Cytosolic Isocitrate Dehydrogenase from Arabidopsis thaliana Is Regulated by Glutathionylation.
Identifieur interne : 000181 ( Main/Exploration ); précédent : 000180; suivant : 000182Cytosolic Isocitrate Dehydrogenase from Arabidopsis thaliana Is Regulated by Glutathionylation.
Auteurs : Adnan Khan Niazi [France, Pakistan] ; Laetitia Bariat [France] ; Christophe Riondet [France] ; Christine Carapito [France] ; Amna Mhamdi [France, Belgique] ; Graham Noctor [France] ; Jean-Philippe Reichheld [France]Source :
- Antioxidants (Basel, Switzerland) [ 2076-3921 ] ; 2019.
Abstract
NADP-dependent (Nicotinamide Adénine Dinucléotide Phosphate-dependent) isocitrate dehydrogenases (NADP-ICDH) are metabolic enzymes involved in 2-oxoglutarate biosynthesis, but they also supply cells with NADPH. Different NADP-ICDH genes are found in Arabidopsis among which a single gene encodes for a cytosolic ICDH (cICDH) isoform. Here, we show that cICDH is susceptible to oxidation and that several cysteine (Cys) residues are prone to S-nitrosylation upon nitrosoglutathione (GSNO) treatment. Moreover, we identified a single S-glutathionylated cysteine Cys363 by mass-spectrometry analyses. Modeling analyses suggest that Cys363 is not located in the close proximity of the cICDH active site. In addition, mutation of Cys363 consistently does not modify the activity of cICDH. However, it does affect the sensitivity of the enzyme to GSNO, indicating that S-glutathionylation of Cys363 is involved in the inhibition of cICDH activity upon GSNO treatments. We also show that glutaredoxin are able to rescue the GSNO-dependent inhibition of cICDH activity, suggesting that they act as a deglutathionylation system in vitro. The glutaredoxin system, conversely to the thioredoxin system, is able to remove S-nitrosothiol adducts from cICDH. Finally, NADP-ICDH activities were decreased both in a catalase2 mutant and in mutants affected in thiol reduction systems, suggesting a role of the thiol reduction systems to protect NADP-ICDH activities in planta. In line with our observations in Arabidopsis, we found that the human recombinant NADP-ICDH activity is also sensitive to oxidation in vitro, suggesting that this redox mechanism might be shared by other ICDH isoforms.
DOI: 10.3390/antiox8010016
PubMed: 30625997
PubMed Central: PMC6356969
Affiliations:
- Belgique, France, Pakistan
- Alsace (région administrative), Grand Est, Languedoc-Roussillon, Occitanie (région administrative), Province de Flandre-Orientale, Région flamande, Île-de-France
- Gand, Orsay, Perpignan, Strasbourg
- Université Paris-Sud, Université de Gand, Université de Strasbourg
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wicri:level="3"><nlm:affiliation>Laboratoire Génome et Développement des Plantes, CNRS, F-66860 Perpignan, France. christophe.riondet@univ-perp.fr.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Laboratoire Génome et Développement des Plantes, CNRS, F-66860 Perpignan</wicri:regionArea><placeName><region type="region" nuts="2">Occitanie (région administrative)</region><region type="old region" nuts="2">Languedoc-Roussillon</region><settlement type="city">Perpignan</settlement></placeName></affiliation></author><author><name sortKey="Carapito, Christine" sort="Carapito, Christine" uniqKey="Carapito C" first="Christine" last="Carapito">Christine Carapito</name><affiliation wicri:level="4"><nlm:affiliation>Laboratoire de Spectrométrie de Masse BioOrganique (LSMBO), IPHC, Université de Strasbourg, CNRS UMR 7178, 67037 Strasbourg, France. ccarapito@unistra.fr.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Laboratoire de Spectrométrie de 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jpr@univ-perp.fr.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Laboratoire Génome et Développement des Plantes, CNRS, F-66860 Perpignan</wicri:regionArea><placeName><region type="region" nuts="2">Occitanie (région administrative)</region><region type="old region" nuts="2">Languedoc-Roussillon</region><settlement type="city">Perpignan</settlement></placeName></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2019">2019</date><idno type="RBID">pubmed:30625997</idno><idno type="pmid">30625997</idno><idno type="doi">10.3390/antiox8010016</idno><idno type="pmc">PMC6356969</idno><idno type="wicri:Area/Main/Corpus">000175</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Corpus" wicri:corpus="PubMed">000175</idno><idno type="wicri:Area/Main/Curation">000175</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Curation">000175</idno><idno type="wicri:Area/Main/Exploration">000175</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">Cytosolic Isocitrate Dehydrogenase from <i>Arabidopsis thaliana</i> Is Regulated by Glutathionylation.