Docking Protein FRS2 Links the Protein Tyrosine Kinase RET and Its Oncogenic Forms with the Mitogen-Activated Protein Kinase Signaling Cascade

REFERENCES

• Airaksinen, M. S., A. Titievsky, and M. Saarma. 1999. GDNF family neurotrophic factor signaling: four masters, one servant?. Mol. Cell Neurosci. 13:313–325.
   PubMed Web of Science ®Google Scholar
• Alberti, L., M. G. Borrello, S. Ghizzoni, F. Torriti, M. G. Rizzetti, and M. A. Pierotti. 1998. Grb2 binding to the different isoforms of Ret tyrosine kinase. Oncogene 17:1079–1087.
   PubMedGoogle Scholar
• Arighi, E., L. Alberti, F. Torriti, S. Ghizzoni, M. G. Rizzetti, G. Pelicci, B. Pasini, I. Bongarzone, C. Piutti, M. A. Pierotti, and M. G. Borrello. 1997. Identification of Shc docking site on Ret tyrosine kinase. Oncogene 14:773–782.
   PubMedGoogle Scholar
• Asai, N., H. Murakami, T. Iwashita, and M. Takahashi. 1996. A mutation at tyrosine 1062 in MEN2A-Ret and MEN2B-Ret impairs their transforming activity and association with shc adaptor proteins. J. Biol. Chem. 271:17644–17649.
   PubMedGoogle Scholar
• Batzer, 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
• Besset, V., R. P. Scott, and C. F. Ibanez. 2000. Signaling complexes and protein-protein interactions involved in the activation of the Ras and PI3K pathways by the c-Ret receptor tyrosine kinase. J. Biol. Chem. 275:39159–39166.
   PubMedGoogle Scholar
• Borrello, M. G., L. Alberti, E. Arighi, I. Bongarzone, C. Battistini, A. Bardelli, B. Pasini, C. Piutti, M. G. Rizzetti, P. Mondellini, M. T. Radice, and M. A. Pierotti. 1996. The full oncogenic activity of Ret/ptc2 depends on tyrosine 539, a docking site for phospholipase C gamma. Mol. Cell. Biol. 16:2151–2163.
   PubMed Web of Science ®Google Scholar
• Carlomagno, F., G. De Vita, M. T. Berlingieri, V. de Franciscis, R. M. Melillo, V. Colantuoni, M. H. Kraus, P. P. Di Fiore, A. Fusco, and M. Santoro. 1996. Molecular heterogeneity of RET loss of function in Hirschsprung's disease. EMBO J. 15:2717–2225.
   PubMed Web of Science ®Google Scholar
• de Nigris, F., R. Visconti, J. Cerutti, D. Califano, A. Mineo, M. Santoro, G. Santelli, and A. Fusco. 1998. Overexpression of the HIP gene coding for a heparin/heparan sulfate-binding protein in human thyroid carcinomas. Cancer Res. 58:4745–4751.
   PubMedGoogle Scholar
• De Vita, G., R. M. Melillo, F. Carlomagno, R. Visconti, M. D. Castellone, A. Bellacosa, M. Billaud, A. Fusco, P. N. Tsichlis, and M. Santoro. 2000. Tyrosine 1062 of RET-MEN2A mediates activation of Akt (protein kinase B) and mitogen-activated protein kinase pathways leading to PC12 cell survival. Cancer Res. 60:3727–3731.
   PubMedGoogle Scholar
• Durick, K., G. N. Gill, and S. S. Taylor. 1998. Shc and Enigma are both required for mitogenic signaling by Ret/ptc2. Mol. Cell. Biol. 18:2298–2308.
   PubMedGoogle Scholar
• Durick, K., R. Y. Wu, G. N. Gill, and S. S. Taylor. 1996. Mitogenic signaling by Ret/ptc2 requires association with Enigma via a LIM domain. J. Biol Chem. 271:12691–12694.
