Glucose repression in Saccharomyces cerevisiae

Glucose is the primary source of energy for the budding yeast Saccharomyces cerevisiae. Although yeast cells can utilize a wide range of carbon sources, presence of glucose suppresses molecular activities involved in the use of alternate carbon sources as well as it represses respiration and gluconeogenesis. This dominant effect of glucose on yeast carbon metabolism is coordinated by several signaling and metabolic interactions that mainly regulate transcriptional activity but are also effective at post-transcriptional and post-translational levels. This review describes effects of glucose repression on yeast carbon metabolism with a focus on roles of the Snf3/Rgt2 glucose-sensing pathway and Snf1 signal transduction in establishment and relief of glucose repression.

[1]  H J Schüller,et al.  Transcriptional control of the yeast acetyl‐CoA synthetase gene, ACS1, by the positive regulators CAT8 and ADR1 and the pleiotropic repressor UME6 , 1997, Molecular microbiology.

[2]  Mark Johnston,et al.  Glucose sensing and signaling by two glucose receptors in the yeast Saccharomyces cerevisiae , 1998, The EMBO journal.

[3]  S. Ozcan.  Two different signals regulate repression and induction of gene expression by glucose. , 2002, The Journal of biological chemistry.

[4]  G. L. Law,et al.  A Poised Initiation Complex Is Activated by SNF1*♦ , 2007, Journal of Biological Chemistry.

[5]  R. McCartney,et al.  Regulation of Snf1 Kinase , 2001, The Journal of Biological Chemistry.

[6]  E. Rubenstein,et al.  Snf1 kinase complexes with different beta subunits display stress-dependent preferences for the three Snf1-activating kinases , 2005, Current Genetics.

[7]  John R Yates,et al.  Reconstruction of the yeast Snf1 kinase regulatory network reveals its role as a global energy regulator , 2009, Molecular systems biology.

[8]  I. Borodina,et al.  Application of synthetic biology for production of chemicals in yeast Saccharomyces cerevisiae. , 2014, FEMS yeast research.

[9]  David Carling,et al.  Activation of yeast Snf1 and mammalian AMP-activated protein kinase by upstream kinases , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[10]  M. Carlson,et al.  SNF1/AMPK pathways in yeast. , 2008, Frontiers in bioscience : a journal and virtual library.

[11]  M. Gerstein,et al.  Global analysis of protein phosphorylation in yeast , 2005, Nature.

[12]  M. Carlson,et al.  Repression by SSN6-TUP1 is directed by MIG1, a repressor/activator protein. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[13]  Johan M Thevelein,et al.  Glucose-induced posttranslational activation of protein phosphatases PP2A and PP1 in yeast , 2012, Cell Research.

[14]  D. Hardie,et al.  Elm1p Is One of Three Upstream Kinases for the Saccharomyces cerevisiae SNF1 Complex , 2003, Current Biology.

[15]  H. Ruis,et al.  Nutritional Control of Nucleocytoplasmic Localization of cAMP-dependent Protein Kinase Catalytic and Regulatory Subunits in Saccharomyces cerevisiae * , 2000, The Journal of Biological Chemistry.

[16]  Hans-Joachim Schüller,et al.  Transcriptional control of nonfermentative metabolism in the yeast Saccharomyces cerevisiae , 2003, Current Genetics.

[17]  K. M. Dombek,et al.  The Reg1-interacting Proteins, Bmh1, Bmh2, Ssb1, and Ssb2, Have Roles in Maintaining Glucose Repression in Saccharomyces cerevisiae* , 2004, Journal of Biological Chemistry.

[18]  E. Young,et al.  Coupling mRNA Synthesis and Decay , 2014, Molecular and Cellular Biology.

[19]  Mark Johnston,et al.  Glucose sensing and signaling in Saccharomyces cerevisiae through the Rgt2 glucose sensor and casein kinase I. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[20]  M. Carlson,et al.  Glucose regulates protein interactions within the yeast SNF1 protein kinase complex. , 1996, Genes & development.

[21]  L. Verdone,et al.  Common chromatin architecture, common chromatin remodeling, and common transcription kinetics of Adr1-dependent genes in Saccharomyces cerevisiae. , 2004, Biochemistry.

[22]  R. McCartney,et al.  Isolation of Mutations in the Catalytic Domain of the Snf1 Kinase That Render Its Activity Independent of the Snf4 Subunit , 2003, Eukaryotic Cell.

[23]  K. Entian,et al.  Glucose derepression of gluconeogenic enzymes in Saccharomyces cerevisiae correlates with phosphorylation of the gene activator Cat8p , 1997, Molecular and cellular biology.

