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. 1991 Oct 1;88(19):8558–8562. doi: 10.1073/pnas.88.19.8558

ACE1, a copper-dependent transcription factor, activates expression of the yeast copper, zinc superoxide dismutase gene.

E B Gralla 1, D J Thiele 1, P Silar 1, J S Valentine 1
PMCID: PMC52548  PMID: 1924315

Abstract

Copper, zinc superoxide dismutase (SOD1 gene product) (superoxide:superoxide oxidoreductase, EC 1.15.1.1) is a copper-containing enzyme that functions to prevent oxygen toxicity. In the yeast Saccharomyces cerevisiae, copper levels exert some control over the level of SOD1 expression. We show that the ACE1 transcriptional activator protein, which is responsible for the induction of yeast metallothionein (CUP1) in response to copper, also controls the SOD1 response to copper. A single binding site for ACE1 is present in the SOD1 promoter region, as demonstrated by DNase I protection and methylation interference experiments, and is highly homologous to a high-affinity ACE1 binding site in the CUP1 promoter. The functional importance of this DNA-protein interaction is demonstrated by the facts that (i) copper induction of SOD1 mRNA does not occur in a strain lacking ACE1 and (ii) it does not occur in a strain containing a genetically engineered SOD1 promoter that lacks a functional ACE1 binding site.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Baldari C., Cesareni G. Plasmids pEMBLY: new single-stranded shuttle vectors for the recovery and analysis of yeast DNA sequences. Gene. 1985;35(1-2):27–32. doi: 10.1016/0378-1119(85)90154-4. [DOI] [PubMed] [Google Scholar]
  2. Bannister J. V., Bannister W. H., Rotilio G. Aspects of the structure, function, and applications of superoxide dismutase. CRC Crit Rev Biochem. 1987;22(2):111–180. doi: 10.3109/10409238709083738. [DOI] [PubMed] [Google Scholar]
  3. Bermingham-McDonogh O., Gralla E. B., Valentine J. S. The copper, zinc-superoxide dismutase gene of Saccharomyces cerevisiae: cloning, sequencing, and biological activity. Proc Natl Acad Sci U S A. 1988 Jul;85(13):4789–4793. doi: 10.1073/pnas.85.13.4789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Biliński T., Krawiec Z., Liczmański A., Litwińska J. Is hydroxyl radical generated by the Fenton reaction in vivo? Biochem Biophys Res Commun. 1985 Jul 31;130(2):533–539. doi: 10.1016/0006-291x(85)90449-8. [DOI] [PubMed] [Google Scholar]
  5. Buchman C., Skroch P., Dixon W., Tullius T. D., Karin M. A single amino acid change in CUP2 alters its mode of DNA binding. Mol Cell Biol. 1990 Sep;10(9):4778–4787. doi: 10.1128/mcb.10.9.4778. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Butler G., Thiele D. J. ACE2, an activator of yeast metallothionein expression which is homologous to SWI5. Mol Cell Biol. 1991 Jan;11(1):476–485. doi: 10.1128/mcb.11.1.476. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Butt T. R., Ecker D. J. Yeast metallothionein and applications in biotechnology. Microbiol Rev. 1987 Sep;51(3):351–364. doi: 10.1128/mr.51.3.351-364.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Carlioz A., Touati D. Isolation of superoxide dismutase mutants in Escherichia coli: is superoxide dismutase necessary for aerobic life? EMBO J. 1986 Mar;5(3):623–630. doi: 10.1002/j.1460-2075.1986.tb04256.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Carri M. T., Galiazzo F., Ciriolo M. R., Rotilio G. Evidence for co-regulation of Cu,Zn superoxide dismutase and metallothionein gene expression in yeast through transcriptional control by copper via the ACE 1 factor. FEBS Lett. 1991 Jan 28;278(2):263–266. doi: 10.1016/0014-5793(91)80131-l. [DOI] [PubMed] [Google Scholar]
  10. Chang E. C., Kosman D. J. Intracellular Mn (II)-associated superoxide scavenging activity protects Cu,Zn superoxide dismutase-deficient Saccharomyces cerevisiae against dioxygen stress. J Biol Chem. 1989 Jul 25;264(21):12172–12178. [PubMed] [Google Scholar]
  11. Evans C. F., Engelke D. R., Thiele D. J. ACE1 transcription factor produced in Escherichia coli binds multiple regions within yeast metallothionein upstream activation sequences. Mol Cell Biol. 1990 Jan;10(1):426–429. doi: 10.1128/mcb.10.1.426. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fridovich I. Superoxide dismutases. Adv Enzymol Relat Areas Mol Biol. 1986;58:61–97. doi: 10.1002/9780470123041.ch2. [DOI] [PubMed] [Google Scholar]