   PubMedGoogle Scholar
• Eng, C., D. Clayton, I. Schuffenecker, G. Lenoir, G. Cote, R. F. Gagel, H. K. van Amstel, C. J. Lips, I. Nishisho, S. I. Takai, D. J. Marsh, B. G. Robinson, K. Frank-Raue, F. Raue, F. Xue, W. W. Noll, C. Romei, F. Pacini, M. Fink, B. Niederle, J. Zedenius, M. Nordenskjold, P. Komminoth, G. N. L. M. Hendy, L. M. Mulligan, et al.. 1996. The relationship between specific RET proto-oncogene mutations and disease phenotype in multiple endocrine neoplasia type 2. International RET mutation consortium analysis. JAMA 276:1575–1579.
   PubMed Web of Science ®Google Scholar
• Geneste, O., C. Bidaud, G. D. Vita, R. M. Hofstra, S. Tartare-Deckert, C. H. Buys, G. M. Lenoir, M. Santoro, and M. Billaud. 1999. Two distinct mutations of the RET receptor causing Hirschsprung's disease impair the binding of signaling effectors to a multifunctional docking site. Hum. Mol. Genet. 8:1989–1999.
   PubMedGoogle Scholar
• Grieco, M., M. Santoro, M. T. Berlingieri, R. M. Melillo, R. Donghi, I. Bongarzone, M. A. Pierotti, G. Della Porta, A. Fusco, and G. Vecchio. 1990. PTC is a novel rearranged form of the ret proto-oncogene and is frequently detected in vivo in human thyroid papillary carcinomas. Cell 60:557–563.
   PubMed Web of Science ®Google Scholar
• Hadari, Y. R., H. Kouhara, I. Lax, and J. Schlessinger. 1998. Binding of Shp2 tyrosine phosphatase to FRS2 is essential for fibroblast growth factor-induced PC12 cell differentiation. Mol. Cell. Biol. 18:3966–3973.
   PubMed Web of Science ®Google Scholar
• Ishizaka, Y., T. Ushijima, T. Sugimura, and M. Nagao. 1990. cDNA cloning and characterization of ret activated in a human papillary thyroid carcinoma cell line. Biochem. Biophys. Res. Commun. 168:402–408.
   PubMedGoogle Scholar
• Iwashita, T., N. Asai, H. Murakami, M. Matsuyama, and M. Takahashi. 1996. Identification of tyrosine residues that are essential for transforming activity of the ret proto-oncogene with MEN2A or MEN2B mutation. Oncogene 12:481–487.
   PubMed Web of Science ®Google Scholar
• Jhiang, S. M., J. E. Sagartz, Q. Tong, J. Parker-Thornburg, C. C. Capen, J. Y. Cho, S. Xing, and C. Ledent. 1996. Targeted expression of the ret/PTC1 oncogene induces papillary thyroid carcinomas. Endocrinology 137:375–378.
   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
• Kouhara, H., Y. R. Hadari, T. Spivak-Kroizman, J. Schilling, D. Bar-Sagi, I. Lax, and J. Schlessinger. 1997. A lipid-anchored Grb2-binding protein that links FGF-receptor activation to the Ras/MAPK signaling pathway. Cell 89:693–702.
   PubMed Web of Science ®Google Scholar
• Li, N., A. Batzer, R. Daly, V. Yajnik, 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 signalling. Nature 363:85–88.
   PubMed Web of Science ®Google Scholar
• Liu, X., Q. C. Vega, R. A. Decker, A. Pandey, C. A. Worby, and J. E. Dixon. 1996. Oncogenic RET receptors display different autophosphorylation sites and substrate binding specificities. J. Biol. Chem. 271:5309–5312.
   PubMedGoogle Scholar
• Lorenzo, M. J., G. D. Gish, C. Houghton, T. J. Stonehouse, T. Pawson, B. A. Ponder, and D. P. Smith. 1997. RET alternate splicing influences the interaction of activated RET with the SH2 and PTB domains of Shc, and the SH2 domain of Grb2. Oncogene 14:763–771.
