Microglial glucocorticoid receptors play a pivotal role in regulating dopaminergic neurodegeneration in parkinsonism
Identifieur interne : 000676 ( Pmc/Checkpoint ); précédent : 000675; suivant : 000677Microglial glucocorticoid receptors play a pivotal role in regulating dopaminergic neurodegeneration in parkinsonism
Auteurs : Francisco Ros-Bernal [France, Espagne] ; Stéphane Hunot [France] ; Maria Trinidad Herrero [Espagne] ; Sebastien Parnadeau [France] ; Jean-Christophe Corvol [France] ; Lixia Lu [France, République populaire de Chine] ; Daniel Alvarez-Fischer [France, Allemagne] ; María Angeles Carrillo-De Sauvage [France, Espagne] ; Françoise Saurini [France] ; Christiane Coussieu [France] ; Kiyoka Kinugawa [France] ; Annick Prigent [France] ; Günter Höglinger [Allemagne] ; Michel Hamon [France] ; François Tronche [France] ; Etienne C. Hirsch [France] ; Sheela Vyas [France]Source :
- Proceedings of the National Academy of Sciences of the United States of America [ 0027-8424 ] ; 2011.
Abstract
Among the pathogenic processes contributing to dopaminergic neuron (DN) death in Parkinson disease (PD), evidence points to non–cell-autonomous mechanisms, particularly chronic inflammation mounted by activated microglia. Yet little is known about endogenous regulatory processes that determine microglial actions in pathological states. We examined the role of glucocorticoid receptors (GRs), activated by glucocorticoids released in response to stress and known to regulate inflammation, in DN survival. Overall GR level was decreased in substantia nigra of PD patients and 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-intoxicated mice. GR changes, specifically in the microglia after MPTP treatment, revealed a rapid augmentation in the number of microglia displaying nuclear localization of GR. Mice with selective inactivation of the GR gene in macrophages/microglia (GRLysMCre) but not in DNs (GRDATCre) showed increased loss of DNs after MPTP intoxication. This DN loss in GRLysMCre mice was not prevented by corticosterone treatment, in contrast to the protection observed in control littermates. Moreover, absence of microglial GRs augmented microglial reactivity and led to their persistent activation. Analysis of inflammatory genes revealed an up-regulation of Toll-like receptors (TLRs) by MPTP treatment, particularly TLR9, the level of which was high in postmortem parkinsonian brains. The regulatory control of GR was reflected by higher expression of proinflammatory genes (e.g., TNF-α) with a concomitant decrease in anti-inflammatory genes (e.g., IL-1R2) in GRLysMCre mice. Indeed, in GRLysMCre mice, alterations in phosphorylated NF-κB levels indicated its protracted activation. Together, our data indicate that GR is important in curtailing microglial reactivity, and its deregulation in PD could lead to sustained inflammation-mediated DN injury.
Url:
DOI: 10.1073/pnas.1017820108
PubMed: 21467220
PubMed Central: 3080980
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<affiliation wicri:level="1"><nlm:aff id="aff9">Department of Regenerative Medicine, School of Medicine,<institution>Tongi University</institution>
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<author><name sortKey="Coussieu, Christiane" sort="Coussieu, Christiane" uniqKey="Coussieu C" first="Christiane" last="Coussieu">Christiane Coussieu</name>
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<author><name sortKey="Kinugawa, Kiyoka" sort="Kinugawa, Kiyoka" uniqKey="Kinugawa K" first="Kiyoka" last="Kinugawa">Kiyoka Kinugawa</name>
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;</nlm:aff>
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;</nlm:aff>
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<author><name sortKey="Hirsch, Etienne C" sort="Hirsch, Etienne C" uniqKey="Hirsch E" first="Etienne C." last="Hirsch">Etienne C. Hirsch</name>
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;</nlm:aff>
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, F-75013 Paris,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
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<author><name sortKey="Vyas, Sheela" sort="Vyas, Sheela" uniqKey="Vyas S" first="Sheela" last="Vyas">Sheela Vyas</name>
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;</nlm:aff>
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;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff4">Institute of Biology,<institution>Collège de France</institution>
, F-75505 Paris,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
</titleStmt>
<publicationStmt><idno type="wicri:source">PMC</idno>
<idno type="pmid">21467220</idno>
<idno type="pmc">3080980</idno>
<idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3080980</idno>
<idno type="RBID">PMC:3080980</idno>