</title><author><name sortKey="Niazi, Adnan Khan" sort="Niazi, Adnan Khan" uniqKey="Niazi A" first="Adnan Khan" last="Niazi">Adnan Khan Niazi</name><affiliation wicri:level="3"><nlm:affiliation>Laboratoire Génome et Développement des Plantes, Université Perpignan Via Domitia, F-66860 Perpignan, France. niazi@uaf.edu.pk.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Laboratoire Génome et Développement des Plantes, Université Perpignan Via Domitia, F-66860 Perpignan</wicri:regionArea><placeName><region type="region" nuts="2">Occitanie (région administrative)</region><region type="old region" nuts="2">Languedoc-Roussillon</region><settlement type="city">Perpignan</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:affiliation>Laboratoire Génome et Développement des Plantes, CNRS, F-66860 Perpignan, France. niazi@uaf.edu.pk.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Laboratoire Génome et Développement des Plantes, CNRS, F-66860 Perpignan</wicri:regionArea><placeName><region type="region" nuts="2">Occitanie (région administrative)</region><region type="old region" nuts="2">Languedoc-Roussillon</region><settlement type="city">Perpignan</settlement></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>Centre of Agricultural Biochemistry and Biotechnology, University of Agriculture Faisalabad, 38000 Faisalabad, Pakistan. niazi@uaf.edu.pk.</nlm:affiliation><country xml:lang="fr">Pakistan</country><wicri:regionArea>Centre of Agricultural Biochemistry and Biotechnology, University of Agriculture Faisalabad, 38000 Faisalabad</wicri:regionArea><wicri:noRegion>38000 Faisalabad</wicri:noRegion></affiliation></author><author><name sortKey="Bariat, Laetitia" sort="Bariat, Laetitia" uniqKey="Bariat L" first="Laetitia" last="Bariat">Laetitia Bariat</name><affiliation wicri:level="3"><nlm:affiliation>Laboratoire Génome et Développement des Plantes, Université Perpignan Via Domitia, F-66860 Perpignan, France. laetitia.bariat@univ-perp.fr.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Laboratoire Génome et Développement des Plantes, Université Perpignan Via Domitia, F-66860 Perpignan</wicri:regionArea><placeName><region type="region" nuts="2">Occitanie (région administrative)</region><region type="old region" nuts="2">Languedoc-Roussillon</region><settlement type="city">Perpignan</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:affiliation>Laboratoire Génome et Développement des Plantes, CNRS, F-66860 Perpignan, France. laetitia.bariat@univ-perp.fr.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Laboratoire Génome et Développement des Plantes, CNRS, F-66860 Perpignan</wicri:regionArea><placeName><region type="region" nuts="2">Occitanie (région administrative)</region><region type="old region" nuts="2">Languedoc-Roussillon</region><settlement type="city">Perpignan</settlement></placeName></affiliation></author><author><name sortKey="Riondet, Christophe" sort="Riondet, Christophe" uniqKey="Riondet C" first="Christophe" last="Riondet">Christophe Riondet</name><affiliation wicri:level="3"><nlm:affiliation>Laboratoire Génome et Développement des Plantes, Université Perpignan Via Domitia, F-66860 Perpignan, France. christophe.riondet@univ-perp.fr.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Laboratoire Génome et Développement des Plantes, Université Perpignan Via Domitia, F-66860 Perpignan</wicri:regionArea><placeName><region type="region" nuts="2">Occitanie (région administrative)</region><region type="old region" nuts="2">Languedoc-Roussillon</region><settlement type="city">Perpignan</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:affiliation>Laboratoire Génome et Développement des Plantes, CNRS, F-66860 Perpignan, France. christophe.riondet@univ-perp.fr.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Laboratoire Génome et Développement des Plantes, CNRS, F-66860 Perpignan</wicri:regionArea><placeName><region type="region" nuts="2">Occitanie (région administrative)</region><region type="old region" nuts="2">Languedoc-Roussillon</region><settlement type="city">Perpignan</settlement></placeName></affiliation></author><author><name sortKey="Carapito, Christine" sort="Carapito, Christine" uniqKey="Carapito C" first="Christine" last="Carapito">Christine Carapito</name><affiliation wicri:level="4"><nlm:affiliation>Laboratoire de Spectrométrie de Masse BioOrganique (LSMBO), IPHC, Université de Strasbourg, CNRS UMR 7178, 67037 Strasbourg, France. ccarapito@unistra.fr.