[24]  Keith Tyo,et al.  Prospects of yeast systems biology for human health: integrating lipid, protein and energy metabolism. , 2010, FEMS yeast research.

[25]  K. Entian,et al.  CAT8, a new zinc cluster-encoding gene necessary for derepression of gluconeogenic enzymes in the yeast Saccharomyces cerevisiae , 1995, Molecular and cellular biology.

[26]  Mark Johnston,et al.  Regulatory Network Connecting Two Glucose Signal Transduction Pathways in Saccharomyces cerevisiae , 2004, Eukaryotic Cell.

[27]  M. Grunstein,et al.  Hyperacetylation of chromatin at the ADH2 promoter allows Adr1 to bind in repressed conditions , 2002, The EMBO journal.

[28]  M. Carlson,et al.  Pak1 Protein Kinase Regulates Activation and Nuclear Localization of Snf1-Gal83 Protein Kinase , 2004, Molecular and Cellular Biology.

[29]  Timothy A. J. Haystead,et al.  Regulatory Interactions between the Reg1-Glc7 Protein Phosphatase and the Snf1 Protein Kinase , 2000, Molecular and Cellular Biology.

[30]  M. Kuo,et al.  Snf1p Regulates Gcn5p Transcriptional Activity by Antagonizing Spt3p , 2010, Genetics.

[31]  P. Brown,et al.  Characterization of three related glucose repressors and genes they regulate in Saccharomyces cerevisiae. , 1998, Genetics.

[32]  Jeong-Ho Kim,et al.  Role of casein kinase 1 in the glucose sensor-mediated signaling pathway in yeast , 2010, BMC Cell Biology.

[33]  A. Kastaniotis,et al.  The biochemistry of peroxisomal β-oxidation in the yeast Saccharomyces cerevisiae , 2003 .

[34]  R. Trumbly,et al.  The yeast GLC7 gene required for glycogen accumulation encodes a type 1 protein phosphatase. , 1991, The Journal of biological chemistry.

[35]  E. Young,et al.  Snf1/AMPK regulates Gcn5 occupancy, H3 acetylation and chromatin remodelling at S. cerevisiae ADY2 promoter. , 2012, Biochimica et biophysica acta.

[36]  Rafael Peláez,et al.  Functional domains of yeast hexokinase 2 , 2010, The Biochemical journal.

[37]  Tong Ihn Lee,et al.  Combined Global Localization Analysis and Transcriptome Data Identify Genes That Are Directly Coregulated by Adr1 and Cat8 , 2005, Molecular and Cellular Biology.

[38]  Nils J Faergeman,et al.  Glucose- and nitrogen sensing and regulatory mechanisms in Saccharomyces cerevisiae. , 2014, FEMS yeast research.

[39]  Simon C Watkins,et al.  Std1 and Mth1 Proteins Interact with the Glucose Sensors To Control Glucose-Regulated Gene Expression in Saccharomyces cerevisiae , 1999, Molecular and Cellular Biology.

[40]  F. Robert,et al.  Transcriptional regulation of nonfermentable carbon utilization in budding yeast. , 2010, FEMS yeast research.

[41]  Noam Slonim,et al.  Glucose regulates transcription in yeast through a network of signaling pathways , 2009, Molecular systems biology.

[42]  M. Carlson,et al.  A regulatory shortcut between the Snf1 protein kinase and RNA polymerase II holoenzyme. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[43]  P. Herrero,et al.  Tpk3 and Snf1 protein kinases regulate Rgt1 association with Saccharomyces cerevisiae HXK2 promoter , 2006, Nucleic acids research.

[44]  E. Young,et al.  Snf1 Dependence of Peroxisomal Gene Expression Is Mediated by Adr1* , 2010, The Journal of Biological Chemistry.

[45]  Rafael Peláez,et al.  Phosphorylation of Yeast Hexokinase 2 Regulates Its Nucleocytoplasmic Shuttling* , 2012, The Journal of Biological Chemistry.

[46]  A. Kastaniotis,et al.  The biochemistry of peroxisomal beta-oxidation in the yeast Saccharomyces cerevisiae. , 2003, FEMS microbiology reviews.

[47]  Karen M. Arndt,et al.  Access Denied: Snf1 Activation Loop Phosphorylation Is Controlled by Availability of the Phosphorylated Threonine 210 to the PP1 Phosphatase* , 2008, Journal of Biological Chemistry.

