Pyruvate Kinase Triggers a Metabolic Feedback Loop that Controls Redox Metabolism in Respiring Cells
In proliferating cells, a transition from aerobic to anaerobic metabolism is known as the Warburg effect, whose reversal inhibits cancer cell proliferation. Studying its regulator pyruvate kinase (PYK) in yeast, we discovered that central metabolism is self-adapting to synchronize redox metabolism w...
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Published in | Cell metabolism Vol. 14; no. 3; pp. 415 - 427 |
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Main Authors | , , , , , , , , |
Format | Journal Article |
Language | English |
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United States
Elsevier Inc
07.09.2011
Cell Press |
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Abstract | In proliferating cells, a transition from aerobic to anaerobic metabolism is known as the Warburg effect, whose reversal inhibits cancer cell proliferation. Studying its regulator pyruvate kinase (PYK) in yeast, we discovered that central metabolism is self-adapting to synchronize redox metabolism when respiration is activated. Low PYK activity activated yeast respiration. However, levels of reactive oxygen species (ROS) did not increase, and cells gained resistance to oxidants. This adaptation was attributable to accumulation of the PYK substrate phosphoenolpyruvate (PEP). PEP acted as feedback inhibitor of the glycolytic enzyme triosephosphate isomerase (TPI). TPI inhibition stimulated the pentose phosphate pathway, increased antioxidative metabolism, and prevented ROS accumulation. Thus, a metabolic feedback loop, initiated by PYK, mediated by its substrate and acting on TPI, stimulates redox metabolism in respiring cells. Originating from a single catalytic step, this autonomous reconfiguration of central carbon metabolism prevents oxidative stress upon shifts between fermentation and respiration.
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► Low pyruvate kinase (PYK) activity activates respiration in yeast ► Accumulation of the PYK substrate PEP inhibits the glycolytic enzyme TPI ► TPI inhibition stimulates the pentose phosphate pathway, preventing ROS accumulation ► The PYK-PEP-TPI feedback loop synchronizes respiration and redox metabolism |
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AbstractList | In proliferating cells, a transition from aerobic to anaerobic metabolism is known as the Warburg effect, whose reversal inhibits cancer cell proliferation. Studying its regulator pyruvate kinase (PYK) in yeast, we discovered that central metabolism is self-adapting to synchronize redox metabolism when respiration is activated. Low PYK activity activated yeast respiration. However, levels of reactive oxygen species (ROS) did not increase, and cells gained resistance to oxidants. This adaptation was attributable to accumulation of the PYK substrate phosphoenolpyruvate (PEP). PEP acted as feedback inhibitor of the glycolytic enzyme triosephosphate isomerase (TPI). TPI inhibition stimulated the pentose phosphate pathway, increased antioxidative metabolism, and prevented ROS accumulation. Thus, a metabolic feedback loop, initiated by PYK, mediated by its substrate and acting on TPI, stimulates redox metabolism in respiring cells. Originating from a single catalytic step, this autonomous reconfiguration of central carbon metabolism prevents oxidative stress upon shifts between fermentation and respiration. In proliferating cells, a transition from aerobic to anaerobic metabolism is known as the Warburg effect, whose reversal inhibits cancer cell proliferation. Studying its regulator pyruvate kinase (PYK) in yeast, we discovered that central metabolism is self-adapting to synchronize redox metabolism when respiration is activated. Low PYK activity activated yeast respiration. However, levels of reactive oxygen species (ROS) did not increase, and cells gained resistance to oxidants. This adaptation was attributable to accumulation of the PYK substrate phosphoenolpyruvate (PEP). PEP acted as feedback inhibitor of the glycolytic enzyme triosephosphate isomerase (TPI). TPI inhibition stimulated the pentose phosphate pathway, increased antioxidative metabolism, and prevented ROS accumulation. Thus, a metabolic feedback loop, initiated by PYK, mediated by its substrate and acting on TPI, stimulates redox metabolism in respiring cells. Originating from a single catalytic step, this autonomous reconfiguration of central carbon metabolism prevents oxidative stress upon shifts between fermentation and respiration. [Display omitted] ► Low pyruvate kinase (PYK) activity activates respiration in yeast ► Accumulation of the PYK substrate PEP inhibits the glycolytic enzyme TPI ► TPI inhibition stimulates the pentose phosphate pathway, preventing ROS accumulation ► The PYK-PEP-TPI feedback loop synchronizes respiration and redox metabolism |
