Deciphering of mitochondrial cardiolipin oxidative signaling in cerebral ischemia-reperfusion
Identifieur interne : 003538 ( Main/Exploration ); précédent : 003537; suivant : 003539Deciphering of mitochondrial cardiolipin oxidative signaling in cerebral ischemia-reperfusion
Auteurs : Jing Ji [États-Unis, République populaire de Chine] ; Sophie Baart [États-Unis, Pays-Bas] ; Anna S. Vikulina [États-Unis] ; Robert Sb Clark [États-Unis] ; Tamil S. Anthonymuthu [États-Unis] ; Vladimir A. Tyurin [États-Unis] ; Lina Du [États-Unis] ; Claudette M. St Croix [États-Unis] ; Yulia Y. Tyurina [États-Unis] ; Jesse Lewis [États-Unis] ; Erin M. Skoda [États-Unis] ; Anthony E. Kline [États-Unis] ; Patrick M. Kochanek [États-Unis] ; Peter Wipf [États-Unis] ; Valerian E. Kagan [États-Unis] ; Hülya Bay R [États-Unis]Source :
- Journal of Cerebral Blood Flow & Metabolism [ 0271-678X ] ; 2014.
Descripteurs français
- KwdFr :
- Angiopathies intracrâniennes (anatomopathologie), Angiopathies intracrâniennes (métabolisme), Animaux, Cardiolipides (métabolisme), Facteurs temps, Lésion d'ischémie-reperfusion (anatomopathologie), Lésion d'ischémie-reperfusion (métabolisme), Mitochondries (anatomopathologie), Mitochondries (métabolisme), Mâle, Oxydoréduction, Rat Sprague-Dawley, Rats, Transduction du signal.
- MESH :
- anatomopathologie : Angiopathies intracrâniennes, Lésion d'ischémie-reperfusion, Mitochondries.
- métabolisme : Angiopathies intracrâniennes, Cardiolipides, Lésion d'ischémie-reperfusion, Mitochondries.
- Animaux, Facteurs temps, Mâle, Oxydoréduction, Rat Sprague-Dawley, Rats, Transduction du signal.
English descriptors
- KwdEn :
- Animals, Cardiolipins (metabolism), Cerebrovascular Disorders (metabolism), Cerebrovascular Disorders (pathology), Male, Mitochondria (metabolism), Mitochondria (pathology), Oxidation-Reduction, Rats, Rats, Sprague-Dawley, Reperfusion Injury (metabolism), Reperfusion Injury (pathology), Signal Transduction, Time Factors.
- MESH :
- chemical , metabolism : Cardiolipins.
- metabolism : Cerebrovascular Disorders, Mitochondria, Reperfusion Injury.
- pathology : Cerebrovascular Disorders, Mitochondria, Reperfusion Injury.
- Animals, Male, Oxidation-Reduction, Rats, Rats, Sprague-Dawley, Signal Transduction, Time Factors.
Abstract
It is believed that biosynthesis of lipid mediators in the central nervous system after cerebral ischemia-reperfusion starts with phospholipid hydrolysis by calcium-dependent phospholipases and is followed by oxygenation of released fatty acids (FAs). Here, we report an alternative pathway whereby cereberal ischemia-reperfusion triggered oxygenation of a mitochondria-specific phospholipid, cardiolipin (CL), is followed by its hydrolysis to yield monolyso-CLs and oxygenated derivatives of fatty (linoleic) acids. We used a model of global cerebral ischemia-reperfusion characterized by 9 minutes of asphyxia leading to asystole followed by cardiopulmonary resuscitation in postnatal day 17 rats. Global ischemia and cardiopulmonary resuscitation resulted in: (1) selective oxidation and hydrolysis of CLs, (2) accumulation of lyso-CLs and oxygenated free FAs, (3) activation of caspase 3/7 in the brain, and (4) motor and cognitive dysfunction. On the basis of these findings, we used a mitochondria targeted nitroxide electron scavenger, which prevented CL oxidation and subsequent hydrolysis, attenuated caspase activation, and improved neurocognitive outcome when administered after cardiac arrest. These data show that calcium-independent CL oxidation and subsequent hydrolysis represent a previously unidentified pathogenic mechanism of brain injury incurred by ischemia-reperfusion and a clinically relevant therapeutic target.