<idno type="doi">10.1073/pnas.1017820108</idno>
<date when="2011">2011</date>
<idno type="wicri:Area/Pmc/Corpus">000536</idno>
<idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000536</idno>
<idno type="wicri:Area/Pmc/Curation">000533</idno>
<idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">000533</idno>
<idno type="wicri:Area/Pmc/Checkpoint">000676</idno>
<idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Checkpoint">000676</idno>
</publicationStmt>
<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Microglial glucocorticoid receptors play a pivotal role in regulating dopaminergic neurodegeneration in parkinsonism</title>
<author><name sortKey="Ros Bernal, Francisco" sort="Ros Bernal, Francisco" uniqKey="Ros Bernal F" first="Francisco" last="Ros-Bernal">Francisco Ros-Bernal</name>
<affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Centre National de la Recherche Scientifique (CNRS)</institution>
, Unité Mixte de Recherche (UMR) 7224, F-75005 Paris,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff2"><institution>Institut National de la Santé et de la Recherche Médicale</institution>
(INSERM), Unité 952, F-75005 Paris,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff3"><institution>Université Pierre et Marie Curie–Paris 06</institution>
, F-75252 Paris Cedex 5,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff4">Institute of Biology,<institution>Collège de France</institution>
, F-75505 Paris,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff5">Clinical and Experimental Neuroscience, Centro de Investigación Biomedica en Red de Enfermedades Neurodegenerativas (CIBERNED), School of Medicine,<institution>University of Murcia</institution>
, 30100 Murcia,<country>Spain</country>
;</nlm:aff>
<country xml:lang="fr">Espagne</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Hunot, Stephane" sort="Hunot, Stephane" uniqKey="Hunot S" first="Stéphane" last="Hunot">Stéphane Hunot</name>
<affiliation wicri:level="1"><nlm:aff id="aff3"><institution>Université Pierre et Marie Curie–Paris 06</institution>
, F-75252 Paris Cedex 5,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff6">Institut National de la Santé et de la Recherche Médicale, Unité Mixte de Recherche U975,<institution>Hôpital de la Salpêtrière</institution>
, F-75013 Paris,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff7">Centre National de la Recherche Scientifique, Unité Mixte de Recherche 7225,<institution>Centre de Recherche de l'Institut du Cerveau et de la Moëlle Épinière</institution>
, F-75013 Paris,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Herrero, Maria Trinidad" sort="Herrero, Maria Trinidad" uniqKey="Herrero M" first="Maria Trinidad" last="Herrero">Maria Trinidad Herrero</name>
<affiliation wicri:level="1"><nlm:aff id="aff5">Clinical and Experimental Neuroscience, Centro de Investigación Biomedica en Red de Enfermedades Neurodegenerativas (CIBERNED), School of Medicine,<institution>University of Murcia</institution>
, 30100 Murcia,<country>Spain</country>
;</nlm:aff>
<country xml:lang="fr">Espagne</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Parnadeau, Sebastien" sort="Parnadeau, Sebastien" uniqKey="Parnadeau S" first="Sebastien" last="Parnadeau">Sebastien Parnadeau</name>
<affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Centre National de la Recherche Scientifique (CNRS)</institution>
, Unité Mixte de Recherche (UMR) 7224, F-75005 Paris,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff2"><institution>Institut National de la Santé et de la Recherche Médicale</institution>
(INSERM), Unité 952, F-75005 Paris,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff3"><institution>Université Pierre et Marie Curie–Paris 06</institution>
, F-75252 Paris Cedex 5,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff4">Institute of Biology,<institution>Collège de France</institution>
, F-75505 Paris,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Corvol, Jean Christophe" sort="Corvol, Jean Christophe" uniqKey="Corvol J" first="Jean-Christophe" last="Corvol">Jean-Christophe Corvol</name>
<affiliation wicri:level="1"><nlm:aff id="aff3"><institution>Université Pierre et Marie Curie–Paris 06</institution>
, F-75252 Paris Cedex 5,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff6">Institut National de la Santé et de la Recherche Médicale, Unité Mixte de Recherche U975,<institution>Hôpital de la Salpêtrière</institution>
, F-75013 Paris,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff7">Centre National de la Recherche Scientifique, Unité Mixte de Recherche 7225,<institution>Centre de Recherche de l'Institut du Cerveau et de la Moëlle Épinière</institution>
, F-75013 Paris,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff8">Assistance-Publique Hôpitaux de Paris, Clinical Investigation Center CIC-9503, Department of Neurology,<institution>Hôpital Salpêtrière</institution>
