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The yeast co-activator GAL11 positively influences transcription of the phosphoglycerate kinase gene, but only when RAP1 is bound to its upstream activation sequence

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Abstract

Transcription of the yeast phosphoglycerate kinase gene (PGK) is activated by an array of nuclear factors including the multifunctional protein RAP1. We have demonstrated that the transcriptional co-activator GAL11, which was identified as an auxiliary factor to GAL4 and which is believed to interact with the zinc finger of the trans-activator, positively influences the level of PGK transcription on both fermentable and non-fermentable carbon sources. This positive effect is only observed when the RAP1 site in the upstream activation sequence (UAS) is present, implying that GAL11 acts through RAP1. Expression of the RAP1 gene is not reduced in the gal11 background, and in vivo footprinting shows that GAL11 does not influence RAP1 DNA-binding activity. Therefore the effect of GAL11 on PGK transcription must be mediated at the PGK UAS, presumably as part of the activation complex. It has been proposed that RAP1 may act as a facilitator of GCR1 binding at the PGK UAS and therefore it is conceivable that the target for GAL11 may in fact be GCR1. A further implication of this study is that GAL11 can interact with proteins such as RAP1 or GCR1 that are apparently structurally dissimilar from GAL4 and other zinc finger DNA-binding proteins.

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References

  • Baker HV (1986) Glycolytic gene expression in Saccharomyces cerevisiae: nucleotide sequence of GCR1, null mutations, and evidece for expression. Mol Cell Biol 6:3774–3784

    Google Scholar 

  • Baker HV (1991) GCR1 of Saccharomyces cerevisiae encodes a DNA binding protein whose binding is abolished by mutations in the CTTCC sequence motif. Proc Natl Acad Sci USA 88:9443–9447

    Google Scholar 

  • Buchman AR, Lue NF, Kornberg RD (1988) Connections between transcriptional activators, silencers and telomeres as revealed by functional analysis of a yeast DNA-binding protein. Mol Cell Biol 8:5086–5099

    Google Scholar 

  • Chambers A, Stanway CA, Kingsman AJ, Kingsman SM (1988) The UAS of the yeast PGK gene is composed of multiple functional elements. Nucleic Acids Res 16:8245–8260

    Google Scholar 

  • Chambers A, Tsang JSH, Stanway CA, Kingsman AJ, Kingsman SM (1989) Transcriptional control of the Saccharomyces cerevisiae PGK gene by RAP1. Mol Cell Biol 9:5516–5524

    Google Scholar 

  • Chambers A, Stanway CA, Tsang JSH, Henry YAL, Kingsman AJ, Kingsman SM (1990) ARS binding factor 1 binds adjacent to RAP1 at the UASs of the yeast glycolytic genes PGK and PYK1. Nucleic Acids Res 18:5393–5399

    Google Scholar 

  • Chasman DL, Lue NF, Buchman AR, LaPointe JW, Lorch Y, Kornberg RD (1990) A yeast protein that influences the chromatin structure of UASG and functions as a powerful auxilliary gene activator. Genes Dev 4:503–514

    Google Scholar 

  • Conrad MN, Wright JH, Wolf AJ, Zakian VA (1990) RAP1 protein interacts with yeast telomeres in vivo: overproduction alters telomere structure and decreases chromosome stability. Cell 63:739–750

    Google Scholar 

  • Della Seta F, Ciafre S-A, Marck C, Santoro B, Presutti C, Sentenac A, Bozzoni I (1990) The ABF1 factor is the transcriptional activaor of the L2 ribosomal protein genes in Saccharomyces cerevisiae. Mol Cell Biol 10:2437–2441

    Google Scholar 

  • Diffley JFX, Stillman B (1988) Purification of a yeast protein that binds to origins of DNA replication and a transcriptional silencer. Proc Natl Acad Sci USA 85:2120–2124

    Google Scholar 

  • Eisenberg S, Civalier C, Tye BK (1988) Specific interaction between a Saccharomyces cerevisiae protein and a DNA element associated with certain autonomously replicating sequences. Proc Natl Acad Sci USA 85:743–746

    Google Scholar 

  • Fassler JS, Winston F (1989) The Saccharomyces cerevisiae SPT13/GAL11 gene has both positive and negative regulatory roles in transcription. Mol Cell Biol 9:5602–5609

    Google Scholar 

  • Giesman D, Best L, Tatchell K (1991) The role of RAP1 in the regulation of the MATα locus. Mol Cell Biol 11:1069–1079

    Google Scholar 

  • Henry YAL (1991) The role of RAP1 and GCR1 in the transcriptional regulation of the Saccharomyces cerevisiae PGK gene. D Phil Thesis, Oxford University

  • Henry YAL, Chambers A, Tsang JSH, Kingsman AJ, Kingsman SM (1990) Characterisation of the DNA binding domain of the yeast RAP1 protein. Nucleic Acids Res 18:2617–2623

    Google Scholar 

  • Himmelfarb HJ, Pearlberg J, Last DH, Ptashne M (1990) GAL11P: a yeast mutation that potentiates the effect of weak GAL4-derived activators. Cell 63:1299–1309

    Google Scholar 

  • Holland MJ, Holland JP (1978) Isolation and identification of yeast messenger RNAs coding for enolase, glyceraldehyde-3phosphate dehydrogenase and phosphoglycerate kinase. Biochemistry 17:4900–4907

    Google Scholar 

  • Holm C, Meeks-Wagner DW, Fangman WL, Botstein D (1986) A rapid efficient method for isolating DNA from yeast. Gene 42:169–173