Url:
DOI: 10.1038/jcbfm.2014.204
PubMed: 25407268
PubMed Central: 4426750
Affiliations:
- Pays-Bas, République populaire de Chine, États-Unis
- Pennsylvanie
- Pittsburgh
- Université de Pittsburgh
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Le document en format XML
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</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff6"><institution>Medical School at VU Medical Centre, Amsterdam</institution>
,<country>The Netherlands</country>
</nlm:aff>
<country xml:lang="fr">Pays-Bas</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Vikulina, Anna S" sort="Vikulina, Anna S" uniqKey="Vikulina A" first="Anna S" last="Vikulina">Anna S. Vikulina</name>
<affiliation wicri:level="1"><nlm:aff id="aff3"><institution>Department of Environmental and Occupational Health, University of Pittsburgh</institution>
, Pittsburgh, PA,<country>USA</country>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff4"><institution>Center for Free Radical and Antioxidant Health, University of Pittsburgh</institution>
, Pittsburgh, PA,<country>USA</country>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Clark, Robert Sb" sort="Clark, Robert Sb" uniqKey="Clark R" first="Robert Sb" last="Clark">Robert Sb Clark</name>
<affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Department of Critical Care Medicine, University of Pittsburgh</institution>
, Pittsburgh, PA,<country>USA</country>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff2"><institution>Safar Center for Resuscitation Research, University of Pittsburgh</institution>
, Pittsburgh, PA,<country>USA</country>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff7"><institution>Children's Hospital of Pittsburgh</institution>
, Pittsburgh, PA,<country>USA</country>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Anthonymuthu, Tamil S" sort="Anthonymuthu, Tamil S" uniqKey="Anthonymuthu T" first="Tamil S" last="Anthonymuthu">Tamil S. Anthonymuthu</name>
<affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Department of Critical Care Medicine, University of Pittsburgh</institution>
, Pittsburgh, PA,<country>USA</country>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff2"><institution>Safar Center for Resuscitation Research, University of Pittsburgh</institution>
, Pittsburgh, PA,<country>USA</country>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff4"><institution>Center for Free Radical and Antioxidant Health, University of Pittsburgh</institution>
, Pittsburgh, PA,<country>USA</country>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Tyurin, Vladimir A" sort="Tyurin, Vladimir A" uniqKey="Tyurin V" first="Vladimir A" last="Tyurin">Vladimir A. Tyurin</name>
<affiliation wicri:level="1"><nlm:aff id="aff3"><institution>Department of Environmental and Occupational Health, University of Pittsburgh</institution>
, Pittsburgh, PA,<country>USA</country>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff4"><institution>Center for Free Radical and Antioxidant Health, University of Pittsburgh</institution>
, Pittsburgh, PA,<country>USA</country>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Du, Lina" sort="Du, Lina" uniqKey="Du L" first="Lina" last="Du">Lina Du</name>
<affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Department of Critical Care Medicine, University of Pittsburgh</institution>
, Pittsburgh, PA,<country>USA</country>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff2"><institution>Safar Center for Resuscitation Research, University of Pittsburgh</institution>
