Poly(ADP-ribose) polymerase-dependent energy depletion occurs through inhibition of glycolysis
Identifieur interne : 000427 ( Pmc/Checkpoint ); précédent : 000426; suivant : 000428Poly(ADP-ribose) polymerase-dependent energy depletion occurs through inhibition of glycolysis
Auteurs : Shaida A. Andrabi ; George K. E. Umanah ; Calvin Chang ; Daniel A. Stevens ; Senthilkumar S. Karuppagounder ; Jean-Philippe Gagné [Canada] ; Guy G. Poirier [Canada] ; Valina L. Dawson ; Ted M. DawsonSource :
- Proceedings of the National Academy of Sciences of the United States of America [ 0027-8424 ] ; 2014.
Abstract
Excessive activation of poly(ADP-ribose) (PAR) polymerase (PARP) is intimately linked to cell death in a variety of organ systems. It has long been thought that the cell death caused by excessive activation of PARP occurs through the catalytic consumption of NAD+ followed by reduction of ATP and bioenergetic collapse. This study shows that the bioenergetic collapse is caused not by the consumption of NAD+ but by PAR-dependent inhibition of hexokinase activity leading to defects in glycolysis. These results are consistent with the notion that cell death induced by excessive PARP activity (parthanatos) is an active cell-death program that is initiated by PAR signaling.
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DOI: 10.1073/pnas.1405158111
PubMed: 24987120
PubMed Central: 4104885
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Umanah</name><affiliation><nlm:aff id="aff1">Neuroregeneration and Stem Cell Programs, Institute for Cell Engineering,</nlm:aff><wicri:noCountry code="subfield">Institute for Cell Engineering</wicri:noCountry></affiliation><affiliation><nlm:aff id="aff2"></nlm:aff></affiliation></author><author><name sortKey="Chang, Calvin" sort="Chang, Calvin" uniqKey="Chang C" first="Calvin" last="Chang">Calvin Chang</name><affiliation><nlm:aff id="aff1">Neuroregeneration and Stem Cell Programs, Institute for Cell Engineering,</nlm:aff><wicri:noCountry code="subfield">Institute for Cell Engineering</wicri:noCountry></affiliation><affiliation><nlm:aff id="aff3">Biomedical Engineering,</nlm:aff></affiliation></author><author><name sortKey="Stevens, Daniel A" sort="Stevens, Daniel A" uniqKey="Stevens D" first="Daniel A." last="Stevens">Daniel A. Stevens</name><affiliation><nlm:aff id="aff1">Neuroregeneration and Stem Cell Programs, Institute for Cell Engineering,</nlm:aff><wicri:noCountry code="subfield">Institute for Cell Engineering</wicri:noCountry></affiliation><affiliation><nlm:aff wicri:cut="; and" id="aff7">Solomon H. Snyder Department of Neuroscience,<institution>The Johns Hopkins University School of Medicine</institution>, Baltimore,<addr-line>MD</addr-line> 21205</nlm:aff></affiliation></author><author><name sortKey="Karuppagounder, Senthilkumar S" sort="Karuppagounder, Senthilkumar S" uniqKey="Karuppagounder S" first="Senthilkumar S." last="Karuppagounder">Senthilkumar S. 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Poirier</name><affiliation wicri:level="1"><nlm:aff id="aff6"><institution>Centre de Recherche du CHU de Québec, Université Laval, Québec</institution>,<country>Canada</country> G1V 4G2</nlm:aff><country xml:lang="fr">Canada</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Dawson, Valina L" sort="Dawson, Valina L" uniqKey="Dawson V" first="Valina L." last="Dawson">Valina L. Dawson</name><affiliation><nlm:aff id="aff1">Neuroregeneration and Stem Cell Programs, Institute for Cell Engineering,</nlm:aff><wicri:noCountry code="subfield">Institute for Cell Engineering</wicri:noCountry></affiliation><affiliation><nlm:aff id="aff2"></nlm:aff></affiliation><affiliation><nlm:aff wicri:cut="; and" id="aff7">Solomon H. Snyder Department of Neuroscience,<institution>The Johns Hopkins University School of Medicine</institution>, Baltimore,<addr-line>MD</addr-line> 21205</nlm:aff></affiliation><affiliation><nlm:aff wicri:cut=", and" id="aff4">Physiology</nlm:aff></affiliation></author><author><name sortKey="Dawson, Ted M" sort="Dawson, Ted M" uniqKey="Dawson T" first="Ted M." last="Dawson">Ted M. Dawson</name><affiliation><nlm:aff