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      Temporal system-level organization of the switch from glycolytic to gluconeogenic operation in yeast

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          Abstract

          • The diauxic shift involves three main events: a reduction in the glycolytic flux and the production of storage compounds before glucose depletion; the reversion of carbon flow through glycolysis and onset of the glyoxylate cycle operation upon glucose exhaustion; and the shutting down of the pentose phosphate (PP) pathway with a change in the source of NADPH regeneration.

          • The redistribution of fluxes toward the production of storage compounds prior glucose depletion drives glycolytic reactions closer to equilibrium, which is essential for the reversion of fluxes upon glucose exhaustion.

          • The onset of the glyoxylate cycle is quantitatively more important than the activation of the tricarboxylic acid cycle for growth on ethanol.

          • Flux through the PP pathway is halted in the later stages of the adaptation and NADPH regeneration is taken over by NADP-dependent enzymes in the glyoxylate cycle and ethanol metabolism.

          Abstract

          The diauxic shift in Saccharomyces cerevisiae is an ideal model to study how eukaryotic cells readjust their metabolism from glycolytic to gluconeogenic operation. In this work, we generated time-resolved physiological data, quantitative metabolome (69 intracellular metabolites) and proteome (72 enzymes) profiles. We found that the diauxic shift is accomplished by three key events that are temporally organized: (i) a reduction in the glycolytic flux and the production of storage compounds before glucose depletion, mediated by downregulation of phosphofructokinase and pyruvate kinase reactions; (ii) upon glucose exhaustion, the reversion of carbon flow through glycolysis and onset of the glyoxylate cycle operation triggered by an increased expression of the enzymes that catalyze the malate synthase and cytosolic citrate synthase reactions; and (iii) in the later stages of the adaptation, the shutting down of the pentose phosphate pathway with a change in NADPH regeneration. Moreover, we identified the transcription factors associated with the observed changes in protein abundances. Taken together, our results represent an important contribution toward a systems-level understanding of how this adaptation is realized.

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          Most cited references 56

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          Global analysis of protein localization in budding yeast.

          A fundamental goal of cell biology is to define the functions of proteins in the context of compartments that organize them in the cellular environment. Here we describe the construction and analysis of a collection of yeast strains expressing full-length, chromosomally tagged green fluorescent protein fusion proteins. We classify these proteins, representing 75% of the yeast proteome, into 22 distinct subcellular localization categories, and provide localization information for 70% of previously unlocalized proteins. Analysis of this high-resolution, high-coverage localization data set in the context of transcriptional, genetic, and protein-protein interaction data helps reveal the logic of transcriptional co-regulation, and provides a comprehensive view of interactions within and between organelles in eukaryotic cells.
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            GO::TermFinder--open source software for accessing Gene Ontology information and finding significantly enriched Gene Ontology terms associated with a list of genes.

            GO::TermFinder comprises a set of object-oriented Perl modules for accessing Gene Ontology (GO) information and evaluating and visualizing the collective annotation of a list of genes to GO terms. It can be used to draw conclusions from microarray and other biological data, calculating the statistical significance of each annotation. GO::TermFinder can be used on any system on which Perl can be run, either as a command line application, in single or batch mode, or as a web-based CGI script. The full source code and documentation for GO::TermFinder are freely available from http://search.cpan.org/dist/GO-TermFinder/.
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              Exploring the metabolic and genetic control of gene expression on a genomic scale.

              DNA microarrays containing virtually every gene of Saccharomyces cerevisiae were used to carry out a comprehensive investigation of the temporal program of gene expression accompanying the metabolic shift from fermentation to respiration. The expression profiles observed for genes with known metabolic functions pointed to features of the metabolic reprogramming that occur during the diauxic shift, and the expression patterns of many previously uncharacterized genes provided clues to their possible functions. The same DNA microarrays were also used to identify genes whose expression was affected by deletion of the transcriptional co-repressor TUP1 or overexpression of the transcriptional activator YAP1. These results demonstrate the feasibility and utility of this approach to genomewide exploration of gene expression patterns.
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                Author and article information

                Affiliations
                [1 ]Molecular Systems Biology, Groningen Biomolecular Sciences and Biotechnology Institute, University of Groningen , Groningen, The Netherlands
                [2 ]ETH Zurich, Institute of Molecular Systems Biology , Zurich, Switzerland
                [3 ]Faculty of Science, University of Zurich , Zurich, Switzerland
                Author notes
                [a ]Molecular Systems Biology, Groningen Biomolecular Sciences and Biotechnology Institute, University of Groningen , Nijenborgh 4, 9747 AG Groningen, The Netherlands. Tel.:+31 50 363 8146; Fax:+31 50 363 4165; m.heinemann@ 123456rug.nl
                Journal
                Mol Syst Biol
                Mol. Syst. Biol
                Molecular Systems Biology
                Nature Publishing Group
                1744-4292
                2013
                02 April 2013
                02 April 2013
                : 9
                : 651
                23549479
                3693829
                msb201311
                10.1038/msb.2013.11
                Copyright © 2013, EMBO and Macmillan Publishers Limited

                This article is licensed under a Creative Commons Attribution 3.0 Unported Licence. To view a copy of this license, visit http://creativecommons.org/licenses/by/3.0/.

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