Abstract
Deletion of the bacterial two-component response regulator homologue Skn7 results in sensitivity of yeast to oxidizing agents indicating that Skn7 is involved in the response to this type of stress. Here we demonstrate that following oxidative stress, Skn7 regulates the induction of two genes: TRX2, encoding thioredoxin, and a gene encoding thioredoxin reductase. TRX2 is already known to be induced by oxidative stress dependent on the Yap1 protein, an AP1-like transcription factor responsible for the induction of gene expression in response to various stresses. The thioredoxin reductase gene has not previously been shown to be activated by oxidative stress and, significantly, we find that it too is regulated by Yap1. The control of at least TRX2 by Skn7 is a direct mechanism as Skn7 binds to the TRX2 gene promoter in vitro. This shows Skn7 to be a transcription factor, at present the only such eukaryotic two-component signalling protein. Our data further suggest that Skn7 and Yap1 co-operate on the TRX2 promoter, to induce transcription in response to oxidative stress.
Full Text
The Full Text of this article is available as a PDF (414.4 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Bourret R. B., Borkovich K. A., Simon M. I. Signal transduction pathways involving protein phosphorylation in prokaryotes. Annu Rev Biochem. 1991;60:401–441. doi: 10.1146/annurev.bi.60.070191.002153. [DOI] [PubMed] [Google Scholar]
- Brown J. L., Bussey H., Stewart R. C. Yeast Skn7p functions in a eukaryotic two-component regulatory pathway. EMBO J. 1994 Nov 1;13(21):5186–5194. doi: 10.1002/j.1460-2075.1994.tb06849.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brown J. L., North S., Bussey H. SKN7, a yeast multicopy suppressor of a mutation affecting cell wall beta-glucan assembly, encodes a product with domains homologous to prokaryotic two-component regulators and to heat shock transcription factors. J Bacteriol. 1993 Nov;175(21):6908–6915. doi: 10.1128/jb.175.21.6908-6915.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chae H. Z., Chung S. J., Rhee S. G. Thioredoxin-dependent peroxide reductase from yeast. J Biol Chem. 1994 Nov 4;269(44):27670–27678. [PubMed] [Google Scholar]
- Collinson L. P., Dawes I. W. Inducibility of the response of yeast cells to peroxide stress. J Gen Microbiol. 1992 Feb;138(2):329–335. doi: 10.1099/00221287-138-2-329. [DOI] [PubMed] [Google Scholar]
- Flattery-O'Brien J., Collinson L. P., Dawes I. W. Saccharomyces cerevisiae has an inducible response to menadione which differs from that to hydrogen peroxide. J Gen Microbiol. 1993 Mar;139(3):501–507. doi: 10.1099/00221287-139-3-501. [DOI] [PubMed] [Google Scholar]
- Gietz R. D., Sugino A. New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene. 1988 Dec 30;74(2):527–534. doi: 10.1016/0378-1119(88)90185-0. [DOI] [PubMed] [Google Scholar]
- Guarente L. Yeast promoters and lacZ fusions designed to study expression of cloned genes in yeast. Methods Enzymol. 1983;101:181–191. doi: 10.1016/0076-6879(83)01013-7. [DOI] [PubMed] [Google Scholar]
- Herskowitz I. MAP kinase pathways in yeast: for mating and more. Cell. 1995 Jan 27;80(2):187–197. doi: 10.1016/0092-8674(95)90402-6. [DOI] [PubMed] [Google Scholar]
- Igual J. C., Johnson A. L., Johnston L. H. Coordinated regulation of gene expression by the cell cycle transcription factor Swi4 and the protein kinase C MAP kinase pathway for yeast cell integrity. EMBO J. 1996 Sep 16;15(18):5001–5013. [PMC free article] [PubMed] [Google Scholar]
- Jamieson D. J. Saccharomyces cerevisiae has distinct adaptive responses to both hydrogen peroxide and menadione. J Bacteriol. 1992 Oct;174(20):6678–6681. doi: 10.1128/jb.174.20.6678-6681.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Johnston L. H. Cell cycle control of gene expression in yeast. Trends Cell Biol. 1992 Dec;2(12):353–357. doi: 10.1016/0962-8924(92)90041-k. [DOI] [PubMed] [Google Scholar]
