14-3-3 Antagonizes Ras-Mediated Raf-1 Recruitment to the Plasma Membrane To Maintain Signaling Fidelity

REFERENCES

• Abraham, D., K. Podar, M. Pacher, M. Kubicek, N. Welzel, B. A. Hemmings, S. M. Dilworth, H. Mischak, W. Kolch, and M. Baccarini. 2000. Raf-1-associated protein phosphatase 2A as a positive regulator of kinase activation. J. Biol. Chem. 275: 22300–22304.
   PubMed Web of Science ®Google Scholar
• Aitken, A. 1995. 14-3-3 proteins on the MAP. Trends Biochem. Sci. 20: 95–97.
   PubMed Web of Science ®Google Scholar
• Avruch, J., A. Khokhlatchev, J. M. Kyriakis, Z. Luo, G. Tzivion, D. Vavvas, and X. F. Zhang. 2001. Ras activation of the Raf kinase: tyrosine kinase recruitment of the MAP kinase cascade. Recent Prog. Horm. Res. 56: 127–155.
   PubMedGoogle Scholar
• Baek, K. H., J. R. Fabian, F. Sprenger, D. K. Morrison, and L. Ambrosio. 1996. The activity of D-raf in torso signal transduction is altered by serine substitution, N-terminal deletion, and membrane targeting. Dev. Biol. 175: 191–204.
   PubMedGoogle Scholar
• Bos, J. 1998. All in the family? New insights and questions regarding interconnectivity of Ras, Rap1 and Ral. EMBO J. 17: 6776–6782.
   PubMed Web of Science ®Google Scholar
• Braselmann, S., and F. McCormick. 1995. BCR and RAF form a complex in vivo via 14-3-3 proteins. EMBO J. 14: 4839–4848.
   PubMedGoogle Scholar
• Brunet, A., A. Bonni, M. J. Zigmond, M. Z. Lin, P. Juo, L. S. Hu, M. J. Anderson, K. C. Arden, J. Blenis, and M. E. Greenberg. 1999. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96: 857–868.
   PubMed Web of Science ®Google Scholar
• Chiloeches, A., C. S. Mason, and R. Marais. 2001. S338 phosphorylation of Raf-1 is independent of phosphatidylinositol 3-kinase and Pak3. Mol. Cell. Biol. 21: 2423–2434.
   PubMed Web of Science ®Google Scholar
• Clark, G. J., J. K. Drugan, K. L. Rossman, J. W. Carpenter, K. Rogers-Graham, H. Fu, C. J. Der, and S. L. Campbell. 1997. 14-3-3 zeta negatively regulates raf-1 activity by interactions with the Raf-1 cysteine-rich domain. J. Biol. Chem. 272: 20990–20993.
   PubMedGoogle Scholar
• Conklin, D. S., K. Galaktionov, and D. Beach. 1995. 14-3-3 proteins associate with cdc25 phosphatases. Proc. Natl. Acad. Sci. USA 92: 7892–7896.
   PubMed Web of Science ®Google Scholar
• Datta, S. R., A. Katsov, L. Hu, A. Petros, S. W. Fesik, M. B. Yaffe, and M. E. Greenberg. 2000. 14-3-3 proteins and survival kinases cooperate to inactivate BAD by BH3 domain phosphorylation. Mol. Cell 6: 41–51.
   PubMedGoogle Scholar
• Daub, M., J. Jockel, T. Quack, C. K. Weber, F. Schmitz, U. R. Rapp, A. Wittinghofer, and C. Block. 1998. The RafC1 cysteine-rich domain contains multiple distinct regulatory epitopes which control Ras-dependent Raf activation. Mol. Cell. Biol. 18: 6698–6710.
   PubMedGoogle Scholar
• Dent, P., T. Jelinek, D. K. Morrison, M. Weber, and T. W. Sturgill. 1995. Reversal of Raf-1 activation by purified and membrane-associated protein phosphatases. Science 269: 1902–1906.
   Google Scholar
• Dhillon, A. S., S. Meikle, Z. Yazici, M. Eulitz, and W. Kolch. 2002. Regulation of Raf-1 activation and signalling by dephosphorylation. EMBO J. 21: 64–71.
   PubMed Web of Science ®Google Scholar
• Diaz, B., D. Barnard, A. Filson, S. MacDonald, A. King, and M. Marshall. 1997. Phosphorylation of Raf-1 serine 338-serine 339 is an essential regulatory event for Ras-dependent activation and biological signaling. Mol. Cell. Biol. 17: 4509–4516.
