Aging-dependent changes in rat heart mitochondrial glutaredoxins--Implications for redox regulation.
Identifieur interne : 000788 ( Main/Exploration ); précédent : 000787; suivant : 000789Aging-dependent changes in rat heart mitochondrial glutaredoxins--Implications for redox regulation.
Auteurs : Xing-Huang Gao [États-Unis] ; Suparna Qanungo [États-Unis] ; Harish V. Pai [États-Unis] ; David W. Starke [États-Unis] ; Kelly M. Steller [États-Unis] ; Hisashi Fujioka [États-Unis] ; Edward J. Lesnefsky [États-Unis] ; Janos Kerner [États-Unis] ; Mariana G. Rosca [États-Unis] ; Charles L. Hoppel [États-Unis] ; John J. Mieyal [États-Unis]Source :
- Redox biology [ 2213-2317 ] ; 2013.
Descripteurs français
- KwdFr :
- MESH :
- enzymologie : Mitochondries du myocarde.
- métabolisme : Glutarédoxines, Mitochondries du myocarde, Vieillissement.
- Animaux, Oxydoréduction, Rats, Rats de lignée F344.
English descriptors
- KwdEn :
- MESH :
- chemical , metabolism : Glutaredoxins.
- enzymology : Mitochondria, Heart.
- metabolism : Aging, Mitochondria, Heart.
- Animals, Oxidation-Reduction, Rats, Rats, Inbred F344.
Abstract
Clinical and animal studies have documented that hearts of the elderly are more susceptible to ischemia/reperfusion damage compared to young adults. Recently we found that aging-dependent increase in susceptibility of cardiomyocytes to apoptosis was attributable to decrease in cytosolic glutaredoxin 1 (Grx1) and concomitant decrease in NF-κB-mediated expression of anti-apoptotic proteins. Besides primary localization in the cytosol, Grx1 also exists in the mitochondrial intermembrane space (IMS). In contrast, Grx2 is confined to the mitochondrial matrix. Here we report that Grx1 is decreased by 50-60% in the IMS, but Grx2 is increased by 1.4-2.6 fold in the matrix of heart mitochondria from elderly rats. Determination of in situ activities of the Grx isozymes from both subsarcolemmal (SSM) and interfibrillar (IFM) mitochondria revealed that Grx1 was fully active in the IMS. However, Grx2 was mostly in an inactive form in the matrix, consistent with reversible sequestration of the active-site cysteines of two Grx2 molecules in complex with an iron-sulfur cluster. Our quantitative evaluations of the active/inactive ratio for Grx2 suggest that levels of dimeric Grx2 complex with iron-sulfur clusters are increased in SSM and IFM in the hearts of elderly rats. We found that the inactive Grx2 can be fully reactivated by sodium dithionite or exogenous superoxide production mediated by xanthine oxidase. However, treatment with rotenone, which generates intramitochondrial superoxide through inhibition of mitochondrial respiratory chain Complex I, did not lead to Grx2 activation. These findings suggest that insufficient ROS accumulates in the vicinity of dimeric Grx2 to activate it in situ.
