Abstract
Transcription of the Saccharomyces cerevisiae CTT1 gene encoding the cytosolic catalase T is activated by a variety of stress conditions: it is derepressed by nitrogen starvation and induced by heat shock. Furthermore, it is activated by osmotic and oxidative stress. This study shows that a CTT1 upstream region previously found to be involved in nitrogen, cAMP and heat control (base pairs -382 to -325) contains a UAS element (STRE, -368 to -356), which is sufficient for the activation of a reporter gene by all types of stress acting on CTT1. Gel retardation experiments demonstrated the existence of a factor specifically binding to STRE, but to a lesser extent to mutated elements having partly or entirely lost the ability to mediate stress control. Heat activation of STRE, but not of a canonical heat shock element, is enhanced by a ras2 defect mutation, which enhances thermotolerance, and is dramatically reduced by a bcy1 disruption mutation, which decreases thermotolerance. It can be hypothesized, therefore, that the novel stress control element is important for the establishment of induced stress tolerance.
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- BEERS R. F., Jr, SIZER I. W. A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem. 1952 Mar;195(1):133–140. [PubMed] [Google Scholar]
- Beggs J. D. Transformation of yeast by a replicating hybrid plasmid. Nature. 1978 Sep 14;275(5676):104–109. doi: 10.1038/275104a0. [DOI] [PubMed] [Google Scholar]
- Belazzi T., Wagner A., Wieser R., Schanz M., Adam G., Hartig A., Ruis H. Negative regulation of transcription of the Saccharomyces cerevisiae catalase T (CTT1) gene by cAMP is mediated by a positive control element. EMBO J. 1991 Mar;10(3):585–592. doi: 10.1002/j.1460-2075.1991.tb07985.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bissinger P. H., Wieser R., Hamilton B., Ruis H. Control of Saccharomyces cerevisiae catalase T gene (CTT1) expression by nutrient supply via the RAS-cyclic AMP pathway. Mol Cell Biol. 1989 Mar;9(3):1309–1315. doi: 10.1128/mcb.9.3.1309. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Boorstein W. R., Craig E. A. Regulation of a yeast HSP70 gene by a cAMP responsive transcriptional control element. EMBO J. 1990 Aug;9(8):2543–2553. doi: 10.1002/j.1460-2075.1990.tb07435.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1006/abio.1976.9999. [DOI] [PubMed] [Google Scholar]
- Cameron S., Levin L., Zoller M., Wigler M. cAMP-independent control of sporulation, glycogen metabolism, and heat shock resistance in S. cerevisiae. Cell. 1988 May 20;53(4):555–566. doi: 10.1016/0092-8674(88)90572-7. [DOI] [PubMed] [Google Scholar]
- Cannon J. F., Tatchell K. Characterization of Saccharomyces cerevisiae genes encoding subunits of cyclic AMP-dependent protein kinase. Mol Cell Biol. 1987 Aug;7(8):2653–2663. doi: 10.1128/mcb.7.8.2653. [DOI] [PMC free article] [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]
- De Virgilio C., Piper P., Boller T., Wiemken A. Acquisition of thermotolerance in Saccharomyces cerevisiae without heat shock protein hsp 104 and in the absence of protein synthesis. FEBS Lett. 1991 Aug 19;288(1-2):86–90. doi: 10.1016/0014-5793(91)81008-v. [DOI] [PubMed] [Google Scholar]
- Gaxiola R., de Larrinoa I. F., Villalba J. M., Serrano R. A novel and conserved salt-induced protein is an important determinant of salt tolerance in yeast. EMBO J. 1992 Sep;11(9):3157–3164. doi: 10.1002/j.1460-2075.1992.tb05392.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hörtner H., Ammerer G., Hartter E., Hamilton B., Rytka J., Bilinski T., Ruis H. Regulation of synthesis of catalases and iso-1-cytochrome c in Saccharomyces cerevisiae by glucose, oxygen and heme. Eur J Biochem. 1982 Nov;128(1):179–184. doi: 10.1111/j.1432-1033.1982.tb06949.x. [DOI] [PubMed] [Google Scholar]
- Iida H. Multistress resistance of Saccharomyces cerevisiae is generated by insertion of retrotransposon Ty into the 5' coding region of the adenylate cyclase gene. Mol Cell Biol. 1988 Dec;8(12):5555–5560. doi: 10.1128/mcb.8.12.5555. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ito H., Fukuda Y., Murata K., Kimura A. Transformation of intact yeast cells treated with alkali cations. J Bacteriol. 1983 Jan;153(1):163–168. doi: 10.1128/jb.153.1.163-168.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kobayashi N., McEntee K. Evidence for a heat shock transcription factor-independent mechanism for heat shock induction of transcription in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1990 Sep;87(17):6550–6554. doi: 10.1073/pnas.87.17.6550. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kobayashi N., McEntee K. Identification of cis and trans components of a novel heat shock stress regulatory pathway in Saccharomyces cerevisiae. Mol Cell Biol. 1993 Jan;13(1):248–256. doi: 10.1128/mcb.13.1.248. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Li G. C., Li L., Liu R. Y., Rehman M., Lee W. M. Heat shock protein hsp70 protects cells from thermal stress even after deletion of its ATP-binding domain. Proc Natl Acad Sci U S A. 1992 Mar 15;89(6):2036–2040. doi: 10.1073/pnas.89.6.2036. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lindquist S., Craig E. A. The heat-shock proteins. Annu Rev Genet. 1988;22:631–677. doi: 10.1146/annurev.ge.22.120188.003215. [DOI] [PubMed] [Google Scholar]
