Phosphorelay-regulated degradation of the yeast Ssk1p response regulator by the ubiquitin-proteasome system

Molecular and Cellular Biology

Volumn 23, Issue 18, 2003, Pages 6662-6671

  Sato, Naoto ^a   Kawahara, Hiroyuki ^b   Toh e, Akio ^a   Maeda, Tatsuya ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b HOKKAIDO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; PROTEASOME; PROTEIN SSK1P; UBIQUITIN; UNCLASSIFIED DRUG;

ARTICLE; DEPHOSPHORYLATION; NONHUMAN; OSMOREGULATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION;

BIOLOGICAL TRANSPORT; CYSTEINE ENDOPEPTIDASES; DNA-BINDING PROTEINS; DOWN-REGULATION; LIGASES; MAP KINASE SIGNALING SYSTEM; MULTIENZYME COMPLEXES; MUTATION; OSMOSIS; PHOSPHORYLATION; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; UBIQUITIN; UBIQUITIN-CONJUGATING ENZYMES;

BACTERIA (MICROORGANISMS); FUNGI; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

EID: 0042691653     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.23.18.6662-6671.2003     Document Type: Article

References (67)

1. Albertyn, J., S. Hohmann, J. M. Thevelein, and B. A. Prior. 1994. GPD1, which encodes glycerol-3-phosphate dehydrogenase, is essential for growth under osmotic stress in Saccharomyces cerevisiae, and its expression is regulated by the high-osmolarity glycerol response pathway. Mol. Cell. Biol. 14:4135-4144.
2. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl. 1989. Current protocols in molecular biology. Wiley, New York, N.Y.
3. Bays, N. W., R. G. Gardner, L. P. Seelig, C. A. Joazeiro, and R. Y. Hampton. 2001. Hrd1p/Der3p is a membrane-anchored ubiquitin ligase required for ER-associated degradation. Nat. Cell Biol. 3:24-29.
4. Bouquin, N., A. L. Johnson, B. A. Morgan, and L. H. Johnston. 1999. Association of the cell cycle transcription factor Mbp1 with the Skn7 response regulator in budding yeast. Mol. Biol. Cell 10:3389-3400.
5. UFD1/NPL4 chaperone (segregase) in ERAD of OLE1 and other substrates. EMBO J. 21:615-621.
6. 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.
7. Brown, J. L., H. Bussey, and R. C. Stewart. 1994. Yeast Skn7p functions in a eukaryotic two-component regulatory pathway. EMBO J. 13:5186-5194.
8. Brown, J. L., S. North, and H. Bussey. 1993. SKN7, a yeast multicopy suppressor of a mutation affecting cell wall 5-glucan assembly, encodes a product with domains homologous to prokaryotic two-component regulators and to heat shock transcription factors. J. Bacteriol. 175:6908-6915.
9. Chang, C., S. F. Kwok, A. B. Bleecker, and E. M. Meyerowitz. 1993. Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. Science 262:539-544.
10. Chen, P., P. Johnson, T. Sommer, S. Jentsch, and M. Hochstrasser. 1993. Multiple ubiquitin-conjugating enzymes participate in the in vivo degradation of the yeast MATα2 repressor. Cell 74:357-369.
11. Christianson, T. W., R. S. Sikorski, M. Dante, J. H. Shero, and P. Hieter. 1992. Multifunctional yeast high-copy-number shuttle vectors. Gene 110: 119-122.
12. de Nadal, E., P. M. Alepuz, and F. Posas. 2002. Dealing with osmostress through MAP kinase activation. EMBO Rep. 3:735-740.
