Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1993 Sep;175(18):5851–5861. doi: 10.1128/jb.175.18.5851-5861.1993

The Saccharomyces cerevisiae DAL80 repressor protein binds to multiple copies of GATAA-containing sequences (URSGATA).

T S Cunningham 1, T G Cooper 1
PMCID: PMC206664  PMID: 8376332

Abstract

Induced expression of the allantoin (DAL) catabolic genes in Saccharomyces cerevisiae has been suggested to be mediated by interaction of three different types of promoter elements. First is an inducer-independent upstream activation sequence, UASNTR, whose operation is sensitive to nitrogen catabolite repression. The GLN3 product is required for UASNTR-mediated transcriptional activation. This site consists of two separated elements, each of which has a GATAA sequence at its core. Response of the DAL genes to inducer is mediated by a second type of cis-acting element, DAL UIS. The DAL82 and DAL81 genes are required for response to inducer; DAL82 protein is the UIS-binding protein. When only the UASNTR and UIS elements are present, DAL gene expression occurs at high levels in the absence of inducer. We, therefore, hypothesized that a third element, an upstream repressor sequence (URS) mediates maintenance of DAL gene expression at a low level when inducer is absent. Since the DAL and UGA genes are overexpressed and largely inducer independent in dal80 deletion mutants, we have suggested DAL80 protein negatively regulates a wide spectrum of nitrogen-catabolic gene expression, likely in conjunction with a URS element. Here we show that DAL80 protein binds to DAL3 and UGA4 upstream DNA sequences, designated URSGATA, consisting of two GATAA-containing sites separated by at least 15 bp. The preferred orientation of the sites is tail to tail, but reasonable binding activity is also observed with a head-to-tail configuration. URSGATA elements contain the sequence GATAA at their core and hence share sequence homology with UASNTR elements.

