Phosphorylated Ssk1 Prevents Unphosphorylated Ssk1 from Activating the Ssk2 Mitogen-Activated Protein Kinase Kinase Kinase in the Yeast High-Osmolarity Glycerol Osmoregulatory Pathway

REFERENCES

• Bettinger, B. T., M. G. Clark, and D. C. Amberg. 2007. Requirement for the polarisome and formin function in Ssk2p-mediated actin recovery from osmotic stress in Saccharomyces cerevisiae. Genetics 175:1637–1648.
   PubMedGoogle Scholar
• Bilsland-Marchesan, E., J. Ariño, H. Saito, P. Sunnerhagen, and F. Posas. 2000. Rck2 kinase is a substrate for the osmotic stress-activated mitogen-activated protein kinase Hog1. Mol. Cell. Biol. 20:3887–3895.
   PubMed Web of Science ®Google Scholar
• Brewster, J. L., T. de Valoir, N. D. Dwyer, E. Winter, and M. C. Gustin. 1993. An osmosensing signal transduction pathway in yeast. Science 259:1760–1763.
   PubMed Web of Science ®Google Scholar
• Cho, H. S., J. G. Pelton, D. Yan, S. Kustu, and D. E. Wemmer. 2001. Phosphoaspartates in bacterial signal transduction. Curr. Opin. Struct. Biol. 11:679–684.
   PubMedGoogle Scholar
• Escote, X., M. Zapater, J. Clotet, and F. Posas. 2004. Hog1 mediates cell-cycle arrest in G1 phase by the dual targeting of Sic1. Nat. Cell Biol. 6:997–1002.
   PubMed Web of Science ®Google Scholar
• Foreman, P. K., and R. W. Davis. 1994. Cloning vectors for the synthesis of epitope-tagged, truncated and chimeric proteins in Saccharomyces cerevisiae. Gene 144:63–68.
   PubMedGoogle Scholar
• Gao, R., T. R. Mack, and A. M. Stock. 2007. Bacterial response regulators: versatile regulatory strategies from common domains. Trends Biochem. Sci. 32:225–234.
   PubMed Web of Science ®Google Scholar
• Gustin, M. C., J. Albertyn, M. Alexander, and K. Davenport. 1998. MAP kinase pathways in the yeast Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 62:1264–1300.
   PubMed Web of Science ®Google Scholar
• Halkides, C. J., M. M. McEvoy, E. Casper, P. Matsumura, K. Volz, and F. W. Dahlquist. 2000. The 1.9 A resolution crystal structure of phosphono-CheY, an analogue of the active form of the response regulator, CheY. Biochemistry 39:5280–5286.
   PubMedGoogle Scholar
• Hersen, P., M. N. McClean, L. Mahadevan, and S. Ramanathan. 2008. Signal processing by the HOG MAP kinase pathway. Proc. Natl. Acad. Sci. USA 105:7165–7170.
   PubMed Web of Science ®Google Scholar
• Hohmann, S. 2002. Osmotic stress signaling and osmoadaptation in yeasts. Microbiol. Mol. Biol. Rev. 66:300–372.
   PubMed Web of Science ®Google Scholar
• Jacoby, T., H. Flanagan, A. Faykin, A. G. Seto, C. Mattison, and I. Ota. 1997. Two protein-tyrosine phosphatases inactivate the osmotic stress response pathway in yeast by targeting the mitogen-activated protein kinase, Hog1. J. Biol. Chem. 272:17749–17755.
   PubMed Web of Science ®Google Scholar
• Janiak-Spens, F., D. P. Sparling, and A. H. West. 2000. Novel role for an HPt domain in stabilizing the phosphorylated state of a response regulator domain. J. Bacteriol. 182:6673–6678.
   PubMedGoogle Scholar
• Janiak-Spens, F., J. M. Sparling, M. Gurfinkel, and A. H. West. 1999. Differential stabilities of phosphorylated response regulator domains reflect functional roles of the yeast osmoregulatory SLN1 and SSK1 proteins. J. Bacteriol. 181:411–417.
