Signal Strength Dictates Phosphoinositide 3-Kinase Contribution to Ras/Extracellular Signal-Regulated Kinase 1 and 2 Activation via Differential Gab1/Shp2 Recruitment: Consequences for Resistance to Epidermal Growth Factor Receptor Inhibition

REFERENCES

• Chou, M. M., W. Hou, J. Johnson, L. K. Graham, M. H. Lee, C. S. Chen, A. C. Newton, B. S. Schaffhausen, and A. Toker. 1998. Regulation of protein kinase C zeta by PI 3-kinase and PDK-1. Curr. Biol. 8:1069–1077.
   PubMed Web of Science ®Google Scholar
• Cunnick, J. M., J. F. Dorsey, T. Munoz-Antonia, L. Mei, and J. Wu. 2000. Requirement of SHP2 binding to Gab1 for MAPK activation in response to LPA and EGF. J. Biol. Chem. 275:13842–13848.
   PubMed Web of Science ®Google Scholar
• Dance, M., A. Montagner, A. Yart, B. Masri, Y. Audigier, B. Perret, J. P. Salles, and P. Raynal. 2006. The adaptor protein Gab1 couples the stimulation of vascular endothelial growth factor-2 to the activation of phosphoinositide 3-kinase. J. Biol. Chem. 281:23285–23295.
   PubMedGoogle Scholar
• de Rooij, J., and J. L. Bos. 1997. Minimal Ras-binding domain of Raf1 can be used as an activation-specific probe for Ras. Oncogene 14:623–625.
   PubMed Web of Science ®Google Scholar
• Downward, J. 2003. Targeting RAS signalling pathways in cancer therapy. Nat. Rev. Cancer 3:11–22.
   PubMed Web of Science ®Google Scholar
• Duckworth, B. C., and L. C. Cantley. 1997. Conditional inhibition of the mitogen-activated protein kinase cascade by wortmannin. Dependence of signal strength. J. Biol. Chem. 272:27665–27670.
   PubMedGoogle Scholar
• Engelman, J. A., K. Zejnullahu, T. Mitsudomi, Y. Song, C. Hyland, J. O. Park, N. Lindeman, C. M. Gale, X. Zhao, J. Christensen, T. Kosaka, A. J. Holmes, A. M. Rogers, F. Cappuzzo, T. Mok, C. Lee, B. E. Johnson, L. C. Cantley, and P. A. Janne. 2007. MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science 316:1039–1043.
   PubMed Web of Science ®Google Scholar
• Gu, H., and B. G. Neel. 2003. The “Gab” in signal transduction. Trends Cell Biol. 13:122–130.
   PubMed Web of Science ®Google Scholar
• Gupta, S., A. R. Ramjaun, P. Haiko, Y. Wang, P. H. Warne, B. Nicke, E. Nye, G. Stamp, K. Alitalo, and J. Downward. 2007. Binding of ras to phosphoinositide 3-kinase p110alpha is required for ras-driven tumorigenesis in mice. Cell 129:957–968.
   PubMed Web of Science ®Google Scholar
• Hanna, N., A. Montagner, W. H. Lee, M. Miteva, M. Vidal, M. Vidaud, B. Parfait, and P. Raynal. 2006. Reduced phosphatase activity of SHP-2 in LEOPARD syndrome: consequences for PI3K binding on Gab1. FEBS Lett. 580:2477–2482.
   PubMedGoogle Scholar
• He, T. C., S. Zhou, L. T. da Costa, J. Yu, K. W. Kinzler, and B. Vogelstein. 1998. A simplified system for generating recombinant adenoviruses. Proc. Natl. Acad. Sci. USA 95:2509–2514.
   PubMed Web of Science ®Google Scholar
• Ihle, N. T., G. Paine-Murrieta, M. I. Berggren, A. Baker, W. R. Tate, P. Wipf, R. T. Abraham, D. L. Kirkpatrick, and G. Powis. 2005. The phosphatidylinositol-3-kinase inhibitor PX-866 overcomes resistance to the epidermal growth factor receptor inhibitor gefitinib in A-549 human non-small cell lung cancer xenografts. Mol. Cancer Ther. 4:1349–1357.
