta chain of the T cell receptor upon T cell activation. Science 1993. 262: 902-905.
10. Chardin, P., Camonis, J. H., Gale, N. W., van Aelst, L., Schlessinger, J., Wigler, M. H. and Bar-Sagi, D., Human Sos1: A guanine nucleotide exchange factor for Ras that binds to GRB2. Science 1993. 260: 1338-1343.
11. Ebinu, J. O., Stang, S. L., Teixeira, C., Bottorff, D. A., Hooton, J., Blumberg, P. M., Barry, M. et al., RasGRP links T-cell receptor signaling to Ras. Blood 2000. 95: 3199-3203.
12. Amrein, K. E., Flint, N., Panholzer, B. and Burn, P., Ras GTPase-activating protein: A substrate and a potential binding protein of the protein-tyrosine kinase p561ck. Proc. Natl. Acad. Sci. USA 1992. 89: 3343-3346.
13. Liu, X. Q. and Pawson, T., The epidermal growth factor receptor phosphorylates GTPase-activating protein (GAP) at Tyr-460, adjacent to the GAP SH2 domains. Mol. Cell. Biol. 1991. 11: 2511-2516.
14. Park, S. and Jove, R., Tyrosine pbosphorylation of Ras GTPase-activating protein stabilizes its association with p62 at membranes of v-Src transformed cells. J. Biol. Chem. 1993. 268: 25728-25734.
15. Yu, X Z., Levin, S. D., Madrenas, J. and Anasetti, C., Lck is required for activation-induced T cell death after TCR ligation with partial agonists. J. Immunol. 2004. 172: 1437-1443.
16. Criado, G. and Madrenas, J., Superantigen stimulation reveals the contribution of Lck to negative regulation of T cell activation. J. Immunol. 2004. 172: 222-230.
17. Methi, T., Ngai, J., Mahic, M., Amarzguioui, M., Vang, T. and Tasken, K., Short-interfering RNA-mediated Lck knockdown results in augmented downstream T cell responses. J. Immunol. 2005. 175: 7398-7406.
18. Bueno, C., Lemke, C. D., Criado, G., Baroja, M. L., Ferguson, S. S., Rahman, A. K., Tsoukas, C. D. et al., Bacterial superantigens bypass Lck-dependent T cell receptor signaling by activating a Galphall-dependent, PLC-beta-mediated pathway. Immunity 2006. 25: 67-78.
19. 2+ mobilization and Erk activation in Jurkat T cells in response to T-cell antigen receptor ligation. Mol. Cell. Biol. 2001. 21: 7137-7149.
20. Chau, L. A. and Madrenas, J., Phospho-LAT-independent activation of the ras-mitogen-activated protein kinase pathway: A differential recruitment model of TCR partial agonist signaling. J. Immunol. 1999. 163: 1853-1858.
21. Ravichandran, K. S., Lee, K. K., Songyang, Z., Cantley, L. C., Burn, P. and Burakoff, S. J., Interaction of Shc with the zeta chain of the T cell receptor upon T cell activation. Science 1993. 262: 902-905.
22. Nel, A. E., Gupta, S., Lee, L., Ledbetter, J. A. and Kanner, S. B., Ligation of the T-cell antigen receptor (TCR) induces association of hSos1, ZAP-70, phospholipase C-gamma 1, and other phosphoproteins with Grb2 and the zeta-chain of the TCR. J. Biol. Chem. 1995. 270: 18428-18436.
23. Osman, N., Lucas, S. C., Turner, H. and Cantrell, D., A comparison of the interaction of Shc and the tyrosine kinase ZAP-70 with the T cell antigen receptor zeta chain tyrosine-based activation motif. J. Biol. Chem. 1995. 270: 13981-13986.
24. Zenner, G., Vorherr, T., Mustelin, T. and Burn, P., Differential and multiple binding of signal transducing molecules to the ITAMS of TCR-zeta chain. J. Cell, Biochem. 1996. 63: 94-103.
25. Strauss, D. and Weiss, A., Genetic evidence for the involvement of the lck tyrosine kinase in signal transduction through the T cell antigen receptor. Cell 1992. 70: 585-593.
26. al-Ramadi, B. K., Nakamura, T., Leitenberg, D. and Bothwell, A. L., Deficient expression of p561ck in Th2 cells leads to partial TCR signaling and a dysregulation of lymphokine mRNA levels. J. Immunol. 1996. 157: 4751-4761.
27. Molina, T. J., Kishihara, K., Siderovski, D. P., van Ewijk, W., Narendran, A., Timms, E., Wakeham, A. et al., Profound block in thymocyte development in mice lacking p561ck. Nature 1992. 357: 161-164.
28. Pitcher, L. A., Mathis, M. A., Young, J. A., Deford, L. M., Purtic, B., Wulfing, C. and van Oers, N. S., The CD3 gammaepsilon/ deltaepsilon signaling module provides normal T cell functions in the absence of the TCR zeta immunoreceptor tyrosine-based activation motifs. Eur. J. Immunol. 2005. 35: 3643-3654.
29. Kersh, E. N., Kersh, G. J. and Allen, P. M., Partially phosphorylated T cell receptor zeta molecules can inhibit T cell activation. J. Exp. Med. 1999. 190: 1627-1636.
30. Chae, W. J., Lee, H. K., Han, J. H., Kim, S. W., Bothwell, A. L., Morio, T. and Lee, S. K., Qualitatively differential regulation of T cell activation and apoptosis by T cell receptor zeta chain ITAMs and their tyrosine residues. Int. Immunol. 2004. 16: 1225-1236.
31. Samraj, A. K., Stroh, C., Fischer, U. and Schulze-Osthoff, K., The tyrosine kinase Lck is a positive regulator of the mitochondrial apoptosis pathway by controlling Bak expression. Oncogene 2006. 25: 186-197.
32. Denny, M. F., Kaufman, H. C., Chan, A. C. and Straus, D. B., The Lck SH3 domain is required for activation of the mitogen-activated protein kinase pathway but not the initiation of T-cell antigen receptor signaling. J. Biol. Chem. 1999. 274: 5146-5152.
33. Greenway, A., Azad, A., Mills, J. and McPhee, D., Human immunodeficiency virus type 1 Nef binds directly to Lck and mitogen-activated protein kinase, inhibiting kinase activity. J. Virol. 1996. 70: 6701-6708.
34. Schrager, J. A., Der Minassian, V. and Marsh, J. W., HIV Nef increases T cell ERK MAP kinase activity. J. Biol. Chem. 2002. 277: 6137-6142.
35. Manninen, A., Renkema, G. H. and Saksela, K., Synergistic activation of NFAT by HIV-1 nef and the Ras/MAPK pathway. J. Biol. Chem. 2000. 275: 16513-16517.
36. Lovatt, M., Filby, A., Parravicini, V., Werlen, G., Palmer, E. and Zamoyska, R., Lck regulates the threshold of activation in primary T cells, while both Lck and Fyn contribute to the magnitude of the ERK response. Mol. Cell. Biol. 2006. 26: 8655-8665.