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. 1994 Dec;176(24):7476–7483. doi: 10.1128/jb.176.24.7476-7483.1994

The URE2 protein regulates nitrogen catabolic gene expression through the GATAA-containing UASNTR element in Saccharomyces cerevisiae.

J A Coffman 1, H M el Berry 1, T G Cooper 1
PMCID: PMC197203  PMID: 8002570

Abstract

Many of the gene products that participate in nitrogen metabolism are sensitive to nitrogen catabolite repression (NCR), i.e., their expression is decreased to low levels when readily used nitrogen sources such as asparagine are provided. Previous work has shown this NCR sensitivity requires the cis-acting UASNTR element and trans-acting GLN3. Here, we extend the analysis to include the response of their expression to deletion of the URE2 locus. The expression of these nitrogen catabolic genes becomes, to various degrees, NCR insensitive in the ure2 deletion. This response is shown to be mediated through the GATAA-containing UASNTR element and supports the current idea that the NCR regulatory circuit involves the following steps: environmental signal-->URE2-->GLN3-->UASNTR operation-->NCR-sensitive gene expression. The various responses of the nitrogen catabolic genes' expression to deletion of the URE2 locus also indicate that not all NCR is mediated through URE2.

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Selected References

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

  1. 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]
  2. 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]
  3. Carlson M., Botstein D. Two differentially regulated mRNAs with different 5' ends encode secreted with intracellular forms of yeast invertase. Cell. 1982 Jan;28(1):145–154. doi: 10.1016/0092-8674(82)90384-1. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. 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]
  6. 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]
  7. 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]
  8. Coschigano P. W., Magasanik B. The URE2 gene product of Saccharomyces cerevisiae plays an important role in the cellular response to the nitrogen source and has homology to glutathione s-transferases. Mol Cell Biol. 1991 Feb;11(2):822–832. doi: 10.1128/mcb.11.2.822. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Courchesne W. E., Magasanik B. Regulation of nitrogen assimilation in Saccharomyces cerevisiae: roles of the URE2 and GLN3 genes. J Bacteriol. 1988 Feb;170(2):708–713. doi: 10.1128/jb.170.2.708-713.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. Cunningham T. S., Cooper T. G. The Saccharomyces cerevisiae DAL80 repressor protein binds to multiple copies of GATAA-containing sequences (URSGATA). J Bacteriol. 1993 Sep;175(18):5851–5861. doi: 10.1128/jb.175.18.5851-5861.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Cunningham T. S., Dorrington R. A., Cooper T. G. The UGA4 UASNTR site required for GLN3-dependent transcriptional activation also mediates DAL80-responsive regulation and DAL80 protein binding in Saccharomyces cerevisiae. J Bacteriol. 1994 Aug;176(15):4718–4725. doi: 10.1128/jb.176.15.4718-4725.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Drillien R., Aigle M., Lacroute F. Yeast mutants pleiotropically impaired in the regulation of the two glutamate dehydrogenases. Biochem Biophys Res Commun. 1973 Jul 17;53(2):367–372. doi: 10.1016/0006-291x(73)90671-2. [DOI] [PubMed] [Google Scholar]
  14. Drillien R., Lacroute F. Ureidosuccinic acid uptake in yeast and some aspects of its regulation. J Bacteriol. 1972 Jan;109(1):203–208. doi: 10.1128/jb.109.1.203-208.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Dubois E., Vissers S., Grenson M., Wiame J. M. Glutamine and ammonia in nitrogen catabolite repression of Saccharomyces cerevisiae. Biochem Biophys Res Commun. 1977 Mar 21;75(2):233–239. doi: 10.1016/0006-291x(77)91033-6. [DOI] [PubMed] [Google Scholar]
  16. Dunlop P. C., Roon R. J. L-Asparaginase of Saccharomyces cerevisiae: an extracellular Enzyme. J Bacteriol. 1975 Jun;122(3):1017–1024. doi: 10.1128/jb.122.3.1017-1024.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Fried H. M., Warner J. R. Cloning of yeast gene for trichodermin resistance and ribosomal protein L3. Proc Natl Acad Sci U S A. 1981 Jan;78(1):238–242. doi: 10.1073/pnas.78.1.238. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. 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]
  20. Grenson M., Dubois E., Piotrowska M., Drillien R., Aigle M. Ammonia assimilation in Saccharomyces cerevisiae as mediated by the two glutamate dehydrogenases. Evidence for the gdhA locus being a structural gene for the NADP-dependent glutamate dehydrogenase. Mol Gen Genet. 1974;128(1):73–85. doi: 10.1007/BF00267295. [DOI] [PubMed] [Google Scholar]
  21. Grenson M., Hou C. Ammonia inhibition of the general amino acid permease and its suppression in NADPH-specific glutamate dehydrogenaseless mutants of saccharomyces cerevisiae. Biochem Biophys Res Commun. 1972 Aug 21;48(4):749–756. doi: 10.1016/0006-291x(72)90670-5. [DOI] [PubMed] [Google Scholar]
  22. 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. doi: 10.1016/0092-8674(83)90309-4. [DOI] [PubMed] [Google Scholar]
  23. Hinnebusch A. G. Mechanisms of gene regulation in the general control of amino acid biosynthesis in Saccharomyces cerevisiae. Microbiol Rev. 1988 Jun;52(2):248–273. doi: 10.1128/mr.52.2.248-273.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Ito H., Fukuda Y., Murata K., Kimura A. Transformation of intact yeast cells treated with alkali cations. J Bacteriol. 1983 Jan;153(1):163–168. doi: 10.1128/jb.153.1.163-168.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. 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]
  26. Jauniaux J. C., Vandenbol M., Vissers S., Broman K., Grenson M. Nitrogen catabolite regulation of proline permease in Saccharomyces cerevisiae. Cloning of the PUT4 gene and study of PUT4 RNA levels in wild-type and mutant strains. Eur J Biochem. 1987 May 4;164(3):601–606. doi: 10.1111/j.1432-1033.1987.tb11169.x. [DOI] [PubMed] [Google Scholar]
  27. Krzywicki K. A., Brandriss M. C. Primary structure of the nuclear PUT2 gene involved in the mitochondrial pathway for proline utilization in Saccharomyces cerevisiae. Mol Cell Biol. 1984 Dec;4(12):2837–2842. doi: 10.1128/mcb.4.12.2837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Ljungdahl P. O., Gimeno C. J., Styles C. A., Fink G. R. SHR3: a novel component of the secretory pathway specifically required for localization of amino acid permeases in yeast. Cell. 1992 Oct 30;71(3):463–478. doi: 10.1016/0092-8674(92)90515-e. [DOI] [PubMed] [Google Scholar]
  29. Miller S. M., Magasanik B. Role of the complex upstream region of the GDH2 gene in nitrogen regulation of the NAD-linked glutamate dehydrogenase in Saccharomyces cerevisiae. Mol Cell Biol. 1991 Dec;11(12):6229–6247. doi: 10.1128/mcb.11.12.6229. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. 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]
  31. 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]
  32. Omichinski J. G., Clore G. M., Schaad O., Felsenfeld G., Trainor C., Appella E., Stahl S. J., Gronenborn A. M. NMR structure of a specific DNA complex of Zn-containing DNA binding domain of GATA-1. Science. 1993 Jul 23;261(5120):438–446. doi: 10.1126/science.8332909. [DOI] [PubMed] [Google Scholar]
  33. 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]
  34. 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]
  35. 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]
  36. Siddiqui A. H., Brandriss M. C. A regulatory region responsible for proline-specific induction of the yeast PUT2 gene is adjacent to its TATA box. Mol Cell Biol. 1988 Nov;8(11):4634–4641. doi: 10.1128/mcb.8.11.4634. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Smith M. M., Andrésson O. S. DNA sequences of yeast H3 and H4 histone genes from two non-allelic gene sets encode identical H3 and H4 proteins. J Mol Biol. 1983 Sep 25;169(3):663–690. doi: 10.1016/s0022-2836(83)80164-8. [DOI] [PubMed] [Google Scholar]
  38. Spormann D. O., Heim J., Wolf D. H. Carboxypeptidase yscS: gene structure and function of the vacuolar enzyme. Eur J Biochem. 1991 Apr 23;197(2):399–405. doi: 10.1111/j.1432-1033.1991.tb15924.x. [DOI] [PubMed] [Google Scholar]
  39. Tsai S. F., Strauss E., Orkin S. H. Functional analysis and in vivo footprinting implicate the erythroid transcription factor GATA-1 as a positive regulator of its own promoter. Genes Dev. 1991 Jun;5(6):919–931. doi: 10.1101/gad.5.6.919. [DOI] [PubMed] [Google Scholar]
  40. Turoscy V., Cooper T. G. Ureidosuccinate is transported by the allantoate transport system in Saccharomyces cerevisiae. J Bacteriol. 1987 Jun;169(6):2598–2600. doi: 10.1128/jb.169.6.2598-2600.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Vandenbol M., Jauniaux J. C., Grenson M. Nucleotide sequence of the Saccharomyces cerevisiae PUT4 proline-permease-encoding gene: similarities between CAN1, HIP1 and PUT4 permeases. Gene. 1989 Nov 15;83(1):153–159. doi: 10.1016/0378-1119(89)90413-7. [DOI] [PubMed] [Google Scholar]
  42. Wang S. S., Brandriss M. C. Proline utilization in Saccharomyces cerevisiae: sequence, regulation, and mitochondrial localization of the PUT1 gene product. Mol Cell Biol. 1987 Dec;7(12):4431–4440. doi: 10.1128/mcb.7.12.4431. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Wiame J. M., Grenson M., Arst H. N., Jr Nitrogen catabolite repression in yeasts and filamentous fungi. Adv Microb Physiol. 1985;26:1–88. doi: 10.1016/s0065-2911(08)60394-x. [DOI] [PubMed] [Google Scholar]
  44. Wickerham L. J. A Critical Evaluation of the Nitrogen Assimilation Tests Commonly Used in the Classification of Yeasts. J Bacteriol. 1946 Sep;52(3):293–301. [PMC free article] [PubMed] [Google Scholar]
  45. Wickner R. B. [URE3] as an altered URE2 protein: evidence for a prion analog in Saccharomyces cerevisiae. Science. 1994 Apr 22;264(5158):566–569. doi: 10.1126/science.7909170. [DOI] [PubMed] [Google Scholar]
  46. 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]
  47. 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]
  48. 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]
  49. 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]
  50. 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]
  51. Zon L. I., Youssoufian H., Mather C., Lodish H. F., Orkin S. H. Activation of the erythropoietin receptor promoter by transcription factor GATA-1. Proc Natl Acad Sci U S A. 1991 Dec 1;88(23):10638–10641. doi: 10.1073/pnas.88.23.10638. [DOI] [PMC free article] [PubMed] [Google Scholar]

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