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

Molecular Biology of the Cell

Volumn 11, Issue 7, 2000, Pages 2335-2347

  Raitt, Desmond C ^a   Johnson, Anthony L ^a   Erkine, Alexander M ^b   Makino, Kozo ^c   Morgan, Brian ^d   Gross, David S ^b   Johnston, Leland H ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^c OSAKA UNIVERSITY   (Japan)

^d NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DNA;

ANIMAL CELL; ARTICLE; CELL SURVIVAL; DNA BINDING; GENE EXPRESSION; GENE INDUCTION; GENE MUTATION; HEAT SHOCK RESPONSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE;

ANIMALIA; SACCHAROMYCES CEREVISIAE;

EID: 0033916138     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.11.7.2335     Document Type: Article

References (63)

1. Alberts, A.S., Bouquin, N., Johnston, L.H., and Treisman, R. (1998). Analysis of RhoA-binding proteins reveals an interaction domain conserved in heterotrimeric G protein β-subunits and the yeast response regulator protein Skn7. J. Biol. Chem. 273, 8616-8622.
2. Bouquin, N., Johnson, A.L., Morgan, B.A., and Johnston, L.H. (1999). Association of the cell cycle transcription factor Mbp1 with the Skn7 response regulator in budding yeast. Mol. Biol. Cell 10, 3389-3400.
3. 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.
4. 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 with homology to prokaryotic two-component regulators and heat shock transcription factors. J. Bacteriol. 175, 6908-6915.
5. Christianson, T.W., Sikorski, R.S., Dante, M., Shero, J.H., and Heiter, P. (1992). Multifunctional yeast high-copy number shuttle vectors. Gene 110, 119-122.
6. Craig, E.A. (1992). The heat shock response of Saccharomyces cerevisiae. In: The Molecular and Cellular Biology of the Yeast Saccharomyces cerevisiae. Vol. 2. Gene Expression, ed. E.W. Jones, J.R. Pringle, and J.R. Broach, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory, 501-538.
7. Craig, E.A., Weissman, J.S., and Horwich, A.L. (1994). Heat shock proteins and molecular chaperones: mediators of protein conformation and turnover in the cell. Cell 78, 365-372.
8. Damberger, F.F., Pelton, J.G., Harrison, C.J., Nelson, H.C., and Wemmer, D.E. (1994). Solution structure of the DNA binding of the heat shock transcription factor determined by multidimensional heteronuclear magnetic resonance spectroscopy. Protein Sci. 3, 1806-1821.
9. Davidson, J.F., Whyte, B., Bissinger, P.H., and Shiestl, R.H. (1996). Oxidative stress is involved in heat-induced cell death in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 93, 5116-5121.
10. Erkine, A.M., Adams, C.C., Diken, T., and Gross, D.S. (1996). Heat shock factor gains access to the yeast HSC82 promoter independently of other sequence specific factors and antagonises nucleosomal repression of basal and induced transcription. Mol. Cell. Biol. 16, 7004-7017.
11. Erkine, A.M., Magrogran, S.F., Sekinger, E.A., and Gross, D.S. (1999). Cooperative binding of heat shock factor to the yeast HSP82 promoter in vivo and in vitro. Mol. Cell. Biol. 19, 1627-1639.
12. Fernandes, M., Xiao, H., and Lis, J.T. (1995). Binding of heat shock factor to and transcriptional activation of heat shock genes in Drosophila. Nucleic Acids Res. 23, 4799-4804.
13. Foreman, P., and Davis, R.W. (1994). Cloning vectors for the synthesis of epitope-tagged, truncated and chimeric proteins in Saccharomyces cerevisiae. Gene 144, 63-68.
14. Giardina, C., and Lis, J.T. (1995). Dynamic protein-DNA architecture of a yeast heat shock promoter. Mol. Cell. Biol. 15, 2737-2744.
15. Gietz, R.D., and Sugino, A. (1988). New yeast-Escherichia coli vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene 74, 527-534.
16. Gross, D.S., English, K.E., Collins, K.W., and Lee, S. (1990). Genomic footprinting of the yeast HSP82 promoter reveals marked distortion of the DNA helix and constitutive occupancy of heat shock and TATA elements. J. Mol. Biol. 216, 611-631.