   PubMedGoogle Scholar
• Maeda, T., M. Takekawa, and H. Saito. 1995. Activation of yeast PBS2 MAPKK by MAPKKKs or by binding of an SH3-containing osmosensor. Science 269:554–558.
   PubMed Web of Science ®Google Scholar
• Maeda, T., S. M. Wurgler-Murphy, and H. Saito. 1994. A two-component system that regulates an osmosensing MAP kinase cascade in yeast. Nature 369:242–245.
   PubMed Web of Science ®Google Scholar
• Miller, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
   Google Scholar
• Miyake, Z., M. Takekawa, Q. Ge, and H. Saito. 2007. Activation of MTK1/MEKK4 by GADD45 through induced N-C dissociation and dimerization-mediated trans autophosphorylation of the MTK1 kinase domain. Mol. Cell. Biol. 27:2765–2776.
   PubMed Web of Science ®Google Scholar
• Mizuno, T. 1998. His-Asp phosphotransfer signal transduction. J. Biochem. 123:555–563.
   PubMedGoogle Scholar
• Mumberg, D., R. Müller, and M. Funk. 1994. Regulatable promoters of Saccharomyces cerevisiae: comparison of transcriptional activity and their use for heterologous expression. Nucleic Acids Res. 22:5767–5768.
   PubMed Web of Science ®Google Scholar
• O'Rourke, S. M., and I. Herskowitz. 1998. The Hog1 MAPK prevents cross talk between the HOG and pheromone response MAPK pathways in Saccharomyces cerevisiae. Genes Dev. 12:2874–2886.
   PubMed Web of Science ®Google Scholar
• Ota, I. M., and A. Varshavsky. 1993. A yeast protein similar to bacterial two-component regulators. Science 262:566–569.
   PubMed Web of Science ®Google Scholar
• Porter, S. W., and A. H. West. 2005. A common docking site for response regulators on the yeast phosphorelay protein YPD1. Biochem. Biophys. Res. Commun. 1748:138–145.
   Google Scholar
• Porter, S. W., Q. Xu, and A. H. West. 2003. Ssk1p response regulator binding surface on histidine-containing phosphotransfer protein Ypd1p. Eukaryot. Cell 2:27–33.
   PubMedGoogle Scholar
• Posas, F., and H. Saito. 1998. Activation of the yeast SSK2 MAP kinase kinase kinase by the SSK1 two-component response regulator. EMBO J. 17:1385–1394.
   PubMed Web of Science ®Google Scholar
• Posas, F., S. M. Wurgler-Murphy, T. Maeda, E. A. Witten, T. C. Thai, and H. Saito. 1996. Yeast HOG1 MAP kinase cascade is regulated by a multistep phosphorelay mechanism in the SLN1-YPD1-SSK1 “two-component” osmosensor. Cell 86:865–875.
   PubMed Web of Science ®Google Scholar
• Reiser, V., D. C. Raitt, and H. Saito. 2003. Yeast osmosensor Sln1 and plant cytokinin receptor Cre1 respond to changes in turgor pressure. J. Cell Biol. 161:1035–1040.
   PubMed Web of Science ®Google Scholar
• Robinson, V. L., D. R. Buckler, and A. M. Stock. 2000. A tale of two components: a novel kinase and a regulatory switch. Nat. Struct. Biol. 7:626–633.
   PubMedGoogle Scholar
• Rose, M. D., F. Winston, and P. Hieter. 1990. Methods in yeast genetics: a laboratory course manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
   Google Scholar
• Sato, N., H. Kawahara, A. Toh-e, and T. Maeda. 2003. Phosphorelay-regulated degradation of the yeast Ssk1p response regulator by the ubiquitin-proteasome system. Mol. Cell. Biol. 23:6662–6671.
   PubMedGoogle Scholar
• Song, H. K., J. Y. Lee, M. G. Lee, J. Moon, K. Min, J. K. Yang, and S. W. Suh. 1999. Insights into eukaryotic multistep phosphorelay signal transduction revealed by the crystal structure of Ypd1 from Saccharomyces cerevisiae. J. Mol. Biol. 293:753–761.