13. Elsasser, S., R. R. Gali, M. Schwickart, C. N. Larsen, D. S. Leggett, B. Müller, M. T. Feng, F. Tübing, G. A. G. Dittmar, and D. Finley. 2002. Proteasome subunit Rpn1 binds ubiquitin-like protein domains. Nat. Cell Biol. 4:725-730.
14. Esch, R. K., and B. Errede. 2002. Pheromone induction promotes Ste11 degradation through a MAPK feedback and ubiquitin-dependent mechanism. Proc. Natl. Acad. Sci. USA 99:9160-9165.
15. Friedlander, R., E. Jarosch, J. Urban, C. Volkwein, and T. Sommer. 2000. A regulatory link between ER-associated protein degradation and the unfolded-protein response. Nat. Cell Biol. 2:379-384.
16. Funakoshi, M., T. Sasaki, T. Nishimoto, and H. Kobayashi. 2002. Budding yeast Dsk2 is a polyubiquitin-binding protein that can interact with the proteasome. Proc. Natl. Acad. Sci. USA 99:745-750.
17. Gardner, R. G., A. G. Shearer, and R. Y. Hampton. 2001. In vivo action of the HRD ubiquitin ligase complex: mechanisms of endoplasmic reticulum quality control and sterol regulation. Mol. Cell. Biol. 21:4276-4291.
18. 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.
19. Hampton, R. Y. 2002. ER-associated degradation in protein quality control and cellular regulation. Curr. Opin. Cell. Biol. 14:476-482.
20. Herskowitz, I. 1995. MAP kinase pathways in yeast: for mating and more. Cell 80:187-197.
21. Hiller, M. M., A. Finger, M. Schweiger, and D. H. Wolf. 1996. ER degradation of a misfolded luminal protein by the cytosolic ubiquitin-proteasome pathway. Science 273:1725-1728.
22. Ho, Y., A. Gruhler, A. Heilbut, G. D. Bader, L. Moore, S.-L. Adams, A. Millar, P. Taylor, K. Bennett, K. Boutilier, L. Yang, C. Wolting, L. Donaldson, S. Schandorff, J. Shewnarane, M. Vo, J. Taggart, M. Goudreault, B. Muskat, C. Alfarano, D. Dewar, Z. Lin, K. Michalickova, A. R. Willems, H. Sassi, P. A. Nielsen, K. J. Rasmussen, J. R. Andersen, L. E. Johansen, L. H. Hansen, H. Jespersen, A. Podtelejnikov, E. Nielsen, J. Crawford, V. Poulsen, B. D. Sørensen, J. Matthiesen, R. C. Hendrickson, F. Gleeson, T. Pawson, M. F. Moran, D. Durocher, M. Mann, C. W. V. Hogue, D. Figeys, and M. Tyers. 2002. Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature 415:180-183.
23. Hua, J., C. Chang, Q. Sun, and E. M. Meyerowitz. 1995. Ethylene insensitivity conferred by Arabidopsis ERS gene. Science 269:1712-1714.
24. Inoue, T., M. Higuchi, Y. Hashimoto, M. Seki, M. Kobayashi, T. Kato, S. Tabata, K. Shinozaki, and T. Kakimoto. 2001. Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature 409:1060-1063.
25. 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.
26. Janiak-Spens, F., D. P. Sparling, and A. H. West. 2000. Novel role for HPt domain in stabilizing the phosphorylated state of a response regulator domain. J. Bacteriol. 182:6673-6678.
27. 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.
28. Kakimoto, T. 1996. CKI1, a histidine kinase homolog implicated in cytokinin signal transduction. Science 274:982-985.
29. Ketela, T., J. L. Brown, R. C. Stewart, and H. Bussey. 1998. Yeast Skn7p activity is modulated by the Sln1p-Ypd1p osmosensor and contributes to regulation of the HOG pathway. Mol. Gen. Genet. 259:372-378.
30. Kominami, K., G. N. DeMartino, C. R. Moomaw, C. A. Slaughter, N. Shimbara, M. Fujimuro, H. Yokosawa, H. Hisamatsu, N. Tanahashi, Y. Shimizu, K. Tanaka, and A. Toh-e. 1995. Nin1p, a regulatory subunit of the 26S proteasome, is necessary for activation of Cdc28p kinase of Saccharomyces cerevisiae. EMBO J. 14:3105-3115.
