Abstract
Expression of the FOX3 gene, which encodes yeast peroxisomal 3-oxoacyl-coenzyme A thiolase, can be induced by oleate and repressed by glucose. Previously, we have shown that induction was mediated by an oleate response element. Just upstream of this element a negatively acting control region that mediated glucose repression was found. In order to study this negative control region, we carried out DNA-binding assays and analyzed phenotypes of mutations in this region and in the trans-acting factor CAR80, which is identical to UME6. DNA-binding assays showed that two multifunctional yeast proteins, ABF1 and RP-A, interacted with the negative control element independently of the transcriptional activity of the FOX3 gene. ABF1 and RP-A, the latter being identical to BUF, were able to bind to DNA independently of one another but also simultaneously. The phenotypes of mutations in either DNA-binding sites of ABF1, RP-A, or both, which affected the DNA binding of these factors in vitro, indicated that these sites and the proteins that interact with them participate in glucose repression. The involvement of the RP-A site in glucose repression was further supported by our observation that the CAR80 gene product, which is required for repression mediated by the RP-A site, was essential for maintenance of glucose repression. In addition to the RP-A site in the FOX3 promoter, similar sequences were observed in other genes involved in peroxisomal function. RP-A proved to bind to all of these sequences, albeit with various affinities. From these results it is concluded that the ABF1 and RP-A sites are being required in concert to mediate glucose repression of the FOX3 gene. In addition, coordinated regulation of expression of genes involved in peroxisomal function in response to glucose is mediated by proteins associated with the RP-A site, probably RP-A and CAR80.
Full Text
The Full Text of this article is available as a PDF (711.9 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- 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: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
- Brand A. H., Micklem G., Nasmyth K. A yeast silencer contains sequences that can promote autonomous plasmid replication and transcriptional activation. Cell. 1987 Dec 4;51(5):709–719. doi: 10.1016/0092-8674(87)90094-8. [DOI] [PubMed] [Google Scholar]
- Brill S. J., Stillman B. Replication factor-A from Saccharomyces cerevisiae is encoded by three essential genes coordinately expressed at S phase. Genes Dev. 1991 Sep;5(9):1589–1600. doi: 10.1101/gad.5.9.1589. [DOI] [PubMed] [Google Scholar]
- Brindle P. K., Holland J. P., Willett C. E., Innis M. A., Holland M. J. Multiple factors bind the upstream activation sites of the yeast enolase genes ENO1 and ENO2: ABFI protein, like repressor activator protein RAP1, binds cis-acting sequences which modulate repression or activation of transcription. Mol Cell Biol. 1990 Sep;10(9):4872–4885. doi: 10.1128/mcb.10.9.4872. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Buchman A. R., Kimmerly W. J., Rine J., Kornberg R. D. Two DNA-binding factors recognize specific sequences at silencers, upstream activating sequences, autonomously replicating sequences, and telomeres in Saccharomyces cerevisiae. Mol Cell Biol. 1988 Jan;8(1):210–225. doi: 10.1128/mcb.8.1.210. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chambers A., Stanway C., Tsang J. S., Henry Y., Kingsman A. J., Kingsman S. M. ARS binding factor 1 binds adjacent to RAP1 at the UASs of the yeast glycolytic genes PGK and PYK1. Nucleic Acids Res. 1990 Sep 25;18(18):5393–5399. doi: 10.1093/nar/18.18.5393. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cohen G., Rapatz W., Ruis H. Sequence of the Saccharomyces cerevisiae CTA1 gene and amino acid sequence of catalase A derived from it. Eur J Biochem. 1988 Sep 1;176(1):159–163. doi: 10.1111/j.1432-1033.1988.tb14263.x. [DOI] [PubMed] [Google Scholar]
- Della Seta F., Ciafré S. A., 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. doi: 10.1128/mcb.10.5.2437. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Diffley J. F. Global regulators of chromosome function in yeast. Antonie Van Leeuwenhoek. 1992 Aug;62(1-2):25–33. doi: 10.1007/BF00584460. [DOI] [PubMed] [Google Scholar]
- Diffley J. F., Stillman B. Purification of a yeast protein that binds to origins of DNA replication and a transcriptional silencer. Proc Natl Acad Sci U S A. 1988 Apr;85(7):2120–2124. doi: 10.1073/pnas.85.7.2120. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Din S., Brill S. J., Fairman M. P., Stillman B. Cell-cycle-regulated phosphorylation of DNA replication factor A from human and yeast cells. Genes Dev. 1990 Jun;4(6):968–977. doi: 10.1101/gad.4.6.968. [DOI] [PubMed] [Google Scholar]