DOI: 10.1016/j.redox.2013.10.010
PubMed: 25126518
PubMed Central: PMC4127417
Affiliations:
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Pai</name><affiliation wicri:level="2"><nlm:affiliation>Department of Pharmacology, Division of Cardiology, Case Western Reserve University, School of Medicine, Cleveland, OH 44106, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Pharmacology, Division of Cardiology, Case Western Reserve University, School of Medicine, Cleveland, OH 44106</wicri:regionArea><placeName><region type="state">Ohio</region></placeName></affiliation></author><author><name sortKey="Starke, David W" sort="Starke, David W" uniqKey="Starke D" first="David W" last="Starke">David W. Starke</name><affiliation wicri:level="2"><nlm:affiliation>Department of Pharmacology, Division of Cardiology, Case Western Reserve University, School of Medicine, Cleveland, OH 44106, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Pharmacology, Division of Cardiology, Case Western Reserve University, School of Medicine, Cleveland, OH 44106</wicri:regionArea><placeName><region type="state">Ohio</region></placeName></affiliation></author><author><name sortKey="Steller, Kelly M" sort="Steller, Kelly M" uniqKey="Steller K" first="Kelly M" last="Steller">Kelly M. Steller</name><affiliation wicri:level="2"><nlm:affiliation>Department of Pharmacology, Division of Cardiology, Case Western Reserve University, School of Medicine, Cleveland, OH 44106, USA ; Louis Stokes Cleveland Veterans Affairs Medical Research Center, Cleveland, OH 44106, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Pharmacology, Division of Cardiology, Case Western Reserve University, School of Medicine, Cleveland, OH 44106, USA ; Louis Stokes Cleveland Veterans Affairs Medical Research Center, Cleveland, OH 44106</wicri:regionArea><placeName><region type="state">Ohio</region></placeName></affiliation></author><author><name sortKey="Fujioka, Hisashi" sort="Fujioka, Hisashi" uniqKey="Fujioka H" first="Hisashi" last="Fujioka">Hisashi Fujioka</name><affiliation wicri:level="2"><nlm:affiliation>Center for Mitochondrial Disease, Division of Cardiology, Case Western Reserve University, School of Medicine, Cleveland, OH 44106, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Center for Mitochondrial Disease, Division of Cardiology, Case Western Reserve University, School of Medicine, Cleveland, OH 44106</wicri:regionArea><placeName><region type="state">Ohio</region></placeName></affiliation></author><author><name sortKey="Lesnefsky, Edward J" sort="Lesnefsky, Edward J" uniqKey="Lesnefsky E" first="Edward J" last="Lesnefsky">Edward J. Lesnefsky</name><affiliation wicri:level="2"><nlm:affiliation>Department of Medicine, Division of Cardiology, Case Western Reserve University, School of Medicine, Cleveland, OH 44106, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Medicine, Division of Cardiology, Case Western Reserve University, School of Medicine, Cleveland, OH 44106</wicri:regionArea><placeName><region type="state">Ohio</region></placeName></affiliation></author><author><name sortKey="Kerner, Janos" sort="Kerner, Janos" uniqKey="Kerner J" first="Janos" last="Kerner">Janos Kerner</name><affiliation wicri:level="2"><nlm:affiliation>Department of Pharmacology, Division of Cardiology, Case Western Reserve University, School of Medicine, Cleveland, OH 44106, USA ; Center for Mitochondrial Disease, Division of Cardiology, Case Western Reserve University, School of Medicine, Cleveland, OH 44106, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Pharmacology, Division of Cardiology, Case Western Reserve University, School of Medicine, Cleveland, OH 44106, USA ; Center for Mitochondrial Disease, Division of Cardiology, Case Western Reserve University, School of Medicine, Cleveland, OH 44106</wicri:regionArea><placeName><region type="state">Ohio</region></placeName></affiliation></author><author><name sortKey="Rosca, Mariana G" sort="Rosca, Mariana G" uniqKey="Rosca M" first="Mariana G" last="Rosca">Mariana G. Rosca</name><affiliation wicri:level="2"><nlm:affiliation>Department of Pharmacology, Division of Cardiology, Case Western Reserve University, School of Medicine, Cleveland, OH 44106, USA ; Center for Mitochondrial Disease, Division of Cardiology, Case Western Reserve University, School of Medicine, Cleveland, OH 44106, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Pharmacology, Division