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Microbiol Rev. 1992 March; 56(1): 1–11.
PMCID: PMC372851

Regulation of gene expression by oxygen in Saccharomyces cerevisiae.


The oxygen regulation of two broad categories of yeast genes is discussed in this review. The first is made up of genes regulated by heme, and the second is made up of genes whose regulation is heme independent. Heme-regulated genes fall into two classes: heme-activated and heme-repressed genes. Activation is achieved through one of two transcriptional activators, the heme-dependent HAP1 protein or the heme-activated, glucose-repressed HAP2/3/4 complex. Some of the properties and the DNA-binding sites of these activators are discussed. Heme repression is achieved through the action of the ROX1 repressor, the expression of which is transcriptionally activated by heme. Once ROX1 is synthesized, its function is heme independent. Evidence that ROX1 binds to DNA or is part of a DNA-binding complex is described. Factors which modulate the function of these regulatory proteins are discussed, and a schematic of heme activation and repression is presented. The mitochondrial subunits of cytochrome c oxidase are induced by oxygen in a heme-independent fashion. The translation of one, cytochrome c oxidase subunit III, is dependent upon three nucleus-encoded initiation factors. One of these, PET494, is itself translationally regulated by oxygen in a heme-independent fashion. The expression of at least four other mitochondrially encoded cytochrome subunits is dependent upon specific translation factors, raising the potential for translational regulation as a general mechanism. Finally, a number of anaerobic genes that show heme-independent, oxygen-repressed expression have been identified. These fall into two kinetic classes, suggesting that there are at least two different regulatory circuitries.

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  • ANDREASEN AA, STIER TJB. Anaerobic nutrition of Saccharomyces cerevisiae. I. Ergosterol requirement for growth in a defined medium. J Cell Physiol. 1953 Feb;41(1):23–36. [PubMed]
  • ANDREASEN AA, STIER TJ. Anaerobic nutrition of Saccharomyces cerevisiae. II. Unsaturated fatty acid requirement for growth in a defined medium. J Cell Physiol. 1954 Jun;43(3):271–281. [PubMed]
  • Arcangioli B, Lescure B. Identification of proteins involved in the regulation of yeast iso- 1-cytochrome C expression by oxygen. EMBO J. 1985 Oct;4(10):2627–2633. [PubMed]
  • Attardi G, Schatz G. Biogenesis of mitochondria. Annu Rev Cell Biol. 1988;4:289–333. [PubMed]
  • 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. [PubMed]
  • Bissinger PH, 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. [PMC free article] [PubMed]
  • Buchman AR, Kornberg RD. A yeast ARS-binding protein activates transcription synergistically in combination with other weak activating factors. Mol Cell Biol. 1990 Mar;10(3):887–897. [PMC free article] [PubMed]
  • Camadro JM, Chambon H, Jolles J, Labbe P. Purification and properties of coproporphyrinogen oxidase from the yeast Saccharomyces cerevisiae. Eur J Biochem. 1986 May 2;156(3):579–587. [PubMed]
  • Carlson M, Osmond BC, Neigeborn L, Botstein D. A suppressor of SNF1 mutations causes constitutive high-level invertase synthesis in yeast. Genetics. 1984 May;107(1):19–32. [PubMed]
  • Celenza JL, Carlson M. A yeast gene that is essential for release from glucose repression encodes a protein kinase. Science. 1986 Sep 12;233(4769):1175–1180. [PubMed]
