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. 1996 May 1;15(9):2227–2235.

The Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress response element (STRE).

M T Martínez-Pastor 1, G Marchler 1, C Schüller 1, A Marchler-Bauer 1, H Ruis 1, F Estruch 1
PMCID: PMC450147  PMID: 8641288

Abstract

The MSN2 and MSN4 genes encode homologous and functionally redundant Cys2His2 zinc finger proteins. A disruption of both MSN2 and MSN4 genes results in a higher sensitivity to different stresses, including carbon source starvation, heat shock and severe osmotic and oxidative stresses. We show that MSN2 and MSN4 are required for activation of several yeast genes such as CTT1, DDR2 and HSP12, whose induction is mediated through stress-response elements (STREs). Msn2p and Msn4p are important factors for the stress-induced activation of STRE dependent promoters and bind specifically to STRE-containing oligonucleotides. Our results suggest that MSN2 and MSN4 encode a DNA-binding component of the stress responsive system and it is likely that they act as positive transcription factors.

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Selected References

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  1. Ammerer G. Sex, stress and integrity: the importance of MAP kinases in yeast. Curr Opin Genet Dev. 1994 Feb;4(1):90–95. doi: 10.1016/0959-437x(94)90096-5. [DOI] [PubMed] [Google Scholar]
  2. Bienz M., Pelham H. R. Mechanisms of heat-shock gene activation in higher eukaryotes. Adv Genet. 1987;24:31–72. doi: 10.1016/s0065-2660(08)60006-1. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. Brewster J. L., de Valoir T., Dwyer N. D., Winter E., Gustin M. C. An osmosensing signal transduction pathway in yeast. Science. 1993 Mar 19;259(5102):1760–1763. doi: 10.1126/science.7681220. [DOI] [PubMed] [Google Scholar]
  5. Choo Y., Klug A. Selection of DNA binding sites for zinc fingers using rationally randomized DNA reveals coded interactions. Proc Natl Acad Sci U S A. 1994 Nov 8;91(23):11168–11172. doi: 10.1073/pnas.91.23.11168. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Choo Y., Sánchez-García I., Klug A. In vivo repression by a site-specific DNA-binding protein designed against an oncogenic sequence. Nature. 1994 Dec 15;372(6507):642–645. doi: 10.1038/372642a0. [DOI] [PubMed] [Google Scholar]
  7. Estruch F., Carlson M. Increased dosage of the MSN1 gene restores invertase expression in yeast mutants defective in the SNF1 protein kinase. Nucleic Acids Res. 1990 Dec 11;18(23):6959–6964. doi: 10.1093/nar/18.23.6959. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Estruch F., Carlson M. Two homologous zinc finger genes identified by multicopy suppression in a SNF1 protein kinase mutant of Saccharomyces cerevisiae. Mol Cell Biol. 1993 Jul;13(7):3872–3881. doi: 10.1128/mcb.13.7.3872. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gallwitz D., Sures I. Structure of a split yeast gene: complete nucleotide sequence of the actin gene in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1980 May;77(5):2546–2550. doi: 10.1073/pnas.77.5.2546. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Han J., Lee J. D., Bibbs L., Ulevitch R. J. A MAP kinase targeted by endotoxin and hyperosmolarity in mammalian cells. Science. 1994 Aug 5;265(5173):808–811. doi: 10.1126/science.7914033. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. Kamada Y., Jung U. S., Piotrowski J., Levin D. E. The protein kinase C-activated MAP kinase pathway of Saccharomyces cerevisiae mediates a novel aspect of the heat shock response. Genes Dev. 1995 Jul 1;9(13):1559–1571. doi: 10.1101/gad.9.13.1559. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. 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]
  15. 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]
  16. Kyriakis J. M., Banerjee P., Nikolakaki E., Dai T., Rubie E. A., Ahmad M. F., Avruch J., Woodgett J. R. The stress-activated protein kinase subfamily of c-Jun kinases. Nature. 1994 May 12;369(6476):156–160. doi: 10.1038/369156a0. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Mager W. H., De Kruijff A. J. Stress-induced transcriptional activation. Microbiol Rev. 1995 Sep;59(3):506–531. doi: 10.1128/mr.59.3.506-531.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Mager W. H., Ferreira P. M. Stress response of yeast. Biochem J. 1993 Feb 15;290(Pt 1):1–13. doi: 10.1042/bj2900001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Marchler G., Schüller C., Adam G., Ruis H. A Saccharomyces cerevisiae UAS element controlled by protein kinase A activates transcription in response to a variety of stress conditions. EMBO J. 1993 May;12(5):1997–2003. doi: 10.1002/j.1460-2075.1993.tb05849.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. Morimoto R. I., Sarge K. D., Abravaya K. Transcriptional regulation of heat shock genes. A paradigm for inducible genomic responses. J Biol Chem. 1992 Nov 5;267(31):21987–21990. [PubMed] [Google Scholar]