of Cardiology, Case Western Reserve University, School of Medicine, Cleveland, OH 44106, USA ; Center for Mitochondrial Disease, Division of Cardiology, Case Western Reserve University, School of Medicine, Cleveland, OH 44106</wicri:regionArea><placeName><region type="state">Ohio</region></placeName></affiliation></author><author><name sortKey="Hoppel, Charles L" sort="Hoppel, Charles L" uniqKey="Hoppel C" first="Charles L" last="Hoppel">Charles L. Hoppel</name><affiliation wicri:level="2"><nlm:affiliation>Department of Pharmacology, Division of Cardiology, Case Western Reserve University, School of Medicine, Cleveland, OH 44106, USA ; Center for Mitochondrial Disease, Division of Cardiology, Case Western Reserve University, School of Medicine, Cleveland, OH 44106, USA ; Department of Medicine, Division of Cardiology, Case Western Reserve University, School of Medicine, Cleveland, OH 44106, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Pharmacology, Division of Cardiology, Case Western Reserve University, School of Medicine, Cleveland, OH 44106, USA ; Center for Mitochondrial Disease, Division of Cardiology, Case Western Reserve University, School of Medicine, Cleveland, OH 44106, USA ; Department of Medicine, Division of Cardiology, Case Western Reserve University, School of Medicine, Cleveland, OH 44106</wicri:regionArea><placeName><region type="state">Ohio</region></placeName></affiliation></author><author><name sortKey="Mieyal, John J" sort="Mieyal, John J" uniqKey="Mieyal J" first="John J" last="Mieyal">John J. Mieyal</name><affiliation wicri:level="2"><nlm:affiliation>Department of Pharmacology, Division of Cardiology, Case Western Reserve University, School of Medicine, Cleveland, OH 44106, USA ; Louis Stokes Cleveland Veterans Affairs Medical Research Center, Cleveland, OH 44106, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Pharmacology, Division of Cardiology, Case Western Reserve University, School of Medicine, Cleveland, OH 44106, USA ; Louis Stokes Cleveland Veterans Affairs Medical Research Center, Cleveland, OH 44106</wicri:regionArea><placeName><region type="state">Ohio</region></placeName></affiliation></author></analytic><series><title level="j">Redox biology</title><idno type="eISSN">2213-2317</idno><imprint><date when="2013" type="published">2013</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Aging (metabolism)</term><term>Animals (MeSH)</term><term>Glutaredoxins (metabolism)</term><term>Mitochondria, Heart (enzymology)</term><term>Mitochondria, Heart (metabolism)</term><term>Oxidation-Reduction (MeSH)</term><term>Rats (MeSH)</term><term>Rats, Inbred F344 (MeSH)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Animaux (MeSH)</term><term>Glutarédoxines (métabolisme)</term><term>Mitochondries du myocarde (enzymologie)</term><term>Mitochondries du myocarde (métabolisme)</term><term>Oxydoréduction (MeSH)</term><term>Rats (MeSH)</term><term>Rats de lignée F344 (MeSH)</term><term>Vieillissement (métabolisme)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Glutaredoxins</term></keywords><keywords scheme="MESH" qualifier="enzymologie" xml:lang="fr"><term>Mitochondries du myocarde</term></keywords><keywords scheme="MESH" qualifier="enzymology" xml:lang="en"><term>Mitochondria, Heart</term></keywords><keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Aging</term><term>Mitochondria, Heart</term></keywords><keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Glutarédoxines</term><term>Mitochondries du myocarde</term><term>Vieillissement</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Animals</term><term>Oxidation-Reduction</term><term>Rats</term><term>Rats, Inbred F344</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Animaux</term><term>Oxydoréduction</term><term>Rats</term><term>Rats de lignée F344</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Clinical and animal studies have documented that hearts of the elderly are more susceptible to ischemia/reperfusion damage compared to young adults. Recently we found that aging-dependent increase in susceptibility of cardiomyocytes to apoptosis was attributable to decrease in cytosolic glutaredoxin 1 (Grx1) and concomitant decrease in NF-κB-mediated expression of anti-apoptotic proteins. Besides primary localization in the cytosol, Grx1 also exists in the mitochondrial intermembrane space (IMS). In contrast, Grx2 is confined to the mitochondrial