, F-75013 Paris,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Lu, Lixia" sort="Lu, Lixia" uniqKey="Lu L" first="Lixia" last="Lu">Lixia Lu</name>
<affiliation wicri:level="1"><nlm:aff id="aff3"><institution>Université Pierre et Marie Curie–Paris 06</institution>
, F-75252 Paris Cedex 5,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff6">Institut National de la Santé et de la Recherche Médicale, Unité Mixte de Recherche U975,<institution>Hôpital de la Salpêtrière</institution>
, F-75013 Paris,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff7">Centre National de la Recherche Scientifique, Unité Mixte de Recherche 7225,<institution>Centre de Recherche de l'Institut du Cerveau et de la Moëlle Épinière</institution>
, F-75013 Paris,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff9">Department of Regenerative Medicine, School of Medicine,<institution>Tongi University</institution>
, Shanghai 200092,<country>China</country>
;</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Alvarez Fischer, Daniel" sort="Alvarez Fischer, Daniel" uniqKey="Alvarez Fischer D" first="Daniel" last="Alvarez-Fischer">Daniel Alvarez-Fischer</name>
<affiliation wicri:level="1"><nlm:aff id="aff3"><institution>Université Pierre et Marie Curie–Paris 06</institution>
, F-75252 Paris Cedex 5,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff6">Institut National de la Santé et de la Recherche Médicale, Unité Mixte de Recherche U975,<institution>Hôpital de la Salpêtrière</institution>
, F-75013 Paris,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff7">Centre National de la Recherche Scientifique, Unité Mixte de Recherche 7225,<institution>Centre de Recherche de l'Institut du Cerveau et de la Moëlle Épinière</institution>
, F-75013 Paris,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff10">Experimental Neurology, Philipps University, D-35033 Marburg,<country>Germany</country>
;</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Carrillo De Sauvage, Maria Angeles" sort="Carrillo De Sauvage, Maria Angeles" uniqKey="Carrillo De Sauvage M" first="María Angeles" last="Carrillo-De Sauvage">María Angeles Carrillo-De Sauvage</name>
<affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Centre National de la Recherche Scientifique (CNRS)</institution>
, Unité Mixte de Recherche (UMR) 7224, F-75005 Paris,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff2"><institution>Institut National de la Santé et de la Recherche Médicale</institution>
(INSERM), Unité 952, F-75005 Paris,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff3"><institution>Université Pierre et Marie Curie–Paris 06</institution>
, F-75252 Paris Cedex 5,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff4">Institute of Biology,<institution>Collège de France</institution>
, F-75505 Paris,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff5">Clinical and Experimental Neuroscience, Centro de Investigación Biomedica en Red de Enfermedades Neurodegenerativas (CIBERNED), School of Medicine,<institution>University of Murcia</institution>
, 30100 Murcia,<country>Spain</country>
;</nlm:aff>
<country xml:lang="fr">Espagne</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Saurini, Francoise" sort="Saurini, Francoise" uniqKey="Saurini F" first="Françoise" last="Saurini">Françoise Saurini</name>
<affiliation wicri:level="1"><nlm:aff id="aff3"><institution>Université Pierre et Marie Curie–Paris 06</institution>
, F-75252 Paris Cedex 5,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff wicri:cut="; and" id="aff11">Institut National de la Santé et de la Recherche Médicale/Le Centre de Psychiatrie et Neurosciences, Unité Mixte de Recherche 894,<institution>Faculté de Médicine Pierre et Marie Curie</institution>
, F-75013 Paris,<country>France</country>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Coussieu, Christiane" sort="Coussieu, Christiane" uniqKey="Coussieu C" first="Christiane" last="Coussieu">Christiane Coussieu</name>
<affiliation wicri:level="1"><nlm:aff id="aff12">Biochemistry Laboratory,<institution>Hôpital de la Salpêtrière</institution>
, F-75013 Paris,<country>France</country>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Kinugawa, Kiyoka" sort="Kinugawa, Kiyoka" uniqKey="Kinugawa K" first="Kiyoka" last="Kinugawa">Kiyoka Kinugawa</name>
<affiliation wicri:level="1"><nlm:aff id="aff3"><institution>Université Pierre et Marie Curie–Paris 06</institution>
, F-75252 Paris Cedex 5,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff6">Institut National de la Santé et de la Recherche Médicale, Unité Mixte de Recherche U975,<institution>Hôpital de la Salpêtrière</institution>