   PubMedGoogle Scholar
• Marshall, C. J.. 1995. Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80:179–185.
   PubMed Web of Science ®Google Scholar
• Meakin, S. O., J. I. MacDonald, E. A. Gryz, C. J. Kubu, and J. M. Verdi. 1999. The signaling adapter FRS-2 competes with Shc for binding to the nerve growth factor receptor TrkA. A model for discriminating proliferation and differentiation. J. Biol. Chem. 274:9861–9870.
   PubMed Web of Science ®Google Scholar
• Myers, S. M., C. Eng, B. A. Ponder, and L. M. Mulligan. 1995. Characterization of RET proto-oncogene 3′ splicing variants and polyadenylation sites: a novel C-terminus for RET. Oncogene 11:2039–2045.
   PubMed Web of Science ®Google Scholar
• Ong, S. H., G. R. Guy, Y. R. Hadari, S. Laks, N. Gotoh, J. Schlessinger, and I. Lax. 2000. FRS2 proteins recruit intracellular signaling pathways by binding to diverse targets on fibroblast growth factor and nerve growth factor receptors. Mol. Cell. Biol. 20:979–989.
   PubMed Web of Science ®Google Scholar
• Ong, S. H., Y. R. Hadari, N. Gotoh, G. R. Guy, J. Schlessinger, and I. Lax. Stimulation of PI-3 kinase by FGF receptors is mediated by coordinated recruitment of multiple docking proteins. Proc. Natl. Acad. Sci. USA, in press.
   Google Scholar
• Pandey, A., H. Duan, P. P. Di Fiore, and V. M. Dixit. 1995. The Ret receptor protein tyrosine kinase associates with the SH2-containing adapter protein Grb10. J. Biol. Chem. 270:21461–21463.
   PubMedGoogle Scholar
• Pandey, A., X. Liu, J. E. Dixon, P. P. Di Fiore, and V. M. Dixit. 1996. Direct association between the Ret receptor tyrosine kinase and the Src homology 2-containing adapter protein Grb7. J. Biol. Chem. 271:10607–10610.
   PubMedGoogle Scholar
• Pasini, B., M. G. Borrello, A. Greco, I. Bongarzone, Y. Luo, P. Mondellini, L. Alberti, C. Miranda, E. R. Arighi, R. Bocciardi, et al.. 1995. Loss of function effect of RET mutations causing Hirschsprung disease. Nat. Genet. 10:35–40.
   PubMed Web of Science ®Google Scholar
• Pawson, T., and J. D. Scott. 1997. Signaling through scaffold, anchoring, and adaptor proteins. Science 278:2075–2080.
   PubMed Web of Science ®Google Scholar
• Pelicci, G., L. Lanfrancone, A. E. Salcini, A. Romano, S. Mele, M. G. Borrello, O. Segatto, P. P. Di Fiore, and P. G. Pelicci. 1995. Constitutive phosphorylation of Shc proteins in human tumors. Oncogene 11:899–907.
   PubMed Web of Science ®Google Scholar
• Pierotti, M. A., I. Bongarzone, M. G. Borello, A. Greco, S. Pilotti, and G. Sozzi. 1996. Cytogenetics and molecular genetics of carcinomas arising from thyroid epithelial follicular cells. Genes Chromosomes Cancer 16:1–14.
   PubMedGoogle Scholar
• Plyte, S., M. B. Majolini, S. Pacini, F. Scarpini, C. Bianchini, L. Lanfrancone, P. Pelicci, and C. T. Baldari. 2000. Constitutive activation of the Ras/MAP kinase pathway and enhanced TCR signaling by targeting the Shc adaptor to membrane rafts. Oncogene 19:1529–1537.
   PubMedGoogle Scholar
• Ponder, B. A.. 1999. The phenotypes associated with ret mutations in the multiple endocrine neoplasia type 2 syndrome. Cancer Res. 59:1736–1741.
