Tyrosine Phosphorylation Sites at Amino Acids 239 and 240 of Shc Are Involved in Epidermal Growth Factor-Induced Mitogenic Signaling That Is Distinct from Ras/Mitogen-Activated Protein Kinase Activation

REFERENCES

• Barone, M. V., and S. A. Courtneidge. 1995. Myc but not Fos rescue of PDGF signaling block caused by kinase-inactive Src. Nature 378:509–512.
   PubMed Web of Science ®Google Scholar
• Basu, T., P. H. Warne, and J. Downward. 1994. Role of Shc in the activation of Ras in response to epidermal growth factor and nerve growth factor. Oncogene 9:3483–3491.
   PubMedGoogle Scholar
• Batzer, A. G., D. Rotin, J. M. Urena, E. Y. Skolnik, and J. Schlessinger. 1994. Hierarchy of binding sites for Grb2 and Shc on the epidermal growth factor receptor. Mol. Cell. Biol. 14:5192–5201.
   PubMed Web of Science ®Google Scholar
• Bazter, A. G., P. Blaikie, K. Nelson, J. Schlessinger, and B. Margolis. 1995. The phosphotyrosine interaction domain of Shc binds an LXNPXY motif on the epidermal growth factor receptor. Mol. Cell. Biol. 15:4403–4409.
   PubMedGoogle Scholar
• Boyle, W. J., P. van der Geer, and T. Hunter. 1991. Phosphopeptide mapping and phosphoamino acid analysis by two-dimensional separation on thin-layer cellulose plates. Methods Enzymol. 201:110–149.
   PubMed Web of Science ®Google Scholar
• Buday, L., and J. Downward. 1993. Epidermal growth factor regulates p21ras through the formation of a complex with receptor, Grb2 adaptor protein, and SOS nucleotide exchange factor. Cell 73:611–620.
   PubMed Web of Science ®Google Scholar
• Burgering, B. M. T., A. M. M. de Vries-Smits, R. H. Medema, P. C. van Weeren, L. G. J. Tertoolen, and J. L. Bos. 1993. Epidermal growth factor induces phosphorylation of extracellular signal-regulated kinase 2 via multiple pathways. Mol. Cell. Biol. 13:7248–7256.
   PubMedGoogle Scholar
• Chardin, P., J. Camonis, W. L. Gale, L. V. Aelst, J. Schlessinger, M. H. Wigler, and D. Bar-Sagi. 1993. Human Sos1: a guanine nucleotide exchange factor for Ras that binds to GRB2. Science 260:1338–1343.
   PubMed Web of Science ®Google Scholar
• Chen, Y.-H., D. Grall, A. E. Salcini, P. G. Pelicci, J. Pouysségur, and E. Van Obberghen-Schilling. 1996. Shc adaptor proteins are key transducers of mitogenic signaling mediated by the G protein-coupled thrombin receptor. EMBO J. 15:1037–1044.
   PubMedGoogle Scholar
• Cohen, G. B., R. Reu, and D. Baltimore. 1995. Modular binding domains in signal transduction proteins. Cell 80:237–248.
   PubMed Web of Science ®Google Scholar
• Decker, S. J. 1993. Transmembrane signaling by epidermal growth factor receptors lacking autophosphorylation sites. J. Biol. Chem. 268:9176–9179.
   PubMed Web of Science ®Google Scholar
• Downward, J., P. Parker, and M. D. Waterfield. 1984. Autophosphorylation sites on the epidermal growth factor receptor. Nature 311:483–485.
   PubMed Web of Science ®Google Scholar
• Eilers, M., S. Schirm, and J. M. Bishop. 1991. The Myc protein activates transcription of the alpha-prothymosin gene. EMBO J. 10:133–141.
   PubMed Web of Science ®Google Scholar
• Feig, L. A., and G. M. Cooper. 1988. Inhibition of NIH 3T3 cell proliferation by a mutant ras protein with preferential affinity for GDP. Mol. Cell. Biol. 8:3235–3243.
   PubMed Web of Science ®Google Scholar
• Gale, N. W., S. Kaplan, E. J. Lowenstein, J. Schlessinger, and D. Bar-Sagi. 1993. Grb2 mediates the EGF-dependent activation of guanine nucleotide exchange on Ras. Nature 363:88–92.
   PubMed Web of Science ®Google Scholar
• Goga, A., J. McLaughilin, D. E. H. Afar, D. C. Saffran, and O. N. Witte. 1995. Alternative signals to RAS for haematopoietic transformation by the BCR- ABL oncogene. Cell 82:981–988.
   PubMed Web of Science ®Google Scholar
• Gotoh, N., K. Muroya, S. Hattori, S. Nakamura, K. Chida, and M. Shibuya. 1995. The SH2 domain of Shc suppresses EGF-induced mitogenesis in a dominant negative manner. Oncogene 11:2525–2533.