id="aff1">Neuroregeneration and Stem Cell Programs, Institute for Cell Engineering,</nlm:aff><wicri:noCountry code="subfield">Institute for Cell Engineering</wicri:noCountry></affiliation><affiliation><nlm:aff id="aff2"></nlm:aff></affiliation><affiliation><nlm:aff wicri:cut="; and" id="aff7">Solomon H. Snyder Department of Neuroscience,<institution>The Johns Hopkins University School of Medicine</institution>, Baltimore,<addr-line>MD</addr-line> 21205</nlm:aff></affiliation><affiliation><nlm:aff wicri:cut=", and" id="aff5">Pharmacology and Molecular Sciences</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">24987120</idno><idno type="pmc">4104885</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4104885</idno><idno type="RBID">PMC:4104885</idno><idno type="doi">10.1073/pnas.1405158111</idno><date when="2014">2014</date><idno type="wicri:Area/Pmc/Corpus">000673</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000673</idno><idno type="wicri:Area/Pmc/Curation">000673</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">000673</idno><idno type="wicri:Area/Pmc/Checkpoint">000427</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Checkpoint">000427</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Poly(ADP-ribose) polymerase-dependent energy depletion occurs through inhibition of glycolysis</title><author><name sortKey="Andrabi, Shaida A" sort="Andrabi, Shaida A" uniqKey="Andrabi S" first="Shaida A." last="Andrabi">Shaida A. Andrabi</name><affiliation><nlm:aff id="aff1">Neuroregeneration and Stem Cell Programs, Institute for Cell Engineering,</nlm:aff><wicri:noCountry code="subfield">Institute for Cell Engineering</wicri:noCountry></affiliation><affiliation><nlm:aff id="aff2"></nlm:aff></affiliation></author><author><name sortKey="Umanah, George K E" sort="Umanah, George K E" uniqKey="Umanah G" first="George K. E." last="Umanah">George K. E. Umanah</name><affiliation><nlm:aff id="aff1">Neuroregeneration and Stem Cell Programs, Institute for Cell Engineering,</nlm:aff><wicri:noCountry code="subfield">Institute for Cell Engineering</wicri:noCountry></affiliation><affiliation><nlm:aff id="aff2"></nlm:aff></affiliation></author><author><name sortKey="Chang, Calvin" sort="Chang, Calvin" uniqKey="Chang C" first="Calvin" last="Chang">Calvin Chang</name><affiliation><nlm:aff id="aff1">Neuroregeneration and Stem Cell Programs, Institute for Cell Engineering,</nlm:aff><wicri:noCountry code="subfield">Institute for Cell Engineering</wicri:noCountry></affiliation><affiliation><nlm:aff id="aff3">Biomedical Engineering,</nlm:aff></affiliation></author><author><name sortKey="Stevens, Daniel A" sort="Stevens, Daniel A" uniqKey="Stevens D" first="Daniel A." last="Stevens">Daniel A. Stevens</name><affiliation><nlm:aff id="aff1">Neuroregeneration and Stem Cell Programs, Institute for Cell Engineering,</nlm:aff><wicri:noCountry code="subfield">Institute for Cell Engineering</wicri:noCountry></affiliation><affiliation><nlm:aff wicri:cut="; and" id="aff7">Solomon H. Snyder Department of Neuroscience,<institution>The Johns Hopkins University School of Medicine</institution>, Baltimore,<addr-line>MD</addr-line> 21205</nlm:aff></affiliation></author><author><name sortKey="Karuppagounder, Senthilkumar S" sort="Karuppagounder, Senthilkumar S" uniqKey="Karuppagounder S" first="Senthilkumar S." last="Karuppagounder">Senthilkumar S. Karuppagounder</name><affiliation><nlm:aff id="aff1">Neuroregeneration and Stem Cell Programs, Institute for Cell Engineering,</nlm:aff><wicri:noCountry code="subfield">Institute for Cell Engineering</wicri:noCountry></affiliation><affiliation><nlm:aff id="aff2"></nlm:aff></affiliation></author><author><name sortKey="Gagne, Jean Philippe" sort="Gagne, Jean Philippe" uniqKey="Gagne J" first="Jean-Philippe" last="Gagné">Jean-Philippe Gagné</name><affiliation wicri:level="1"><nlm:aff id="aff6"><institution>Centre de Recherche du CHU de Québec, Université Laval, Québec</institution>,<country>Canada</country> G1V 4G2</nlm:aff><country xml:lang="fr">Canada</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Poirier, Guy G" sort="Poirier, Guy G" uniqKey="Poirier