17. Guarente, L., and Mason, T. (1983). Heme regulates transcription of a CYC1 gene of S. cerevisiae via an upstream activation site. Cell 32, 1279-1286.
18. Halliwell, B. (1994). Free radicals and antioxidants: a personal view. Nutr. Rev. 52, 253-265.
19. Harbury, P.B., Zhang, T., Kim, P.S., and Alber, T. (1993). A switch between two-, three- and four-stranded coiled-coils in GCN4 leucine zipper mutants. Science 262, 1401-1407.
20. Harrison, C.J., Bohm, A.A., and Nelson, H.C. (1994). Crystal structure of the DNA binding domain of the heat shock transcription factor. Science 263, 224-227.
21. Høj, A., and Jakobsen, B.K. (1994). A short element required for turning off heat shock transcription factor: evidence that phosphorylation enhances deactivation. EMBO J. 13, 2617-2624.
22. Jakobsen, B., and Pelham, H.R. (1988). Constitutive binding of yeast heat-shock transcription factor to DNA in vivo. Mol. Cell. Biol. 8, 5040-5042.
23. Jamieson, D.J. (1992). Saccharomyces cerevisiae has distinct adaptive responses to both hydrogen peroxide and menadione. J. Bacteriol. 174, 6678-6681.
24. Krems, B., Charizanis, C., and Entian, K.D. (1995). Mutants of Saccharomyces cerevisiae sensitive to oxidative and osmotic stress. Curr. Genet. 27, 427-434.
25. Krems, B., Charizanis, C., and Entian, K.D. (1996). The response regulator-like protein Pos9/Skn7 of Saccharomyces cerevisiae is involved in oxidative stress resistance. Curr. Genet. 29, 327-334.
26. Kuge, S., and Jones, N.J. (1994). YAP1 dependent activation of TRX2 is essential for the response of Saccharomyces cerevisiae to oxidative stress by hydrogen peroxides. EMBO J. 13, 655-664.
27. Lee, J., Lagniel, C., Spector, D., Garin, J., Labarre, J., and Toledano, M.B. (1999). Yap1 and Skn7 control two specialized oxidative stress response regulons in yeast. J. Biol. Chem. 274, 16040-16046.
28. Li, S., Ault, A., Malone, C.L., Raitt, D.C., Dean, S., Johnston, L.H., Deschenes, R.J., and Fassler, J. (1998). The yeast histidine protein kinase, Slnlp, mediates phosphotransfer to two response regulators, Ssk1p and Skn7p. EMBO J. 17, 6952-6962.
29. Lin, J.T., and Lis, J.T. (1999). Glycogen synthase phosphatase interacts with heat shock factor to activate CUPI gene transcription in Saccharomyces cerevisiae. Mol. Cell. Biol. 19, 3237-3245.
30. Lindquist, S., and Craig, E.A. (1988). The heat shock proteins. Annu. Rev. Genet. 22, 631-677.
31. Liu, X., and Thiele, D.J. (1996). Oxidative stress induces heat shock factor phosphorylation and HSF-dependent activation of yeast metallothionein gene transcription. Genes Dev. 10, 592-603.
32. Lowndes, N.F., Johnson, A.L., Breeden, L., and Johnston, L.H. (1991). Coordination of expression of DNA synthesis genes in budding yeast by a cell-cycle regulated trans factor. Nature 350, 247-248.
33. Lupas, A. (1996). Coiled-coils: new structures and new functions. Trends Biochem. Sci. 21, 375-382.
34. Mager, W.H., and De Kruijff, A.J.J. (1995). Stress-induced transcriptional activation. Microbiol. Rev. 59, 506-531.
35. Mager, W.H., and Ferreira, P.M. (1993). Stress response in yeast. Biochem. J. 290, 1-13.
36. Martínez-Pastor, M.T., Marchler, G., Schüller, C., Marchler-Bauer, A., Ruis, H., and Estruch, F. (1996). The Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress response element (STRE). EMBO J. 15, 2227-2235.
37. Mason, P.B.J., and Lis, J.T. (1997). Cooperative and competitive protein interactions at the hsp70 promoter. J. Biol. Chem. 272, 33227-33233.
38. Morgan, B.A., Banks, G.R., Toone, W.M., Raitt, D.C., 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.
39. 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.
40. Murray, J.A.H. (1987). Molecular Analysis of the Yeast Two-Micron Plasmid. Ph.D. Thesis. Heidelberg, Germany: Euro Mol Biol Lab.
41. Park, H.O., and Craig, E.A. (1989). Positive and negative regulation of basal expression of a yeast HSP70 gene. Mol. Cell. Biol. 9, 2025-2033.
