A Drosophila shc Gene Product Is Implicated in Signaling by the DER Receptor Tyrosine Kinase

REFERENCES

• Ashburner, M. 1989. Drosophila: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
   Google 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. Biol. Cell 14:5192–5201.
   Google Scholar
• Blaikie, P., D. Immanuel, J. Wu, N. Li, V. Yajnik, and B. Margolis. 1994. A region in Shc distinct from the SH2 domain can bind tyrosine phosphory-lated growth factor receptors. J. Biol. Chem. 269:32031–32034.
   PubMed Web of Science ®Google Scholar
• Bonfini, L., C. A. Karlovich, C. Dasgupta, and V. Banerjee. 1992. The Son of sevenless gene product: a putative activator of Ras. Science 255:603–606.
   PubMed Web of Science ®Google Scholar
• Buday, L., and J. Downward. 1993. Epidermal growth factor regulates P21ras through the formation of a complex of receptor, Grb2 adaptor protein, and Sos nucleotide exchange factor. Cell 73:611–620.
   PubMed Web of Science ®Google Scholar
• Burns, L. A., L. M. Karnitz, S. L. Sutor, and R. T. Abraham. 1993. Interleukin-2-induced tyrosine phosphorylation of p52shc in T lymphocytes. J. Biol. Chem. 268:17659–17661.
   PubMedGoogle Scholar
• Campbell, K. S., E. Ogris, B. Burke, W. Su, K. R. Auger, B. J. Druker, B. S. Schaffhausen, T. M. Roberts, and D. C. Pallas. 1994. Polyoma middle tumor antigen interacts with SHC protein via the NPTY (Asn-Pro-Thr-Tyr) motif in middle tumor antigen. Proc. Natl. Acad. Sci. USA 91:6344–6348.
   PubMedGoogle Scholar
• Crowe, A. J., J. McGlade, T. Pawson, and M. G. Hayman. 1994. Phosphor-ylation of the SHC proteins on tyrosine correlates with the transformation of fibroblasts and erythroblasts by the v-Sea tyrosine kinase. Oncogene 9:537–544.
   PubMedGoogle Scholar
• Cutler, R. L., L. Liu, J. E. Damen, and G. Krystal. 1993. Multiple cytokines induce the tyrosine phosphorylation of Shc and its association with Grb2 in hematopoietic cells. J. Biol. Chem. 268:21463–21465.
   PubMed Web of Science ®Google Scholar
• Dickson, B., and E. Hafen. 1994. Genetics of signal transduction in invertebrates. Curr. Opin. Genet. Dev. 4:64–70.
   PubMedGoogle Scholar
• Dickson, B., F. Sprenger, and E. Hafen. 1992. Prepattern in the developing Drosophila eye revealed by an activated torso-sevenless chimeric receptor. Genes Dev. 6:2327–2339.
   PubMedGoogle Scholar
• Dilworth, S. M., C. E. Brewster, M. D. Jones, L. Lanfrancone, G. Pelicci, and P. G. Pelicci. 1994. Transformation by polyoma virus middle T-antigen involves the binding and tyrosine phosphorylation of Shc. Nature (London) 367:87–90.
   PubMed Web of Science ®Google Scholar
• Doyle, H. J., and J. M. Bishop. 1993. Torso, a receptor tyrosine kinase required for embryonic pattern formation, shares substrates with the sevenless and EGF-R pathways in Drosophila. Genes Dev. 7:633–646.
   PubMedGoogle Scholar
• Egan, S. E., B. W. Giddings, M. W. Brooks, L. Buday, A. M. Sizeland, and R. Weinberg. 1993. Association of Sos Ras exchange protein with Grb2 is implicated in tyrosine kinase signal transduction and transformation. Nature (London) 363:45–51.
   PubMed Web of Science ®Google Scholar
• Gale, W. N., D. Kaplan, E. J. Lowenstein, J. Schlessinger, and D. Bar-Sagi. 1993. Grb2 mediates the EGF-dependent activation of guanine nucleotide exchange on Ras. Nature (London) 363:88–92.
   PubMed Web of Science ®Google Scholar
• Hafen, E., K. Basler, J. E. Edstroem, and G. M. Rubin. 1987. Sevenless, a cell-specific homoeotic gene of Drosophila, encodes a putative transmem-brane receptor with a tyrosine kinase domain. Science 236:55–63.
   PubMedGoogle Scholar
• Hirai, H., Y. Maru, K. Hagiwara, J. Nishida, and F. Takaku. 1987. A novel putative tyrosine kinase receptor encoded by the eph gene. Science 238: 1717–1719.
   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
• Lai, K.-M. V. Unpublished data.