G" first="Guy G." last="Poirier">Guy G. Poirier</name><affiliation wicri:level="1"><nlm:aff id="aff6"><institution>Centre de Recherche du CHU de Québec, Université Laval, Québec</institution>,<country>Canada</country> G1V 4G2</nlm:aff><country xml:lang="fr">Canada</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Dawson, Valina L" sort="Dawson, Valina L" uniqKey="Dawson V" first="Valina L." last="Dawson">Valina L. Dawson</name><affiliation><nlm:aff id="aff1">Neuroregeneration and Stem Cell Programs, Institute for Cell Engineering,</nlm:aff><wicri:noCountry code="subfield">Institute for Cell Engineering</wicri:noCountry></affiliation><affiliation><nlm:aff id="aff2"></nlm:aff></affiliation><affiliation><nlm:aff wicri:cut="; and" id="aff7">Solomon H. Snyder Department of Neuroscience,<institution>The Johns Hopkins University School of Medicine</institution>, Baltimore,<addr-line>MD</addr-line> 21205</nlm:aff></affiliation><affiliation><nlm:aff wicri:cut=", and" id="aff4">Physiology</nlm:aff></affiliation></author><author><name sortKey="Dawson, Ted M" sort="Dawson, Ted M" uniqKey="Dawson T" first="Ted M." last="Dawson">Ted M. Dawson</name><affiliation><nlm:aff id="aff1">Neuroregeneration and Stem Cell Programs, Institute for Cell Engineering,</nlm:aff><wicri:noCountry code="subfield">Institute for Cell Engineering</wicri:noCountry></affiliation><affiliation><nlm:aff id="aff2"></nlm:aff></affiliation><affiliation><nlm:aff wicri:cut="; and" id="aff7">Solomon H. Snyder Department of Neuroscience,<institution>The Johns Hopkins University School of Medicine</institution>, Baltimore,<addr-line>MD</addr-line> 21205</nlm:aff></affiliation><affiliation><nlm:aff wicri:cut=", and" id="aff5">Pharmacology and Molecular Sciences</nlm:aff></affiliation></author></analytic><series><title level="j">Proceedings of the National Academy of Sciences of the United States of America</title><idno type="ISSN">0027-8424</idno><idno type="eISSN">1091-6490</idno><imprint><date when="2014">2014</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><title>Significance</title><p>Excessive activation of poly(ADP-ribose) (PAR) polymerase (PARP) is intimately linked to cell death in a variety of organ systems. It has long been thought that the cell death caused by excessive activation of PARP occurs through the catalytic consumption of NAD<sup>+</sup> followed by reduction of ATP and bioenergetic collapse. This study shows that the bioenergetic collapse is caused not by the consumption of NAD<sup>+</sup> but by PAR-dependent inhibition of hexokinase activity leading to defects in glycolysis. These results are consistent with the notion that cell death induced by excessive PARP activity (parthanatos) is an active cell-death program that is initiated by PAR signaling.</p></div></front></TEI><pmc article-type="research-article"><pmc-comment>The publisher of this article does not allow downloading of the full text in XML form.</pmc-comment>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Proc Natl Acad Sci U S A</journal-id><journal-id journal-id-type="iso-abbrev">Proc. Natl. Acad. Sci. U.S.A</journal-id><journal-id journal-id-type="hwp">pnas</journal-id><journal-id journal-id-type="pmc">pnas</journal-id><journal-id journal-id-type="publisher-id">PNAS</journal-id><journal-title-group><journal-title>Proceedings of the National Academy of Sciences of the United States of America</journal-title></journal-title-group><issn pub-type="ppub">0027-8424</issn><issn pub-type="epub">1091-6490</issn><publisher><publisher-name>National Academy of Sciences</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">24987120</article-id><article-id pub-id-type="pmc">4104885</article-id><article-id pub-id-type="publisher-id">201405158</article-id><article-id pub-id-type="doi">10.1073/pnas.1405158111</article-id><article-categories><subj-group subj-group-type="heading"><subject>Biological Sciences</subject><subj-group><subject>Cell Biology</subject></subj-group></subj-group></article-categories><title-group><article-title>Poly(ADP-ribose) polymerase-dependent energy depletion occurs through inhibition of glycolysis</article-title><alt-title alt-title-type="short">Poly(ADP-ribose) inhibition of glycolysis</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Andrabi</surname><given-names>Shaida A.