  13. Fürst P., Hu S., Hackett R., Hamer D. Copper activates metallothionein gene transcription by altering the conformation of a specific DNA binding protein. Cell. 1988 Nov 18;55(4):705–717. doi: 10.1016/0092-8674(88)90229-2. [DOI] [PubMed] [Google Scholar]
  14. Galiazzo F., Schiesser A., Rotilio G. Oxygen-independent induction of enzyme activities related to oxygen metabolism in yeast by copper. Biochim Biophys Acta. 1988 Apr 14;965(1):46–51. doi: 10.1016/0304-4165(88)90149-3. [DOI] [PubMed] [Google Scholar]
  15. Greco M. A., Hrab D. I., Magner W., Kosman D. J. Cu,Zn superoxide dismutase and copper deprivation and toxicity in Saccharomyces cerevisiae. J Bacteriol. 1990 Jan;172(1):317–325. doi: 10.1128/jb.172.1.317-325.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gregory E. M., Goscin S. A., Fridovich I. Superoxide dismutase and oxygen toxicity in a eukaryote. J Bacteriol. 1974 Feb;117(2):456–460. doi: 10.1128/jb.117.2.456-460.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Huibregtse J. M., Engelke D. R., Thiele D. J. Copper-induced binding of cellular factors to yeast metallothionein upstream activation sequences. Proc Natl Acad Sci U S A. 1989 Jan;86(1):65–69. doi: 10.1073/pnas.86.1.65. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Köhrer K., Domdey H. Preparation of high molecular weight RNA. Methods Enzymol. 1991;194:398–405. doi: 10.1016/0076-6879(91)94030-g. [DOI] [PubMed] [Google Scholar]
  19. Lee F. J., Hassan H. M. Biosynthesis of superoxide dismutase in Saccharomyces cerevisiae: effects of paraquat and copper. J Free Radic Biol Med. 1985;1(4):319–325. doi: 10.1016/0748-5514(85)90138-2. [DOI] [PubMed] [Google Scholar]
  20. Moody C. S., Hassan H. M. Anaerobic biosynthesis of the manganese-containing superoxide dismutase in Escherichia coli. J Biol Chem. 1984 Oct 25;259(20):12821–12825. [PubMed] [Google Scholar]
  21. Myers A. M., Tzagoloff A., Kinney D. M., Lusty C. J. Yeast shuttle and integrative vectors with multiple cloning sites suitable for construction of lacZ fusions. Gene. 1986;45(3):299–310. doi: 10.1016/0378-1119(86)90028-4. [DOI] [PubMed] [Google Scholar]
  22. Niederhoffer E. C., Naranjo C. M., Bradley K. L., Fee J. A. Control of Escherichia coli superoxide dismutase (sodA and sodB) genes by the ferric uptake regulation (fur) locus. J Bacteriol. 1990 Apr;172(4):1930–1938. doi: 10.1128/jb.172.4.1930-1938.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Scott M. D., Meshnick S. R., Eaton J. W. Superoxide dismutase-rich bacteria. Paradoxical increase in oxidant toxicity. J Biol Chem. 1987 Mar 15;262(8):3640–3645. [PubMed] [Google Scholar]
  24. Silar P., Butler G., Thiele D. J. Heat shock transcription factor activates transcription of the yeast metallothionein gene. Mol Cell Biol. 1991 Mar;11(3):1232–1238. doi: 10.1128/mcb.11.3.1232. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Studier F. W., Rosenberg A. H., Dunn J. J., Dubendorff J. W. Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol. 1990;185:60–89. doi: 10.1016/0076-6879(90)85008-c. [DOI] [PubMed] [Google Scholar]
  26. Su T. Z., el-Gewely M. R. A multisite-directed mutagenesis using T7 DNA polymerase: application for reconstructing a mammalian gene. Gene. 1988 Sep 15;69(1):81–89. doi: 10.1016/0378-1119(88)90380-0. [DOI] [PubMed] [Google Scholar]
  27. Szczypka M. S., Thiele D. J. A cysteine-rich nuclear protein activates yeast metallothionein gene transcription. Mol Cell Biol. 1989 Feb;9(2):421–429. doi: 10.1128/mcb.9.2.421. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Thiele D. J. ACE1 regulates expression of the Saccharomyces cerevisiae metallothionein gene. Mol Cell Biol. 1988 Jul;8(7):2745–2752. doi: 10.1128/mcb.8.7.2745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Thiele D. J., Hamer D. H. Tandemly duplicated upstream control sequences mediate copper-induced transcription of the Saccharomyces cerevisiae copper-metallothionein gene. Mol Cell Biol. 1986 Apr;6(4):1158–1163. doi: 10.1128/mcb.6.4.1158. [DOI] [PMC free article] [PubMed] [Google Scholar]

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