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Laboratoire de Spectrométrie de Masse BioOrganique (LSMBO), IPHC, Université de Strasbourg, CNRS UMR 7178, 67037 Strasbourg</wicri:regionArea><placeName><region type="region" nuts="2">Grand Est</region><region type="old region" nuts="2">Alsace (région administrative)</region><settlement type="city">Strasbourg</settlement></placeName><orgName type="university">Université de Strasbourg</orgName></affiliation></author><author><name sortKey="Mhamdi, Amna" sort="Mhamdi, Amna" uniqKey="Mhamdi A" first="Amna" last="Mhamdi">Amna Mhamdi</name><affiliation wicri:level="4"><nlm:affiliation>Institute of Plant Sciences Paris Saclay IPS2, Université Paris-Sud, CNRS, INRA, Université Evry, Paris Diderot, Sorbonne Paris-Cité, Université Paris-Saclay, Bâtiment 630, 91405 Orsay, France. amna.mhamdi@psb.vib-ugent.be.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Institute of Plant Sciences Paris Saclay IPS2, Université Paris-Sud, CNRS, INRA, Université Evry, Paris Diderot, Sorbonne Paris-Cité, Université Paris-Saclay, Bâtiment 630, 91405 Orsay</wicri:regionArea><placeName><region type="region" nuts="2">Île-de-France</region><settlement type="city">Orsay</settlement></placeName><orgName type="university">Université Paris-Sud</orgName></affiliation><affiliation wicri:level="4"><nlm:affiliation>Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Gent, Belgium. amna.mhamdi@psb.vib-ugent.be.</nlm:affiliation><country xml:lang="fr">Belgique</country><wicri:regionArea>Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Gent</wicri:regionArea><orgName type="university">Université de Gand</orgName><placeName><settlement type="city">Gand</settlement><region>Région flamande</region><region type="district" nuts="2">Province de Flandre-Orientale</region></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>Center for Plant Systems Biology, VIB, 9052 Gent, Belgium. amna.mhamdi@psb.vib-ugent.be.</nlm:affiliation><country xml:lang="fr">Belgique</country><wicri:regionArea>Center for Plant Systems Biology, VIB, 9052 Gent</wicri:regionArea><wicri:noRegion>9052 Gent</wicri:noRegion></affiliation></author><author><name sortKey="Noctor, Graham" sort="Noctor, Graham" uniqKey="Noctor G" first="Graham" last="Noctor">Graham Noctor</name><affiliation wicri:level="4"><nlm:affiliation>Institute of Plant Sciences Paris Saclay IPS2, Université Paris-Sud, CNRS, INRA, Université Evry, Paris Diderot, Sorbonne Paris-Cité, Université Paris-Saclay, Bâtiment 630, 91405 Orsay, France. graham.noctor@u-psud.fr.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Institute of Plant Sciences Paris Saclay IPS2, Université Paris-Sud, CNRS, INRA, Université Evry, Paris Diderot, Sorbonne Paris-Cité, Université Paris-Saclay, Bâtiment 630, 91405 Orsay</wicri:regionArea><placeName><region type="region" nuts="2">Île-de-France</region><settlement type="city">Orsay</settlement></placeName><orgName type="university">Université Paris-Sud</orgName></affiliation></author><author><name sortKey="Reichheld, Jean Philippe" sort="Reichheld, Jean Philippe" uniqKey="Reichheld J" first="Jean-Philippe" last="Reichheld">Jean-Philippe Reichheld</name><affiliation wicri:level="3"><nlm:affiliation>Laboratoire Génome et Développement des Plantes, Université Perpignan Via Domitia, F-66860 Perpignan, France. jpr@univ-perp.fr.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Laboratoire Génome et Développement des Plantes, Université Perpignan Via Domitia, F-66860 Perpignan</wicri:regionArea><placeName><region type="region" nuts="2">Occitanie (région administrative)</region><region type="old region" nuts="2">Languedoc-Roussillon</region><settlement type="city">Perpignan</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:affiliation>Laboratoire Génome et Développement des Plantes, CNRS, F-66860 Perpignan, France. jpr@univ-perp.fr.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Laboratoire Génome et Développement des Plantes, CNRS, F-66860 Perpignan</wicri:regionArea><placeName><region type="region" nuts="2">Occitanie (région administrative)</region><region type="old region" nuts="2">Languedoc-Roussillon</region><settlement type="city">Perpignan</settlement></placeName></affiliation></author></analytic><series><title level="j">Antioxidants (Basel, Switzerland)</title><idno type="ISSN">2076-3921</idno><imprint><date when="2019" type="published">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">NADP-dependent (Nicotinamide Adénine Dinucléotide Phosphate-dependent) isocitrate dehydrogenases (NADP-ICDH) are metabolic enzymes involved in 2-oxoglutarate biosynthesis, but they also supply cells with NADPH. Different NADP-ICDH