- McClanahan T., McEntee K. DNA damage and heat shock dually regulate genes in Saccharomyces cerevisiae. Mol Cell Biol. 1986 Jan;6(1):90–96. doi: 10.1128/mcb.6.1.90. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ozkaynak E., Finley D., Solomon M. J., Varshavsky A. The yeast ubiquitin genes: a family of natural gene fusions. EMBO J. 1987 May;6(5):1429–1439. doi: 10.1002/j.1460-2075.1987.tb02384.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Praekelt U. M., Meacock P. A. HSP12, a new small heat shock gene of Saccharomyces cerevisiae: analysis of structure, regulation and function. Mol Gen Genet. 1990 Aug;223(1):97–106. doi: 10.1007/BF00315801. [DOI] [PubMed] [Google Scholar]
- Sanchez Y., Lindquist S. L. HSP104 required for induced thermotolerance. Science. 1990 Jun 1;248(4959):1112–1115. doi: 10.1126/science.2188365. [DOI] [PubMed] [Google Scholar]
- Sanchez Y., Taulien J., Borkovich K. A., Lindquist S. Hsp104 is required for tolerance to many forms of stress. EMBO J. 1992 Jun;11(6):2357–2364. doi: 10.1002/j.1460-2075.1992.tb05295.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sarokin L., Carlson M. Short repeated elements in the upstream regulatory region of the SUC2 gene of Saccharomyces cerevisiae. Mol Cell Biol. 1986 Jul;6(7):2324–2333. doi: 10.1128/mcb.6.7.2324. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shin D. Y., Matsumoto K., Iida H., Uno I., Ishikawa T. Heat shock response of Saccharomyces cerevisiae mutants altered in cyclic AMP-dependent protein phosphorylation. Mol Cell Biol. 1987 Jan;7(1):244–250. doi: 10.1128/mcb.7.1.244. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Smith B. J., Yaffe M. P. Uncoupling thermotolerance from the induction of heat shock proteins. Proc Natl Acad Sci U S A. 1991 Dec 15;88(24):11091–11094. doi: 10.1073/pnas.88.24.11091. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sorger P. K., Pelham H. R. Purification and characterization of a heat-shock element binding protein from yeast. EMBO J. 1987 Oct;6(10):3035–3041. doi: 10.1002/j.1460-2075.1987.tb02609.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
- Spevak W., Hartig A., Meindl P., Ruis H. Heme control region of the catalase T gene of the yeast Saccharomyces cerevisiae. Mol Gen Genet. 1986 Apr;203(1):73–78. doi: 10.1007/BF00330386. [DOI] [PubMed] [Google Scholar]
- Susek R. E., Lindquist S. L. hsp26 of Saccharomyces cerevisiae is related to the superfamily of small heat shock proteins but is without a demonstrable function. Mol Cell Biol. 1989 Nov;9(11):5265–5271. doi: 10.1128/mcb.9.11.5265. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tatchell K., Chaleff D. T., DeFeo-Jones D., Scolnick E. M. Requirement of either of a pair of ras-related genes of Saccharomyces cerevisiae for spore viability. Nature. 1984 Jun 7;309(5968):523–527. doi: 10.1038/309523a0. [DOI] [PubMed] [Google Scholar]
- Thevelein J. M. Fermentable sugars and intracellular acidification as specific activators of the RAS-adenylate cyclase signalling pathway in yeast: the relationship to nutrient-induced cell cycle control. Mol Microbiol. 1991 Jun;5(6):1301–1307. doi: 10.1111/j.1365-2958.1991.tb00776.x. [DOI] [PubMed] [Google Scholar]
- Toda T., Cameron S., Sass P., Zoller M., Scott J. D., McMullen B., Hurwitz M., Krebs E. G., Wigler M. Cloning and characterization of BCY1, a locus encoding a regulatory subunit of the cyclic AMP-dependent protein kinase in Saccharomyces cerevisiae. Mol Cell Biol. 1987 Apr;7(4):1371–1377. doi: 10.1128/mcb.7.4.1371. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Varela J. C., van Beekvelt C., Planta R. J., Mager W. H. Osmostress-induced changes in yeast gene expression. Mol Microbiol. 1992 Aug;6(15):2183–2190. doi: 10.1111/j.1365-2958.1992.tb01392.x. [DOI] [PubMed] [Google Scholar]
- Watson K. Microbial stress proteins. Adv Microb Physiol. 1990;31:183–223. doi: 10.1016/s0065-2911(08)60122-8. [DOI] [PubMed] [Google Scholar]
- Wieser R., Adam G., Wagner A., Schüller C., Marchler G., Ruis H., Krawiec Z., Bilinski T. Heat shock factor-independent heat control of transcription of the CTT1 gene encoding the cytosolic catalase T of Saccharomyces cerevisiae. J Biol Chem. 1991 Jul 5;266(19):12406–12411. [PubMed] [Google Scholar]
- Winkler H., Adam G., Mattes E., Schanz M., Hartig A., Ruis H. Co-ordinate control of synthesis of mitochondrial and non-mitochondrial hemoproteins: a binding site for the HAP1 (CYP1) protein in the UAS region of the yeast catalase T gene (CTT1). EMBO J. 1988 Jun;7(6):1799–1804. doi: 10.1002/j.1460-2075.1988.tb03011.x. [DOI] [PMC free article] [PubMed] [Google Scholar]