   PubMed Web of Science ®Google Scholar
• Evan, G. I., G. K. Lewis, G. Ramsay, and J. M. Bishop. 1985. Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol. Cell. Biol. 5: 3610–3616.
   PubMed Web of Science ®Google Scholar
• Fabian, J. R., I. O. Daar, and D. K. Morrison. 1993. Critical tyrosine residues regulate the enzymatic and biological activity of Raf-1 kinase. Mol. Cell. Biol. 13: 7170–7179.
   PubMed Web of Science ®Google Scholar
• Fabian, J. R., A. B. Vojtek, J. A. Cooper, and D. K. Morrison. 1994. A single amino acid change in Raf-1 inhibits Ras binding and alters Raf-1 function. Proc. Natl. Acad. Sci. USA 91: 5982–5986.
   PubMed Web of Science ®Google Scholar
• Fantl, W. J., A. J. Muslin, A. Kikuchi, J. A. Martin, A. M. MacNicol, R. W. Gross, and L. T. Williams. 1994. Activation of Raf-1 by 14-3-3 proteins. Nature 371: 612–614.
   PubMed Web of Science ®Google Scholar
• Freed, E., M. Symons, S. G. Macdonald, F. McCormick, and R. Ruggieri. 1994. Binding of 14-3-3 proteins to the protein kinase Raf and effects on its activation. Science 265: 1713–1716.
   PubMed Web of Science ®Google Scholar
• Fu, H., K. Xia, D. C. Pallas, C. Cui, K. Conroy, R. P. Narsimhan, H. Mamon, R. J. Collier, and T. M. Roberts. 1994. Interaction of the protein kinase Raf-1 with 14-3-3 proteins. Science 266: 126–129.
   PubMed Web of Science ®Google Scholar
• Hagemann, C., and U. R. Rapp. 1999. Isotype-specific functions of Raf kinases. Exp. Cell Res. 253: 34–46.
   PubMed Web of Science ®Google Scholar
• Irie, K., Y. Gotoh, B. M. Yashar, B. Errede, E. Nishida, and K. Matsumoto. 1994. Stimulatory effects of yeast and mammalian 14-3-3 proteins on the Raf protein kinase. Science 265: 1716–1719.
   PubMed Web of Science ®Google Scholar
• IUPAC-IUB Commission on Biochemical Nomenclature. 1969. A one-letter notation for amino acid sequences. Tentative rules. Biochem. J. 113: 1–4.
   Google Scholar
• Jaitner, B. K., J. Becker, T. Linnemann, C. Herrmann, A. Wittinghofer, and C. Block. 1997. Discrimination of amino acids mediating Ras binding from noninteracting residues affecting raf activation by double mutant analysis. J. Biol. Chem. 272: 29927–29933.
   PubMedGoogle Scholar
• Jaumot, M., and J. F. Hancock. 2001. Protein phosphatases 1 and 2A promote Raf-1 activation by regulating 14-3-3 interactions. Oncogene 20: 3949–3958.
   PubMed Web of Science ®Google Scholar
• Kolch, W. 2000. Meaningful relationships: the regulation of the Ras/Raf/MEK/ERK pathway by protein interactions. Biochem. J. 351: 289–305.
   PubMed Web of Science ®Google Scholar
• Koyama, S., L. T. Williams, and A. Kikuchi. 1995. Characterization of the interaction of Raf-1 with ras p21 or 14-3-3 protein in intact cells. FEBS Lett. 368: 321–325.
   PubMedGoogle Scholar
• Leevers, S. J., and C. J. Marshall. 1992. Activation of extracellular signal-regulated kinase, ERK2, by p21ras oncoprotein. EMBO J. 11: 569–574.
   PubMed Web of Science ®Google Scholar
• Leevers, S. J., H. F. Paterson, and C. J. Marshall. 1994. Requirement for Ras in Raf activation is overcome by targeting Raf to the plasma membrane. Nature 369: 411–414.
   PubMed Web of Science ®Google Scholar
• Li, S., P. Janosch, M. Tanji, G. C. Rosenfeld, J. C. Waymire, H. Mischak, W. Kolch, and J. M. Sedivy. 1995. Regulation of Raf-1 kinase activity by the 14-3-3 family of proteins. EMBO J. 14: 685–696.
