Tyr-716 in the Platelet-Derived Growth Factor β-Receptor Kinase Insert Is Involved in GRB2 Binding and Ras Activation

REFERENCES

• Aebersold, R. H., J. Leavitt, R. A. Saavedra, L. E. Hood, and S. B. H. Kent. 1987. Internal amino acid sequence analysis of proteins separated by one- or two-dimensional gel electrophoresis after in situ protease digestion on nitrocellulose. Biochemistry 84:6970–6974.
   Google Scholar
• Andrews, D. M., J. Kitchin, and P. W. Seale. 1991. Solid-phase synthesis of a range of O-phosphorylated peptides by post-assembly phosphitylation and oxidation. Int. J. Pept. Protein Res. 38:469–475.
   PubMedGoogle Scholar
• Arvidsson, A.-K., C.-H. Heldin, and L. Claesson-Welsh. 1992. Transduction of circular membrane ruffling by the platelet-derived growth factor β-receptor is dependent on its kinase insert. Cell Growth Differ. 3:881–887.
   PubMedGoogle Scholar
• Basu, T. N., D. H. Gutmann, J. A. Fletcher, T. W. Glover, F. S. Collins, and J. Downward. 1992. Aberrant regulation of ras proteins in malignant tumour cells from type 1 neurofibromatosis patients. Nature (London) 356:713–715.
   PubMed Web of Science ®Google Scholar
• Boguski, M. S., and F. McCormick. 1993. Proteins regulating Ras and its relatives. Nature (London) 366:643–654.
   PubMed Web of Science ®Google Scholar
• Boudewijn, M. T. B., 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
• 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 of receptor, Grb2 adapter protein, and Sos nucleotide exchange factor. Cell 73:1–20.
   PubMedGoogle Scholar
• Claesson-Welsh, L. 1994. Signal transduction by the PDGF receptors. Prog. Growth Factor Res. 5:37–54.
   PubMedGoogle Scholar
• Claesson-Welsh, L., A. Eriksson, A. Moren, L. Severinsson, B. Ek, A. Östman, C. Betsholtz, and C.-H. Heldin. 1988. cDNA cloning and expression of a human platelet-derived growth factor (PDGF) receptor specific for B-chain-containing PDGF molecules. Mol. Cell. Biol. 8:3476–3486.
   PubMed Web of Science ®Google Scholar
• Claesson-Welsh, L., A. Hammacher, B. Westermark, C.-H. Heldin, and M. Nistér. 1989. Identification and structural analysis of the A type receptor for platelet-derived growth factor. Similarities with the B type receptor. J. Biol. Chem. 264:1742–1747.
   PubMed Web of Science ®Google Scholar
• Clark, S. G., M. J. Stern, and H. R. Horvitz. 1992. C. elegans cell-signaling gene sem-5 encodes a protein with SH2 and SH3 domains. Nature (London) 356:340–344.
   PubMed Web of Science ®Google Scholar
• Davis, R. J. 1993. The mitogen-activated protein kinase signal transduction pathway. J. Biol. Chem. 268:14553–14556.
   PubMed Web of Science ®Google Scholar
• Downward, J., J. D. Graves, P. H. Warne, S. Rayter, and D. A. Cantrell. 1990. Stimulation of p21ras upon T-cell activation. Nature (London) 346:719–723.
   PubMed Web of Science ®Google Scholar
• Egan, S. E., B. W. Giddings, M. W. Brooks, L. Buday, A. M. Sizeland, and R. A. 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
• Fantl, W. J., J. A. Escobedo, G. A. Martin, C. W. Turck, M. del Rosario, F. McCormick, and L. T. Williams. 1992. Distinct phosphotyrosines on a growth factor receptor bind to specific molecules that mediate different signaling pathways. Cell 69:413–423.
   PubMedGoogle Scholar
• Fukui, Y., and H. Hanafusa. 1989. Phosphatidylinositol kinase activity associates with viral p60src protein. Mol. Cell. Biol. 9:1651–1658.
   PubMedGoogle 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 (London) 363:88–92.
   PubMed Web of Science ®Google Scholar
• Gatoh, N., A. Tojo, K. Muroya, Y. Hashimoto, S. Hattori, S. Nakamura, T. Takenawa, Y. Yazaki, and M. Shibuya. 1994. Epidermal growth factor-receptor mutant lacking the autophosphorylation sites induces phosphorylation of Shc protein and Shc-Grb2/ASH association and retains mitogenic activity. Proc. Natl. Acad. Sci. USA 91:167–171.
   PubMedGoogle Scholar
• Gibbs, J. B., M. S. Marshall, E. M. Scolnick, R. A. F. Dixon, and U. S. Vogel. 1990. Modulation of guanine nucleotides bound to Ras in NIH3T3 cells by oncogenes, growth factors, and the GTPase activating protein (GAP). J. Biol. Chem. 265:20437–20442.