  • Cerdan ME, Zitomer RS. Oxygen-dependent upstream activation sites of Saccharomyces cerevisiae cytochrome c genes are related forms of the same sequence. Mol Cell Biol. 1988 Jun;8(6):2275–2279. [PMC free article] [PubMed]
  • Chodosh LA, Olesen J, Hahn S, Baldwin AS, Guarente L, Sharp PA. A yeast and a human CCAAT-binding protein have heterologous subunits that are functionally interchangeable. Cell. 1988 Apr 8;53(1):25–35. [PubMed]
  • Clavilier L, Péré G, Slonimski PP. Mise en évidence de plusieurs loci indépendants impliqués dans la synthèse de l'iso-2-cytochrome c chez la levure. Mol Gen Genet. 1969;104(2):195–218. [PubMed]
  • Costanzo MC, Fox TD. Product of Saccharomyces cerevisiae nuclear gene PET494 activates translation of a specific mitochondrial mRNA. Mol Cell Biol. 1986 Nov;6(11):3694–3703. [PMC free article] [PubMed]
  • Costanzo MC, Fox TD. Specific translational activation by nuclear gene products occurs in the 5' untranslated leader of a yeast mitochondrial mRNA. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2677–2681. [PubMed]
  • Creusot F, Verdière J, Gaisne M, Slonimski PP. CYP1 (HAP1) regulator of oxygen-dependent gene expression in yeast. I. Overall organization of the protein sequence displays several novel structural domains. J Mol Biol. 1988 Nov 20;204(2):263–276. [PubMed]
  • Cumsky MG, Ko C, Trueblood CE, Poyton RO. Two nonidentical forms of subunit V are functional in yeast cytochrome c oxidase. Proc Natl Acad Sci U S A. 1985 Apr;82(8):2235–2239. [PubMed]
  • Cumsky MG, Trueblood CE, Ko C, Poyton RO. Structural analysis of two genes encoding divergent forms of yeast cytochrome c oxidase subunit V. Mol Cell Biol. 1987 Oct;7(10):3511–3519. [PMC free article] [PubMed]
  • Decoster E, Simon M, Hatat D, Faye G. The MSS51 gene product is required for the translation of the COX1 mRNA in yeast mitochondria. Mol Gen Genet. 1990 Oct;224(1):111–118. [PubMed]
  • Dieckmann CL, Tzagoloff A. Assembly of the mitochondrial membrane system. CBP6, a yeast nuclear gene necessary for synthesis of cytochrome b. J Biol Chem. 1985 Feb 10;260(3):1513–1520. [PubMed]
  • Dorsman JC, Doorenbosch MM, Maurer CT, de Winde JH, Mager WH, Planta RJ, Grivell LA. An ARS/silencer binding factor also activates two ribosomal protein genes in yeast. Nucleic Acids Res. 1989 Jul 11;17(13):4917–4923. [PMC free article] [PubMed]
  • Dorsman JC, Grivell LA. Expression of the gene encoding subunit II of yeast QH2: cytochrome c oxidoreductase is regulated by multiple factors. Curr Genet. 1990 Jun;17(6):459–464. [PubMed]
  • Dorsman JC, van Heeswijk WC, Grivell LA. Identification of two factors which bind to the upstream sequences of a number of nuclear genes coding for mitochondrial proteins and to genetic elements important for cell division in yeast. Nucleic Acids Res. 1988 Aug 11;16(15):7287–7301. [PMC free article] [PubMed]
  • Dorsman JC, van Heeswijk WC, Grivell LA. Yeast general transcription factor GFI: sequence requirements for binding to DNA and evolutionary conservation. Nucleic Acids Res. 1990 May 11;18(9):2769–2776. [PMC free article] [PubMed]
  • Forsbach V, Pillar T, Gottenöf T, Rödel G. Chromosomal localization and expression of CBS1, a translational activator of cytochrome b in yeast. Mol Gen Genet. 1989 Jul;218(1):57–63. [PubMed]
  • Forsburg SL, Guarente L. Mutational analysis of upstream activation sequence 2 of the CYC1 gene of Saccharomyces cerevisiae: a HAP2-HAP3-responsive site. Mol Cell Biol. 1988 Feb;8(2):647–654. [PMC free article] [PubMed]
  • Forsburg SL, Guarente L. Identification and characterization of HAP4: a third component of the CCAAT-bound HAP2/HAP3 heteromer. Genes Dev. 1989 Aug;3(8):1166–1178. [PubMed]