42. Parkinson, J.S. (1993). Signal transduction schemes in bacteria. Cell 73, 857-871.
43. Peteranderl, R., and Nelson, H.C. (1992). Trimerization of the heat shock transcription factor by a triple-stranded α-helical coiled-coil. Biochemistry 31, 12272-12276.
44. Posas, F., Wurgler-Murphy, S., 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.
45. Rabindran, S.K., Haroun, R.L., Clos, J., Wisniewski, J., and Wu, C. (1993). Regulation of heat shock factor trimer formation: role of a conserved leucine zipper. Science 259, 230-233.
46. Rassow, J., von Ahsen, O., Börner, U., and Pfanner, N. (1997). Molecular chaperones: towards a characterization of the heat-shock protein 70 family. Trends Cell Biol. 7, 129-133.
47. Ruis, H., and Schüller, C. (1995). Stress signaling in yeast. BioEssays 17, 959-965.
48. Sanchez, Y., Taulien, J., Borkovich, K.A., and Lindquist, S. (1992). Hsp104 is required for tolerance to many forms of stress. EMBO J. 11, 2357-2364.
49. Schmitt, A.P., and McEntee, K. (1996). Msn2p, a zinc finger DNA-binding protein, is the transcriptional activator of the multistress response in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 93, 5777-5782.
50. Schüller, C., Brewster, J.L., Alexander, M.R., Gustin, M.C., and Ruis, H. (1994). The HOG pathway controls osmotic regulation of transcription via the stress response element (STRE) of the Saccharomyces cerevisiae CTT1 gene. EMBO J. 13, 4382-4389.
51. Sewell, A.K., Yokoya, F., Yu, W., Miyagawa, T., Muragama, T., and Winge, D.R. (1995). Mutated yeast heat shock transcription factor exhibits elevated basal transcriptional activation and confers metal resistance. J. Biol. Chem. 270, 25079-25086.
52. Sherman, F., Fink, J.R., and Hicks, J.B. (1996). Methods in Yeast Genetics, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
53. Silar, P., Butler, G., and Thiele, D.J. (1991). Heat shock transcription factor activates transcription of the yeast metallothionein gene. Mol. Cell. Biol. 11, 1232-1238.
54. Slater, M.R., and Craig, E.A. (1987). Transcriptional regulation of an hsp70 heat shock gene in the yeast Saccharomyces cerevisiae. Mol. Cell. Biol. 7, 1906-1916.
55. Smith, B.J., and Yaffe, M.P. (1991). A mutation in the yeast heat shock factor gene causes temperature-sensitive defects in both mitochondrial protein import and the cell cycle. Mol. Cell. Biol. 11, 2647-2655.
56. Sorger, P.K. (1990). Yeast heat shock factor contains separable transient and sustained response transcriptional activators. Cell 62, 793-805.
57. Sorger, P.K., and Nelson, H.C. (1989). Trimerization of a yeast transcription activator via a coiled-coil motif. Cell 59, 807-813.
58. Sorger, P.K., and Pelham, H.R. (1987). Purification and characterization of a heat shock element binding protein from yeast. EMBO J. 6, 3035-3041.
59. Sorger, P.K., and Pelham, H.R. (1988). Yeast heat shock factor is an essential binding protein that exhibits temperature dependent phosphorylation. Cell 54, 855-864.
60. Stevens, D.W.S., Rivers, S.L., and Jamieson, D.J. (1995). The role of the YAP1 and YAP2 genes in the regulation of the adaptive oxidative stress responses of Saccharomyces cerevisiae. Mol. Microbiol. 16, 415-423.
61. Stock, A., Ninfa, A.J., and Stock, A.M. (1989). Protein phosphorylation and regulation of adaptive responses in bacteria. Microbiol. Rev. 53, 450-490.
62. Varela, J.C.S., Praekeldt, U., Meacock, P.A., Planta, R.J., and Mager, W.H. (1995). The Saccharomyces cerevisiae HSP12 gene is activated by the high-osmolarity glycerol pathway and negatively regulated by protein kinase A. Mol. Cell. Biol. 15, 6232-6245.
63. White, J.H.M., Barker, D.G., Nurse, P., and Johnston, L.H. (1986). Periodic transcription as a means of regulating gene expression during the cell cycle: contrasting mode of expression of DNA ligase genes in budding and fission yeast. EMBO J. 5, 1705-1709.