   PubMed Web of Science ®Google Scholar
• Heldin, C.-H., and B. Westermark. 1990. Platelet-derived growth factor: mechanism of action and possible in vivo function. Cell Regul. 1:555–566.
   PubMedGoogle Scholar
• Kashishian, A., A. Kazlauskas, and J. A. Cooper. 1992. Phosphorylation sites in the PDGF receptor with different specificities for binding GAP and PI3 kinase in vivo. EMBO J. 11:1373–1382.
   PubMed Web of Science ®Google Scholar
• Kazlauskas, A., G.-S. Feng, T. Pawson, and M. Valius. 1993. The 64-kDa protein that associates with the platelet-derived growth factor receptor β subunit via Tyr-1009 is the SH2-containing phosphotyrosine phosphatase Syp. Proc. Natl. Acad. Sci. USA 90:6939–6943.
   PubMed Web of Science ®Google Scholar
• Kitas, E. A., R. Knorr, A. Trzeciak, and W. Bannwarth. 1991. Alternative strategies for the Fmoc solid-phase synthesis of O4-phospho-L-tyrosine-containing peptides. Helv. Chim. Acta 74:1314–1328.
   Google Scholar
• Lechleider, R. J., S. Sugimoto, A. M. Bennett, A. S. Kashishian, J. A. Cooper, S. E. Shoelson, C. T. Walsh, and B. G. Neel. 1993. Activation of the SH2-containing phosphotyrosine phosphatase SH-PTP2 by its binding site, phosphotyrosine 1009, on the human platelet-derived growth factor receptor β. J. Biol. Chem. 268:21478–21481.
   PubMedGoogle Scholar
• Li, N., A. Batzer, R. Dahy, V. Yayrik, E. Skolnik, P. Chardin, D. Bar-Sagi, B. Margolis, and J. Schlessinger. 1993. Guanine-nucleotide-releasing factor hSosl binds to Grb2 and links receptor tyrosine kinases to Ras signaling. Nature (London) 363:85–88.
   PubMed Web of Science ®Google Scholar
• Li, W., R. Nishimura, A. Kashishian, A. G. Batzer, W. J. H. Kim, J. A. Cooper, and J. Schlessinger. 1994. A new function for a phosphotyrosine phosphatase: Linking GRB2-Sos to a receptor tyrosine kinase. Mol. Cell. Biol. 14:509–517.
   PubMed Web of Science ®Google Scholar
• Lowenstein, E. J., R. J. Daly, A. G. Batzer, W. Li, B. Margolis, R. Lammers, A. Ullrich, E. Y. Skolnick, D. Bar-Sagi, and J. Schlessinger. 1992. The SH2 and SH3 domain-containing protein GRB2 links receptor tyrosine kinases to ras signaling. Cell 70:431–442.
   PubMed Web of Science ®Google Scholar
• Matuoka, K., F. Shibasaki, M. Shibata, and T. Takenawa. 1993. Ash/Grb-2, a SH2/SH3-containing protein, couples to signaling for mitogenesis and cytoskeletal reorganization by EGF and PDGF. EMBO J. 12:3467–3473.
   PubMed Web of Science ®Google Scholar
• Medema, R., and J. L. Bos. 1993. The role of p21ras in receptor tyrosine kinase signaling. Crit. Rev. Oncogenesis 4:615–661.
   PubMedGoogle Scholar
• Miyazono, K., U. Heilman, C. Wernstedt, and C.-H. Heldin. 1988. Latent high molecular weight complex of transforming growth factor β1. Purification from human platelets and structural characterization. J. Biol. Chem. 263:6407–6415.
   PubMed Web of Science ®Google Scholar
• Mori, S., C.-H. Heldin, and L. Claesson-Welsh. 1993. Ligand-induced ubiquitination of the platelet-derived growth factor β-re-ceptor plays a negative regulatoiy role in its mitogenic signaling. J. Biol. Chem. 268:577–583.
   PubMedGoogle Scholar
• Mori, S., L. Rönnstrand, K. Yokote, Å. Engstrom, S. A. Courtneidge, L. Claesson-Welsh, and C.-H. Heldin. 1993. Identification of two juxtamembrane autophosphorylation sites in the PDGF β-receptor; involvement in the interaction with Src family tyrosine kinases. EMBO J. 12:2257–2264.
   PubMed Web of Science ®Google Scholar
• Mulcahy, L. S., M. R. Smith, and D. W. Stacey. 1985. Requirement for ras proto-oncogene function during serum stimulated growth of NIH 3T3 cells. Nature (London) 313:241–243.
   PubMed Web of Science ®Google Scholar
• Nånberg, E., and B. Westermark. 1993. Platelet-derived growth factor increases the turnover of GTP/GDP on Ras in permeabilized fibroblasts. J. Biol. Chem. 268:18187–18194.
   PubMedGoogle 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 adapter 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, 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
• Rozakis-Adcock, M., R. Femley, 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 (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, 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 (London) 360:689–692.