, Pittsburgh, PA,<country>USA</country>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="St Croix, Claudette M" sort="St Croix, Claudette M" uniqKey="St Croix C" first="Claudette M" last="St Croix">Claudette M. St Croix</name>
<affiliation wicri:level="1"><nlm:aff id="aff3"><institution>Department of Environmental and Occupational Health, University of Pittsburgh</institution>
, Pittsburgh, PA,<country>USA</country>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Tyurina, Yulia Y" sort="Tyurina, Yulia Y" uniqKey="Tyurina Y" first="Yulia Y" last="Tyurina">Yulia Y. Tyurina</name>
<affiliation wicri:level="1"><nlm:aff id="aff3"><institution>Department of Environmental and Occupational Health, University of Pittsburgh</institution>
, Pittsburgh, PA,<country>USA</country>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff4"><institution>Center for Free Radical and Antioxidant Health, University of Pittsburgh</institution>
, Pittsburgh, PA,<country>USA</country>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Lewis, Jesse" sort="Lewis, Jesse" uniqKey="Lewis J" first="Jesse" last="Lewis">Jesse Lewis</name>
<affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Department of Critical Care Medicine, University of Pittsburgh</institution>
, Pittsburgh, PA,<country>USA</country>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff2"><institution>Safar Center for Resuscitation Research, University of Pittsburgh</institution>
, Pittsburgh, PA,<country>USA</country>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Skoda, Erin M" sort="Skoda, Erin M" uniqKey="Skoda E" first="Erin M" last="Skoda">Erin M. Skoda</name>
<affiliation wicri:level="1"><nlm:aff id="aff8"><institution>Department of Chemistry, University of Pittsburgh</institution>
, Pittsburgh, PA,<country>USA</country>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Kline, Anthony E" sort="Kline, Anthony E" uniqKey="Kline A" first="Anthony E" last="Kline">Anthony E. Kline</name>
<affiliation wicri:level="1"><nlm:aff id="aff9"><institution>Department of Physical Medicine & Rehabilitation, University of Pittsburgh</institution>
, Pittsburgh, PA,<country>USA</country>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Kochanek, Patrick M" sort="Kochanek, Patrick M" uniqKey="Kochanek P" first="Patrick M" last="Kochanek">Patrick M. Kochanek</name>
<affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Department of Critical Care Medicine, University of Pittsburgh</institution>
, Pittsburgh, PA,<country>USA</country>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff2"><institution>Safar Center for Resuscitation Research, University of Pittsburgh</institution>
, Pittsburgh, PA,<country>USA</country>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff7"><institution>Children's Hospital of Pittsburgh</institution>
, Pittsburgh, PA,<country>USA</country>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Wipf, Peter" sort="Wipf, Peter" uniqKey="Wipf P" first="Peter" last="Wipf">Peter Wipf</name>
<affiliation wicri:level="1"><nlm:aff id="aff8"><institution>Department of Chemistry, University of Pittsburgh</institution>
, Pittsburgh, PA,<country>USA</country>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
<placeName><settlement type="city">Pittsburgh</settlement>
<region type="state">Pennsylvanie</region>
</placeName>
<orgName type="university" n="3">Université de Pittsburgh</orgName>
</affiliation>
</author>
<author><name sortKey="Kagan, Valerian E" sort="Kagan, Valerian E" uniqKey="Kagan V" first="Valerian E" last="Kagan">Valerian E. Kagan</name>
<affiliation wicri:level="1"><nlm:aff id="aff3"><institution>Department of Environmental and Occupational Health, University of Pittsburgh</institution>