Full text

PDF
5851

Images in this article

Selected References

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

  1. André B., Jauniaux J. C. Nucleotide sequence of the yeast UGA1 gene encoding GABA transaminase. Nucleic Acids Res. 1990 May 25;18(10):3049–3049. doi: 10.1093/nar/18.10.3049. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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: 10.1006/abio.1976.9999. [DOI] [PubMed] [Google Scholar]
  3. Bricmont P. A., Cooper T. G. A gene product needed for induction of allantoin system genes in Saccharomyces cerevisiae but not for their transcriptional activation. Mol Cell Biol. 1989 Sep;9(9):3869–3877. doi: 10.1128/mcb.9.9.3869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bricmont P. A., Daugherty J. R., Cooper T. G. The DAL81 gene product is required for induced expression of two differently regulated nitrogen catabolic genes in Saccharomyces cerevisiae. Mol Cell Biol. 1991 Feb;11(2):1161–1166. doi: 10.1128/mcb.11.2.1161. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Buckholz R. G., Cooper T. G. The allantoinase (DAL1) gene of Saccharomyces cerevisiae. Yeast. 1991 Dec;7(9):913–923. doi: 10.1002/yea.320070903. [DOI] [PubMed] [Google Scholar]
  6. Bysani N., Daugherty J. R., Cooper T. G. Saturation mutagenesis of the UASNTR (GATAA) responsible for nitrogen catabolite repression-sensitive transcriptional activation of the allantoin pathway genes in Saccharomyces cerevisiae. J Bacteriol. 1991 Aug;173(16):4977–4982. doi: 10.1128/jb.173.16.4977-4982.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chisholm G., Cooper T. G. Isolation and characterization of mutants that produce the allantoin-degrading enzymes constitutively in Saccharomyces cerevisiae. Mol Cell Biol. 1982 Sep;2(9):1088–1095. doi: 10.1128/mcb.2.9.1088. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cooper T. G., Ferguson D., Rai R., Bysani N. The GLN3 gene product is required for transcriptional activation of allantoin system gene expression in Saccharomyces cerevisiae. J Bacteriol. 1990 Feb;172(2):1014–1018. doi: 10.1128/jb.172.2.1014-1018.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cooper T. G., Rai R., Yoo H. S. Requirement of upstream activation sequences for nitrogen catabolite repression of the allantoin system genes in Saccharomyces cerevisiae. Mol Cell Biol. 1989 Dec;9(12):5440–5444. doi: 10.1128/mcb.9.12.5440. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Coornaert D., Vissers S., André B., Grenson M. The UGA43 negative regulatory gene of Saccharomyces cerevisiae contains both a GATA-1 type zinc finger and a putative leucine zipper. Curr Genet. 1992 Apr;21(4-5):301–307. doi: 10.1007/BF00351687. [DOI] [PubMed] [Google Scholar]
  11. Cunningham T. S., Cooper T. G. Expression of the DAL80 gene, whose product is homologous to the GATA factors and is a negative regulator of multiple nitrogen catabolic genes in Saccharomyces cerevisiae, is sensitive to nitrogen catabolite repression. Mol Cell Biol. 1991 Dec;11(12):6205–6215. doi: 10.1128/mcb.11.12.6205. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Daugherty J. R., Rai R., el Berry H. M., Cooper T. G. Regulatory circuit for responses of nitrogen catabolic gene expression to the GLN3 and DAL80 proteins and nitrogen catabolite repression in Saccharomyces cerevisiae. J Bacteriol. 1993 Jan;175(1):64–73. doi: 10.1128/jb.175.1.64-73.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. ElBerry H. M., Majumdar M. L., Cunningham T. S., Sumrada R. A., Cooper T. G. Regulation of the urea active transporter gene (DUR3) in Saccharomyces cerevisiae. J Bacteriol. 1993 Aug;175(15):4688–4698. doi: 10.1128/jb.175.15.4688-4698.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Fong T. C., Emerson B. M. The erythroid-specific protein cGATA-1 mediates distal enhancer activity through a specialized beta-globin TATA box. Genes Dev. 1992 Apr;6(4):521–532. doi: 10.1101/gad.6.4.521. [DOI] [PubMed] [Google Scholar]
  15. Genbauffe F. S., Cooper T. G. Induction and repression of the urea amidolyase gene in Saccharomyces cerevisiae. Mol Cell Biol. 1986 Nov;6(11):3954–3964. doi: 10.1128/mcb.6.11.3954. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Jauniaux J. C., Grenson M. GAP1, the general amino acid permease gene of Saccharomyces cerevisiae. Nucleotide sequence, protein similarity with the other bakers yeast amino acid permeases, and nitrogen catabolite repression. Eur J Biochem. 1990 May 31;190(1):39–44. doi: 10.1111/j.1432-1033.1990.tb15542.x. [DOI] [PubMed] [Google Scholar]
  17. Kolodziej P. A., Young R. A. Epitope tagging and protein surveillance. Methods Enzymol. 1991;194:508–519. doi: 10.1016/0076-6879(91)94038-e. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Kovari L., Sumrada R., Kovari I., Cooper T. G. Multiple positive and negative cis-acting elements mediate induced arginase (CAR1) gene expression in Saccharomyces cerevisiae. Mol Cell Biol. 1990 Oct;10(10):5087–5097. doi: 10.1128/mcb.10.10.5087. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Margolin W., Howe M. M. Activation of the bacteriophage Mu lys promoter by Mu C protein requires the sigma 70 subunit of Escherichia coli RNA polymerase. J Bacteriol. 1990 Mar;172(3):1424–1429. doi: 10.1128/jb.172.3.1424-1429.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Martin D. I., Orkin S. H. Transcriptional activation and DNA binding by the erythroid factor GF-1/NF-E1/Eryf 1. Genes Dev. 1990 Nov;4(11):1886–1898. doi: 10.1101/gad.4.11.1886. [DOI] [PubMed] [Google Scholar]
