Kinetic analysis of YPD1-dependent phosphotransfer reactions in the yeast osmoregulatory phosphorelay system

Biochemistry

Volumn 44, Issue 1, 2005, Pages 377-386

  Janiak Spens, Fabiola ^a   Cook, Paul F ^a   West, Ann H ^a  

^a UNIVERSITY OF OKLAHOMA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; MUTAGENESIS; ORGANIC ACIDS; OSMOSIS; PHOTOCHEMICAL REACTIONS; RATE CONSTANTS;

HISTIDINE-CONTAINING PHOSPHOTRANSFER (HPT); OSMOTIC CONDITIONS; RESIDUES; TRANSFER REACTIONS;

YEAST;

ASPARTIC ACID; FUNGAL PROTEIN; HISTIDINE; PROTEIN HISTIDINE KINASE; PROTEIN HISTIDINE KINASE SLN1; PROTEIN YPD1; REGULATOR PROTEIN; REGULATOR PROTEIN SKN7; REGULATOR PROTEIN SSK1; UNCLASSIFIED DRUG;

ALPHA HELIX; ANIMAL CELL; ARTICLE; BINDING AFFINITY; CHEMICAL REACTION KINETICS; CONTROLLED STUDY; GENE MUTATION; NONHUMAN; OSMOREGULATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; YEAST;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ASPARTIC ACID; CLONING, MOLECULAR; DNA-BINDING PROTEINS; GLUTATHIONE TRANSFERASE; HISTIDINE; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PEPTIDE FRAGMENTS; PHOSPHORYLATION; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT FUSION PROTEINS; RESTRICTION MAPPING; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

ANIMALIA; BACTERIA (MICROORGANISMS); EUKARYOTA; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

EID: 11844275257     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi048433s     Document Type: Article

References (45)