[48]  R. McCartney,et al.  Yeast Pak1 Kinase Associates with and Activates Snf1 , 2003, Molecular and Cellular Biology.

[49]  Jens Nielsen,et al.  Improving Production of Malonyl Coenzyme A-Derived Metabolites by Abolishing Snf1-Dependent Regulation of Acc1 , 2014, mBio.

[50]  Verena Siewers,et al.  Editorial: Yeast synthetic biology: new tools to unlock cellular function. , 2015, FEMS yeast research.

[51]  T. Kalashnikova,et al.  Regulation and Recognition of SCFGrr1 Targets in the Glucose and Amino Acid Signaling Pathways , 2004, Molecular and Cellular Biology.

[52]  J. Nielsen,et al.  The β‐subunits of the Snf1 kinase in Saccharomyces cerevisiae, Gal83 and Sip2, but not Sip1, are redundant in glucose derepression and regulation of sterol biosynthesis , 2010, Molecular microbiology.

[53]  Chao Zhang,et al.  The AMP-activated Protein Kinase Snf 1 Regulates Transcription Factor Binding , RNA Polymerase II Activity , and mRNA Stability of Glucose-repressed Genes in Saccharomyces cerevisiae * , 2012 .

[54]  Curt Wittenberg,et al.  Grr1-dependent inactivation of Mth1 mediates glucose-induced dissociation of Rgt1 from HXT gene promoters. , 2003, Molecular biology of the cell.

[55]  Karen M. Arndt,et al.  Snf 1 Activation Loop Phosphorylation Is Controlled by Availability of the Phosphorylated Threonine 210 to the PP 1 Phosphatase * , 2007 .

[56]  Pilar Herrero,et al.  Hxk2 Regulates the Phosphorylation State of Mig1 and Therefore Its Nucleocytoplasmic Distribution* , 2007, Journal of Biological Chemistry.

[57]  Jeong-Ho Kim,et al.  Understanding the mechanism of glucose-induced relief of Rgt1-mediated repression in yeast☆ , 2014, FEBS open bio.

[58]  Ruedi Aebersold,et al.  Mapping the interaction of Snf1 with TORC1 in Saccharomyces cerevisiae , 2011, Molecular systems biology.

[59]  Gustav Ammerer,et al.  A dual role for PP1 in shaping the Msn2‐dependent transcriptional response to glucose starvation , 2005, The EMBO journal.

[60]  Filip Rolland,et al.  Glucose-sensing and -signalling mechanisms in yeast. , 2002, FEMS yeast research.

[61]  A. Hinnebusch,et al.  Snf1 Promotes Phosphorylation of the α Subunit of Eukaryotic Translation Initiation Factor 2 by Activating Gcn2 and Inhibiting Phosphatases Glc7 and Sit4 , 2010, Molecular and Cellular Biology.

[62]  J. Piškur,et al.  Molecular Mechanisms in Yeast Carbon Metabolism , 2014, Springer Berlin Heidelberg.

[63]  K. Karhumaa,et al.  Conditions with high intracellular glucose inhibit sensing through glucose sensor Snf3 in Saccharomyces cerevisiae , 2010, Journal of cellular biochemistry.

[64]  Liang Tong,et al.  Crystal structure of the heterotrimer core of Saccharomyces cerevisiae AMPK homologue SNF1 , 2007, Nature.

[65]  M. Carlson,et al.  Glucose-regulated interaction of a regulatory subunit of protein phosphatase 1 with the Snf1 protein kinase in Saccharomyces cerevisiae. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[66]  Chao Zhang,et al.  The AMP-activated Protein Kinase Snf1 Regulates Transcription Factor Binding, RNA Polymerase II Activity, and mRNA Stability of Glucose-repressed Genes in Saccharomyces cerevisiae* , 2012, The Journal of Biological Chemistry.

[67]  David Carling,et al.  ADP Regulates SNF1, the Saccharomyces cerevisiae Homolog of AMP-Activated Protein Kinase , 2011, Cell metabolism.

[68]  J. Gancedo.  Yeast Carbon Catabolite Repression , 1998, Microbiology and Molecular Biology Reviews.

[69]  E. Young,et al.  Snf1 Controls the Activity of Adr1 Through Dephosphorylation of Ser230 , 2009, Genetics.

[70]  M. Carlson,et al.  REG1 binds to protein phosphatase type 1 and regulates glucose repression in Saccharomyces cerevisiae. , 1995, The EMBO journal.

[71]  G. Daum,et al.  Yeast lipid metabolism at a glance. , 2014, FEMS yeast research.