, Pittsburgh, PA,<country>USA</country>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff4"><institution>Center for Free Radical and Antioxidant Health, University of Pittsburgh</institution>
, Pittsburgh, PA,<country>USA</country>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Bay R, Hulya" sort="Bay R, Hulya" uniqKey="Bay R H" first="Hülya" last="Bay R">Hülya Bay R</name>
<affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Department of Critical Care Medicine, University of Pittsburgh</institution>
, Pittsburgh, PA,<country>USA</country>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff2"><institution>Safar Center for Resuscitation Research, University of Pittsburgh</institution>
, Pittsburgh, PA,<country>USA</country>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff3"><institution>Department of Environmental and Occupational Health, University of Pittsburgh</institution>
, Pittsburgh, PA,<country>USA</country>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff4"><institution>Center for Free Radical and Antioxidant Health, University of Pittsburgh</institution>
, Pittsburgh, PA,<country>USA</country>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff7"><institution>Children's Hospital of Pittsburgh</institution>
, Pittsburgh, PA,<country>USA</country>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
</analytic>
<series><title level="j">Journal of Cerebral Blood Flow & Metabolism</title>
<idno type="ISSN">0271-678X</idno>
<idno type="eISSN">1559-7016</idno>
<imprint><date when="2014">2014</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
</fileDesc>
<profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Animals</term>
<term>Cardiolipins (metabolism)</term>
<term>Cerebrovascular Disorders (metabolism)</term>
<term>Cerebrovascular Disorders (pathology)</term>
<term>Male</term>
<term>Mitochondria (metabolism)</term>
<term>Mitochondria (pathology)</term>
<term>Oxidation-Reduction</term>
<term>Rats</term>
<term>Rats, Sprague-Dawley</term>
<term>Reperfusion Injury (metabolism)</term>
<term>Reperfusion Injury (pathology)</term>
<term>Signal Transduction</term>
<term>Time Factors</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr"><term>Angiopathies intracrâniennes (anatomopathologie)</term>
<term>Angiopathies intracrâniennes (métabolisme)</term>
<term>Animaux</term>
<term>Cardiolipides (métabolisme)</term>
<term>Facteurs temps</term>
<term>Lésion d'ischémie-reperfusion (anatomopathologie)</term>
<term>Lésion d'ischémie-reperfusion (métabolisme)</term>
<term>Mitochondries (anatomopathologie)</term>
<term>Mitochondries (métabolisme)</term>
<term>Mâle</term>
<term>Oxydoréduction</term>
<term>Rat Sprague-Dawley</term>
<term>Rats</term>
<term>Transduction du signal</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Cardiolipins</term>
</keywords>
<keywords scheme="MESH" qualifier="anatomopathologie" xml:lang="fr"><term>Angiopathies intracrâniennes</term>
<term>Lésion d'ischémie-reperfusion</term>
<term>Mitochondries</term>
</keywords>
<keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Cerebrovascular Disorders</term>
<term>Mitochondria</term>
<term>Reperfusion Injury</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Angiopathies intracrâniennes</term>
<term>Cardiolipides</term>
<term>Lésion d'ischémie-reperfusion</term>
<term>Mitochondries</term>
</keywords>
<keywords scheme="MESH" qualifier="pathology" xml:lang="en"><term>Cerebrovascular Disorders</term>
<term>Mitochondria</term>
<term>Reperfusion Injury</term>
</keywords>
