Regulation of yeast central metabolism by enzyme phosphorylation

Abstract As a frequent post‐translational modification, protein phosphorylation regulates many cellular processes. Although several hundred phosphorylation sites have been mapped to metabolic enzymes in Saccharomyces cerevisiae, functionality was demonstrated for few of them. Here, we describe a nov...

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Main Authors: Ana Paula Oliveira, Christina Ludwig, Paola Picotti, Maria Kogadeeva, Ruedi Aebersold, Uwe Sauer
Format: Article
Language:English
Published: Springer Nature 2012-11-01
Series:Molecular Systems Biology
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Online Access:https://doi.org/10.1038/msb.2012.55
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author Ana Paula Oliveira
Christina Ludwig
Paola Picotti
Maria Kogadeeva
Ruedi Aebersold
Uwe Sauer
author_facet Ana Paula Oliveira
Christina Ludwig
Paola Picotti
Maria Kogadeeva
Ruedi Aebersold
Uwe Sauer
author_sort Ana Paula Oliveira
collection DOAJ
description Abstract As a frequent post‐translational modification, protein phosphorylation regulates many cellular processes. Although several hundred phosphorylation sites have been mapped to metabolic enzymes in Saccharomyces cerevisiae, functionality was demonstrated for few of them. Here, we describe a novel approach to identify in vivo functionality of enzyme phosphorylation by combining flux analysis with proteomics and phosphoproteomics. Focusing on the network of 204 enzymes that constitute the yeast central carbon and amino‐acid metabolism, we combined protein and phosphoprotein levels to identify 35 enzymes that change their degree of phosphorylation during growth under five conditions. Correlations between previously determined intracellular fluxes and phosphoprotein abundances provided first functional evidence for five novel phosphoregulated enzymes in this network, adding to nine known phosphoenzymes. For the pyruvate dehydrogenase complex E1 α subunit Pda1 and the newly identified phosphoregulated glycerol‐3‐phosphate dehydrogenase Gpd1 and phosphofructose‐1‐kinase complex β subunit Pfk2, we then validated functionality of specific phosphosites through absolute peptide quantification by targeted mass spectrometry, metabolomics and physiological flux analysis in mutants with genetically removed phosphosites. These results demonstrate the role of phosphorylation in controlling the metabolic flux realised by these three enzymes.
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spelling doaj-art-eb7769db5d2c42d29b5d6afa8ba4dbe52025-08-20T02:18:28ZengSpringer NatureMolecular Systems Biology1744-42922012-11-018111310.1038/msb.2012.55Regulation of yeast central metabolism by enzyme phosphorylationAna Paula Oliveira0Christina Ludwig1Paola Picotti2Maria Kogadeeva3Ruedi Aebersold4Uwe Sauer5Department of Biology, Institute of Molecular Systems Biology, ETH ZurichDepartment of Biology, Institute of Molecular Systems Biology, ETH ZurichDepartment of Biology, Institute of Molecular Systems Biology, ETH ZurichDepartment of Biology, Institute of Molecular Systems Biology, ETH ZurichDepartment of Biology, Institute of Molecular Systems Biology, ETH ZurichDepartment of Biology, Institute of Molecular Systems Biology, ETH ZurichAbstract As a frequent post‐translational modification, protein phosphorylation regulates many cellular processes. Although several hundred phosphorylation sites have been mapped to metabolic enzymes in Saccharomyces cerevisiae, functionality was demonstrated for few of them. Here, we describe a novel approach to identify in vivo functionality of enzyme phosphorylation by combining flux analysis with proteomics and phosphoproteomics. Focusing on the network of 204 enzymes that constitute the yeast central carbon and amino‐acid metabolism, we combined protein and phosphoprotein levels to identify 35 enzymes that change their degree of phosphorylation during growth under five conditions. Correlations between previously determined intracellular fluxes and phosphoprotein abundances provided first functional evidence for five novel phosphoregulated enzymes in this network, adding to nine known phosphoenzymes. For the pyruvate dehydrogenase complex E1 α subunit Pda1 and the newly identified phosphoregulated glycerol‐3‐phosphate dehydrogenase Gpd1 and phosphofructose‐1‐kinase complex β subunit Pfk2, we then validated functionality of specific phosphosites through absolute peptide quantification by targeted mass spectrometry, metabolomics and physiological flux analysis in mutants with genetically removed phosphosites. These results demonstrate the role of phosphorylation in controlling the metabolic flux realised by these three enzymes.https://doi.org/10.1038/msb.2012.55metabolic fluxmetabolismphosphoproteomepost‐translational regulationselected reaction monitoring
spellingShingle Ana Paula Oliveira
Christina Ludwig
Paola Picotti
Maria Kogadeeva
Ruedi Aebersold
Uwe Sauer
Regulation of yeast central metabolism by enzyme phosphorylation
Molecular Systems Biology
metabolic flux
metabolism
phosphoproteome
post‐translational regulation
selected reaction monitoring
title Regulation of yeast central metabolism by enzyme phosphorylation
title_full Regulation of yeast central metabolism by enzyme phosphorylation
title_fullStr Regulation of yeast central metabolism by enzyme phosphorylation
title_full_unstemmed Regulation of yeast central metabolism by enzyme phosphorylation
title_short Regulation of yeast central metabolism by enzyme phosphorylation
title_sort regulation of yeast central metabolism by enzyme phosphorylation
topic metabolic flux
metabolism
phosphoproteome
post‐translational regulation
selected reaction monitoring
url https://doi.org/10.1038/msb.2012.55
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AT christinaludwig regulationofyeastcentralmetabolismbyenzymephosphorylation
AT paolapicotti regulationofyeastcentralmetabolismbyenzymephosphorylation
AT mariakogadeeva regulationofyeastcentralmetabolismbyenzymephosphorylation
AT ruediaebersold regulationofyeastcentralmetabolismbyenzymephosphorylation
AT uwesauer regulationofyeastcentralmetabolismbyenzymephosphorylation