  • Fujita A, Matsumoto S, Kuhara S, Misumi Y, Kobayashi H. Cloning of the yeast SFL2 gene: its disruption results in pleiotropic phenotypes characteristic for tup1 mutants. Gene. 1990 Apr 30;89(1):93–99. [PubMed]
  • Gollub EG, Liu KP, Dayan J, Adlersberg M, Sprinson DB. Yeast mutants deficient in heme biosynthesis and a heme mutant additionally blocked in cyclization of 2,3-oxidosqualene. J Biol Chem. 1977 May 10;252(9):2846–2854. [PubMed]
  • Grivell LA. Nucleo-mitochondrial interactions in yeast mitochondrial biogenesis. Eur J Biochem. 1989 Jul 1;182(3):477–493. [PubMed]
  • Forsburg SL, Guarente L. Communication between mitochondria and the nucleus in regulation of cytochrome genes in the yeast Saccharomyces cerevisiae. Annu Rev Cell Biol. 1989;5:153–180. [PubMed]
  • Guarente L, Lalonde B, Gifford P, Alani E. Distinctly regulated tandem upstream activation sites mediate catabolite repression of the CYC1 gene of S. cerevisiae. Cell. 1984 Feb;36(2):503–511. [PubMed]
  • Guarente L, Mason T. Heme regulates transcription of the CYC1 gene of S. cerevisiae via an upstream activation site. Cell. 1983 Apr;32(4):1279–1286. [PubMed]
  • Gubbay J, Collignon J, Koopman P, Capel B, Economou A, Münsterberg A, Vivian N, Goodfellow P, Lovell-Badge R. A gene mapping to the sex-determining region of the mouse Y chromosome is a member of a novel family of embryonically expressed genes. Nature. 1990 Jul 19;346(6281):245–250. [PubMed]
  • Guiard B. Structure, expression and regulation of a nuclear gene encoding a mitochondrial protein: the yeast L(+)-lactate cytochrome c oxidoreductase (cytochrome b2). EMBO J. 1985 Dec 1;4(12):3265–3272. [PubMed]
  • Hahn S, Guarente L. Yeast HAP2 and HAP3: transcriptional activators in a heteromeric complex. Science. 1988 Apr 15;240(4850):317–321. [PubMed]
  • Hahn S, Pinkham J, Wei R, Miller R, Guarente L. The HAP3 regulatory locus of Saccharomyces cerevisiae encodes divergent overlapping transcripts. Mol Cell Biol. 1988 Feb;8(2):655–663. [PMC free article] [PubMed]
  • Hodge MR, Kim G, Singh K, Cumsky MG. Inverse regulation of the yeast COX5 genes by oxygen and heme. Mol Cell Biol. 1989 May;9(5):1958–1964. [PMC free article] [PubMed]
  • Hodge MR, Singh K, Cumsky MG. Upstream activation and repression elements control transcription of the yeast COX5b gene. Mol Cell Biol. 1990 Oct;10(10):5510–5520. [PMC free article] [PubMed]
  • 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. [PubMed]
  • Jantzen HM, Admon A, Bell SP, Tjian R. Nucleolar transcription factor hUBF contains a DNA-binding motif with homology to HMG proteins. Nature. 1990 Apr 26;344(6269):830–836. [PubMed]
  • Kelly M, Burke J, Smith M, Klar A, Beach D. Four mating-type genes control sexual differentiation in the fission yeast. EMBO J. 1988 May;7(5):1537–1547. [PubMed]
  • Keng T, Guarente L. Constitutive expression of the yeast HEM1 gene is actually a composite of activation and repression. Proc Natl Acad Sci U S A. 1987 Dec;84(24):9113–9117. [PubMed]
  • Kloeckener-Gruissem B, McEwen JE, Poyton RO. Nuclear functions required for cytochrome c oxidase biogenesis in Saccharomyces cerevisiae: multiple trans-acting nuclear genes exert specific effects on expression of each of the cytochrome c oxidase subunits encoded on mitochondrial DNA. Curr Genet. 1987;12(5):311–322. [PubMed]
  • Kolodrubetz D, Burgum A. Duplicated NHP6 genes of Saccharomyces cerevisiae encode proteins homologous to bovine high mobility group protein 1. J Biol Chem. 1990 Feb 25;265(6):3234–3239. [PubMed]