<keywords scheme="MESH" xml:lang="en"><term>Animals</term>
<term>Male</term>
<term>Oxidation-Reduction</term>
<term>Rats</term>
<term>Rats, Sprague-Dawley</term>
<term>Signal Transduction</term>
<term>Time Factors</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr"><term>Animaux</term>
<term>Facteurs temps</term>
<term>Mâle</term>
<term>Oxydoréduction</term>
<term>Rat Sprague-Dawley</term>
<term>Rats</term>
<term>Transduction du signal</term>
</keywords>
</textClass>
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<front><div type="abstract" xml:lang="en"><p>It is believed that biosynthesis of lipid mediators in the central nervous system after cerebral ischemia-reperfusion starts with phospholipid hydrolysis by calcium-dependent phospholipases and is followed by oxygenation of released fatty acids (FAs). Here, we report an alternative pathway whereby cereberal ischemia-reperfusion triggered oxygenation of a mitochondria-specific phospholipid, cardiolipin (CL), is followed by its hydrolysis to yield monolyso-CLs and oxygenated derivatives of fatty (linoleic) acids. We used a model of global cerebral ischemia-reperfusion characterized by 9 minutes of asphyxia leading to asystole followed by cardiopulmonary resuscitation in postnatal day 17 rats. Global ischemia and cardiopulmonary resuscitation resulted in: (1) selective oxidation and hydrolysis of CLs, (2) accumulation of lyso-CLs and oxygenated free FAs, (3) activation of caspase 3/7 in the brain, and (4) motor and cognitive dysfunction. On the basis of these findings, we used a mitochondria targeted nitroxide electron scavenger, which prevented CL oxidation and subsequent hydrolysis, attenuated caspase activation, and improved neurocognitive outcome when administered after cardiac arrest. These data show that calcium-independent CL oxidation and subsequent hydrolysis represent a previously unidentified pathogenic mechanism of brain injury incurred by ischemia-reperfusion and a clinically relevant therapeutic target.</p>
</div>
</front>
</TEI>
<affiliations><list><country><li>Pays-Bas</li>
<li>République populaire de Chine</li>
<li>États-Unis</li>
</country>
<region><li>Pennsylvanie</li>
</region>
<settlement><li>Pittsburgh</li>
</settlement>
<orgName><li>Université de Pittsburgh</li>
</orgName>
</list>
<tree><country name="États-Unis"><noRegion><name sortKey="Ji, Jing" sort="Ji, Jing" uniqKey="Ji J" first="Jing" last="Ji">Jing Ji</name>
</noRegion>
<name sortKey="Anthonymuthu, Tamil S" sort="Anthonymuthu, Tamil S" uniqKey="Anthonymuthu T" first="Tamil S" last="Anthonymuthu">Tamil S. Anthonymuthu</name>
<name sortKey="Anthonymuthu, Tamil S" sort="Anthonymuthu, Tamil S" uniqKey="Anthonymuthu T" first="Tamil S" last="Anthonymuthu">Tamil S. Anthonymuthu</name>
<name sortKey="Anthonymuthu, Tamil S" sort="Anthonymuthu, Tamil S" uniqKey="Anthonymuthu T" first="Tamil S" last="Anthonymuthu">Tamil S. Anthonymuthu</name>
<name sortKey="Baart, Sophie" sort="Baart, Sophie" uniqKey="Baart S" first="Sophie" last="Baart">Sophie Baart</name>
<name sortKey="Baart, Sophie" sort="Baart, Sophie" uniqKey="Baart S" first="Sophie" last="Baart">Sophie Baart</name>
<name sortKey="Bay R, Hulya" sort="Bay R, Hulya" uniqKey="Bay R H" first="Hülya" last="Bay R">Hülya Bay R</name>
<name sortKey="Bay R, Hulya" sort="Bay R, Hulya" uniqKey="Bay R H" first="Hülya" last="Bay R">Hülya Bay R</name>
<name sortKey="Bay R, Hulya" sort="Bay R, Hulya" uniqKey="Bay R H" first="Hülya" last="Bay R">Hülya Bay R</name>
<name sortKey="Bay R, Hulya" sort="Bay R, Hulya" uniqKey="Bay R H" first="Hülya" last="Bay R">Hülya Bay R</name>