[72]  Jens Nielsen,et al.  Can yeast systems biology contribute to the understanding of human disease? , 2008, Trends in biotechnology.

[73]  Trey Ideker,et al.  Multiple Pathways Are Co-regulated by the Protein Kinase Snf1 and the Transcription Factors Adr1 and Cat8* , 2003, Journal of Biological Chemistry.

[74]  Kyu Hong Cho,et al.  Mth1 regulates the interaction between the Rgt1 repressor and the Ssn6-Tup1 corepressor complex by modulating PKA-dependent phosphorylation of Rgt1 , 2013, Molecular biology of the cell.

[75]  M. Carlson,et al.  Mutational analysis of the Saccharomyces cerevisiae SNF1 protein kinase and evidence for functional interaction with the SNF4 protein , 1989, Molecular and cellular biology.

[76]  M. Johnston,et al.  Two Glucose-sensing Pathways Converge on Rgt1 to Regulate Expression of Glucose Transporter Genes in Saccharomyces cerevisiae* , 2006, Journal of Biological Chemistry.

[77]  J. Pérez-Ortín,et al.  Gene Expression Is Circular: Factors for mRNA Degradation Also Foster mRNA Synthesis , 2013, Cell.

[78]  D. Botstein,et al.  Mutants of yeast defective in sucrose utilization. , 1981, Genetics.

[79]  S. Kendrew,et al.  Two Distinct Nucleosome Alterations Characterize Chromatin Remodeling at the Saccharomyces cerevisiae ADH2Promoter* , 2000, The Journal of Biological Chemistry.

[80]  Yun Chen,et al.  Advances in metabolic pathway and strain engineering paving the way for sustainable production of chemical building blocks. , 2013, Current opinion in biotechnology.

[81]  L. T. Jensen,et al.  Zinc cluster protein Znf1, a novel transcription factor of non-fermentative metabolism in Saccharomyces cerevisiae. , 2015, FEMS yeast research.

[82]  Marija Cvijovic,et al.  Yeast AMP-activated Protein Kinase Monitors Glucose Concentration Changes and Absolute Glucose Levels* , 2014, The Journal of Biological Chemistry.

[83]  J. Nielsen,et al.  Glucose control in Saccharomyces cerevisiae: the role of Mig1 in metabolic functions. , 1998, Microbiology.

[84]  K. Walther,et al.  Adr1 and Cat8 synergistically activate the glucose-regulated alcohol dehydrogenase gene ADH2 of the yeast Saccharomyces cerevisiae. , 2001, Microbiology.

[85]  C. Hollenberg,et al.  Concurrent knock‐out of at least 20 transporter genes is required to block uptake of hexoses in Saccharomyces cerevisiae , 1999, FEBS letters.

[86]  J. Scott,et al.  Yeast SNF1 is functionally related to mammalian AMP-activated protein kinase and regulates acetyl-CoA carboxylase in vivo. , 1994, The Journal of biological chemistry.

[87]  Xueli Zhang,et al.  Yeast synthetic biology for high-value metabolites. , 2014, FEMS yeast research.

[88]  Mark Johnston,et al.  Function and Regulation of Yeast Hexose Transporters , 1999, Microbiology and Molecular Biology Reviews.

[89]  Anton Glieder,et al.  Carbon source dependent promoters in yeasts , 2014, Microbial Cell Factories.

[90]  E. Young,et al.  Snf1 Protein Kinase Regulates Adr1 Binding to Chromatin but Not Transcription Activation* , 2002, The Journal of Biological Chemistry.

[91]  G. L. Law,et al.  Adr1 and Cat8 Mediate Coactivator Recruitment and Chromatin Remodeling at Glucose-Regulated Genes , 2008, PloS one.

[92]  S. Henry,et al.  Inhibition of Acetyl Coenzyme A Carboxylase Activity Restores Expression of the INO1 Gene in a snf1Mutant Strain of Saccharomyces cerevisiae , 2001, Molecular and Cellular Biology.

[93]  Chao Zhang,et al.  A Chemical Genomics Study Identifies Snf1 as a Repressor of GCN4 Translation* , 2008, Journal of Biological Chemistry.

[94]  Hans-Joachim Schüller,et al.  Transcriptional activators Cat8 and Sip4 discriminate between sequence variants of the carbon source-responsive promoter element in the yeast Saccharomyces cerevisiae , 2004, Current Genetics.

[95]  M. Carlson,et al.  Subcellular localization of the Snf1 kinase is regulated by specific beta subunits and a novel glucose signaling mechanism. , 2001, Genes & development.