matrix. Here we report that Grx1 is decreased by 50-60% in the IMS, but Grx2 is increased by 1.4-2.6 fold in the matrix of heart mitochondria from elderly rats. Determination of in situ activities of the Grx isozymes from both subsarcolemmal (SSM) and interfibrillar (IFM) mitochondria revealed that Grx1 was fully active in the IMS. However, Grx2 was mostly in an inactive form in the matrix, consistent with reversible sequestration of the active-site cysteines of two Grx2 molecules in complex with an iron-sulfur cluster. Our quantitative evaluations of the active/inactive ratio for Grx2 suggest that levels of dimeric Grx2 complex with iron-sulfur clusters are increased in SSM and IFM in the hearts of elderly rats. We found that the inactive Grx2 can be fully reactivated by sodium dithionite or exogenous superoxide production mediated by xanthine oxidase. However, treatment with rotenone, which generates intramitochondrial superoxide through inhibition of mitochondrial respiratory chain Complex I, did not lead to Grx2 activation. These findings suggest that insufficient ROS accumulates in the vicinity of dimeric Grx2 to activate it in situ. </div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">25126518</PMID><DateCompleted><Year>2015</Year><Month>04</Month><Day>09</Day></DateCompleted><DateRevised><Year>2018</Year><Month>11</Month><Day>13</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Electronic">2213-2317</ISSN><JournalIssue CitedMedium="Internet"><Volume>1</Volume><PubDate><Year>2013</Year></PubDate></JournalIssue><Title>Redox biology</Title><ISOAbbreviation>Redox Biol</ISOAbbreviation></Journal><ArticleTitle>Aging-dependent changes in rat heart mitochondrial glutaredoxins--Implications for redox regulation.</ArticleTitle><Pagination><MedlinePgn>586-98</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1016/j.redox.2013.10.010</ELocationID><Abstract><AbstractText>Clinical and animal studies have documented that hearts of the elderly are more susceptible to ischemia/reperfusion damage compared to young adults. Recently we found that aging-dependent increase in susceptibility of cardiomyocytes to apoptosis was attributable to decrease in cytosolic glutaredoxin 1 (Grx1) and concomitant decrease in NF-κB-mediated expression of anti-apoptotic proteins. Besides primary localization in the cytosol, Grx1 also exists in the mitochondrial intermembrane space (IMS). In contrast, Grx2 is confined to the mitochondrial matrix. Here we report that Grx1 is decreased by 50-60% in the IMS, but Grx2 is increased by 1.4-2.6 fold in the matrix of heart mitochondria from elderly rats. Determination of in situ activities of the Grx isozymes from both subsarcolemmal (SSM) and interfibrillar (IFM) mitochondria revealed that Grx1 was fully active in the IMS. However, Grx2 was mostly in an inactive form in the matrix, consistent with reversible sequestration of the active-site cysteines of two Grx2 molecules in complex with an iron-sulfur cluster. Our quantitative evaluations of the active/inactive ratio for Grx2 suggest that levels of dimeric Grx2 complex with iron-sulfur clusters are increased in SSM and IFM in the hearts of elderly rats. We found that the inactive Grx2 can be fully reactivated by sodium dithionite or exogenous superoxide production mediated by xanthine oxidase. However, treatment with rotenone, which generates intramitochondrial superoxide through inhibition of mitochondrial respiratory chain Complex I, did not lead to Grx2 activation. These findings suggest that insufficient ROS accumulates in the vicinity of dimeric Grx2 to activate it in situ. </AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Gao</LastName><ForeName>Xing-Huang</ForeName><Initials>XH</Initials><AffiliationInfo><Affiliation>Department of Pharmacology, Division of Cardiology, Case Western Reserve University, School of Medicine, Cleveland, OH 44106, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Qanungo</LastName><ForeName>Suparna</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Department of Pharmacology, Division of Cardiology, Case Western Reserve University, School of Medicine, Cleveland, OH 44106, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Pai</LastName><ForeName>Harish V</ForeName><Initials>HV</Initials><AffiliationInfo><Affiliation>Department of Pharmacology, Division of Cardiology, Case Western Reserve University, School of Medicine, Cleveland, OH 