   PubMedGoogle Scholar
• Gotoh, N., A. Tojo, K. Muroya, Y. Hashimoto, S. Hattori, S. Nakamura, T. Takenawa, Y. Yazaki, and M. Shibuya. 1994. Epidermal growth factorreceptor mutant lacking the autophosphorylation sites induces phosphorylation of Shc protein and Shc-Grb2/Ash association and retains mitogenic activity.1994. Proc. Natl. Acad. Sci. USA 91:167–171.
   PubMedGoogle Scholar
• Gotoh, N., A. Tojo, M. Hino, Y. Yazaki, and M. Shibuya. 1992. A highly conserved tyrosine residue at codon 845 within the kinase domain is not required for the transforming activity of human epidermal growth factor receptor. Biochem. Biophys. Res. Commun. 186:768–774.
   PubMedGoogle Scholar
• Gotoh, N., A. Tojo, and M. Shibuya. 1996. A novel pathway from phosphorylation of tyrosine residues 239/240 of Shc, contributing to suppress apoptosis by IL3. EMBO J. 15:6197–6204.
   PubMedGoogle Scholar
• Greenberg, M. E., and E. B. Ziff. 1984. Stimulation of 3T3 cells induces transcription of the c-fos proto-oncogene. Nature 311:433–437.
   PubMed Web of Science ®Google Scholar
• Hasegawa, H., E. Kiyokawa, S. Tanaka, K. Nagashima, N. Gotoh, M. Shibuya, T. Kurata, and M. Matsuda. 1996. DOCK 180, a major CRK- binding protein, alters cell morphology upon translocation to the cell membrane. Mol. Cell. Biol. 16:1770–1776.
   PubMed Web of Science ®Google Scholar
• Heikkila, R., G. Schwab, E. Wickstrom, S. L. Loke, D. H. Pluznik, R. Watt, and L. M. Neckers. 1987. A c-myc antisense oligodeoxynucleotide inhibits entry into S phase but not progress from G0 to G1. Nature 328:445–449.
   PubMed Web of Science ®Google Scholar
• Helin, K., T. Velu, P. Martin, W. C. Vass, G. Allevato, D. R. Lowy, and L. Beguinot. 1991. The biological activity of the human epidermal growth factor receptor is positively regulated by its C-terminal tyrosines. Oncogene 6:825–832.
   PubMedGoogle Scholar
• Hill, C. S., and R. Treisman. 1995. Transcriptional regulation by extracellular signals: mechanisms and specificity. Cell 80:199–211.
   PubMed Web of Science ®Google Scholar
• Honegger, A., T. J. Dull, F. Bellot, E. Van Obberghen, D. Szapery, A. Schmidt, A. Ullrich, and J. Schlessinger. 1988. Biological activities of EGF- receptor mutants with individually altered autophosphorylation sites. EMBO J. 7:3045–3052.
   PubMedGoogle Scholar
• Karunagaran, D., E. Tzahar, R. R. Beerli, X. Chen, D. Graus-Prota, B. J. Ratzkin, R. Segar, N. E. Hynes, and Y. Yarden. 1996. ErbB-2 is a common auxiliary subunit of NDF and EGF receptors: implications for breast cancer. EMBO J. 15:254–264.
   PubMed Web of Science ®Google Scholar
• Kavanaugh, W. M., and L. T. Williams. 1994. An alternative to SH2 domains for binding tyrosine-phosphorylated proteins. Science 266:1862–1865.
   PubMed Web of Science ®Google Scholar
• Kim, H. K., J. W. Kim, A. Zilberstein, B. Margolis, J. G. Kim, J. Schlessinger, and S. G. Rhee. 1991. PDGF stimulation of inositol phospholipid hydrolyses requires PLC-g1 phosphorylation on tyrosine residues 783 and 1254. Cell 65:435–441.
   PubMed Web of Science ®Google Scholar
• Koch, C. A., D. Anderson, M. F. Moran, C. Ellis, and T. Pawson. 1991. SH2 and SH3 domains; elements that control interactions of cytoplasmic signaling proteins. Science 252:668–674.
   PubMed Web of Science ®Google Scholar
• Lai, K. M., J. P. Olivier, G. D. Gish, M. Henkemeyer, J. McGlade, and T. Pawson. 1995. A Drosophila Shc gene product is implicated in signaling by the DER receptor tyrosine kinase. Mol. Cell. Biol. 15:4810–4818.
   PubMedGoogle Scholar
• Land, H., L. F. Parada, and R. A. Weinberg. 1983. Tumorigenic conversion of primary embryo fibroblasts requires at least two cooperating oncogenes. Nature 304:596–602.