    Google Scholar 

  • Huie MA, Scott EW, Drazinic CM, Lopez MC, Hornstra IK, Yang TP, Baker HV (1992) Characterization of the DNA-binding activity of GCR1: in vivo evidence for two GCR1-binding sites in the upstream activating sequence of TPI of Saccharomyces cerevisiae. Mol Cell Biol 12:2690–2700

    Google Scholar 

  • Kipling D, Tambini C, Kearsey SE (1991) rar mutations which increase artificial chromosome stability in Saccharomyces cerevisiae identify transcription and recombination proteins. Nucleic Acids Res 19:1385–1391

    Google Scholar 

  • Kurtz S, Shore D (1991) RAP1 protein activates and silences transcription of mating type genes in yeast. Genes Dev 5:616–628

    Google Scholar 

  • Long RM, Mylin LM, Hopper JE (1991) GAL11 (SPT13), a transcriptional regulator of diverse yeast genes, affects the phosphorylation state of GAL4, a highly specific transcriptional activator. Mol Cell Biol 11:2311–2314

    Google Scholar 

  • Lustig A, Kurtz S, Shore D (1990) Involvement of the silencer and UAS binding protein RAP1 in regulation of telomere length. Science 250:549–553

    Google Scholar 

  • Marmorstein R, Carey M, Ptashne M, Harrison SC (1992) DNA recognition by GAL4: structure of a protein-DNA complex. Nature 356:408–414

    Google Scholar 

  • Nishizawa M, Suzuki Y, Nogi Y, Matsumoto K, Fukasawa T (1990) Yeast Gal11 protein mediates the transcriptional activation signal of two different transacting factors, Gal4 and general regulatory factor I/repressor/activator site binding protein1/translation upstream factor. Proc Natl Acad Sci USA 87:5373–5377

    Google Scholar 

  • Ogden JE, Stanway CA, Kim S, Mellor J, Kingsman AJ, Kingsman SM (1986) Efficient expression of the Saccharomyces cerevisiae PGK gene depends upon an upstream activation sequence but does not require TATA sequences. Mol Cell Biol 6:4335–4343

    Google Scholar 

  • Pfeifer K, Kim K-S, Kogan S, Guarente L (1989) Functional dissection and sequence of yeast HAP1 activator. Cell 56:291–301

    Google Scholar 

  • Piper PW, Curran B, Davies MW, Hirst K, Lockheart A, Ogden JE, Stanway CA, Kingsman AJ, Kingsman SM (1988) A heat shock element in the phosphoglycerate kinase gene promoter of yeast. Nucleic Acids Res 16:1333–1348

    Google Scholar 

  • Ptashne M, Gann AAF (1990) Activators and targets. Nature 346:329–331

    Google Scholar 

  • Roeder RG (1991) The complexities of eukaryotic transcription initiation: regulation of preinitiation complex assembly. TIBS 16:402–408

    Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning, a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

  • Schmitt ME, Brown TA, Trumpower BL (1990) A rapid and simple method for preparation of RNA from Saccharomyces cerevisiae. Nucleic Acids Res 18:3091–3092

    Google Scholar 

  • Scott EW, Baker HV (1993) Concerted action of the transcriptional activators REB1, RAP1 and GCR1 in the high level expression of the glycolytic gene TPI. Mol Cell Biol 13:543–550

    Google Scholar 

  • Sharp PA (1992) TATA-binding protein is a classless factor. Cell 68:819–821

    Google Scholar 

  • Shore D, Nasmyth K (1987) Purification and cloning of a DNA binding protein from yeast that binds to both silencer and activator elements. Cell 51:721–732

    Google Scholar 

  • Stanway CA, Chambers A, Kingsman AJ, Kingsman SM (1989a) Characterization of the transcriptional potency of sub-elements of the UAS of the yeast PGK gene in a PGK mini-promoter. Nucleic Acids Res 17:9205–9218

    Google Scholar 

  • Stanway CA, Sowden MP, Wilson LE, Kingsman AJ, Kingsman SM (1989b) Efficient activation of transcription in yeast by the BPV1 E2 protein. Nucleic Acids Res 17:2187–2196

    Google Scholar 

  • Suzuki Y, Nogi Y, Abe A, Fukusawa T (1986) GAL11 protein, an auxilliary transcription activator genes encoding galactose-metabolizing enzymes in Saccharomyces cerevisiae. Mol Cell Biol 8:4991–4999

    Google Scholar 

  • Suzuki Y, Nogi Y, Abe A, Fukusawa T (1992) Erratum. GAL11 protein, an auxilliary transcription activator for genes encoding galactose-metabolizing enzymes in Saccharomyces cerevisiae. Mol Cell Biol 12:4806

    Google Scholar 

  • Uemura H, Fraenkel DG (1990) gcr2, a new mutation affecting glycolytic gene expression in Saccharomyces cerevisiae. Mol Cell Biol 10:6389–6396

    Google Scholar 

  • Uemura H, Jigami Y (1992) Role of GCR2 in transcriptional activation of yeast glycolytic genes. Mol Cell Biol 12:3834–3842

    Google Scholar 

  • Yu G, Fassler J (1993) SPT13 (GAL11) of Saccharomyces cerevisiae negatively regulates activity of the MCM1 transcription factor in Ty1 elements. Mol Cell Biol 13:63–71

    Google Scholar 

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Communicated by D. Thomas

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Stanway, C.A., Gibbs, J.M., Kearsey, S.E. et al. The yeast co-activator GAL11 positively influences transcription of the phosphoglycerate kinase gene, but only when RAP1 is bound to its upstream activation sequence. Molec. Gen. Genet. 243, 207–214 (1994). https://doi.org/10.1007/BF00280318

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  • DOI: https://doi.org/10.1007/BF00280318

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