1. West, A. H., and Stock, A. M. (2001) Histidine kinases and response regulator proteins in two-component signaling systems, Trends Biochem. Sci. 26, 369-376.
2. Appleby, J. L., Parkinson, J. S., and Bourret, R. B. (1996) Signal transduction via the multistep phosphorelay: not necessarily a road less traveled, Cell 86, 845-848.
3. Maeda, T., Wurgler-Murphy, S. M., and Saito, H. (1994) A two-component system that regulates an osmosensing MAP kinase cascade in yeast, Nature 369, 242-245.
4. Posas, F., Wurgler-Murphy, S. M., Maeda, T., Witten, E. A., Thai, T. C., and Saito, H. (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.
5. Saito, H. (2001) Histidine phosphorylation and two-component signaling in eukaryotic cells, Chem. Rev. 101, 2497-2509.
6. Posas, F., and Saito, H. (1998) Activation of the yeast SSK2 MAP kinase kinase kinase by the SSK1 two-component response regulator, EMBO J. 17, 1385-1394.
7. Mager, W. H., and Varela, J. C. S. (1993) Osmostress response of the yeast Saccharomyces, Mol. Microbiol. 10, 253-258.
8. Brown, J. L., Bussey, H., and Stewart, R. C. (1994) Yeast Skn7p functions in a eukaryotic two-component regulatory pathway, EMBO J. 13, 5186-5194.
9. Raitt, D. C., Johnson, A. L., Erkine, A. M., Makino, K., Morgan, B., Gross, D. S., and Johnston, L. H. (2000) The Skn7 response regulator of Saccharomyces cerevisiae interacts with Hsf1 in vivo and is required for the induction of heat shock genes by oxidative stress, Mol. Biol. Cell 11, 2335-2347.
10. Morgan, B. A., Banks, G. R., Toone, W. M., Raitt, D., Kuge, S., and Johnston, L. H. (1997) The Skn7 response regulator controls gene expression in the oxidative stress response of the budding yeast Saccharomyces cerevisiae, EMBO J. 16, 1035-1044.
11. Li, S., Dean, S., Li, Z., Horecka, J., Deschenes, R. J., and Fassler, J. S. (2002) The eukaryotic two-component histidine kinase Sln1p regulates OCH1 via the transcription factor, Skn7p, Mol. Biol. Cell 13, 412-424.
12. Li, S., Ault, A., Malone, C. L., Raitt, D., Dean, S., Johnston, L. H., Deschenes, R. J., and Fassler, J. S. (1998) The yeast histidine protein kinase, Sln1p, mediates phosphotransfer to two response regulators, Ssk1p and Skn7p, EMBO J. 17, 6952-6962.
13. Brown, J. L., North, S., and Bussey, H. (1993) SKN7, a yeast multicopy suppressor of a mutation affecting cell wall β-glucan assembly, encodes a product with domains homologous to prokaryotic two-component regulators and to heat shock transcription factors, J. Bacteriol. 175, 6908-6915.
14. Morgan, B. A., Bouquin, N., Merrill, G. F., and Johnston, L. H. (1995) A yeast transcription factor bypassing the requirement for SBF and DSC1/MBF in budding yeast has homology to bacterial signal transduction proteins, EMBO J. 14, 5679-5689.
15. Janiak-Spens, F., Sparling, D. P., and West, A. H. (2000) Novel role for an HPt domain in stabilizing the phosphorylated state of a response regulator domain, J. Bacteriol. 182, 6673-6678.
16. Janiak-Spens, F., Sparling, J. M., Gurfinkel, M., and West, A. H. (1999) Differential stabilities of phosphorylated response regulator domains reflect functional roles of the yeast osmoregulatory SLN1 and SSK1 proteins, J. Bacteriol. 181, 411-417.
17. Stock, A. M., Robinson, V. L., and Goudreau, P. N. (2000) Two-component signal transduction, Annu. Rev. Biochem. 69, 183-215.
18. Stock, A. M., and West, A. H. (2002) in Histidine kinases in signal transduction (Inouye, M., and Dutta, R., Eds.) pp 237-271, Academic Press, New York.
19. Lukat, G. S., McCleary, W. R., Stock, A. M., and Stock, J. B. (1992) Phosphorylation of bacterial response regulator proteins by low molecular weight phospho-donors. Proc. Natl. Acad. Sci. U.S.A. 89, 718-722.
20. Mayover, T. L., Halkides, C. J., and Stewart, R. C. (1999) Kinetic characterization of CheY phosphorylation reactions: Comparison of P-CheA and small-molecule phosphodonors, Biochemistry 38, 2259-2271.
21. Silversmith, R. E., Appleby, J. L., and Bourret, R. B. (1997) Catalytic mechanism of phosphorylation and dephosphorylation of CheY: Kinetic characterization of imidazole phosphates as phosphodonors and the role of acid catalysis, Biochemistry 36, 14965-14974.
22. Xu, Q., and West, A. H. (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.
23. Song, H. K., Lee, J. Y., Lee, M. G., Min, J. M. K., Yang, J. K., and Suh, S. W. (1999) Insights into eukaryotic multistep phosphorelay signal transduction revealed by the crystal structure of Ypdlp from Saccharomyces cerevisiae, J. Mol. Biol. 293, 753-761.