   PubMed Web of Science ®Google Scholar
• Li, N., A. Batzer, R. Daley, V. Yajnik, E. Skolnik, P. Chardin, D. Bar-Sagi, B. Margolis, and J. Schlessinger. 1993. Guanine-nucleotides-releasing factor hSOS1 binds to Grb2 and links receptor tyrosine kinases to Ras signalling. Nature 363:85–88.
   PubMed Web of Science ®Google Scholar
• Li, N., J. Schlessinger, and B. Margolis. 1994. Autophosphorylation mutants of the EGF-receptor signal through auxiliary mechanisms involving SH2 domain proteins. Oncogene 9:3457–3465.
   PubMedGoogle Scholar
• Lowenstein, E. J., R. J. Daly, A. G. Batzer, W. Li, B. Margolis, R. Lammers, A. Ullrich, and J. Schlessinger. 1992. The SH2 and SH3 domain-containing protein GRB2 links receptor tyrosine kinases to ras signaling. Cell 7:431–442.
   Google Scholar
• Marais, R., J. Wynne, and R. Treisman. 1993. The SRF accessory protein Elk-1 contains a growth factor-regulated transcriptional activation domain. Cell 73:381–393.
   PubMed Web of Science ®Google Scholar
• Margolis, B. L., I. Lax, R. Kris, M. Dombalagian, A. M. Honegger, R. Howk, D. Givol, A. Ullrich, and J. Schlessinger. 1989. All autophosphorylation sites of epidermal growth factor (EGF) receptor and HER2/neu are located in their carboxyl-terminal tails. J. Biol. Chem. 264:10667–10671.
   PubMed Web of Science ®Google Scholar
• Marshall, C. J. 1994. MAP kinase kinase kinase, MAP kinase kinase and MAP kinase. Curr. Opin. Genet. Dev. 4:82–89.
   PubMed Web of Science ®Google Scholar
• Matsuoka, K., M. Shibata, A. Yamakawa, and T. Takenawa. 1992. Cloning of ASH, a ubiquitous protein composed of one Src homology region (SH) 2 and two SH3 domains, from human and rat cDNA libraries. Proc. Natl. Acad. Sci. USA 89:9015–9019.
   PubMed Web of Science ®Google Scholar
• McGlade, J., A. Cheng, G. Pellici, P. G. Pelicci, and T. Pawson. 1992. Shc proteins are phosphorylated and regulated by the v-src and c-fps protein tyrosine kinases. Proc. Natl. Acad. Sci. USA 89:8869–8873.
   PubMedGoogle Scholar
• Mulcahy, L. S., M. R. Smith, and D. W. Stacey. 1985. Requirement of ras proto-oncogene function during serum-stimulated growth of NIH 3T3 cells. Nature 313:241–243.
   PubMed Web of Science ®Google Scholar
• MuÈller, R., R. Bravo, J. Burckhardt, and T. Curran. 1984. Induction of c-fos gene and protein by growth factors precedes activation of c-myc. Nature 312:716–720.
   PubMedGoogle Scholar
• Pawson, T. 1995. Protein modules and signalling networks. Nature 373:573–580.
   PubMed Web of Science ®Google Scholar
• Pelicci, G., L. Lanfrancone, F. Grignani, J. McGlade, F. Cavallo, G. Forni, I. Nicoletti, F. Grignani, T. Pawson, and P. G. Pelicci. 1992. A novel transforming protein (SHC) with an SH2 domain is implicated in mitogenic signal transduction. Cell 70:93–104.
   PubMed Web of Science ®Google Scholar
• Pronk, G. J., A. M. M. Vries-Smits, L. Buday, J. Downward, J. A. Maassen, R. H. Medema, and J. L. Bos. 1994. Involvement of Shc in insulin- and epidermal growth factor-induced activation of p21ras. Mol. Cell. Biol. 14:1575–1581.
   PubMedGoogle Scholar
• Rollins, B. J., and C. D. Stiles. 1989. Serum inducible genes. Adv. Cancer Res. 53:1–32.
   PubMedGoogle Scholar
• Rotin, D., B. Margolis, M. Mohammadi, R. J. Daly, G. Daum, N. Li, E. H. Fischer, W. H. Burgess, A. Ullrich, and J. Schlessinger. 1992. SH2 domains prevent tyrosine dephosphorylation of the EGF receptor: identification of Y992 as the high-affinity binding site for SH2 domain of phospholipase Cγ. EMBO J. 11:559–567.
   PubMedGoogle Scholar
• Roussel, M. F., S. A. Shurtleff, J. R. Downing, and C. J. Sherr. 1990. A point mutation at tyrosine-809 in the human colony-stimulating factor 1 receptor impairs mitogenesis without abrogating tyrosine kinase activity, association with phosphatidyl inositol 3-kinase, or induction of c-fos and jun B genes. Proc. Natl. Acad. Sci. USA 87:6738–6742.