   PubMedGoogle Scholar
• Sopko, R., D. Huang, N. Preston, G. Chua, B. Rapp, K. Kafadar, M. Snyder, S. G. Oliver, M. Cyert, T. R. Hughes, C. Boone, and B. Andrews. 2006. Mapping pathways and phenotypes by systematic gene overexpression. Mol. Cell 21:319–330.
   PubMed Web of Science ®Google Scholar
• Stock, A. M., V. L. Robinson, and P. N. Goudreau. 2000. Two-component signal transduction. Annu. Rev. Biochem. 69:183–215.
   PubMed Web of Science ®Google Scholar
• Studier, F. W., and B. A. Moffatt. 1986. Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J. Mol. Biol. 189:113–130.
   PubMed Web of Science ®Google Scholar
• Takekawa, M., and H. Saito. 1998. A family of stress-inducible GADD45-like proteins mediate activation of the stress-responsive MTK1/MEKK4 MAPKKK. Cell 95:521–530.
   PubMed Web of Science ®Google Scholar
• Tatebayashi, K., M. Takekawa, and H. Saito. 2003. A docking site determining specificity of Pbs2 MAPKK for Ssk2/Ssk22 MAPKKKs in the yeast HOG pathway. EMBO J. 22:3624–3634.
   PubMed Web of Science ®Google Scholar
• Tatebayashi, K., K. Tanaka, H.-Y. Yang, K. Yamamoto, Y. Matsushita, T. Tomida, M. Imai, and H. Saito. 2007. Transmembrane mucins Hkr1 and Msb2 are putative osmosensors in the SHO1 branch of yeast HOG pathway. EMBO J. 26:3521–3533.
   PubMed Web of Science ®Google Scholar
• Tatebayashi, K., K. Yamamoto, K. Tanaka, T. Tomida, T. Maruoka, E. Kasukawa, and H. Saito. 2006. Adaptor functions of Cdc42, Ste50, and Sho1 in the yeast osmoregulatory HOG MAPK pathway. EMBO J. 25:3033–3044.
   PubMed Web of Science ®Google Scholar
• Teige, M., E. Scheikl, V. Reiser, H. Ruis, and G. Ammerer. 2001. Rck2, a member of the calmodulin-protein kinase family, links protein synthesis to high osmolarity MAP kinase signaling in budding yeast. Proc. Natl. Acad. Sci. USA 98:5625–5630.
   PubMed Web of Science ®Google Scholar
• Volz, K., and P. Matsumura. 1991. Crystal structure of Escherichia coli CheY refined at 1.7-angstrom resolution. J. Biol. Chem. 266:15511–15519.
   PubMed Web of Science ®Google Scholar
• Wurgler-Murphy, S. M., T. Maeda, E. A. Witten, and H. Saito. 1997. Regulation of the Saccharomyces cerevisiae HOG1 mitogen-activated protein kinase by the PTP2 and PTP3 protein tyrosine phosphatases. Mol. Cell. Biol. 17:1289–1297.
   PubMed Web of Science ®Google Scholar
• Xu, Q., S. W. Porter, and A. H. West. 2003. The yeast YPD1/SLN1 complex: insights into molecular recognition in two-component signaling systems. Structure 11:1569–1581.
   PubMedGoogle Scholar
• Xu, Q., and A. H. West. 1999. Conservation of structure and function among histidine-containing phosphotransfer (HPt) domains as revealed by the crystal structure of YPD1. J. Mol. Biol. 292:1039–1050.
   PubMed Web of Science ®Google Scholar
• Yuzyuk, T., and D. C. Amberg. 2003. Actin recovery and bud emergence in osmotically stressed cells requires the conserved actin interacting mitogen-activated protein kinase kinase kinase Ssk2p/MTK1 and the scaffold protein Spa2p. Mol. Biol. Cell 14:3013–3026.
   PubMedGoogle Scholar
• Yuzyuk, T., M. Foehr, and D. C. Amberg. 2002. The MEK kinase Ssk2p promotes actin cytoskeleton recovery after osmotic stress. Mol. Biol. Cell 13:2869–2880.
   PubMedGoogle Scholar