44106, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Starke</LastName><ForeName>David W</ForeName><Initials>DW</Initials><AffiliationInfo><Affiliation>Department of Pharmacology, Division of Cardiology, Case Western Reserve University, School of Medicine, Cleveland, OH 44106, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Steller</LastName><ForeName>Kelly M</ForeName><Initials>KM</Initials><AffiliationInfo><Affiliation>Department of Pharmacology, Division of Cardiology, Case Western Reserve University, School of Medicine, Cleveland, OH 44106, USA ; Louis Stokes Cleveland Veterans Affairs Medical Research Center, Cleveland, OH 44106, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Fujioka</LastName><ForeName>Hisashi</ForeName><Initials>H</Initials><AffiliationInfo><Affiliation>Center for Mitochondrial Disease, Division of Cardiology, Case Western Reserve University, School of Medicine, Cleveland, OH 44106, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lesnefsky</LastName><ForeName>Edward J</ForeName><Initials>EJ</Initials><AffiliationInfo><Affiliation>Department of Medicine, Division of Cardiology, Case Western Reserve University, School of Medicine, Cleveland, OH 44106, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kerner</LastName><ForeName>Janos</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Department of Pharmacology, Division of Cardiology, Case Western Reserve University, School of Medicine, Cleveland, OH 44106, USA ; Center for Mitochondrial Disease, Division of Cardiology, Case Western Reserve University, School of Medicine, Cleveland, OH 44106, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Rosca</LastName><ForeName>Mariana G</ForeName><Initials>MG</Initials><AffiliationInfo><Affiliation>Department of Pharmacology, Division of Cardiology, Case Western Reserve University, School of Medicine, Cleveland, OH 44106, USA ; Center for Mitochondrial Disease, Division of Cardiology, Case Western Reserve University, School of Medicine, Cleveland, OH 44106, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hoppel</LastName><ForeName>Charles L</ForeName><Initials>CL</Initials><AffiliationInfo><Affiliation>Department of Pharmacology, Division of Cardiology, Case Western Reserve University, School of Medicine, Cleveland, OH 44106, USA ; Center for Mitochondrial Disease, Division of Cardiology, Case Western Reserve University, School of Medicine, Cleveland, OH 44106, USA ; Department of Medicine, Division of Cardiology, Case Western Reserve University, School of Medicine, Cleveland, OH 44106, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Mieyal</LastName><ForeName>John J</ForeName><Initials>JJ</Initials><AffiliationInfo><Affiliation>Department of Pharmacology, Division of Cardiology, Case Western 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Article</PublicationType><PublicationType UI="D052061">Research Support, N.I.H., Extramural</PublicationType><PublicationType UI="D013486">Research Support, U.S. Gov't, Non-P.H.S.</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2013</Year><Month>11</Month><Day>12</Day></ArticleDate></Article><MedlineJournalInfo><Country>Netherlands</Country><MedlineTA>Redox Biol</MedlineTA><NlmUniqueID>101605639</NlmUniqueID><ISSNLinking>2213-2317</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D054477">Glutaredoxins</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D000375" MajorTopicYN="N">Aging</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D000818" MajorTopicYN="N">Animals</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D054477" MajorTopicYN="N">Glutaredoxins</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D008929" MajorTopicYN="N">Mitochondria, Heart</DescriptorName><QualifierName UI="Q000201" MajorTopicYN="Y">enzymology</QualifierName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D010084" MajorTopicYN="N">Oxidation-Reduction</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D051381" MajorTopicYN="N">Rats</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D011916" MajorTopicYN="N">Rats, Inbred F344</DescriptorName></MeshHeading></MeshHeadingList><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Aging</Keyword><Keyword MajorTopicYN="N">Cys-SSG, l-cysteine–glutathione mixed disulfide</Keyword><Keyword MajorTopicYN="N">DT, sodium dithionite</Keyword><Keyword MajorTopicYN="N">GSH, reduced 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