- Koch C., Nasmyth K. Cell cycle regulated transcription in yeast. Curr Opin Cell Biol. 1994 Jun;6(3):451–459. doi: 10.1016/0955-0674(94)90039-6. [DOI] [PubMed] [Google Scholar]
- Krems B., Charizanis C., Entian K. D. The response regulator-like protein Pos9/Skn7 of Saccharomyces cerevisiae is involved in oxidative stress resistance. Curr Genet. 1996 Mar;29(4):327–334. doi: 10.1007/BF02208613. [DOI] [PubMed] [Google Scholar]
- Kuge S., Jones N. YAP1 dependent activation of TRX2 is essential for the response of Saccharomyces cerevisiae to oxidative stress by hydroperoxides. EMBO J. 1994 Feb 1;13(3):655–664. doi: 10.1002/j.1460-2075.1994.tb06304.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Maeda T., Takekawa M., Saito H. Activation of yeast PBS2 MAPKK by MAPKKKs or by binding of an SH3-containing osmosensor. Science. 1995 Jul 28;269(5223):554–558. doi: 10.1126/science.7624781. [DOI] [PubMed] [Google Scholar]
- Maeda T., Wurgler-Murphy S. M., Saito H. A two-component system that regulates an osmosensing MAP kinase cascade in yeast. Nature. 1994 May 19;369(6477):242–245. doi: 10.1038/369242a0. [DOI] [PubMed] [Google Scholar]
- Moradas-Ferreira P., Costa V., Piper P., Mager W. The molecular defences against reactive oxygen species in yeast. Mol Microbiol. 1996 Feb;19(4):651–658. doi: 10.1046/j.1365-2958.1996.403940.x. [DOI] [PubMed] [Google Scholar]
- Morgan B. A., Bouquin N., Johnston L. H. Two-component signal-transduction systems in budding yeast MAP a different pathway? Trends Cell Biol. 1995 Dec;5(12):453–457. doi: 10.1016/s0962-8924(00)89114-x. [DOI] [PubMed] [Google Scholar]
- Morgan B. A., Bouquin N., Merrill G. F., Johnston L. H. A yeast transcription factor bypassing the requirement for SBF and DSC1/MBF in budding yeast has homology to bacterial signal transduction proteins. EMBO J. 1995 Nov 15;14(22):5679–5689. doi: 10.1002/j.1460-2075.1995.tb00255.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Morgan B. A., Conlon F. L., Manzanares M., Millar J. B., Kanuga N., Sharpe J., Krumlauf R., Smith J. C., Sedgwick S. G. Transposon tools for recombinant DNA manipulation: characterization of transcriptional regulators from yeast, Xenopus, and mouse. Proc Natl Acad Sci U S A. 1996 Apr 2;93(7):2801–2806. doi: 10.1073/pnas.93.7.2801. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Parkinson J. S. Signal transduction schemes of bacteria. Cell. 1993 Jun 4;73(5):857–871. doi: 10.1016/0092-8674(93)90267-t. [DOI] [PubMed] [Google Scholar]
- Plummer J. L., Smith B. R., Sies H., Bend J. R. Chemical depletion of glutathione in vivo. Methods Enzymol. 1981;77:50–59. doi: 10.1016/s0076-6879(81)77010-1. [DOI] [PubMed] [Google Scholar]
- Rowley A., Johnston G. C., Butler B., Werner-Washburne M., Singer R. A. Heat shock-mediated cell cycle blockage and G1 cyclin expression in the yeast Saccharomyces cerevisiae. Mol Cell Biol. 1993 Feb;13(2):1034–1041. doi: 10.1128/mcb.13.2.1034. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ruis H., Schüller C. Stress signaling in yeast. Bioessays. 1995 Nov;17(11):959–965. doi: 10.1002/bies.950171109. [DOI] [PubMed] [Google Scholar]
- Schiestl R. H., Gietz R. D. High efficiency transformation of intact yeast cells using single stranded nucleic acids as a carrier. Curr Genet. 1989 Dec;16(5-6):339–346. doi: 10.1007/BF00340712. [DOI] [PubMed] [Google Scholar]
- Stephen D. W., Rivers S. L., Jamieson D. J. The role of the YAP1 and YAP2 genes in the regulation of the adaptive oxidative stress responses of Saccharomyces cerevisiae. Mol Microbiol. 1995 May;16(3):415–423. doi: 10.1111/j.1365-2958.1995.tb02407.x. [DOI] [PubMed] [Google Scholar]