- Dmochowska A., Dignard D., Maleszka R., Thomas D. Y. Structure and transcriptional control of the Saccharomyces cerevisiae POX1 gene encoding acyl-coenzyme A oxidase. Gene. 1990 Apr 16;88(2):247–252. doi: 10.1016/0378-1119(90)90038-s. [DOI] [PubMed] [Google Scholar]
- Dorsman J. C., Doorenbosch M. M., Maurer C. T., de Winde J. H., Mager W. H., Planta R. J., Grivell L. A. An ARS/silencer binding factor also activates two ribosomal protein genes in yeast. Nucleic Acids Res. 1989 Jul 11;17(13):4917–4923. doi: 10.1093/nar/17.13.4917. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dorsman J. C., van Heeswijk W. C., Grivell L. A. Yeast general transcription factor GFI: sequence requirements for binding to DNA and evolutionary conservation. Nucleic Acids Res. 1990 May 11;18(9):2769–2776. doi: 10.1093/nar/18.9.2769. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Einerhand A. W., Kos W. T., Distel B., Tabak H. F. Characterization of a transcriptional control element involved in proliferation of peroxisomes in yeast in response to oleate. Eur J Biochem. 1993 May 15;214(1):323–331. doi: 10.1111/j.1432-1033.1993.tb17927.x. [DOI] [PubMed] [Google Scholar]
- Einerhand A. W., Van Der Leij I., Kos W. T., Distel B., Tabak H. F. Transcriptional regulation of genes encoding proteins involved in biogenesis of peroxisomes in Saccharomyces cerevisiae. Cell Biochem Funct. 1992 Sep;10(3):185–191. doi: 10.1002/cbf.290100308. [DOI] [PubMed] [Google Scholar]
- Einerhand A. W., Voorn-Brouwer T. M., Erdmann R., Kunau W. H., Tabak H. F. Regulation of transcription of the gene coding for peroxisomal 3-oxoacyl-CoA thiolase of Saccharomyces cerevisiae. Eur J Biochem. 1991 Aug 15;200(1):113–122. doi: 10.1111/j.1432-1033.1991.tb21056.x. [DOI] [PubMed] [Google Scholar]
- Erdmann R., Veenhuis M., Mertens D., Kunau W. H. Isolation of peroxisome-deficient mutants of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1989 Jul;86(14):5419–5423. doi: 10.1073/pnas.86.14.5419. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Filipits M., Simon M. M., Rapatz W., Hamilton B., Ruis H. A Saccharomyces cerevisiae upstream activating sequence mediates induction of peroxisome proliferation by fatty acids. Gene. 1993 Sep 30;132(1):49–55. doi: 10.1016/0378-1119(93)90513-3. [DOI] [PubMed] [Google Scholar]
- Griggs D. W., Johnston M. Regulated expression of the GAL4 activator gene in yeast provides a sensitive genetic switch for glucose repression. Proc Natl Acad Sci U S A. 1991 Oct 1;88(19):8597–8601. doi: 10.1073/pnas.88.19.8597. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Halfter H., Kavety B., Vandekerckhove J., Kiefer F., Gallwitz D. Sequence, expression and mutational analysis of BAF1, a transcriptional activator and ARS1-binding protein of the yeast Saccharomyces cerevisiae. EMBO J. 1989 Dec 20;8(13):4265–4272. doi: 10.1002/j.1460-2075.1989.tb08612.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Halfter H., Müller U., Winnacker E. L., Gallwitz D. Isolation and DNA-binding characteristics of a protein involved in transcription activation of two divergently transcribed, essential yeast genes. EMBO J. 1989 Oct;8(10):3029–3037. doi: 10.1002/j.1460-2075.1989.tb08453.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hamil K. G., Nam H. G., Fried H. M. Constitutive transcription of yeast ribosomal protein gene TCM1 is promoted by uncommon cis- and trans-acting elements. Mol Cell Biol. 1988 Oct;8(10):4328–4341. doi: 10.1128/mcb.8.10.4328. [DOI] [PMC free article] [PubMed] [Google Scholar]
- He Z., Brinton B. T., Greenblatt J., Hassell J. A., Ingles C. J. The transactivator proteins VP16 and GAL4 bind replication factor A. Cell. 1993 Jun 18;73(6):1223–1232. doi: 10.1016/0092-8674(93)90650-f. [DOI] [PubMed] [Google Scholar]
- Heyer W. D., Rao M. R., Erdile L. F., Kelly T. J., Kolodner R. D. An essential Saccharomyces cerevisiae single-stranded DNA binding protein is homologous to the large subunit of human RP-A. EMBO J. 1990 Jul;9(7):2321–2329. doi: 10.1002/j.1460-2075.1990.tb07404.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hiltunen J. K., Wenzel B., Beyer A., Erdmann R., Fosså A., Kunau W. H. Peroxisomal multifunctional beta-oxidation protein of Saccharomyces cerevisiae. Molecular analysis of the fox2 gene and gene product. J Biol Chem. 1992 Apr 5;267(10):6646–6653. [PubMed] [Google Scholar]
