Abstract
The glucokinase gene GLK1 of the yeast Saccharomyces cerevisiae is transcriptionally regulated in response to the carbon source of the growth medium. Northern-blot analysis shows that the GLK1 gene is expressed at a basal level in the presence of glucose, de-repressed more than 6-fold under conditions of sugar limitation and more than 25-fold under conditions of ethanol induction. lacZ fusions of the GLK1 gene promoter were constructed and a deletion analysis was performed in order to identify the cis-acting regulatory elements of the promoter that controls GLK1 gene expression. First, the expression seemed to be mediated mainly by one GCR1 and three stress-responsive element (STRE) activating elements. Secondly, an ethanol repression autoregulation (ERA)/twelve-fold TA repeat (TAB) repressor element was identified within the promoter region of the GLK1 gene. A specific and differential protein binding to the STRE was observed with extracts from de-repressed and repressed cells. No differential binding to the GCR1 or ERA/TAB elements was observed with extracts from de-repressed and repressed cells, but, in both cases, the binding was competed for by an excess of the unlabelled GLK1(GCR1) and GLK1(ERA) sequence. The transcription factors Msn2 and Msn4, which bind to the GLK1 upstream region through the STRE, contribute to inductive activation. The transcription factor Gcr1, which binds through the GCR1 element, contributes to constitutive activation. In order to achieve the severe glucose repression of GLK1, constitutive repressor factors acting through the ERA/TAB element must counteract constitutive activation generated by Gcr1 binding to the GCR1 element. Full expression of the GLK1 gene is produced by inductive activation of three STRE when Msn2 and Msn4 proteins are translocated to the nucleus by covalent modification. The combinatorial effect of the entire region leads to the regulated transcription of GLK1, i.e., silent in media with glucose and other preferred carbon sources, such as fructose or mannose, and increased levels of expression upon glucose depletion.
MeSH Terms
Base Sequence
Binding Sites
Carbon/metabolism
DNA/genetics,metabolism
DNA-Binding Proteins/metabolism
Ethanol/metabolism,pharmacology
Fungal Proteins/metabolism
Gene Expression Regulation, Fungal/drug effects
Glucokinase/genetics
Glucose/metabolism
Promoter Regions, Genetic/genetics
RNA, Messenger/genetics,metabolism
Repressor Proteins/metabolism
Response Elements/genetics
Saccharomyces cerevisiae/drug effects,enzymology,genetics,metabolism
Saccharomyces cerevisiae Proteins
Sequence Deletion
Transcription Factors/metabolism
Chemicals
DNA-Binding Proteins
Fungal Proteins
MSN2 protein, S cerevisiae
MSN4 protein, S cerevisiae
RNA, Messenger
Repressor Proteins
Saccharomyces cerevisiae Proteins
Transcription Factors
Ethanol
Carbon
DNA
Glucokinase
Glucose
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Herrero P
Departamento de Bioqu approximately ímica y Biolog approximately ía Molecular, Instituto Universitario de Biotecnolog approximately ía de Asturias, Universidad de Oviedo, 33006 Oviedo, Spain.
Flores L
de la Cera T
Moreno F
References (29)
29 references, click to expand
-
Multiple effects of trehalose on protein folding in vitro and in vivo.
Mol Cell. 1998 Apr;1(5):639-48
PMID: 9660948
-
GCR1-dependent transcriptional activation of yeast retrotransposon Ty2-917.
Yeast. 1997 Aug;13(10):917-30
PMID: 9271107
-
Control of glycolytic gene expression in the budding yeast (Saccharomyces cerevisiae).
Curr Genet. 1995 Dec;29(1):1-9
PMID: 8595651
-
Stress-induced transcriptional activation.
Microbiol Rev. 1995 Sep;59(3):506-31
PMID: 7565416
-
The role of Gcr1p in the transcriptional activation of glycolytic genes in yeast Saccharomyces cerevisiae.
Genetics. 1997 Oct;147(2):521-32
PMID: 9335590
-
Preservation of membranes in anhydrobiotic organisms: the role of trehalose.
Science. 1984 Feb 17;223(4637):701-3
PMID: 17841031
-
The Saccharomyces cerevisiae HSP12 gene is activated by the high-osmolarity glycerol pathway and negatively regulated by protein kinase A.
Mol Cell Biol. 1995 Nov;15(11):6232-45
PMID: 7565776
-
A Saccharomyces cerevisiae UAS element controlled by protein kinase A activates transcription in response to a variety of stress conditions.