   PubMedGoogle Scholar
• Powell, D. J. Jr., J. Russell, K. Nibu, G. Li, E. Rhee, M. Liao, M. Goldstein, W. M. Keane, M. Santoro, A. Fusco, and J. L. Rothstein. 1998. The RET/PTC3 oncogene: metastatic solid-type papillary carcinomas in murine thyroids. Cancer Res. 58:5523–5528.
   PubMed Web of Science ®Google Scholar
• Rosenthal, A.. 1999. The GDNF protein family: gene ablation studies reveal what they really do and how. Neuron 22:201–203.
   PubMedGoogle Scholar
• Santoro, M., F. Carlomagno, A. Romano, D. P. Bottaro, N. A. Dathan, M. Grieco, A. Fusco, G. Vecchio, B. Matoskova, M. H. Kraus, et al.. 1995. Activation of RET as a dominant transforming gene by germline mutations of MEN2A and MEN2B. Science 267:381–383.
   PubMed Web of Science ®Google Scholar
• Santoro, M., N. A. Dathan, M. T. Berlingieri, I. Bongarzone, C. Paulin, M. Grieco, M. A. Pierotti, G. Vecchio, and A. Fusco. 1994. Molecular characterization of RET/PTC3; a novel rearranged version of the RET proto-oncogene in a human thyroid papillary carcinoma. Oncogene 9:509–516.
   PubMed Web of Science ®Google Scholar
• Santoro, M., W. T. Wong, P. Aroca, E. Santos, B. Matoskova, M. Grieco, A. Fusco, and P. P. di Fiore. 1994. An epidermal growth factor receptor/ret chimera generates mitogenic and transforming signals: evidence for a ret-specific signaling pathway. Mol. Cell. Biol. 14:663–675.
   PubMed Web of Science ®Google Scholar
• Santoro, M., G. Chiappetta, A. Cerrato, D. Salvatore, L. Zhang, G. Manzo, A. Picone, G. Portella, G. Santelli, G. Vecchio, and A. Fusco. 1996. Development of thyroid papillary carcinomas secondary to tissue-specific expression of the RET/PTC1 oncogene in transgenic mice. Oncogene 12:1821–1826.
   PubMed Web of Science ®Google Scholar
• Santoro, M., R. M. Melillo, M. Grieco, M. T. Berlingieri, G. Vecchio, and A. Fusco. 1993. The TRK and RET tyrosine kinase oncogenes cooperate with ras in the neoplastic transformation of a rat thyroid epithelial cell line. Cell Growth Differ. 4:77–84.
   PubMedGoogle Scholar
• Schlessinger, J.. 2000. Cell signaling by receptor tyrosine kinases. Cell 103:211–225.
   PubMed Web of Science ®Google Scholar
• Segouffin-Cariou, C., and M. Billaud. 2000. Transforming ability of MEN2A-RET requires activation of the phosphatidylinositol 3-kinase/AKT signaling pathway. J. Biol. Chem. 275:3568–3576.
   PubMed Web of Science ®Google Scholar
• Tansey, M. G., R. H. Baloh, J. Milbrandt, and E. M. Johnson Jr.. 2000. GFR alpha-mediated localization of RET to lipid rafts is required for effective downstream signaling, differentiation, and neuronal survival. Neuron 25:611–623.
   PubMed Web of Science ®Google Scholar
• Tong, Q., S. Xing, and S. M. Jhiang. 1997. Leucine zipper-mediated dimerization is essential for the PTC1 oncogenic activity. J. Biol. Chem. 272:9043–9047.
   PubMedGoogle Scholar
• Trupp, M., R. Scott, S. R. Whittemore, and C. F. Ibanez. 1999. Ret-dependent and -independent mechanisms of glial cell line-derived neurotrophic factor signaling in neuronal cells. J. Biol. Chem. 274:20885–20894.
   PubMedGoogle Scholar
• Xu, H., K. W. Lee, and M. Goldfarb. 1998. Novel recognition motif on fibroblast growth factor receptor mediates direct association and activation of SNT adapter proteins. J. Biol. Chem. 273:17987–17990.
   PubMedGoogle Scholar