   PubMed Web of Science ®Google Scholar
• Isakoff, S. J., T. Cardozo, J. Andreev, Z. Li, K. M. Ferguson, R. Abagyan, M. A. Lemmon, A. Aronheim, and E. Y. Skolnik. 1998. Identification and analysis of PH domain-containing targets of phosphatidylinositol 3-kinase using a novel in vivo assay in yeast. EMBO J. 17:5374–5387.
   PubMed Web of Science ®Google Scholar
• Itoh, M., Y. Yoshida, K. Nishida, M. Narimatsu, M. Hibi, and T. Hirano. 2000. Role of Gab1 in heart, placenta, and skin development and growth factor- and cytokine-induced extracellular signal-regulated kinase mitogen-activated protein kinase activation. Mol. Cell. Biol. 20:3695–3704.
   PubMed Web of Science ®Google Scholar
• Kassouf, W., C. P. Dinney, G. Brown, D. J. McConkey, A. J. Diehl, M. Bar-Eli, and L. Adam. 2005. Uncoupling between epidermal growth factor receptor and downstream signals defines resistance to the antiproliferative effect of Gefitinib in bladder cancer cells. Cancer Res. 65:10524–10535.
   PubMed Web of Science ®Google Scholar
• Kiyatkin, A., E. Aksamitiene, N. I. Markevich, N. M. Borisov, J. B. Hoek, and B. N. Kholodenko. 2006. Scaffolding protein GAB1 sustains epidermal growth factor-induced mitogenic and survival signaling by multiple positive feedback loops. J. Biol. Chem. 281:19925–19938.
   PubMed Web of Science ®Google Scholar
• Li, B., C. M. Chang, M. Yuan, W. G. McKenna, and H. K. Shu. 2003. Resistance to small molecule inhibitors of epidermal growth factor receptor in malignant gliomas. Cancer Res. 63:7443–7450.
   PubMed Web of Science ®Google Scholar
• Mattoon, D. R., B. Lamothe, I. Lax, and J. Schlessinger. 2004. The docking protein Gab1 is the primary mediator of EGF-stimulated activation of the PI-3K/Akt cell survival pathway. BMC Biol. 2:24.
   PubMedGoogle Scholar
• Montagner, A., A. Yart, M. Dance, B. Perret, J. P. Salles, and P. Raynal. 2005. A novel role for Gab1 and SHP2 in EGF-induced Ras activation. J. Biol. Chem. 280:5350–5360.
   PubMed Web of Science ®Google Scholar
• Neel, B. G., H. Gu, and L. Pao. 2003. The ′Shp'ing news: SH2 domain-containing tyrosine phosphatases in cell signaling. Trends Biochem. Sci. 28:284–293.
   PubMed Web of Science ®Google Scholar
• Qiao, M., P. Shapiro, R. Kumar, and A. Passaniti. 2004. Insulin-like growth factor-1 regulates endogenous RUNX2 activity in endothelial cells through a phosphatidylinositol 3-kinase/ERK-dependent and Akt-independent signaling pathway. J. Biol. Chem. 279:42709–42718.
   PubMedGoogle Scholar
• Rodrigues, G. A., M. Falasca, Z. Zhang, S. H. Ong, and J. Schlessinger. 2000. A novel positive feedback loop mediated by the docking protein Gab1 and phosphatidylinositol 3-kinase in epidermal growth factor receptor signaling. Mol. Cell. Biol. 20:1448–1459.
   PubMedGoogle Scholar
• Rubin, B. P., and A. Duensing. 2006. Mechanisms of resistance to small molecule kinase inhibition in the treatment of solid tumors. Lab. Investig. 86:981–986.
   PubMed Web of Science ®Google Scholar
• Rubio, I., and R. Wetzker. 2000. A permissive function of PI3K in Ras activation mediated by inhibition of GTPase-activating proteins. Curr. Biol. 10:1225–1228.
   PubMedGoogle Scholar
• Schaeper, U., N. H. Gehring, K. P. Fuchs, M. Sachs, B. Kempkes, and W. Birchmeier. 2000. Coupling of Gab1 to c-Met, Grb2, and Shp2 mediates biological responses. J. Cell Biol. 149:1419–1432.