  • Kolarov J, Kolarova N, Nelson N. A third ADP/ATP translocator gene in yeast. J Biol Chem. 1990 Jul 25;265(21):12711–12716. [PubMed]
  • Lalonde B, Arcangioli B, Guarente L. A single Saccharomyces cerevisiae upstream activation site (UAS1) has two distinct regions essential for its activity. Mol Cell Biol. 1986 Dec;6(12):4690–4696. [PMC free article] [PubMed]
  • Larkin JC, Thompson JR, Woolford JL., Jr Structure and expression of the Saccharomyces cerevisiae CRY1 gene: a highly conserved ribosomal protein gene. Mol Cell Biol. 1987 May;7(5):1764–1775. [PMC free article] [PubMed]
  • Laz TM, Pietras DF, Sherman F. Differential regulation of the duplicated isocytochrome c genes in yeast. Proc Natl Acad Sci U S A. 1984 Jul;81(14):4475–4479. [PubMed]
  • Lodi T, Guiard B. Complex transcriptional regulation of the Saccharomyces cerevisiae CYB2 gene encoding cytochrome b2: CYP1(HAP1) activator binds to the CYB2 upstream activation site UAS1-B2. Mol Cell Biol. 1991 Jul;11(7):3762–3772. [PMC free article] [PubMed]
  • Lowry CV, Cerdán ME, Zitomer RS. A hypoxic consensus operator and a constitutive activation region regulate the ANB1 gene of Saccharomyces cerevisiae. Mol Cell Biol. 1990 Nov;10(11):5921–5926. [PMC free article] [PubMed]
  • Lowry CV, Lieber RH. Negative regulation of the Saccharomyces cerevisiae ANB1 gene by heme, as mediated by the ROX1 gene product. Mol Cell Biol. 1986 Dec;6(12):4145–4148. [PMC free article] [PubMed]
  • Lowry CV, Weiss JL, Walthall DA, Zitomer RS. Modulator sequences mediate oxygen regulation of CYC1 and a neighboring gene in yeast. Proc Natl Acad Sci U S A. 1983 Jan;80(1):151–155. [PubMed]
  • Lowry CV, Zitomer RS. Oxygen regulation of anaerobic and aerobic genes mediated by a common factor in yeast. Proc Natl Acad Sci U S A. 1984 Oct;81(19):6129–6133. [PubMed]
  • Lowry CV, Zitomer RS. ROX1 encodes a heme-induced repression factor regulating ANB1 and CYC7 of Saccharomyces cerevisiae. Mol Cell Biol. 1988 Nov;8(11):4651–4658. [PMC free article] [PubMed]
  • Lue NF, Buchman AR, Kornberg RD. Activation of yeast RNA polymerase II transcription by a thymidine-rich upstream element in vitro. Proc Natl Acad Sci U S A. 1989 Jan;86(2):486–490. [PubMed]
  • Marykwas DL, Fox TD. Control of the Saccharomyces cerevisiae regulatory gene PET494: transcriptional repression by glucose and translational induction by oxygen. Mol Cell Biol. 1989 Feb;9(2):484–491. [PMC free article] [PubMed]
  • Mehta KD, Leung D, Lefebvre L, Smith M. The ANB1 locus of Saccharomyces cerevisiae encodes the protein synthesis initiation factor eIF-4D. J Biol Chem. 1990 May 25;265(15):8802–8807. [PubMed]
  • Miyake S, Sugimura T. Coproporphyrinogenase in a respiration-deficient mutant of yeast lacking all cytochromes and accumulating coproporphyrin. J Bacteriol. 1968 Dec;96(6):1997–2003. [PMC free article] [PubMed]
  • Myers AM, Crivellone MD, Koerner TJ, Tzagoloff A. Characterization of the yeast HEM2 gene and transcriptional regulation of COX5 and COR1 by heme. J Biol Chem. 1987 Dec 15;262(35):16822–16829. [PubMed]
  • Olesen J, Hahn S, Guarente L. Yeast HAP2 and HAP3 activators both bind to the CYC1 upstream activation site, UAS2, in an interdependent manner. Cell. 1987 Dec 24;51(6):953–961. [PubMed]
  • Padmanaban G, Venkateswar V, Rangarajan PN. Haem as a multifunctional regulator. Trends Biochem Sci. 1989 Dec;14(12):492–496. [PubMed]
  • Pfeifer K, Arcangioli B, Guarente L. Yeast HAP1 activator competes with the factor RC2 for binding to the upstream activation site UAS1 of the CYC1 gene. Cell. 1987 Apr 10;49(1):9–18. [PubMed]