genes are found in <i>Arabidopsis</i> among which a single gene encodes for a cytosolic ICDH (cICDH) isoform. Here, we show that cICDH is susceptible to oxidation and that several cysteine (Cys) residues are prone to S-nitrosylation upon nitrosoglutathione (GSNO) treatment. Moreover, we identified a single S-glutathionylated cysteine Cys363 by mass-spectrometry analyses. Modeling analyses suggest that Cys363 is not located in the close proximity of the cICDH active site. In addition, mutation of Cys363 consistently does not modify the activity of cICDH. However, it does affect the sensitivity of the enzyme to GSNO, indicating that S-glutathionylation of Cys363 is involved in the inhibition of cICDH activity upon GSNO treatments. We also show that glutaredoxin are able to rescue the GSNO-dependent inhibition of cICDH activity, suggesting that they act as a deglutathionylation system <i>in vitro</i>. The glutaredoxin system, conversely to the thioredoxin system, is able to remove S-nitrosothiol adducts from cICDH. Finally, NADP-ICDH activities were decreased both in a <i>catalase2</i> mutant and in mutants affected in thiol reduction systems, suggesting a role of the thiol reduction systems to protect NADP-ICDH activities <i>in planta</i>. In line with our observations in Arabidopsis, we found that the human recombinant NADP-ICDH activity is also sensitive to oxidation <i>in vitro</i>, suggesting that this redox mechanism might be shared by other ICDH isoforms.</div></front></TEI><pubmed><MedlineCitation Status="PubMed-not-MEDLINE" Owner="NLM"><PMID Version="1">30625997</PMID><DateRevised><Year>2020</Year><Month>10</Month><Day>01</Day></DateRevised><Article PubModel="Electronic"><Journal><ISSN IssnType="Print">2076-3921</ISSN><JournalIssue CitedMedium="Print"><Volume>8</Volume><Issue>1</Issue><PubDate><Year>2019</Year><Month>Jan</Month><Day>08</Day></PubDate></JournalIssue><Title>Antioxidants (Basel, Switzerland)</Title><ISOAbbreviation>Antioxidants (Basel)</ISOAbbreviation></Journal><ArticleTitle>Cytosolic Isocitrate Dehydrogenase from <i>Arabidopsis thaliana</i> Is Regulated by Glutathionylation.</ArticleTitle><ELocationID EIdType="pii" ValidYN="Y">E16</ELocationID><ELocationID EIdType="doi" ValidYN="Y">10.3390/antiox8010016</ELocationID><Abstract><AbstractText>NADP-dependent (Nicotinamide Adénine Dinucléotide Phosphate-dependent) isocitrate dehydrogenases (NADP-ICDH) are metabolic enzymes involved in 2-oxoglutarate biosynthesis, but they also supply cells with NADPH. Different NADP-ICDH genes are found in <i>Arabidopsis</i> among which a single gene encodes for a cytosolic ICDH (cICDH) isoform. Here, we show that cICDH is susceptible to oxidation and that several cysteine (Cys) residues are prone to S-nitrosylation upon nitrosoglutathione (GSNO) treatment. Moreover, we identified a single S-glutathionylated cysteine Cys363 by mass-spectrometry analyses. Modeling analyses suggest that Cys363 is not located in the close proximity of the cICDH active site. In addition, mutation of Cys363 consistently does not modify the activity of cICDH. However, it does affect the sensitivity of the enzyme to GSNO, indicating that S-glutathionylation of Cys363 is involved in the inhibition of cICDH activity upon GSNO treatments. We also show that glutaredoxin are able to rescue the GSNO-dependent inhibition of cICDH activity, suggesting that they act as a deglutathionylation system <i>in vitro</i>. The glutaredoxin system, conversely to the thioredoxin system, is able to remove S-nitrosothiol adducts from cICDH. Finally, NADP-ICDH activities were decreased both in a <i>catalase2</i> mutant and in mutants affected in thiol reduction systems, suggesting a role of the thiol reduction systems to protect NADP-ICDH activities <i>in planta</i>. In line with our observations in Arabidopsis, we found that the human recombinant NADP-ICDH activity is also sensitive to oxidation <i>in vitro</i>, suggesting that this redox mechanism might be shared by other ICDH isoforms.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Niazi</LastName><ForeName>Adnan Khan</ForeName><Initials>AK</Initials><Identifier Source="ORCID">0000-0002-9006-7377</Identifier><AffiliationInfo><Affiliation>Laboratoire Génome et Développement des Plantes, Université Perpignan Via Domitia, F-66860 Perpignan, France. niazi@uaf.edu.pk.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Laboratoire Génome et Développement des Plantes, CNRS, F-66860 Perpignan, France. niazi@uaf.edu.pk.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Centre of Agricultural Biochemistry and Biotechnology, University of Agriculture Faisalabad, 38000 Faisalabad, Pakistan. niazi@uaf.edu.pk.