EMBO J. 1993 May;12(5):1997-2003
PMID: 8387917
-
Nuclear localization of the C2H2 zinc finger protein Msn2p is regulated by stress and protein kinase A activity.
Genes Dev. 1998 Feb 15;12(4):586-97
PMID: 9472026
-
The role of trehalose synthesis for the acquisition of thermotolerance in yeast. II. Physiological concentrations of trehalose increase the thermal stability of proteins in vitro.
Eur J Biochem. 1994 Jan 15;219(1-2):187-93
PMID: 8306985
-
Effects of different carbon fluxes on G1 phase duration, cyclin expression, and reserve carbohydrate metabolism in Saccharomyces cerevisiae.
J Bacteriol. 1997 Nov;179(21):6560-5
PMID: 9352900
-
The Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress response element (STRE).
EMBO J. 1996 May 1;15(9):2227-35
PMID: 8641288
-
DNA sequencing with chain-terminating inhibitors.
Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463-7
PMID: 271968
-
Characterization of TPI gene expression in isogeneic wild-type and gcr1-deletion mutant strains of Saccharomyces cerevisiae.
Nucleic Acids Res. 1990 Dec 11;18(23):7099-107
PMID: 2263469
-
The essential function of yeast protein disulfide isomerase does not reside in its isomerase activity.
Cell. 1993 Sep 10;74(5):899-908
PMID: 8374956
-
Identification and characterisation of two transcriptional repressor elements within the coding sequence of the Saccharomyces cerevisiae HXK2 gene.
Nucleic Acids Res. 1996 May 15;24(10):1822-8
PMID: 8657561
-
Function of trehalose and glycogen in cell cycle progression and cell viability in Saccharomyces cerevisiae.
J Bacteriol. 1999 Jan;181(2):396-400
PMID: 9882651
-
Glycolytic gene expression in Saccharomyces cerevisiae: nucleotide sequence of GCR1, null mutants, and evidence for expression.
Mol Cell Biol. 1986 Nov;6(11):3774-84
PMID: 3025612
-
Determination of the sequence of the yeast YCL313 gene localized on chromosome III. Homology with the protein disulfide isomerase (PDI gene product) of other organisms.
Yeast. 1991 Feb;7(2):185-93
PMID: 2063627
-
Msn2p, a zinc finger DNA-binding protein, is the transcriptional activator of the multistress response in Saccharomyces cerevisiae.
Proc Natl Acad Sci U S A. 1996 Jun 11;93(12):5777-82
PMID: 8650168
-
The ICL1 gene from Saccharomyces cerevisiae.
Eur J Biochem. 1992 Mar 15;204(3):983-90
PMID: 1551398
-
Exploring the metabolic and genetic control of gene expression on a genomic scale.
Science. 1997 Oct 24;278(5338):680-6
PMID: 9381177
-
Msn2p and Msn4p control a large number of genes induced at the diauxic transition which are repressed by cyclic AMP in Saccharomyces cerevisiae.
J Bacteriol. 1998 Mar;180(5):1044-52
PMID: 9495741
-
Yeast shuttle and integrative vectors with multiple cloning sites suitable for construction of lacZ fusions.
Gene. 1986;45(3):299-310
PMID: 3026915
-
Changes in gene expression in the Ras/adenylate cyclase system of Saccharomyces cerevisiae: correlation with cAMP levels and growth arrest.
Mol Biol Cell. 1993 Jul;4(7):757-65
PMID: 8400461
-
ERA, a novel cis-acting element required for autoregulation and ethanol repression of PDC1 transcription in Saccharomyces cerevisiae.
Mol Microbiol. 1996 Aug;21(3):621-32
PMID: 8866484
-
Transcriptional regulation of the Saccharomyces cerevisiae HXK1, HXK2 and GLK1 genes.
Yeast. 1995 Feb;11(2):137-44
PMID: 7732723
-
The gcr (glycolysis regulation) mutation of Saccharomyces cerevisiae.
J Biol Chem. 1981 Dec 25;256(24):13074-8
PMID: 7031056
-
Changes in the concentration of cAMP, fructose 2,6-bisphosphate and related metabolites and enzymes in Saccharomyces cerevisiae during growth on glucose.
Eur J Biochem. 1987 Apr 15;164(2):369-73
PMID: 3032616