   Google Scholar
• Lanfrancone, L., G. Pelicci, M. F. Brizzi, M. G. Arouica, C. Casciari, S. Giuli, L. Pegoraro, T. Pawson, and P. G. Pelicci. 1995. Overexpression of Shc proteins potentiates the proliferative response to the granulocyte-macrophage colony-stimulating factor and recruitment of Grb2/Sos and Grb2/p140 complexes to the β receptor subunit. Oncogene 10:905–917.
   Google Scholar
• Leicht, B., and J. Bonner. 1988. Genetic analysis of chromosome region 67A-D of Drosophila. Genetics 119:579–593.
   PubMedGoogle Scholar
• Li, N., A. Batzer, R. Daly, E. Skolnik, P. Chardin, D. Bar-Sagi, B. Margolis, and J. Schlessinger. 1993. Guanine nucleotide releasing factor hSos1 binds to Grb2 and links receptor tyrosine kinases to Ras signaling. Nature (London) 363:85–88.
   PubMed Web of Science ®Google Scholar
• Livneh, E., L. Glazer, D. Segal, J. Schlessinger, and B.-Z. Shilo. 1985. The Drosophila EGF receptor gene homolog: conservation of both hormone binding and kinase domains. Cell 40:599–607.
   PubMedGoogle Scholar
• McGlade, J., A. Cheng, G. Pelicci, P. G. Pelicci, and T. Pawson. 1992. Shc proteins are phosphorylated and regulated by the v-Src and v-Fps protein-tyrosine kinases. Proc. Natl. Acad. Sci. USA 89:8869–8873.
   PubMedGoogle Scholar
• Migliaccio, E., S. Mele, A. E. Salcini, G. Pelicci, K.-M. V. Lai, P. P. Di Fiore, T. Pawson, L. Lanfrancone, and P. G. Pelicci. Submitted for publication.
   Google Scholar
• Obermeier, A., R. Lammers, K. H. Wiesmuller, G. Jung, J. Schlessinger, and A. Ullrich. 1993. Identification of Trk binding sites for SHC and phospha-tidylinositol 39-kinase and formation of a multimeric signaling complex. J. Biol. Chem. 268:22963–22966.
   PubMed Web of Science ®Google Scholar
• O'Bryan, J., T. Saxton, and T. Pawson. Unpublished data.
   Google Scholar
• O'Connell, P. O., and M. Rosbash. 1984. Sequence, structure and codon preference of the Drosophila ribosomal protein 49 gene. Nucleic Acids Res. 12:5495–5513.
   PubMed Web of Science ®Google Scholar
• Olivier, J. P., T. Raabe, M. Henkemeyer, B. Dickson, G. Mbamalu, B. Margolis, J. Schlessinger, E. Hafen, and T. Pawson. 1993. A Drosophila SH2-SH3 adaptor protein implicated in coupling the sevenless tyrosine kinase to an activator of Ras guanine nucleotide exchange, Sos. Cell 73:179–191.
   PubMed Web of Science ®Google Scholar
• Pelicci, G., L. Lanfrancone, F. Grignani, J. McGlade, F. Cavallo, G. Forni, I. Nicoletti, 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
• Prigent, S. A., and W. J. Gullick. 1994. Identification of C-erbB-3 binding sites for phosphatidylinositol 39-kinase and SHC using an EGF-receptor/C-erbB-3 chimera. EMBO J. 13:2831–2841.
   PubMed Web of Science ®Google Scholar
• Pronk, G. J., J. McGlade, G. Pelicci, T. Pawson, and J. L. Bos. 1993. Insulin-induced phosphorylation of the 46- and 52-kDa Shc proteins. J. Biol. Chem. 268:5748–5753.
   PubMed Web of Science ®Google Scholar
• Puil, L., X. Liu, G. Gish, G. Mbamalu, D. Bowtell, P. G. Pelicci, R. Arlinghaus, and T. Pawson. 1994. BCR-ABL oncoproteins bind directly to activators of the ras signalling pathway. EMBO J. 13:764–773.
   PubMed Web of Science ®Google Scholar
• Raabe, T., J. P. Olivier, B. Dickson, X. Liu, G. D. Gish, T. Pawson, and E. Hafen. Biochemical and genetic analysis of Drk SH2/SH3 adaptor protein of Drosophila. EMBO J. 14:2509–2518.
   PubMedGoogle Scholar
• Ravichandran, K. S., and S. J. Burakoff. 1994. The adapter protein Shc interacts with the interleukin-2 (IL-2) receptor upon IL-2 stimulation. J. Biol. Chem. 269:1599–1602.
   PubMedGoogle Scholar
• Ravichandran, K. S., K. K. Lee, Z. Songyang, L. C. Cantley, P. Burn, and S. J. Burakoff. 1993. Interaction of Shc with the ζ chain of the T cell receptor upon T cell activation. Science 262:902–905.