24. Mourey, L., Da Re, S., Pédelacq, J.-D., Tolstykh, T., Faune, C., Guillet, V., Stock, J. B., and Samama, J.-P. (2001) Crystal structure of the CheA histidine phosphotransfer domain that mediates response regulator phosphorylation in bacterial chemotaxis, J. Biol. Chem. 276, 31074-31082.
25. Janiak-Spens, F., and West, A. H. (2000) Functional roles of conserved amino acid residues surrounding the phosphorylatable histidine of the yeast phosphorelay protein YPD1, Mol. Microbiol. 37, 136-144.
26. Grimshaw, C. E., Huang, S., Hanstein, C. G., Strauch, M. A., Burbulys, D., Wang, L., Hoch, J. A., and Whiteley, J. M. (1998) Synergistic kinetic interactions between components of the phosphorelay controlling sporulation in Bacillus subtilis, Biochemistry 37, 1365-1375.
27. Stewart, R. C. (1997) Kinetic characterization of phosphotransfer between CheA and CheY in the bacterial chemotaxis signal transduction pathway, Biochemistry 36, 2030-2040.
28. Fisher, S. L., Kim, S.-K., Wanner, B. L., and Walsh, C. T. (1996) Kinetic comparisons of the specificity of the vancomycin resistance kinase VanS for two response regulators, VanR and PhoB, Biochemistry 35, 4732-4740.
29. Xu, Q., Nguyen, V., and West, A. H. (1999) Purification, crystallization, and preliminary X-ray diffraction analysis of the yeast phosphorelay protein YPD1, Acta Crystallogr. D55, 291-293.
30. Guan, K. L., and Dixon, J. E. (1991) Eukaryotic proteins expressed in Escherichia coli. An improved thrombin cleavage and purification procedure of fusion proteins with glutathione S-transferase, Anal. Biochem. 192, 262-267.
31. Zapf, J. W., Hoch, J. A., and Whiteley, J. M. (1996) A phosphotransferase activity of the Bacillus subtilis sporulation protein SpoOF that employs phosphoramidate substrates, Biochemistry 35, 2926-2933.
32. Lukat, G. S., Stock, A. M., and Stock, J. B. (1990) Divalent metal ion binding to the CheY protein and its significance to phosphotransfer in bacterial chemotaxis, Biochemistry 29, 5436-5442.
33. Da Re, S. S., Deville-Bonne, D., Tolstykh, T., Véron, M., and Stock, J. B. (1999) Kinetics of CheY phosphorylation by small molecule phosphodonors, FEBS Lett. 457, 323-326.
34. Fersht, A. (1999) Structure and mechanism in protein science, W. H. Freeman and Company, New York.
35. Ketela, T., Brown, J. L., Stewart, R. C., and Bussey, H. (1998) Yeast Skn7p activity is modulated by the Sln1p-Ypd1p osmosensor and contributes to regulation of the HOG1 pathway, Mol. Gen. Genet. 259, 372-378.
36. Lu, J. M.-Y., Deschenes, R. J., and Fassler, J. S. (2003) Saccharomyces cerevisiae histidine phosphotransferase Ypdlp shuttles between the nucleus and cytoplasm for SLN1-dependent phosphorylation of Ssklp and Skn7p, Eukaryotic Cell 2, 1304-1314.
37. Xu, Q., Porter, S. W., and West, A. H. (2003) The yeast YPD1/ SLN1 complex: Insights into molecular recognition in two-component systems, Structure 11, 1569-1581.
38. Stewart, R. C., Jahreis, K., and Parkinson, J. S. (2000) Rapid phosphotransfer to CheY from a CheA protein lacking the CheY-binding domain, Biochemistry 39, 13157-13165.
39. Swanson, R. V., Schuster, S. C., and Simon, M. I. (1993) Expression of CheA fragments which define domains encoding kinase, phosphotransfer, and CheY binding activities, Biochemistry 32, 7623-7629.
40. Li, J., Swanson, R. V., Simon, M. I., and Weis, R. M. (1995) The response regulators CheB and CheY exhibit competitive binding to the kinase CheA, Biochemistry 34, 14626-14636.
41. Hess, J. F., Oosawa, K., Kaplan, N., and Simon, M. I. (1988) Phosphorylation of three proteins in the signaling pathway of bacterial chemotaxis, Cell 53, 79-87.
42. Stewart, R. C., and Van Bruggen, R. (2004) Association and dissociation kinetics for CheY interacting with the P2 domain of CheA, J. Mol. Biol. 336, 287-301.
43. Brewster, J. L., de Valoir, T., Dwyer, N. D., Winter, E., and Gustin, M. C. (1993) An osmosensing signal transduction pathway in yeast, Science 259, 1760-1763.
44. Maeda, T., Takekawa, M., and Saito, H. (1995) Activation of yeast PBS2 MAPKK by MAPKKKs or by binding of an SH3-containing osmosensor, Science 269, 554-558.
45. Sato, N., Kawahara, H., Toh-e, A., and Maeda, T. (2003) Phosphorelay-regulated degradation of the yeast Ssk1p response regulator by the ubiquitin-proteosome system, Mol. Cell, Biol. 23, 6662-6671.