  • Pfeifer K, Kim KS, Kogan S, Guarente L. Functional dissection and sequence of yeast HAP1 activator. Cell. 1989 Jan 27;56(2):291–301. [PubMed]
  • Pfeifer K, Prezant T, Guarente L. Yeast HAP1 activator binds to two upstream activation sites of different sequence. Cell. 1987 Apr 10;49(1):19–27. [PubMed]
  • Pinkham JL, Guarente L. Cloning and molecular analysis of the HAP2 locus: a global regulator of respiratory genes in Saccharomyces cerevisiae. Mol Cell Biol. 1985 Dec;5(12):3410–3416. [PMC free article] [PubMed]
  • Pinkham JL, Olesen JT, Guarente LP. Sequence and nuclear localization of the Saccharomyces cerevisiae HAP2 protein, a transcriptional activator. Mol Cell Biol. 1987 Feb;7(2):578–585. [PMC free article] [PubMed]
  • PORRA RJ, JONES OT. Studies on ferrochelatase. 2. An in vestigation of the role offerrochelatase in the biosynthesis of various haem prosthetic groups. Biochem J. 1963 Apr;87:186–192. [PubMed]
  • Poutre CG, Fox TD. PET111, a Saccharomyces cerevisiae nuclear gene required for translation of the mitochondrial mRNA encoding cytochrome c oxidase subunit II. Genetics. 1987 Apr;115(4):637–647. [PubMed]
  • Repetto B, Tzagoloff A. Structure and regulation of KGD1, the structural gene for yeast alpha-ketoglutarate dehydrogenase. Mol Cell Biol. 1989 Jun;9(6):2695–2705. [PMC free article] [PubMed]
  • Rödel G. Two yeast nuclear genes, CBS1 and CBS2, are required for translation of mitochondrial transcripts bearing the 5'-untranslated COB leader. Curr Genet. 1986;11(1):41–45. [PubMed]
  • Rödel G, Fox TD. The yeast nuclear gene CBS1 is required for translation of mitochondrial mRNAs bearing the cob 5' untranslated leader. Mol Gen Genet. 1987 Jan;206(1):45–50. [PubMed]
  • Rosenblum-Vos LS, Rhodes L, Evangelista CC, Jr, Boayke KA, Zitomer RS. The ROX3 gene encodes an essential nuclear protein involved in CYC7 gene expression in Saccharomyces cerevisiae. Mol Cell Biol. 1991 Nov;11(11):5639–5647. [PMC free article] [PubMed]
  • Rotenberg MO, Woolford JL., Jr Tripartite upstream promoter element essential for expression of Saccharomyces cerevisiae ribosomal protein genes. Mol Cell Biol. 1986 Feb;6(2):674–687. [PMC free article] [PubMed]
  • Rothstein RJ, Sherman F. Genes affecting the expression of cytochrome c in yeast: genetic mapping and genetic interactions. Genetics. 1980 Apr;94(4):871–889. [PubMed]
  • Russell DW, Smith M, Cox D, Williamson VM, Young ET. DNA sequences of two yeast promoter-up mutants. Nature. 1983 Aug 18;304(5927):652–654. [PubMed]
  • Rymond BC, Zitomer RS, Schümperli D, Rosenberg M. The expression in yeast of the Escherichia coli galK gene on CYC1::galK fusion plasmids. Gene. 1983 Nov;25(2-3):249–262. [PubMed]
  • Saltzgaber-Müller J, Schatz G. Heme is necessary for the accumulation and assembly of cytochrome c oxidase subunits in Saccharomyces cerevisiae. J Biol Chem. 1978 Jan 10;253(1):305–310. [PubMed]
  • Schamhart DH, Ten Berge AM, Van De Poll KW. Isolation of a catabolite repression mutant of yeast as a revertant of a strain that is maltose negative in the respiratory-deficient state. J Bacteriol. 1975 Mar;121(3):747–752. [PMC free article] [PubMed]
  • Schnier J, Schwelberger HG, Smit-McBride Z, Kang HA, Hershey JW. Translation initiation factor 5A and its hypusine modification are essential for cell viability in the yeast Saccharomyces cerevisiae. Mol Cell Biol. 1991 Jun;11(6):3105–3114. [PMC free article] [PubMed]
  • Schultz J, Carlson M. Molecular analysis of SSN6, a gene functionally related to the SNF1 protein kinase of Saccharomyces cerevisiae. Mol Cell Biol. 1987 Oct;7(10):3637–3645. [PMC free article] [PubMed]