   PubMed Web of Science ®Google Scholar
• Rozakis-Adcock, M., J. McGlade, G. Mbamalu, G. Pelicci, R. Daly, W. Li, A. Batzer, S. Thomas, J. Brugge, P. G. Pelicci, J. Schlessinger, and T. Pawson. 1992. Association of the Shc and Grb2/sem5 SH2-containing proteins is implicated in activation of the Ras pathway by tyrosine kinases. Nature 360:689–692.
   PubMed Web of Science ®Google Scholar
• Rozakis-Adcock, M., R. Fernley, J. Wade, T. Pawson, and D. Bowtell. 1993. The SH2 and SH3 domains of mammalian Grb2 couple the EGF receptor to the Ras activator mSOS1. Nature 363:83–85.
   PubMed Web of Science ®Google Scholar
• Salcini, A. E., J. McGlade, G. Pelicci, I. Nicoletti, T. Pawson, and P. G. Pelicci. 1994. Formation of Shc-Grb2 complexes is necessary to induce neoplastic transformation by overexpression of Shc proteins. Oncogene 9:2827–2836.
   PubMedGoogle Scholar
• Sasaoka, T., D. W. Rose, B. H. Jhun, A. R. Saltiel, B. Draznin, and J. M. Olfesky. 1994. Evidence for a functional role of Shc proteins in mitogenic signaling induced by insulin, insulin-like growth factor-1, and epidermal growth factor. J. Biol. Chem. 269:13689–13694.
   PubMed Web of Science ®Google Scholar
• Sasaoka, T., W. J. Langlois, F. Bai, D. W. Rose, J. W. Leiter, S. J. Decker, A. Saltiel, G. N. Gill, M. Kobayashi, B. Draznin, and J. M. Olfesky. 1996. Involvement of ErbB2 in the signaling pathway leading to cell cycle progression from a truncated epidermal growth factor receptor lacking the C- terminal autophosphorylation sites. J. Biol. Chem. 271:8338–8344.
   PubMedGoogle Scholar
• Satoh, T., M. Endo, M. Nakafuku, T. Akiyama, T. Yamamoto, and Y. Kaziro. 1990. Accumulation of p21ras-GTP in response to stimulation with epidermal growth factor and oncogene products with tyrosine kinase activity. Proc. Natl. Acad. Sci. USA 87:7926–7929.
   PubMed Web of Science ®Google Scholar
• Seetharam, L., N. Gotoh, Y. Maru, G. Neureld, S. Yamaguchi, and M. Shibuya. 1995. A unique signal transduction from FLT tyrosine kinase, a receptor for vascular endothelial growth factor VEGF. Oncogene 10:135–147.
   PubMed Web of Science ®Google Scholar
• Skolnik, E. Y., C. H. Lee, A. G. Batzer, L. M. Vincentini, M. Zhou, R. Daly, M. J. Myers, Jr., J. M. Backer, A. Ullrich, M. F. White, and J. Schlessinger. 1993. The SH2/SH3 domain-containing protein GRB2 interacts with tyrosine-phosphorylated IRS1 and Shc: implications for insulin control of ras signaling. EMBO J. 12:1929–1936.
   PubMed Web of Science ®Google Scholar
• Spencer, C. A., and M. Groudine. 1991. Control of c-myc regulation in normal and neoplastic cells. Adv. Cancer Res. 56:1–48.
   PubMed Web of Science ®Google Scholar
• SzebereÂngi, H. C. J., and G. M. Cooper. 1990. Effect of a dominant inhibitory Ha-ras mutation on mitogenic signal transduction in NIH 3T3 cells. Mol. Cell. Biol. 10:5314–5323.
   PubMedGoogle Scholar
• Ullrich, A., and J. Schlessinger. 1990. Signal transduction by receptors with tyrosine kinase activity. Cell 61:203–212.
   PubMed Web of Science ®Google Scholar
• Walton, G. M., W. S. Chen, M. G. Rosenfeld, and G. N. Gill. 1990. Analysis of deletions of the carboxy terminus of the epidermal growth factor receptor reveals self-phosphorylation at tyrosine 992 and enhanced in vivo tyrosine phosphorylation of cell substrates. J. Biol. Chem. 265:1750–1754.
   PubMedGoogle Scholar
• Wary, K. K., F. Mainiero, S. J. Isakoff, E. E. Marcantonio, and F. G. Giancotti. 1996. The adaptor protein Shc couples a class of integrins to the control of cell cycle progression. Cell 87:733–743.
   PubMed Web of Science ®Google Scholar