</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref><xref ref-type="aff" rid="aff2"><sup>b</sup></xref><xref ref-type="corresp" rid="cor1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Umanah</surname><given-names>George K. E.</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref><xref ref-type="aff" rid="aff2"><sup>b</sup></xref></contrib><contrib contrib-type="author"><name><surname>Chang</surname><given-names>Calvin</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref><xref ref-type="aff" rid="aff3"><sup>c</sup></xref></contrib><contrib contrib-type="author"><name><surname>Stevens</surname><given-names>Daniel A.</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref><xref ref-type="aff" rid="aff7"><sup>d</sup></xref></contrib><contrib contrib-type="author"><name><surname>Karuppagounder</surname><given-names>Senthilkumar S.</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref><xref ref-type="aff" rid="aff2"><sup>b</sup></xref></contrib><contrib contrib-type="author"><name><surname>Gagné</surname><given-names>Jean-Philippe</given-names></name><xref ref-type="aff" rid="aff6"><sup>e</sup></xref></contrib><contrib contrib-type="author"><name><surname>Poirier</surname><given-names>Guy G.</given-names></name><xref ref-type="aff" rid="aff6"><sup>e</sup></xref></contrib><contrib contrib-type="author"><name><surname>Dawson</surname><given-names>Valina L.</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref><xref ref-type="aff" rid="aff2"><sup>b</sup></xref><xref ref-type="aff" rid="aff7"><sup>d</sup></xref><xref ref-type="aff" rid="aff4"><sup>f</sup></xref><xref ref-type="corresp" rid="cor1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Dawson</surname><given-names>Ted M.</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref><xref ref-type="aff" rid="aff2"><sup>b</sup></xref><xref ref-type="aff" rid="aff7"><sup>d</sup></xref><xref ref-type="aff" rid="aff5"><sup>g</sup></xref><xref ref-type="corresp" rid="cor1"><sup>1</sup></xref></contrib><aff id="aff1"><sup>a</sup>Neuroregeneration and Stem Cell Programs, Institute for Cell Engineering,</aff><aff id="aff2">Departments of<sup>b</sup>Neurology,</aff><aff id="aff3"><sup>c</sup>Biomedical Engineering,</aff><aff id="aff4"><sup>f</sup>Physiology, and</aff><aff id="aff5"><sup>g</sup>Pharmacology and Molecular Sciences, and</aff><aff id="aff7"><sup>d</sup>Solomon H. Snyder Department of Neuroscience,<institution>The Johns Hopkins University School of Medicine</institution>, Baltimore,<addr-line>MD</addr-line> 21205; and</aff><aff id="aff6"><sup>e</sup><institution>Centre de Recherche du CHU de Québec, Université Laval, Québec</institution>,<country>Canada</country> G1V 4G2</aff></contrib-group><author-notes><corresp id="cor1"><sup>1</sup>To whom correspondence may be addressed. Email: <email>sandrabi@jhmi.edu</email>, <email>vdawson@jhmi.edu</email>, or <email>tdawson@jhmi.edu</email>.</corresp><fn fn-type="edited-by"><p>Edited by Salvador Moncada, University of Manchester, Manchester, United Kingdom, and approved June 12, 2014 (received for review March 19, 2014)</p></fn><fn fn-type="con"><p>Author contributions: S.A.A., V.L.D., and T.M.D. formulated the hypothesis and initiated and organized the study; S.A.A., G.K.E.U., V.L.D., and T.M.D. designed research; S.A.A., G.K.E.U., C.C., D.A.S., and S.S.K. performed research; J.-P.G. and G.G.P. contributed new reagents/analytic tools; S.A.A., G.K.E.U., C.C., D.A.S., S.S.K., J.-P.G., G.G.P., V.L.D., and T.M.D. analyzed data; and S.A.A., V.L.D., and T.M.D. wrote the paper.