  • Seeman NC, Rosenberg JM, Rich A. Sequence-specific recognition of double helical nucleic acids by proteins. Proc Natl Acad Sci U S A. 1976 Mar;73(3):804–808. [PubMed]
  • Della Seta F, Ciafré SA, Marck C, Santoro B, Presutti C, Sentenac A, Bozzoni I. The ABF1 factor is the transcriptional activator of the L2 ribosomal protein genes in Saccharomyces cerevisiae. Mol Cell Biol. 1990 May;10(5):2437–2441. [PMC free article] [PubMed]
  • Sinclair AH, Berta P, Palmer MS, Hawkins JR, Griffiths BL, Smith MJ, Foster JW, Frischauf AM, Lovell-Badge R, Goodfellow PN. A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Nature. 1990 Jul 19;346(6281):240–244. [PubMed]
  • Sousa R, Arcangioli B. A point mutation in the CYC1 UAS1 creates a new combination of regulatory elements that activate transcription synergistically. EMBO J. 1989 Jun;8(6):1801–1808. [PubMed]
  • Staben C, Yanofsky C. Neurospora crassa a mating-type region. Proc Natl Acad Sci U S A. 1990 Jul;87(13):4917–4921. [PubMed]
  • Strick CA, Fox TD. Saccharomyces cerevisiae positive regulatory gene PET111 encodes a mitochondrial protein that is translated from an mRNA with a long 5' leader. Mol Cell Biol. 1987 Aug;7(8):2728–2734. [PMC free article] [PubMed]
  • Struhl K. Naturally occurring poly(dA-dT) sequences are upstream promoter elements for constitutive transcription in yeast. Proc Natl Acad Sci U S A. 1985 Dec;82(24):8419–8423. [PubMed]
  • Struhl K. Constitutive and inducible Saccharomyces cerevisiae promoters: evidence for two distinct molecular mechanisms. Mol Cell Biol. 1986 Nov;6(11):3847–3853. [PMC free article] [PubMed]
  • Stukey JE, McDonough VM, Martin CE. The OLE1 gene of Saccharomyces cerevisiae encodes the delta 9 fatty acid desaturase and can be functionally replaced by the rat stearoyl-CoA desaturase gene. J Biol Chem. 1990 Nov 25;265(33):20144–20149. [PubMed]
  • Thorsness M, Schafer W, D'Ari L, Rine J. Positive and negative transcriptional control by heme of genes encoding 3-hydroxy-3-methylglutaryl coenzyme A reductase in Saccharomyces cerevisiae. Mol Cell Biol. 1989 Dec;9(12):5702–5712. [PMC free article] [PubMed]
  • Thrash-Bingham C, Fangman WL. A yeast mutation that stabilizes a plasmid bearing a mutated ARS1 element. Mol Cell Biol. 1989 Feb;9(2):809–816. [PMC free article] [PubMed]
  • Trawick JD, Wright RM, Poyton RO. Transcription of yeast COX6, the gene for cytochrome c oxidase subunit VI, is dependent on heme and on the HAP2 gene. J Biol Chem. 1989 Apr 25;264(12):7005–7008. [PubMed]
  • Trueblood CE, Wright RM, Poyton RO. Differential regulation of the two genes encoding Saccharomyces cerevisiae cytochrome c oxidase subunit V by heme and the HAP2 and REO1 genes. Mol Cell Biol. 1988 Oct;8(10):4537–4540. [PMC free article] [PubMed]
  • Trumbly RJ. Isolation of Saccharomyces cerevisiae mutants constitutive for invertase synthesis. J Bacteriol. 1986 Jun;166(3):1123–1127. [PMC free article] [PubMed]
  • Trumbly RJ. Cloning and characterization of the CYC8 gene mediating glucose repression in yeast. Gene. 1988 Dec 15;73(1):97–111. [PubMed]
  • Tzagoloff A, Dieckmann CL. PET genes of Saccharomyces cerevisiae. Microbiol Rev. 1990 Sep;54(3):211–225. [PMC free article] [PubMed]
  • Urban-Grimal D, Labbe-Bois R. Genetic and biochemical characterization of mutants of Saccharomyces cerevisiae blocked in six different steps of heme biosynthesis. Mol Gen Genet. 1981;183(1):85–92. [PubMed]