  23. Pavletich N. P., Pabo C. O. Zinc finger-DNA recognition: crystal structure of a Zif268-DNA complex at 2.1 A. Science. 1991 May 10;252(5007):809–817. doi: 10.1126/science.2028256. [DOI] [PubMed] [Google Scholar]
  24. Piper P. W. Molecular events associated with acquisition of heat tolerance by the yeast Saccharomyces cerevisiae. FEMS Microbiol Rev. 1993 Aug;11(4):339–355. doi: 10.1111/j.1574-6976.1993.tb00005.x. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. Rose M., Botstein D. Construction and use of gene fusions to lacZ (beta-galactosidase) that are expressed in yeast. Methods Enzymol. 1983;101:167–180. doi: 10.1016/0076-6879(83)01012-5. [DOI] [PubMed] [Google Scholar]
  27. Rothstein R. J. One-step gene disruption in yeast. Methods Enzymol. 1983;101:202–211. doi: 10.1016/0076-6879(83)01015-0. [DOI] [PubMed] [Google Scholar]
  28. Rouse J., Cohen P., Trigon S., Morange M., Alonso-Llamazares A., Zamanillo D., Hunt T., Nebreda A. R. A novel kinase cascade triggered by stress and heat shock that stimulates MAPKAP kinase-2 and phosphorylation of the small heat shock proteins. Cell. 1994 Sep 23;78(6):1027–1037. doi: 10.1016/0092-8674(94)90277-1. [DOI] [PubMed] [Google Scholar]
  29. Ruis H., Schüller C. Stress signaling in yeast. Bioessays. 1995 Nov;17(11):959–965. doi: 10.1002/bies.950171109. [DOI] [PubMed] [Google Scholar]
  30. Schena M., Picard D., Yamamoto K. R. Vectors for constitutive and inducible gene expression in yeast. Methods Enzymol. 1991;194:389–398. doi: 10.1016/0076-6879(91)94029-c. [DOI] [PubMed] [Google Scholar]
  31. Schüller C., Brewster J. L., Alexander M. R., Gustin M. C., Ruis H. The HOG pathway controls osmotic regulation of transcription via the stress response element (STRE) of the Saccharomyces cerevisiae CTT1 gene. EMBO J. 1994 Sep 15;13(18):4382–4389. doi: 10.1002/j.1460-2075.1994.tb06758.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Smith D. B., Johnson K. S. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene. 1988 Jul 15;67(1):31–40. doi: 10.1016/0378-1119(88)90005-4. [DOI] [PubMed] [Google Scholar]
  33. Spevak W., Fessl F., Rytka J., Traczyk A., Skoneczny M., Ruis H. Isolation of the catalase T structural gene of Saccharomyces cerevisiae by functional complementation. Mol Cell Biol. 1983 Sep;3(9):1545–1551. doi: 10.1128/mcb.3.9.1545. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Susek R. E., Lindquist S. Transcriptional derepression of the Saccharomyces cerevisiae HSP26 gene during heat shock. Mol Cell Biol. 1990 Dec;10(12):6362–6373. doi: 10.1128/mcb.10.12.6362. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Tamai K. T., Liu X., Silar P., Sosinowski T., Thiele D. J. Heat shock transcription factor activates yeast metallothionein gene expression in response to heat and glucose starvation via distinct signalling pathways. Mol Cell Biol. 1994 Dec;14(12):8155–8165. doi: 10.1128/mcb.14.12.8155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Thiele D. J. Metal-regulated transcription in eukaryotes. Nucleic Acids Res. 1992 Mar 25;20(6):1183–1191. doi: 10.1093/nar/20.6.1183. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Thomas B. J., Rothstein R. Elevated recombination rates in transcriptionally active DNA. Cell. 1989 Feb 24;56(4):619–630. doi: 10.1016/0092-8674(89)90584-9. [DOI] [PubMed] [Google Scholar]
  38. Varela J. C., Praekelt U. M., Meacock P. A., Planta R. J., Mager W. H. The Saccharomyces cerevisiae HSP12 gene is activated by the high-osmolarity glycerol pathway and negatively regulated by protein kinase A. Mol Cell Biol. 1995 Nov;15(11):6232–6245. doi: 10.1128/mcb.15.11.6232. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Werner-Washburne M., Stone D. E., Craig E. A. Complex interactions among members of an essential subfamily of hsp70 genes in Saccharomyces cerevisiae. Mol Cell Biol. 1987 Jul;7(7):2568–2577. doi: 10.1128/mcb.7.7.2568. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. 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]
  41. Wu A. L., Moye-Rowley W. S. GSH1, which encodes gamma-glutamylcysteine synthetase, is a target gene for yAP-1 transcriptional regulation. Mol Cell Biol. 1994 Sep;14(9):5832–5839. doi: 10.1128/mcb.14.9.5832. [DOI] [PMC free article] [PubMed] [Google Scholar]

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