</p></fn></author-notes><pub-date pub-type="ppub"><day>15</day><month>7</month><year>2014</year></pub-date><pub-date pub-type="epub"><day>1</day><month>7</month><year>2014</year></pub-date><volume>111</volume><issue>28</issue><fpage>10209</fpage><lpage>10214</lpage><self-uri xlink:title="pdf" xlink:type="simple" xlink:href="pnas.201405158.pdf"></self-uri><abstract abstract-type="executive-summary"><title>Significance</title><p>Excessive activation of poly(ADP-ribose) (PAR) polymerase (PARP) is intimately linked to cell death in a variety of organ systems. It has long been thought that the cell death caused by excessive activation of PARP occurs through the catalytic consumption of NAD<sup>+</sup> followed by reduction of ATP and bioenergetic collapse. This study shows that the bioenergetic collapse is caused not by the consumption of NAD<sup>+</sup> but by PAR-dependent inhibition of hexokinase activity leading to defects in glycolysis. These results are consistent with the notion that cell death induced by excessive PARP activity (parthanatos) is an active cell-death program that is initiated by PAR signaling.</p></abstract><abstract><p>Excessive poly(ADP-ribose) (PAR) polymerase-1 (PARP-1) activation kills cells via a cell-death process designated “parthanatos” in which PAR induces the mitochondrial release and nuclear translocation of apoptosis-inducing factor to initiate chromatinolysis and cell death. Accompanying the formation of PAR are the reduction of cellular NAD<sup>+</sup> and energetic collapse, which have been thought to be caused by the consumption of cellular NAD<sup>+</sup> by PARP-1. Here we show that the bioenergetic collapse following PARP-1 activation is not dependent on NAD<sup>+</sup> depletion. Instead PARP-1 activation initiates glycolytic defects via PAR-dependent inhibition of hexokinase, which precedes the NAD<sup>+</sup> depletion in <italic>N</italic>-methyl-<italic>N</italic>-nitroso-<italic>N</italic>-nitroguanidine (MNNG)-treated cortical neurons. Mitochondrial defects are observed shortly after PARP-1 activation and are mediated largely through defective glycolysis, because supplementation of the mitochondrial substrates pyruvate and glutamine reverse the PARP-1–mediated mitochondrial dysfunction. Depleting neurons of NAD<sup>+</sup> with FK866, a highly specific noncompetitive inhibitor of nicotinamide phosphoribosyltransferase, does not alter glycolysis or mitochondrial function. Hexokinase, the first regulatory enzyme to initiate glycolysis by converting glucose to glucose-6-phosphate, contains a strong PAR-binding motif. PAR binds to hexokinase and inhibits hexokinase activity in MNNG-treated cortical neurons. Preventing PAR formation with PAR glycohydrolase prevents the PAR-dependent inhibition of hexokinase. These results indicate that bioenergetic collapse induced by overactivation of PARP-1 is caused by PAR-dependent inhibition of glycolysis through inhibition of hexokinase.</p></abstract><counts><page-count count="6"></page-count></counts></article-meta></front></pmc><affiliations><list><country><li>Canada</li></country></list><tree><noCountry><name sortKey="Andrabi, Shaida A" sort="Andrabi, Shaida A" uniqKey="Andrabi S" first="Shaida A." last="Andrabi">Shaida A. Andrabi</name><name sortKey="Chang, Calvin" sort="Chang, Calvin" uniqKey="Chang C" first="Calvin" last="Chang">Calvin Chang</name><name sortKey="Dawson, Ted M" sort="Dawson, Ted M" uniqKey="Dawson T" first="Ted M." last="Dawson">Ted M. Dawson</name><name sortKey="Dawson, Valina L" sort="Dawson, Valina L" uniqKey="Dawson V" first="Valina L." last="Dawson">Valina L. Dawson</name><name sortKey="Karuppagounder, Senthilkumar S" sort="Karuppagounder, Senthilkumar S" uniqKey="Karuppagounder S" first="Senthilkumar S." last="Karuppagounder">Senthilkumar S. Karuppagounder</name><name sortKey="Stevens, Daniel A" sort="Stevens, Daniel A" uniqKey="Stevens D" first="Daniel A." last="Stevens">Daniel A. Stevens</name><name sortKey="Umanah, George K E" sort="Umanah, George K E" uniqKey="Umanah G" first="George K. E." last="Umanah">George K. E. Umanah</name></noCountry><country name="Canada"><noRegion><name sortKey="Gagne, Jean Philippe" sort="Gagne, Jean Philippe" uniqKey="Gagne J" first="Jean-Philippe" last="Gagné">Jean-Philippe Gagné</name></noRegion><name sortKey="Poirier, Guy G" sort="Poirier, Guy G" uniqKey="Poirier G" first="Guy G." last="Poirier">Guy G. Poirier</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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