  • Verdière J, Creusot F, Guarente L, Slonimski PP. The overproducing CYP1 and the underproducing hap1 mutations are alleles of the same gene which regulates in trans the expression of the structural genes encoding iso-cytochromes c. Curr Genet. 1986;10(5):339–342. [PubMed]
  • Verdière J, Creusot F, Guérineau M. Regulation of the expression of iso 2-cytochrome c gene in S. cerevisiae: cloning of the positive regulatory gene CYP1 and identification of the region of its target sequence on the structural gene CYP3. Mol Gen Genet. 1985;199(3):524–533. [PubMed]
  • Verdière J, Gaisne M, Guiard B, Defranoux N, Slonimski PP. CYP1 (HAP1) regulator of oxygen-dependent gene expression in yeast. II. Missense mutation suggests alternative Zn fingers as discriminating agents of gene control. J Mol Biol. 1988 Nov 20;204(2):277–282. [PubMed]
  • Verdière J, Gaisne M, Labbe-Bois R. CYP1 (HAP1) is a determinant effector of alternative expression of heme-dependent transcribed genes in yeast [corrected]. Mol Gen Genet. 1991 Aug;228(1-2):300–306. [PubMed]
  • Waterland RA, Basu A, Chance B, Poyton RO. The isoforms of yeast cytochrome c oxidase subunit V alter the in vivo kinetic properties of the holoenzyme. J Biol Chem. 1991 Mar 5;266(7):4180–4186. [PubMed]
  • Wen L, Huang JK, Johnson BH, Reeck GR. A human placental cDNA clone that encodes nonhistone chromosomal protein HMG-1. Nucleic Acids Res. 1989 Feb 11;17(3):1197–1214. [PMC free article] [PubMed]
  • Wickner RB. Mutants of Saccharomyces cerevisiae that incorporate deoxythymidine-5'-monophosphate into deoxyribonucleic acid in vivo. J Bacteriol. 1974 Jan;117(1):252–260. [PMC free article] [PubMed]
  • Williams FE, Trumbly RJ. Characterization of TUP1, a mediator of glucose repression in Saccharomyces cerevisiae. Mol Cell Biol. 1990 Dec;10(12):6500–6511. [PMC free article] [PubMed]
  • Williams FE, Varanasi U, Trumbly RJ. The CYC8 and TUP1 proteins involved in glucose repression in Saccharomyces cerevisiae are associated in a protein complex. Mol Cell Biol. 1991 Jun;11(6):3307–3316. [PMC free article] [PubMed]
  • 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. [PubMed]
  • Woodrow G, Schatz G. The role of oxygen in the biosynthesis of cytochrome c oxidase of yeast mitochondria. J Biol Chem. 1979 Jul 10;254(13):6088–6093. [PubMed]
  • Wright CF, Zitomer RS. A positive regulatory site and a negative regulatory site control the expression of the Saccharomyces cerevisiae CYC7 gene. Mol Cell Biol. 1984 Oct;4(10):2023–2030. [PMC free article] [PubMed]
  • Wright RM, Poyton RO. Release of two Saccharomyces cerevisiae cytochrome genes, COX6 and CYC1, from glucose repression requires the SNF1 and SSN6 gene products. Mol Cell Biol. 1990 Mar;10(3):1297–1300. [PMC free article] [PubMed]
  • Zagorec M, Buhler JM, Treich I, Keng T, Guarente L, Labbe-Bois R. Isolation, sequence, and regulation by oxygen of the yeast HEM13 gene coding for coproporphyrinogen oxidase. J Biol Chem. 1988 Jul 15;263(20):9718–9724. [PubMed]
  • Zagorec M, Labbe-Bois R. Negative control of yeast coproporphyrinogen oxidase synthesis by heme and oxygen. J Biol Chem. 1986 Feb 25;261(6):2506–2509. [PubMed]
  • Zhang M, Rosenblum-Vos LS, Lowry CV, Boakye KA, Zitomer RS. A yeast protein with homology to the beta-subunit of G proteins is involved in control of heme-regulated and catabolite-repressed genes. Gene. 1991 Jan 15;97(2):153–161. [PubMed]
  • Zitomer RS, Sellers JW, McCarter DW, Hastings GA, Wick P, Lowry CV. Elements involved in oxygen regulation of the Saccharomyces cerevisiae CYC7 gene. Mol Cell Biol. 1987 Jun;7(6):2212–2220. [PMC free article] [PubMed]

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