   PubMed Web of Science ®Google Scholar
• Ronnstrand, L., S. Mori, A.-K. Arvidsson, A. Eriksson, C. Wernstedt, U. Heilman, L. Claesson-Welsh, and C.-H. Heldin. 1992. Identification of two C-terminal autophosphorylation sites in the PDGF β-receptor: involvement in the interaction with phospholipase C-y. EMBO J. 11:3911–3919.
   PubMedGoogle Scholar
• Rönnstrand, L., L. Terracio, L. Claesson-Welsh, C.-H. Heldin, and K. Rubin. 1988. Characterization of two monoclonal antibodies reactive with the external domain of the platelet-derived growth factor receptor. J. Biol. Chem. 263:10429–10435.
   PubMed Web of Science ®Google Scholar
• Satoh, T., M. Endo, M. Nakafiiku, S. Nakamura, and Y. Kaziro. 1990. Platelet-derived growth factor stimulates formation of active p21ras GTP complex in Swiss mouse 3T3 cells. Proc. Natl. Acad. Sci. USA 87:5993–5997.
   PubMed Web of Science ®Google Scholar
• Satoh, T., W. J. Fantl, J. A. Escobedo, L. T. Williams, and Y. Kaziro. 1993. Platelet-derived growth factor receptor mediates activation of Ras through different signaling pathways in different cell types. Mol. Cell. Biol. 13:3706–3713.
   PubMed Web of Science ®Google Scholar
• Schlessinger, J., and A. Ullrich. 1992. Growth factor signaling by receptor tyrosine kinases. Neuron 9:383–391.
   PubMed Web of Science ®Google Scholar
• Segatto, O., G. Pelicci, S. Giuli, G. Digesi, P. P. DiFiore, J. McGlade, T. Pawson, and P. G. Pelicci. 1993. Shc products are substrates of erb B-2 kinase. Oncogene 8:2105–2112.
   PubMedGoogle Scholar
• Simon, M. 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
• Skolnik, E. Y., C.-H. Lee, A. Batzer, L. M. Vicentini, M. Zhou, R. Daly, M. J. J. Myers, 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 She: implications for insulin control of ras signalling. EMBO J. 12:1929–1936.
   PubMed Web of Science ®Google Scholar
• Smith, M. R., S. J. DeGudicubus, and D. W. Stacey. 1986. Requirement for c-ras proteins during viral oncogene transformation. Nature (London) 320:540–543.
   PubMed Web of Science ®Google Scholar
• Songyang, Z., S. E. Shoelson, J. McGlade, P. Olivier, T. Pawson, X. R. Bustelo, M. Barbacid, H. Sabe, 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, Fps/Fes, GRB-2, HCP, SHC, Syk, and Vav. Mol. Cell. Biol. 14:2777–2785.
   PubMed Web of Science ®Google Scholar
• Songyang, Z., S. E. Shoelson, M. Chaudhuri, G. Gish, T. Pawson, W. G. Haser, F. King, T. Roberts, S. Ratnofsky, R. J. Lechleider, B. G. Neel, R. B. Birge, J. E. Fajardo, M. M. Chou, H. Hanafusa, B. Schaffhausen, and L. C. Cantley. 1993. SH2 domains recognize specific phosphopeptide sequences. Cell 72:767–778.
   PubMed Web of Science ®Google Scholar
• Valius, M., and A. Kazlauskas. 1993. Phospholipase C-γ1 and phosphatidylinositol 3 kinase are the downstream mediators of the PDGF receptor's mitogenic signal. Cell 73:321–334.
   PubMed Web of Science ®Google Scholar
• Van der Geer, P., and T. Hunter. 1993. Mutation of Tyr697, a GRB2-binding site, and Tyr721, a PI 3-kinase binding site, abrogates signal transduction by the murine CSF-1 receptor expressed in rat-2 fibroblasts. EMBO J. 12:5161–5172.
   PubMed Web of Science ®Google Scholar
• Weima, S. M., M. A. van Rooijen, C. L. Mummery, A. Feyen, S. W. de Laat, and E. J. J. van Zoelen. 1990. Identification of the type-B receptor for platelet-derived growth factor in human embryonal carcinoma cells. Exp. Cell Res. 186:324–331.
   PubMedGoogle Scholar
• Wennström, S., A. Siegbahn, K. Yokote, A.-K. Arvidsson, C.-H. Heldin, S. Mori, and L. Claesson-Welsh. 1994. Membrane ruffling and chemotaxis transduced by the PDGF β-receptor require the binding site for phosphatidylinositol 3′ kinase. Oncogene 9:651–660.
   PubMed Web of Science ®Google Scholar
• Westermark, B., A. Siegbahn, C.-H. Heldin, and L. Claesson-Welsh. 1990. B-type receptor for platelet-derived growth factor mediates a chemotactic response by means of ligand-induced activation of the receptor protein-tyrosine kinase. Proc. Natl. Acad. Sci. USA 87:128–132.
   PubMed Web of Science ®Google 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