31. Krems, B., C. Charizanis, and K. D. Entian. 1996. The response regulator-like protein Pos9/Skn7 of Saccharomyces cerevisiae is involved in oxidative stress resistance. Curr. Genet. 29:327-334.
32. Li, S., A. Ault, C. L. Malone, D. Raitt, S. Dean, L. H. Johnston, R. J. Deschenes, and J. S. Fassler. 1998. The yeast histidine protein kinase, Sln1p, mediates phosphotransfer to two response regulators, Ssk1p and Skn7p. EMBO J. 17:6952-6962.
33. Li, S., S. Dean, Z. Li, J. Horecka, R. J. Deschenes, and J. S. Fassler. 2002. The eukaryotic two-component histidine kinase Sln1p regulates OCH1 via the transcription factor, Skn7p. Mol. Biol. Cell 13:412-424.
34. Longtine, M. S., A. McKenzie III, D. J. Demarini, N. G. Shah, A. Wach, A. Brachat, P. Philippsen, and J. R. Pringle. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14:953-961.
35. Lu, Z., S. Xu, C. Joazeiro, M. H. Cobb, and T. Hunter. 2002. The PHD domain of MEKK1 acts as an E3 ubiquitin ligase and mediates ubiquitination and degradation of ERK1/2. Mol. Cell 9:945-956.
36. Maeda, T., M. Takekawa, and H. Salto. 1995. Activation of yeast PBS2 MAPKK by MAPKKKs or by binding of an SH3-containing osmosensor. Science 269:554-558.
37. Maeda, T., A. Y. M. Tsai, and H. Saito. 1993. Mutations in a protein tyrosine phosphatase gene (PTP2) and a protein serine/threonine phosphatase gene (PTC1) cause a synthetic growth defect in Saccharomyces cerevisiae. Mol. Cell. Biol. 13:5408-5417.
38. 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.
39. Morgan, B. A., G. R. Banks, W. M. Toone, D. Raitt, S. Kuge, and L. H. Johnston. 1997. The Skn7 response regulator controls gene expression in the oxidative stress response of the budding yeast Saccharomyces cerevisiae. EMBO J. 16:1035-1044.
40. Morgan, B. A., N. Bouquin, G. F. Merrill, and L. H. Johnston. 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.
41. 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.
42. Mumberg, D., R. Müller, and M. Funk. 1995. Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds. Gene 156:119-122.
43. O'Rourke, S. M., and I. Herskowitz. 2002. A third osmosensing branch in Saccharomyces cerevisiae requires the Msb2 protein and functions in parallel with the Sho1 branch. Mol. Cell. Biol. 22:4739-4749.
44. Ostrander, D. B., and J. A. Gorman. 1999. The extracellular domain of Saccharomyces cerevisiae Sln1p membrane osmolarity sensor is necessary for kinase activity. J. Bacteriol. 181:2527-2534.
45. Ota, I. M., and A. Varshavsky. 1993. A yeast protein similar to bacterial two-component regulators. Science 262:566-569.
46. Plemper, R. K., and D. H. Wolf. 1999. Retrograde protein translocation: ERADication of secretory proteins in health and disease. Trends Biochem. Sci. 24:266-270.
47. Posas, F., and H. Saito. 1997. Osmotic activation of the HOG MAPK pathway via Ste11p MAPKKK: scaffold role of Pbs2p MAPKK. Science 276:1702-1705.
48. 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.
49. Posas, F., M. Takekawa, and H. Saito. 1998. Signal transduction by MAP kinase cascades in budding yeast. Curr. Opin. Microbiol. 1:175-182.