   PubMed Web of Science ®Google Scholar
• Marais, R., Y. Light, C. Mason, H. Paterson, M. Olson, and C. J. Marshall. 1998. Requirement of Ras-GTP-Raf complexes for activation of Raf-1 by protein kinase C. Science 280: 109–112.
   PubMed Web of Science ®Google Scholar
• Marais, R., Y. Light, H. F. Paterson, and C. J. Marshall. 1995. Ras recruits Raf-1 to the plasma membrane for activation by tyrosine phosphorylation. EMBO J. 14: 3136–3145.
   PubMed Web of Science ®Google Scholar
• Marais, R., Y. Light, H. F. Paterson, C. S. Mason, and C. J. Marshall. 1997. Differential regulation of Raf-1, A-Raf and B-Raf by oncogenic Ras and tyrosine kinases. J. Biol. Chem. 272: 4378–4383.
   PubMed Web of Science ®Google Scholar
• Marais, R., and C. J. Marshall. 1996. Control of the ERK MAP kinase cascade by Ras and Raf, p. 101–125. In P. J. Parker and T. Pawson (ed.), Cell signalling, vol. 27. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
   Google Scholar
• Marais, R., J. Wynne, and R. Treismann. 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
• Marshall, C. J. 1995. Specificity of receptor tyrosine kinase signalling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80: 179–185.
   PubMed Web of Science ®Google Scholar
• Mason, C. S., C. Springer, R. G. Cooper, G. Superti-Furga, C. J. Marshall, and R. Marais. 1999. Serine and tyrosine phosphorylations cooperate in Raf-1, but not B-Raf activation. EMBO J. 18: 2137–2148.
   PubMed Web of Science ®Google Scholar
• McPherson, R. A., A. Harding, S. Roy, A. Lane, and J. F. Hancock. 1999. Interactions of c-Raf-1 with phosphatidylserine and 14-3-3. Oncogene 18: 3862–3869.
   PubMed Web of Science ®Google Scholar
• Michaud, N. R., J. R. Fabian, K. D. Mathes, and D. K. Morrison. 1995. 14-3-3 is not essential for Raf-1 function: identification of Raf-1 proteins that are biologically activated in a 14-3-3- and Ras-independent manner. Mol. Cell. Biol. 15: 3390–3397.
   PubMed Web of Science ®Google Scholar
• Mineo, C., R. G. W. Anderson, and M. A. White. 1997. Physical interaction with Ras enhances activation of membrane-bound Raf (RafCAAX). J. Biol. Chem. 272: 10345–10348.
   PubMed Web of Science ®Google Scholar
• Mischak, H., T. Seitz, P. Janosh, M. Eulitz, H. Steen, M. Schellerer, A. Philipp, and W. Kolch. 1996. Negative regulation of Raf-1 by phosphorylation of serine 621. Mol. Cell. Biol. 16: 5409–5418.
   PubMedGoogle Scholar
• Morrison, D. K., and R. E. J. Cutler. 1997. The complexity of Raf-1 regulation. Curr. Opin. Cell Biol. 9: 174–179.
   PubMed Web of Science ®Google Scholar
• Morrison, D. K., G. Heidecker, U. R. Rapp, and T. D. Copeland. 1993. Identification of the major phosphorylation sites of the Raf-1 kinase. J. Biol. Chem. 268: 17309–17316.
   PubMedGoogle Scholar
• Muslin, A. J., J. W. Tanner, P. M. Allen, and A. S. Shaw. 1996. Interaction of 14-3-3 with signaling proteins is mediated by the recognition of phosphoserine. Cell 84: 889–897.
   PubMed Web of Science ®Google Scholar
• Muslin, A. J., and H. Xing. 2000. 14-3-3 proteins: regulation of subcellular localization by molecular interference. Cell. Signal. 12: 703–709.
   PubMed Web of Science ®Google Scholar
• Petosa, C., S. C. Masters, L. A. Bankston, J. Pohl, B. Wang, H. Fu, and R. C. Liddington. 1998. 14-3-3ζ binds a phosphorylated Raf peptide and an unphosphorylated peptide via its conserved amphipathic groove. J. Biol. Chem. 273: 16305–16310.
   PubMed Web of Science ®Google Scholar
• Rittinger, K., J. Budman, J. Xu, S. Volinia, L. C. Cantley, S. J. Smerdon, S. J. Gamblin, and M. B. Yaffe. 1999. Structural analysis of 14-3-3 phosphopeptide complexes identifies a dual role for the nuclear export signal of 14-3-3 in ligand binding. Mol. Cell 4: 153–166.