Author | Bluemlein, Katharina Wamelink, Mirjam M.C. Grüning, Nana-Maria Mülleder, Michael Breitenbach, Michael Rinnerthaler, Mark Jakobs, Cornelis Lehrach, Hans Ralser, Markus |
AuthorAffiliation | 2 Department of Cell Biology, University of Salzburg, Hellbrunnerstrasse 34, 5020 Salzburg, Austria 5 Department of Biochemistry, University of Cambridge, Sanger Building, 50 Tennis Court Road, Cambridge CB2 1GA, UK 1 Max Planck Institute for Molecular Genetics, Ihnestrasse 73, 14195 Berlin, Germany 3 Metabolic Unit, Department of Clinical Chemistry, VU University Medical Center, De Boelelaan 1117, 1081 HV Amsterdam, The Netherlands 4 Cambridge Systems Biology Centre, University of Cambridge, Sanger Building, 50 Tennis Court Road, Cambridge CB2 1GA, UK |
AuthorAffiliation_xml | – name: 2 Department of Cell Biology, University of Salzburg, Hellbrunnerstrasse 34, 5020 Salzburg, Austria – name: 4 Cambridge Systems Biology Centre, University of Cambridge, Sanger Building, 50 Tennis Court Road, Cambridge CB2 1GA, UK – name: 3 Metabolic Unit, Department of Clinical Chemistry, VU University Medical Center, De Boelelaan 1117, 1081 HV Amsterdam, The Netherlands – name: 5 Department of Biochemistry, University of Cambridge, Sanger Building, 50 Tennis Court Road, Cambridge CB2 1GA, UK – name: 1 Max Planck Institute for Molecular Genetics, Ihnestrasse 73, 14195 Berlin, Germany |
Author_xml | – sequence: 1 givenname: Nana-Maria surname: Grüning fullname: Grüning, Nana-Maria organization: Max Planck Institute for Molecular Genetics, Ihnestrasse 73, 14195 Berlin, Germany – sequence: 2 givenname: Mark surname: Rinnerthaler fullname: Rinnerthaler, Mark organization: Department of Cell Biology, University of Salzburg, Hellbrunnerstrasse 34, 5020 Salzburg, Austria – sequence: 3 givenname: Katharina surname: Bluemlein fullname: Bluemlein, Katharina organization: Max Planck Institute for Molecular Genetics, Ihnestrasse 73, 14195 Berlin, Germany – sequence: 4 givenname: Michael surname: Mülleder fullname: Mülleder, Michael organization: Max Planck Institute for Molecular Genetics, Ihnestrasse 73, 14195 Berlin, Germany – sequence: 5 givenname: Mirjam M.C. surname: Wamelink fullname: Wamelink, Mirjam M.C. organization: Metabolic Unit, Department of Clinical Chemistry, VU University Medical Center, De Boelelaan 1117, 1081 HV Amsterdam, The Netherlands – sequence: 6 givenname: Hans surname: Lehrach fullname: Lehrach, Hans organization: Max Planck Institute for Molecular Genetics, Ihnestrasse 73, 14195 Berlin, Germany – sequence: 7 givenname: Cornelis surname: Jakobs fullname: Jakobs, Cornelis organization: Metabolic Unit, Department of Clinical Chemistry, VU University Medical Center, De Boelelaan 1117, 1081 HV Amsterdam, The Netherlands – sequence: 8 givenname: Michael surname: Breitenbach fullname: Breitenbach, Michael organization: Department of Cell Biology, University of Salzburg, Hellbrunnerstrasse 34, 5020 Salzburg, Austria – sequence: 9 givenname: Markus surname: Ralser fullname: Ralser, Markus email: mr559@cam.ac.uk organization: Max Planck Institute for Molecular Genetics, Ihnestrasse 73, 14195 Berlin, Germany |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/21907146$$D View this record in MEDLINE/PubMed |
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SubjectTerms | Cell Proliferation Cell Respiration - physiology Chromatography, Liquid Feedback, Physiological Galactose - metabolism Gene Expression Regulation, Fungal Glucose - metabolism Glycolysis - physiology Oxidation-Reduction Oxidative Stress - genetics Pentose Phosphate Pathway Phosphoenolpyruvate - metabolism Polymerase Chain Reaction Pyruvate Kinase - genetics Pyruvate Kinase - metabolism Reactive Oxygen Species - metabolism Saccharomyces cerevisiae - genetics Saccharomyces cerevisiae - metabolism Saccharomyces cerevisiae Proteins - genetics Saccharomyces cerevisiae Proteins - metabolism Tandem Mass Spectrometry Triose-Phosphate Isomerase - genetics Triose-Phosphate Isomerase - metabolism |
Title | Pyruvate Kinase Triggers a Metabolic Feedback Loop that Controls Redox Metabolism in Respiring Cells |
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