   PubMed Web of Science ®Google Scholar
• Schlessinger, J. 2000. Cell signaling by receptor tyrosine kinases. Cell 103:211–225.
   PubMed Web of Science ®Google Scholar
• Schmidt, E. K., S. Fichelson, and S. M. Feller. 2004. PI3 kinase is important for Ras, MEK and Erk activation of Epo-stimulated human erythroid progenitors. BMC Biol. 2:7.
   PubMedGoogle Scholar
• Schönwasser, D. C., R. M. Marais, C. J. Marshall, and P. J. Parker. 1998. Activation of mitogen-activated protein kinase/extracellular signal-regulated kinase pathway by conventional, novel, and atypical protein kinase C isotypes. Mol. Cell. Biol. 18:790–798.
   PubMed Web of Science ®Google Scholar
• Sergina, N. V., M. Rausch, D. Wang, J. Blair, B. Hann, K. M. Shokat, and M. M. Moasser. 2007. Escape from HER-family tyrosine kinase inhibitor therapy by the kinase-inactive HER3. Nature 445:437–441.
   PubMed Web of Science ®Google Scholar
• Shi, Z. Q., D. H. Yu, M. Park, M. Marshall, and G. S. Feng. 2000. Molecular mechanisms for the Shp-2 tyrosine function in promoting growth factor stimulation of Erk activity. Mol. Cell. Biol. 20:1526–1536.
   PubMedGoogle Scholar
• Sondermann, H., S. M. Soisson, S. Boykevisch, S. S. Yang, D. Bar-Sagi, and J. Kuriyan. 2004. Structural analysis of autoinhibition in the Ras activator Son of sevenless. Cell 119:393–405.
   PubMed Web of Science ®Google Scholar
• Stea, B., R. Falsey, K. Kislin, J. Patel, H. Glanzberg, S. Carey, A. A. Ambrad, E. J. Meuillet, and J. D. Martinez. 2003. Time and dose-dependent radiosensitization of the glioblastoma multiforme U251 cells by the EGF receptor tyrosine kinase inhibitor ZD1839 (′Iressa'). Cancer Lett. 202:43–51.
   PubMed Web of Science ®Google Scholar
• Toker, A., and M. Yoeli-Lerner. 2006. Akt signaling and cancer: surviving but not moving on. Cancer Res. 66:3963–3966.
   PubMed Web of Science ®Google Scholar
• Wandzioch, E., C. E. Edling, R. H. Palmer, L. Carlsson, and B. Hallberg. 2004. Activation of the MAP kinase pathway by c-Kit is PI-3 kinase dependent in hematopoietic progenitor/stem cell lines. Blood 104:51–57.
   PubMed Web of Science ®Google Scholar
• Wennström, S., and J. Downward. 1999. Role of phosphoinositide 3-kinase in activation of Ras and mitogen-activated protein kinase by epidermal growth factor. Mol. Cell. Biol. 19:4279–4288.
   PubMedGoogle Scholar
• Yart, A., M. Laffargue, P. Mayeux, S. Chretien, C. Peres, N. K. Tonks, S. Roche, B. Payrastre, H. Chap, and P. Raynal. 2001. A critical role for phosphoinositide 3-kinase upstream of Gab1 and SHP2 in the activation of Ras and mitogen-activated protein kinases by epidermal growth factor. J. Biol. Chem. 276:8856–8864.
   PubMedGoogle Scholar
• Yart, A., S. Roche, R. Wetzker, M. Laffargue, N. K. Tonks, P. Mayeux, H. Chap, and P. Raynal. 2002. A function for phosphoinositide 3-kinase beta lipid products in coupling beta gamma to Ras activation in response to lysophosphatidic acid. J. Biol. Chem. 277:21167–21178.
   PubMedGoogle Scholar
• Zhang, S. Q., W. Yang, M. I. Kontaridis, T. G. Bivona, G. Wen, T. Araki, J. Luo, J. A. Thompson, B. L. Schraven, M. R. Philips, and B. G. Neel. 2004. Shp2 regulates SRC family kinase activity and Ras/Erk activation by controlling Csk recruitment. Mol. Cell 13:341–355.
   PubMed Web of Science ®Google Scholar