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Bariat</LastName><ForeName>Laetitia</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>Laboratoire Génome et Développement des Plantes, Université Perpignan Via Domitia, F-66860 Perpignan, France. laetitia.bariat@univ-perp.fr.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Laboratoire Génome et Développement des Plantes, CNRS, F-66860 Perpignan, France. laetitia.bariat@univ-perp.fr.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Riondet</LastName><ForeName>Christophe</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>Laboratoire Génome et Développement des Plantes, Université Perpignan Via Domitia, F-66860 Perpignan, France. christophe.riondet@univ-perp.fr.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Laboratoire Génome et Développement des Plantes, CNRS, F-66860 Perpignan, France. christophe.riondet@univ-perp.fr.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Carapito</LastName><ForeName>Christine</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>Laboratoire de Spectrométrie de Masse BioOrganique (LSMBO), IPHC, Université de Strasbourg, CNRS UMR 7178, 67037 Strasbourg, France. ccarapito@unistra.fr.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Mhamdi</LastName><ForeName>Amna</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Institute of Plant Sciences Paris Saclay IPS2, Université Paris-Sud, CNRS, INRA, Université Evry, Paris Diderot, Sorbonne Paris-Cité, Université Paris-Saclay, Bâtiment 630, 91405 Orsay, France. amna.mhamdi@psb.vib-ugent.be.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Gent, Belgium. amna.mhamdi@psb.vib-ugent.be.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Center for Plant Systems Biology, VIB, 9052 Gent, Belgium. amna.mhamdi@psb.vib-ugent.be.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Noctor</LastName><ForeName>Graham</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>Institute of Plant Sciences Paris Saclay IPS2, Université Paris-Sud, CNRS, INRA, Université Evry, Paris Diderot, Sorbonne Paris-Cité, Université Paris-Saclay, Bâtiment 630, 91405 Orsay, France. graham.noctor@u-psud.fr.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Reichheld</LastName><ForeName>Jean-Philippe</ForeName><Initials>JP</Initials><AffiliationInfo><Affiliation>Laboratoire Génome et Développement des Plantes, Université Perpignan Via Domitia, F-66860 Perpignan, France. jpr@univ-perp.fr.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Laboratoire Génome et Développement des Plantes, CNRS, F-66860 Perpignan, France. jpr@univ-perp.fr.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>12-BSV6-0011</GrantID><Agency>Agence Nationale de la Recherche</Agency><Country></Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2019</Year><Month>01</Month><Day>08</Day></ArticleDate></Article><MedlineJournalInfo><Country>Switzerland</Country><MedlineTA>Antioxidants (Basel)</MedlineTA><NlmUniqueID>101668981</NlmUniqueID><ISSNLinking>2076-3921</ISSNLinking></MedlineJournalInfo><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Arabidopsis thaliana</Keyword><Keyword MajorTopicYN="N">Isocitrate dehydrogenase</Keyword><Keyword MajorTopicYN="N">glutaredoxin</Keyword><Keyword MajorTopicYN="N">glutathionylation</Keyword><Keyword MajorTopicYN="N">nitrosylation</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2018</Year><Month>11</Month><Day>15</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2018</Year><Month>12</Month><Day>19</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2018</Year><Month>12</Month><Day>22</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2019</Year><Month>1</Month><Day>11</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2019</Year><Month>1</Month><Day>11</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2019</Year><Month>1</Month><Day>11</Day><Hour>6</Hour><Minute>1</Minute></PubMedPubDate></History><PublicationStatus>epublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">30625997</ArticleId><ArticleId IdType="pii">antiox8010016</ArticleId><ArticleId 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last="Niazi">Adnan Khan Niazi</name></noRegion></country><country name="Belgique"><region name="Région flamande"><name sortKey="Mhamdi, Amna" sort="Mhamdi, Amna" uniqKey="Mhamdi A" first="Amna" last="Mhamdi">Amna Mhamdi</name></region><name sortKey="Mhamdi, Amna" sort="Mhamdi, Amna" uniqKey="Mhamdi A" first="Amna" last="Mhamdi">Amna Mhamdi</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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