- Kimmerly W., Buchman A., Kornberg R., Rine J. Roles of two DNA-binding factors in replication, segregation and transcriptional repression mediated by a yeast silencer. EMBO J. 1988 Jul;7(7):2241–2253. doi: 10.1002/j.1460-2075.1988.tb03064.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kovari L. Z., Cooper T. G. Participation of ABF-1 protein in expression of the Saccharomyces cerevisiae CAR1 gene. J Bacteriol. 1991 Oct;173(20):6332–6338. doi: 10.1128/jb.173.20.6332-6338.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Li R., Botchan M. R. The acidic transcriptional activation domains of VP16 and p53 bind the cellular replication protein A and stimulate in vitro BPV-1 DNA replication. Cell. 1993 Jun 18;73(6):1207–1221. doi: 10.1016/0092-8674(93)90649-b. [DOI] [PubMed] [Google Scholar]
- Luche R. M., Smart W. C., Cooper T. G. Purification of the heteromeric protein binding to the URS1 transcriptional repression site in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1992 Aug 15;89(16):7412–7416. doi: 10.1073/pnas.89.16.7412. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Luche R. M., Smart W. C., Marion T., Tillman M., Sumrada R. A., Cooper T. G. Saccharomyces cerevisiae BUF protein binds to sequences participating in DNA replication in addition to those mediating transcriptional repression (URS1) and activation. Mol Cell Biol. 1993 Sep;13(9):5749–5761. doi: 10.1128/mcb.13.9.5749. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Luche R. M., Sumrada R., Cooper T. G. A cis-acting element present in multiple genes serves as a repressor protein binding site for the yeast CAR1 gene. Mol Cell Biol. 1990 Aug;10(8):3884–3895. doi: 10.1128/mcb.10.8.3884. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lue N. F., Buchman A. R., Kornberg R. D. 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. doi: 10.1073/pnas.86.2.486. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mager W. H., Planta R. J. Coordinate expression of ribosomal protein genes in yeast as a function of cellular growth rate. 1991 May 29-Jun 12Mol Cell Biochem. 104(1-2):181–187. doi: 10.1007/BF00229818. [DOI] [PubMed] [Google Scholar]
- McBroom L. D., Sadowski P. D. Contacts of the ABF1 protein of Saccharomyces cerevisiae with a DNA binding site at MATa. J Biol Chem. 1994 Jun 10;269(23):16455–16460. [PubMed] [Google Scholar]
- McBroom L. D., Sadowski P. D. DNA bending by Saccharomyces cerevisiae ABF1 and its proteolytic fragments. J Biol Chem. 1994 Jun 10;269(23):16461–16468. [PubMed] [Google Scholar]
- Nehlin J. O., Carlberg M., Ronne H. Control of yeast GAL genes by MIG1 repressor: a transcriptional cascade in the glucose response. EMBO J. 1991 Nov;10(11):3373–3377. doi: 10.1002/j.1460-2075.1991.tb04901.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nehlin J. O., Ronne H. Yeast MIG1 repressor is related to the mammalian early growth response and Wilms' tumour finger proteins. EMBO J. 1990 Sep;9(9):2891–2898. doi: 10.1002/j.1460-2075.1990.tb07479.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Park H. D., Luche R. M., Cooper T. G. The yeast UME6 gene product is required for transcriptional repression mediated by the CAR1 URS1 repressor binding site. Nucleic Acids Res. 1992 Apr 25;20(8):1909–1915. doi: 10.1093/nar/20.8.1909. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rhode P. R., Elsasser S., Campbell J. L. Role of multifunctional autonomously replicating sequence binding factor 1 in the initiation of DNA replication and transcriptional control in Saccharomyces cerevisiae. Mol Cell Biol. 1992 Mar;12(3):1064–1077. doi: 10.1128/mcb.12.3.1064. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shore D., Stillman D. J., Brand A. H., Nasmyth K. A. Identification of silencer binding proteins from yeast: possible roles in SIR control and DNA replication. EMBO J. 1987 Feb;6(2):461–467. doi: 10.1002/j.1460-2075.1987.tb04776.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sumrada R. A., Cooper T. G. Ubiquitous upstream repression sequences control activation of the inducible arginase gene in yeast. Proc Natl Acad Sci U S A. 1987 Jun;84(12):3997–4001. doi: 10.1073/pnas.84.12.3997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sweder K. S., Rhode P. R., Campbell J. L. Purification and characterization of proteins that bind to yeast ARSs. J Biol Chem. 1988 Nov 25;263(33):17270–17277. [PubMed] [Google Scholar]
- Veenhuis M., Mateblowski M., Kunau W. H., Harder W. Proliferation of microbodies in Saccharomyces cerevisiae. Yeast. 1987 Jun;3(2):77–84. doi: 10.1002/yea.320030204. [DOI] [PubMed] [Google Scholar]
- Wang T. W., Lewin A. S., Small G. M. A negative regulating element controlling transcription of the gene encoding acyl-CoA oxidase in Saccharomyces cerevisiae. Nucleic Acids Res. 1992 Jul 11;20(13):3495–3500. doi: 10.1093/nar/20.13.3495. [DOI] [PMC free article] [PubMed] [Google Scholar]