  22. Minehart P. L., Magasanik B. Sequence and expression of GLN3, a positive nitrogen regulatory gene of Saccharomyces cerevisiae encoding a protein with a putative zinc finger DNA-binding domain. Mol Cell Biol. 1991 Dec;11(12):6216–6228. doi: 10.1128/mcb.11.12.6216. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Minehart P. L., Magasanik B. Sequence of the GLN1 gene of Saccharomyces cerevisiae: role of the upstream region in regulation of glutamine synthetase expression. J Bacteriol. 1992 Mar;174(6):1828–1836. doi: 10.1128/jb.174.6.1828-1836.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Mitchell A. P., Magasanik B. Regulation of glutamine-repressible gene products by the GLN3 function in Saccharomyces cerevisiae. Mol Cell Biol. 1984 Dec;4(12):2758–2766. doi: 10.1128/mcb.4.12.2758. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Olive M. G., Daugherty J. R., Cooper T. G. DAL82, a second gene required for induction of allantoin system gene transcription in Saccharomyces cerevisiae. J Bacteriol. 1991 Jan;173(1):255–261. doi: 10.1128/jb.173.1.255-261.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Orkin S. H. Globin gene regulation and switching: circa 1990. Cell. 1990 Nov 16;63(4):665–672. doi: 10.1016/0092-8674(90)90133-y. [DOI] [PubMed] [Google Scholar]
  27. Rai R., Genbauffe F. S., Cooper T. G. Structure and transcription of the allantoate permease gene (DAL5) from Saccharomyces cerevisiae. J Bacteriol. 1988 Jan;170(1):266–271. doi: 10.1128/jb.170.1.266-271.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Rai R., Genbauffe F. S., Sumrada R. A., Cooper T. G. Identification of sequences responsible for transcriptional activation of the allantoate permease gene in Saccharomyces cerevisiae. Mol Cell Biol. 1989 Feb;9(2):602–608. doi: 10.1128/mcb.9.2.602. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Rai R., Genbauffe F., Lea H. Z., Cooper T. G. Transcriptional regulation of the DAL5 gene in Saccharomyces cerevisiae. J Bacteriol. 1987 Aug;169(8):3521–3524. doi: 10.1128/jb.169.8.3521-3524.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. 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]
  31. Turoscy V., Cooper T. G. Pleiotropic control of five eucaryotic genes by multiple regulatory elements. J Bacteriol. 1982 Sep;151(3):1237–1246. doi: 10.1128/jb.151.3.1237-1246.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Vissers S., Andre B., Muyldermans F., Grenson M. Induction of the 4-aminobutyrate and urea-catabolic pathways in Saccharomyces cerevisiae. Specific and common transcriptional regulators. Eur J Biochem. 1990 Feb 14;187(3):611–616. doi: 10.1111/j.1432-1033.1990.tb15344.x. [DOI] [PubMed] [Google Scholar]
  33. Yamamoto M., Ko L. J., Leonard M. W., Beug H., Orkin S. H., Engel J. D. Activity and tissue-specific expression of the transcription factor NF-E1 multigene family. Genes Dev. 1990 Oct;4(10):1650–1662. doi: 10.1101/gad.4.10.1650. [DOI] [PubMed] [Google Scholar]
  34. Yang H. Y., Evans T. Distinct roles for the two cGATA-1 finger domains. Mol Cell Biol. 1992 Oct;12(10):4562–4570. doi: 10.1128/mcb.12.10.4562. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Yoo H. S., Cooper T. G. Sequences of two adjacent genes, one (DAL2) encoding allantoicase and another (DCG1) sensitive to nitrogen-catabolite repression in Saccharomyces cerevisiae. Gene. 1991 Jul 31;104(1):55–62. doi: 10.1016/0378-1119(91)90464-m. [DOI] [PubMed] [Google Scholar]
  36. Yoo H. S., Cooper T. G. The DAL7 promoter consists of multiple elements that cooperatively mediate regulation of the gene's expression. Mol Cell Biol. 1989 Aug;9(8):3231–3243. doi: 10.1128/mcb.9.8.3231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Yoo H. S., Cooper T. G. The ureidoglycollate hydrolase (DAL3) gene in Saccharomyces cerevisiae. Yeast. 1991 Oct;7(7):693–698. doi: 10.1002/yea.320070705. [DOI] [PubMed] [Google Scholar]
  38. Yoo H. S., Cunningham T. S., Cooper T. G. The allantoin and uracil permease gene sequences of Saccharomyces cerevisiae are nearly identical. Yeast. 1992 Dec;8(12):997–1006. doi: 10.1002/yea.320081202. [DOI] [PubMed] [Google Scholar]
  39. Yoo H. S., Genbauffe F. S., Cooper T. G. Identification of the ureidoglycolate hydrolase gene in the DAL gene cluster of Saccharomyces cerevisiae. Mol Cell Biol. 1985 Sep;5(9):2279–2288. doi: 10.1128/mcb.5.9.2279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. van Vuuren H. J., Daugherty J. R., Rai R., Cooper T. G. Upstream induction sequence, the cis-acting element required for response to the allantoin pathway inducer and enhancement of operation of the nitrogen-regulated upstream activation sequence in Saccharomyces cerevisiae. J Bacteriol. 1991 Nov;173(22):7186–7195. doi: 10.1128/jb.173.22.7186-7195.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES