Home LiteratureArticle Details
PMID: 10559172 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Synergistic operation of the CAR2 (Ornithine transaminase) promoter elements in Saccharomyces cerevisiae.

Journal of bacteriology ·Vol. 181 ·No. 22 ·1999-11-00 ·Pages 7052-64

Park HD, Scott S, Rai R, Dorrington R, Cooper TG

Abstract

Dal82p binds to the UIS(ALL) sites of allophanate-induced genes of the allantoin-degradative pathway and functions synergistically with the GATA family Gln3p and Gat1p transcriptional activators that are responsible for nitrogen catabolite repression-sensitive gene expression. CAR2, which encodes the arginine-degradative enzyme ornithine transaminase, is not nitrogen catabolite repression sensitive, but its expression can be modestly induced by the allantoin pathway inducer. The dominant activators of CAR2 transcription have been thought to be the ArgR and Mcm1 factors, which mediate arginine-dependent induction. These observations prompted us to investigate the structure of the CAR2 promoter with the objectives of determining whether other transcription factors were required for CAR2 expression and, if so, of ascertaining their relative contributions to CAR2's expression and control. We show that Rap1p binds upstream of CAR2 and plays a central role in its induced expression irrespective of whether the inducer is arginine or the allantoin pathway inducer analogue oxalurate (OXLU). Our data also explain the early report that ornithine transaminase production is induced when cells are grown with urea. OXLU induction derives from the Dal82p binding site, which is immediately downstream of the Rap1p site, and Dal82p functions synergistically with Rap1p. This synergism is unlike all other known instances of Dal82p synergism, namely, that with the GATA family transcription activators Gln3p and Gat1p, which occurs only in the presence of an inducer. The observations reported suggest that CAR2 gene expression results from strong constitutive transcriptional activation mediated by Rap1p and Dal82p being balanced by the down regulation of an equally strong transcriptional repressor, Ume6p. This balance is then tipped in the direction of expression by the presence of the inducer. The formal structure of the CAR2 promoter and its operation closely follow the model proposed for CAR1.

MeSH Terms
5' Untranslated Regions/genetics Base Sequence Binding Sites DNA-Binding Proteins/metabolism Fungal Proteins/metabolism Gene Deletion Molecular Sequence Data Ornithine-Oxo-Acid Transaminase/genetics,metabolism Plasmids/genetics Promoter Regions, Genetic Saccharomyces cerevisiae/enzymology,genetics Saccharomyces cerevisiae Proteins Shelterin Complex Telomere-Binding Proteins Trans-Activators Transcription Factors/metabolism Transcriptional Activation Transformation, Genetic beta-Galactosidase/metabolism
Chemicals
5' Untranslated Regions DAL82 protein, S cerevisiae DNA-Binding Proteins Fungal Proteins RAP1 protein, S cerevisiae Saccharomyces cerevisiae Proteins Shelterin Complex Telomere-Binding Proteins Trans-Activators Transcription Factors Ornithine-Oxo-Acid Transaminase beta-Galactosidase
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Park H D
Department of Food Science and Technology, Kyungpook National University, Taegu 702-701, Korea.
Scott S
Rai R
Dorrington R
Cooper T G
References (56)
56 references, click to expand
  1. Functional analysis of the regulatory region adjacent to the cargB gene of Saccharomyces cerevisiae. Nucleotide sequence, gene fusion experiments and cis-dominant regulatory mutation analysis.
    Eur J Biochem. 1987 Nov 16;169(1):193-200 PMID: 2824201
  2. L-Ornithine transaminase synthesis in Saccharomyces cerevisiae: regulation by inducer exclusion.
    Mol Gen Genet. 1979 Jul 24;174(3):225-32 PMID: 384165
  3. The induction of arginase in Saccharomyces cerevisiae.
    J Biol Chem. 1973 Sep 10;248(17):6197-202 PMID: 4580052
  4. Purification and cloning of a DNA binding protein from yeast that binds to both silencer and activator elements.
    Cell. 1987 Dec 4;51(5):721-32 PMID: 3315231
  5. 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):7186-95 PMID: 1938916
  6. Participation of RAP1 protein in expression of the Saccharomyces cerevisiae arginase (CAR1) gene.
    J Bacteriol. 1993 Feb;175(4):941-51 PMID: 8432717
  7. UME6 is a key regulator of nitrogen repression and meiotic development.
    Genes Dev. 1994 Apr 1;8(7):796-810 PMID: 7926768
  8. Nucleotide sequence of the ARGRII regulatory gene and amino acid sequence homologies between ARGRII PPRI and GAL4 regulatory proteins.
    Eur J Biochem. 1986 May 15;157(1):77-81 PMID: 3709534
  9. Genetic evidence for a role for MCM1 in the regulation of arginine metabolism in Saccharomyces cerevisiae.
    Mol Cell Biol. 1993 Apr;13(4):2586-92 PMID: 8455631
  10. Enzyme repression in the arginine pathway of Saccharomyces cerevisiae.
    Antonie Van Leeuwenhoek. 1969;35(2):215-26 PMID: 5310448
  11. 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 PMID: 3295874
  12. Characterisation of the DNA binding domain of the yeast RAP1 protein.
    Nucleic Acids Res. 1990 May 11;18(9):2617-23 PMID: 2187178
  13. The derepression of arginase and of ornithine transaminase in nitrogen-starved baker's yeast.
    Biochim Biophys Acta. 1968 Mar 11;156(2):440-3 PMID: 5641927
  14. THE PATHWAY OF ARGININE BREAKDOWN IN SACCHAROMYCES CEREVISIAE.
    Biochim Biophys Acta. 1964 Dec 9;93:650-2 PMID: 14263163
  15. 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):2120-4 PMID: 3281162
  16. On the nature of argR mutations is Saccharomyces cerevisiae.
    Eur J Biochem. 1974 Mar 15;43(1):87-92 PMID: 4365239
  17. Multiple positive and negative cis-acting elements mediate induced arginase (CAR1) gene expression in Saccharomyces cerevisiae.
    Mol Cell Biol. 1990 Oct;10(10):5087-97 PMID: 2204806
  18. Point mutation generates constitutive expression of an inducible eukaryotic gene.
    Proc Natl Acad Sci U S A. 1985 Feb;82(3):643-7 PMID: 2983306
  19. Mutations affecting the repressibility of arginine biosynthetic enzymes in Saccharomyces cerevisiae.
    Eur J Biochem. 1970 Jan;12(1):31-9 PMID: 5434281
  20. UME6, a negative regulator of meiosis in Saccharomyces cerevisiae, contains a C-terminal Zn2Cys6 binuclear cluster that binds the URS1 DNA sequence in a zinc-dependent manner.
    Protein Sci. 1995 Sep;4(9):1832-43 PMID: 8528081
  21. Sequence of a yeast DNA fragment containing a chromosomal replicator and the TRP1 gene.
    Gene. 1980 Jul;10(2):157-66 PMID: 6248420
  22. The DAL7 promoter consists of multiple elements that cooperatively mediate regulation of the gene's expression.
    Mol Cell Biol. 1989 Aug;9(8):3231-43 PMID: 2552287
  23. UASNTR functioning in combination with other UAS elements underlies exceptional patterns of nitrogen regulation in Saccharomyces cerevisiae.
    Yeast. 1995 Mar;11(3):247-60 PMID: 7785325
  24. DNA sequence analysis with a modified bacteriophage T7 DNA polymerase.
    Proc Natl Acad Sci U S A. 1987 Jul;84(14):4767-71 PMID: 3474623
  25. Tripartite structure of the Saccharomyces cerevisiae arginase (CAR1) gene inducer-responsive upstream activation sequence.
    J Bacteriol. 1992 Nov;174(21):6831-9 PMID: 1400233
  26. Two differentially regulated mRNAs with different 5' ends encode secreted with intracellular forms of yeast invertase.
    Cell. 1982 Jan;28(1):145-54 PMID: 7039847
  27. 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):5393-9 PMID: 2120676
  28. Fusion of Escherichia coli lacZ to the cytochrome c gene of Saccharomyces cerevisiae.
    Proc Natl Acad Sci U S A. 1981 Apr;78(4):2199-203 PMID: 6264467
  29. Determination of the DNA-binding sequences of ARGR proteins to arginine anabolic and catabolic promoters.
    Mol Cell Biol. 1991 May;11(5):2852-63 PMID: 2017180
  30. Functional analysis of ARGRI and ARGRIII regulatory proteins involved in the regulation of arginine metabolism in Saccharomyces cerevisiae.
    Mol Gen Genet. 1990 Jul;222(2-3):192-200 PMID: 2274024
  31. The minimal transactivation region of Saccharomyces cerevisiae Gln3p is localized to 13 amino acids.
    J Bacteriol. 1997 Dec;179(24):7644-52 PMID: 9401021
  32. Characterization of two genes, ARGRI and ARGRIII required for specific regulation of arginine metabolism in yeast.
    Mol Gen Genet. 1987 Apr;207(1):142-8 PMID: 3298999
  33. Isolation and characterization of the yeast ARGRII gene involved in regulating both anabolism and catabolism of arginine.
    Mol Gen Genet. 1985;198(2):283-9 PMID: 3884975
  34. Combinatorial regulation of the Saccharomyces cerevisiae CAR1 (arginase) promoter in response to multiple environmental signals.
    Mol Cell Biol. 1996 Oct;16(10):5876-87 PMID: 8816501
  35. Pleiotropic control of five eucaryotic genes by multiple regulatory elements.
    J Bacteriol. 1982 Sep;151(3):1237-46 PMID: 7050082
  36. The DAL82 protein of Saccharomyces cerevisiae binds to the DAL upstream induction sequence (UIS).
    Nucleic Acids Res. 1993 Aug 11;21(16):3777-84 PMID: 8367295
  37. 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):1161-6 PMID: 1990272
  38. Participation of ABF-1 protein in expression of the Saccharomyces cerevisiae CAR1 gene.
    J Bacteriol. 1991 Oct;173(20):6332-8 PMID: 1917865
  39. Heme regulates transcription of the CYC1 gene of S. cerevisiae via an upstream activation site.
    Cell. 1983 Apr;32(4):1279-86 PMID: 6301690
  40. Overlapping positive and negative GATA factor binding sites mediate inducible DAL7 gene expression in Saccharomyces cerevisiae.
    J Biol Chem. 1999 Sep 24;274(39):28026-34 PMID: 10488154
  41. Isolation of the CAR1 gene from Saccharomyces cerevisiae and analysis of its expression.
    Mol Cell Biol. 1982 Dec;2(12):1514-23 PMID: 14582193
  42. 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):3884-95 PMID: 2115115
  43. 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):1909-15 PMID: 1579492
  44. Calcium-dependent bacteriophage DNA infection.
    J Mol Biol. 1970 Oct 14;53(1):159-62 PMID: 4922220
  45. Involvement of the silencer and UAS binding protein RAP1 in regulation of telomere length.
    Science. 1990 Oct 26;250(4980):549-53 PMID: 2237406
  46. Yeast promoters and lacZ fusions designed to study expression of cloned genes in yeast.
    Methods Enzymol. 1983;101:181-91 PMID: 6310321
  47. L-ornithine transaminase synthesis in Saccharomyces cerevisiae: Induction by allophanate, intermediate and inducer of the urea degradative pathway adds to arginine induction.
    Curr Genet. 1981 Sep;4(1):69-72 PMID: 24185870
  48. Regulation of arginine metabolism in Saccharomyces cerevisiae: expression of the three ARGR regulatory genes and cellular localization of their products.
    Gene. 1987;55(2-3):277-85 PMID: 3311884
  49. Molecular events associated with induction of arginase in Saccharomyces cerevisiae.
    J Bacteriol. 1977 Jul;131(1):163-73 PMID: 326758
  50. Further definition of the sequence and position requirements of the arginine control element that mediates repression and induction by arginine in Saccharomyces cerevisiae.
    Yeast. 1995 Nov;11(14):1367-80 PMID: 8585320
  51. Characterization of the DNA target site for the yeast ARGR regulatory complex, a sequence able to mediate repression or induction by arginine.
    Mol Cell Biol. 1992 Jan;12(1):68-81 PMID: 1729616
  52. Cross regulation of four GATA factors that control nitrogen catabolic gene expression in Saccharomyces cerevisiae.
    J Bacteriol. 1997 Jun;179(11):3416-29 PMID: 9171383
  53. RAP1 protein activates and silences transcription of mating-type genes in yeast.
    Genes Dev. 1991 Apr;5(4):616-28 PMID: 2010087
  54. Similarity between the transcriptional silencer binding proteins ABF1 and RAP1.
    Science. 1989 Nov 24;246(4933):1034-8 PMID: 2511628
  55. Induction and repression of arginase and ornithine transaminase in baker's yeast.
    Antonie Van Leeuwenhoek. 1970;36(1):1-19 PMID: 4912187
  56. Transformation of intact yeast cells treated with alkali cations.
    J Bacteriol. 1983 Jan;153(1):163-8 PMID: 6336730
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
1999-11-00
Pages
7052-64
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC94181
Subset
IM
Grants
NIGMS NIH HHS · R01 GM035642 · United States
NIGMS NIH HHS · GM-35642 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]