<name sortKey="Bay R, Hulya" sort="Bay R, Hulya" uniqKey="Bay R H" first="Hülya" last="Bay R">Hülya Bay R</name>
<name sortKey="Clark, Robert Sb" sort="Clark, Robert Sb" uniqKey="Clark R" first="Robert Sb" last="Clark">Robert Sb Clark</name>
<name sortKey="Clark, Robert Sb" sort="Clark, Robert Sb" uniqKey="Clark R" first="Robert Sb" last="Clark">Robert Sb Clark</name>
<name sortKey="Clark, Robert Sb" sort="Clark, Robert Sb" uniqKey="Clark R" first="Robert Sb" last="Clark">Robert Sb Clark</name>
<name sortKey="Du, Lina" sort="Du, Lina" uniqKey="Du L" first="Lina" last="Du">Lina Du</name>
<name sortKey="Du, Lina" sort="Du, Lina" uniqKey="Du L" first="Lina" last="Du">Lina Du</name>
<name sortKey="Ji, Jing" sort="Ji, Jing" uniqKey="Ji J" first="Jing" last="Ji">Jing Ji</name>
<name sortKey="Ji, Jing" sort="Ji, Jing" uniqKey="Ji J" first="Jing" last="Ji">Jing Ji</name>
<name sortKey="Ji, Jing" sort="Ji, Jing" uniqKey="Ji J" first="Jing" last="Ji">Jing Ji</name>
<name sortKey="Kagan, Valerian E" sort="Kagan, Valerian E" uniqKey="Kagan V" first="Valerian E" last="Kagan">Valerian E. Kagan</name>
<name sortKey="Kagan, Valerian E" sort="Kagan, Valerian E" uniqKey="Kagan V" first="Valerian E" last="Kagan">Valerian E. Kagan</name>
<name sortKey="Kline, Anthony E" sort="Kline, Anthony E" uniqKey="Kline A" first="Anthony E" last="Kline">Anthony E. Kline</name>
<name sortKey="Kochanek, Patrick M" sort="Kochanek, Patrick M" uniqKey="Kochanek P" first="Patrick M" last="Kochanek">Patrick M. Kochanek</name>
<name sortKey="Kochanek, Patrick M" sort="Kochanek, Patrick M" uniqKey="Kochanek P" first="Patrick M" last="Kochanek">Patrick M. Kochanek</name>
<name sortKey="Kochanek, Patrick M" sort="Kochanek, Patrick M" uniqKey="Kochanek P" first="Patrick M" last="Kochanek">Patrick M. Kochanek</name>
<name sortKey="Lewis, Jesse" sort="Lewis, Jesse" uniqKey="Lewis J" first="Jesse" last="Lewis">Jesse Lewis</name>
<name sortKey="Lewis, Jesse" sort="Lewis, Jesse" uniqKey="Lewis J" first="Jesse" last="Lewis">Jesse Lewis</name>
<name sortKey="Skoda, Erin M" sort="Skoda, Erin M" uniqKey="Skoda E" first="Erin M" last="Skoda">Erin M. Skoda</name>
<name sortKey="St Croix, Claudette M" sort="St Croix, Claudette M" uniqKey="St Croix C" first="Claudette M" last="St Croix">Claudette M. St Croix</name>
<name sortKey="Tyurin, Vladimir A" sort="Tyurin, Vladimir A" uniqKey="Tyurin V" first="Vladimir A" last="Tyurin">Vladimir A. Tyurin</name>
<name sortKey="Tyurin, Vladimir A" sort="Tyurin, Vladimir A" uniqKey="Tyurin V" first="Vladimir A" last="Tyurin">Vladimir A. Tyurin</name>
<name sortKey="Tyurina, Yulia Y" sort="Tyurina, Yulia Y" uniqKey="Tyurina Y" first="Yulia Y" last="Tyurina">Yulia Y. Tyurina</name>
<name sortKey="Tyurina, Yulia Y" sort="Tyurina, Yulia Y" uniqKey="Tyurina Y" first="Yulia Y" last="Tyurina">Yulia Y. Tyurina</name>
<name sortKey="Vikulina, Anna S" sort="Vikulina, Anna S" uniqKey="Vikulina A" first="Anna S" last="Vikulina">Anna S. Vikulina</name>
<name sortKey="Vikulina, Anna S" sort="Vikulina, Anna S" uniqKey="Vikulina A" first="Anna S" last="Vikulina">Anna S. Vikulina</name>
<name sortKey="Wipf, Peter" sort="Wipf, Peter" uniqKey="Wipf P" first="Peter" last="Wipf">Peter Wipf</name>
</country>
<country name="République populaire de Chine"><noRegion><name sortKey="Ji, Jing" sort="Ji, Jing" uniqKey="Ji J" first="Jing" last="Ji">Jing Ji</name>
</noRegion>
</country>
<country name="Pays-Bas"><noRegion><name sortKey="Baart, Sophie" sort="Baart, Sophie" uniqKey="Baart S" first="Sophie" last="Baart">Sophie Baart</name>
</noRegion>
</country>
</tree>
</affiliations>
</record>
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