   PubMedGoogle Scholar
• Reichman-Fried, M., B. Dickson, E. Hafen, and B.-Z. Shilo. 1994. Elucidation of the role of breathless, a Drosophila FGF receptor homolog, in tracheal cell migration. Genes Dev. 8:428–439.
   PubMedGoogle 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 mSos1, an activator of Ras. Nature (London) 363:83–85.
   PubMed Web of Science ®Google Scholar
• Rozakis-Adcock, M., J. McGlade, G. Mbamalu, G. Pelicci, R. Daly, W. Li, A. Batzer, P. G. Pelicci, J. Schlessinger, and T. Pawson. 1992. Association of the Shc and Grb2/Sem-5 SH2-containing proteins is implicated in activation of the Ras pathway by tyrosine kinases. Nature (London) 360:689–692.
   PubMed Web of Science ®Google Scholar
• Ruff-Jamison, S., J. McGlade, T. Pawson, K. Chen, and S. Cohen. 1993. Epidermal growth factor stimulates the tyrosine phosphorylation of SHC in the mouse. J. Biol. Chem. 268:7610–7612.
   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
• Saxton, T. M., I. V. Oostveen, D. Bowtell, T. Aebersold, and M. R. Gold. 1994. B cell antigen receptor cross-linking induces phosphorylation of the p21 ras oncoprotein activators SHC and mSOS1 as well as assembly of complexes containing SHC, GRB-2, mSOS1, and a 145-kDa tyrosine-phos-phorylated protein. J. Immunol. 153:623–636.
   PubMed Web of Science ®Google Scholar
• Segatto, O., G. Pelicci, S. Giuli, G. Digiesi, P. O. DiFiore, J. McGlade, T. Pawson, and P. G. Pelicci. 1993. Shc products are substrates of Erb-2 kinase. Oncogene 8:2105–2112.
   PubMedGoogle Scholar
• Simon, L. A., G. S. Dodson, and G. M. Rubin. 1993. An SH3-SH2-SH3 protein is required for p21Ras1 activation and binds to sevenless and Sos proteins in vitro. Cell 73:169–177.
   PubMed Web of Science ®Google Scholar
• Simon, M. A., D. D. L. Bowtell, G. S. Dodson, T. R. Laverty, and G. M. Rubin. 1991. Ras1 and a putative guanine nucleotide exchange factor perform crucial steps in signaling by the sevenless protein tyrosine kinase. Cell 67:701–716.
   PubMedGoogle Scholar
• Songyang, Z., S. E. Shoelson, M. Chadhuri, G. Gish, T. Pawson, F. King, T. Roberts, S. Ratnofsky, B. Schaffhausen, and L. C. Cantley. 1993. Identification of phosphotyrosine peptide motifs which bind to SH2 domains. Cell 72:767–778.
   PubMed Web of Science ®Google Scholar
• Songyang, Z., S. E. Shoelson, J. McGlade, P. Olivier, T. Pawson, R. X. Bustelo, H. Hanafusa, T. Yi, R. Ren, D. Baltimore, S. Ratnofsky, R. A. Feldman, and L. C. Cantley. 1994. Specific motifs recognized by the SH2 domains of Csk, 3BP2, fes/fps, GRB-2, HCP, SHC, Syk, and Vav. Mol. Cell. Biol. 14:2777–2785.
   PubMed Web of Science ®Google Scholar
• Stephens, R. M., D. M. Loeb, T. D. Copeland, T. Pawson, L. A. Greene, and D. R. Kaplan. 1994. Trk receptors use redundant signal transduction pathways involving SHC and PLC-gamma1 to mediate NGF responses. Neuron 12:691–705.
   PubMed Web of Science ®Google Scholar
• Tantz, D., and C. Pfeifle. 1989. A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma 98:81–85.
   PubMedGoogle Scholar
• van der Geer, P., S. Wiley, V. K.-M. Lai, J. P. Olivier, G. D. Gish, T. Stephens, D. Kaplan, S. Shoelson, and T. Pawson. 1995. A conserved amino-terminal SHC domain binds to phosphotyrosine motifs in activated receptors and phosphopeptides. Curr. Biol. 5:404–412.
   PubMedGoogle Scholar
• Yokote, K., S. Mori, K. Hansen, J. McGlade, T. Pawson, C.-H. Heldin, and L. Claesson-Welsh. 1994. Direct interaction between Shc and the platelet-derived growth factor β-receptor. J. Biol. Chem. 269:15337–15343.
   PubMedGoogle Scholar
• Yun, B., R. Farkas, K. Lee, and L. Rabinow. 1994. The Doa locus encodes a member of a new protein kinase family and is essential for eye and embryonic development in Drosophila melanogaster. Genes Dev. 8:1160–1173.
   PubMed Web of Science ®Google Scholar