50. 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.
51. Raitt, D. C., F. Posas, and H. Saito. 2000. Yeast Cdc42 GTPase and Ste20 PAK-like kinase regulate Sho1-dependent activation of the Hog1 MAPK pathway. EMBO J. 19:4623-4631.
52. Reiser, V., S. M. Salah, and G. Ammerer. 2000. Polarized localization of yeast Pbs2 depends on osmostress, the membrane protein Sho1 and Cdc42. Nat. Cell Biol. 2:620-627.
53. Rep, M., V. Reiser, U. Gartner, J. M. Thevelein, S. Hohmann, G. Ammerer, and H. Ruis. 1999. Osmotic stress-induced gene expression in Saccharomyces cerevisiae requires Msn1p and the novel nuclear factor Hotlp. Mol. Cell. Biol. 19:5474-5485.
54. Robinson, M. J., and M. H. Cobb. 1997. Mitogen-activated protein kinase pathways. Curr. Opin. Cell Biol. 9:180-186.
55. Sakai, H., T. Honma, T. Aoyama, S. Sato, T. Kato, S. Tabata, and A. Oka. 2001. ARR1, a transcription factor for genes immediately responsive to cytokinins. Science 294:1519-1521.
56. Schauber, C., L. Chen, P. Tongaonkar, I. Vega, D. Lambertson, W. Potts, and K. Madura. 1998. Rad23 links DNA repair to the ubiquitin/proteasome pathway. Nature 391:715-718.
57. Sheen, J. 2002. Phosphorelay and transcriptional control in cytokinin signal transduction. Science 296:1650-1652.
58. Sikorski, R. S., and P. Hieter. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122:19-27.
59. Smalle, J., J. Kurepa, P. Yang, E. Babiychuk, S. Kushnir, A. Durski, and R. D. Vierstra. 2002. Cytokinin growth responses in Arabidopsis involve the 26S proteasome subunit RPN12. Plant Cell 14:17-32.
60. Swanson, R., M, Locher, and M. Hochstrasser. 2001. A conserved ubiquitin ligase of the nuclear envelope/endoplasmic reticulum that functions in both ER-associated and Mata2 repressor degradation. Genes Dev. 15:2660-2674.
61. Takeuchi, J., M. Fujimuro, H. Yokosawa, K. Tanaka, and A. Toh-e. 1999. Rpn9 is required for efficient assembly of the yeast 26S proteasome. Mol. Cell. Biol. 19:6575-6584.
62. Tanaka, K., T. Yoshimura, A. Kumatori, A. Ichihara, A. Ikai, M. Nisihigai, K. Kameyama, and T. Takagi. 1988. Proteasomes (multi-protease complexes) as 20S ring-shaped particles in a variety of eukaryotic cells. J. Biol. Chem. 263:16209-16217.
63. Tao, W., R. J. Deschenes, and J. S. Fassler. 1999. Intracellular glycerol levels modulate the activity of Sln1p, a Saccharomyces cerevisiae two-component regulator. J. Biol. Chem. 274:360-367.
64. Warmka, J., J. Hanneman, J. Lee, D. Amin, and I. Ota. 2001. Ptc1, a type 2C Ser/Thr phosphatase, inactivates the HOG pathway by dephosphorylating the mitogen-activated protein kinase Hog1. Mol. Cell. Biol. 21:51-60.
65. Watkins, J. F., P. Sung, L. Prakash, and S. Prakash. 1993. The Saccharomyces cerevisiae DNA repair gene RAD23 encodes a nuclear protein containing a ubiquitin-like domain required for biological function. Mol. Cell. Biol. 13:7757-7765.
66. 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.
67. Yamada, H., T. Suzuki, K. Terada, K. Takei, K. Ishikawa, K. Miwa, T. Yamashino, and T. Mizuno. 2001. The Arabidopsis AHK4 histidine kinase is a cytokinin-binding receptor that transduces cytokinin signals across the membrane. Plant Cell Physiol. 42:1017-1023.