   PubMed Web of Science ®Google Scholar
• Robinson, M. J., and M. H. Cobb. 1997. Mitogen-activated protein kinase pathways. Curr. Opin. Cell Biol. 9: 180–186.
   PubMed Web of Science ®Google Scholar
• Rommel, C., B. A. Clarke, S. Zimmermann, L. Nunez, R. Rossman, K. Reid, K. Moelling, G. D. Yancopoulos, and D. J. Glass. 1999. Differentiation stage-specific inhibition of the Raf-MEK-ERK pathway by Akt. Science 286: 1738–1741.
   PubMed Web of Science ®Google Scholar
• Rommel, C., G. Radziwill, J. Lovric, J. Noeldeke, T. Heinicke, D. Jones, A. Aitken, and K. Moelling. 1996. Activated Ras displaces 14-3-3 proteins from the amino terminus of c-Raf-1. Oncogene 12: 609–619.
   PubMedGoogle Scholar
• Roy, S., R. A. McPherson, A. Apolloni, J. Yan, A. Lane, J. Clyde-Smith, and J. F. Hancock. 1998. 14-3-3 facilitates Ras-dependent Raf-1 activation in vitro and in vivo. Mol. Cell. Biol. 18: 3947–3955.
   PubMed Web of Science ®Google Scholar
• Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd edition. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
   Google Scholar
• Stokoe, D., S. G. Macdonald, K. Cadwallader, M. Symons, and J. F. Hancock. 1994. Activation of Raf as a result of recruitment to the plasma membrane. Science 264: 1463–1467.
   PubMed Web of Science ®Google Scholar
• Suen, K. L., X. R. Bustelo, and M. Barbacid. 1995. Lack of evidence for the activation of the Ras/Raf mitogenic pathway by 14-3-3 proteins in mammalian cells. Oncogene 11: 825–831.
   PubMedGoogle Scholar
• Thorson, J. A., L. W. Yu, A. L. Hsu, N. Y. Shih, P. R. Graves, J. W. Tanner, P. M. Allen, H. Piwnica-Worms, and A. S. Shaw. 1998. 14-3-3 proteins are required for maintenance of Raf-1 phosphorylation and kinase activity. Mol. Cell Biol. 18: 5229–5238.
   PubMedGoogle Scholar
• Tzivion, G., Z. Lou, and J. Avruch. 1998. A dimeric 14-3-3 protein is an essential cofactor for Raf kinase activity. Nature 394: 536–539.
   Google Scholar
• Wang, B., H. Yang, Y.-C. Liu, T. Jelinek, L. Zhang, E. Ruoslahti, and H. Fu. 1999. Isolation of high-affinity peptide antagonists of 14-3-3 proteins by phage display. Biochemistry 38: 12499–12504.
   PubMed Web of Science ®Google Scholar
• White, M. A., C. Nicolette, A. Minden, A. Polverino, A. L. Van, M. Karin, and M. H. Wigler. 1995. Multiple Ras functions can contribute to mammalian cell transformation. Cell 80: 533–541.
   PubMed Web of Science ®Google Scholar
• Williams, J. G., J. K. Drugan, G. S. Yi, G. J. Clark, C. J. Der, and S. L. Campbell. 2000. Elucidation of binding determinants and functional consequences of Ras/Raf-cysteine-rich domain interactions. J. Biol. Chem. 275: 22172–22179.
   PubMed Web of Science ®Google Scholar
• Yaffe, M. B., K. Rittinger, S. Volinia, P. R. Caron, A. Aitken, H. Leffers, S. J. Gamblin, S. J. Smerdon, and L. C. Cantley. 1997. The structural basis for 14-3-3:phosphopeptide binding specificity. Cell 91: 961–971.
   PubMed Web of Science ®Google Scholar
• Yip-Schneider, M. T., W. Miao, A. Lin, D. S. Barnard, G. Tzivion, and M. S. Marshall. 2000. Regulation of the Raf-1 kinase domain by phosphorylation and 14-3-3 association. Biochem. J. 351: 151–159.
   PubMedGoogle Scholar
• Zimmermann, S., and K. Moelling. 1999. Phosphorylation and regulation of Raf by Akt (protein kinase B). Science 286: 1741–1744.
   PubMed Web of Science ®Google Scholar