, F-75013 Paris,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff7">Centre National de la Recherche Scientifique, Unité Mixte de Recherche 7225,<institution>Centre de Recherche de l'Institut du Cerveau et de la Moëlle Épinière</institution>
, F-75013 Paris,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Prigent, Annick" sort="Prigent, Annick" uniqKey="Prigent A" first="Annick" last="Prigent">Annick Prigent</name>
<affiliation wicri:level="1"><nlm:aff id="aff3"><institution>Université Pierre et Marie Curie–Paris 06</institution>
, F-75252 Paris Cedex 5,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff6">Institut National de la Santé et de la Recherche Médicale, Unité Mixte de Recherche U975,<institution>Hôpital de la Salpêtrière</institution>
, F-75013 Paris,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff7">Centre National de la Recherche Scientifique, Unité Mixte de Recherche 7225,<institution>Centre de Recherche de l'Institut du Cerveau et de la Moëlle Épinière</institution>
, F-75013 Paris,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Hoglinger, Gunter" sort="Hoglinger, Gunter" uniqKey="Hoglinger G" first="Günter" last="Höglinger">Günter Höglinger</name>
<affiliation wicri:level="1"><nlm:aff id="aff10">Experimental Neurology, Philipps University, D-35033 Marburg,<country>Germany</country>
;</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Hamon, Michel" sort="Hamon, Michel" uniqKey="Hamon M" first="Michel" last="Hamon">Michel Hamon</name>
<affiliation wicri:level="1"><nlm:aff id="aff3"><institution>Université Pierre et Marie Curie–Paris 06</institution>
, F-75252 Paris Cedex 5,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff wicri:cut="; and" id="aff11">Institut National de la Santé et de la Recherche Médicale/Le Centre de Psychiatrie et Neurosciences, Unité Mixte de Recherche 894,<institution>Faculté de Médicine Pierre et Marie Curie</institution>
, F-75013 Paris,<country>France</country>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Tronche, Francois" sort="Tronche, Francois" uniqKey="Tronche F" first="François" last="Tronche">François Tronche</name>
<affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Centre National de la Recherche Scientifique (CNRS)</institution>
, Unité Mixte de Recherche (UMR) 7224, F-75005 Paris,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff2"><institution>Institut National de la Santé et de la Recherche Médicale</institution>
(INSERM), Unité 952, F-75005 Paris,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff3"><institution>Université Pierre et Marie Curie–Paris 06</institution>
, F-75252 Paris Cedex 5,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff4">Institute of Biology,<institution>Collège de France</institution>
, F-75505 Paris,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Hirsch, Etienne C" sort="Hirsch, Etienne C" uniqKey="Hirsch E" first="Etienne C." last="Hirsch">Etienne C. Hirsch</name>
<affiliation wicri:level="1"><nlm:aff id="aff3"><institution>Université Pierre et Marie Curie–Paris 06</institution>
, F-75252 Paris Cedex 5,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff6">Institut National de la Santé et de la Recherche Médicale, Unité Mixte de Recherche U975,<institution>Hôpital de la Salpêtrière</institution>
, F-75013 Paris,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff7">Centre National de la Recherche Scientifique, Unité Mixte de Recherche 7225,<institution>Centre de Recherche de l'Institut du Cerveau et de la Moëlle Épinière</institution>
, F-75013 Paris,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Vyas, Sheela" sort="Vyas, Sheela" uniqKey="Vyas S" first="Sheela" last="Vyas">Sheela Vyas</name>
<affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Centre National de la Recherche Scientifique (CNRS)</institution>
, Unité Mixte de Recherche (UMR) 7224, F-75005 Paris,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff2"><institution>Institut National de la Santé et de la Recherche Médicale</institution>
(INSERM), Unité 952, F-75005 Paris,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff3"><institution>Université Pierre et Marie Curie–Paris 06</institution>
, F-75252 Paris Cedex 5,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff4">Institute of Biology,<institution>Collège de France</institution>
, F-75505 Paris,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</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="2011">2011</date>
</imprint>
</series>
</biblStruct>
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<front><div type="abstract" xml:lang="en"><p>Among the pathogenic processes contributing to dopaminergic neuron (DN) death in Parkinson disease (PD), evidence points to non–cell-autonomous mechanisms, particularly chronic inflammation mounted by activated microglia. Yet little is known about endogenous regulatory processes that determine microglial actions in pathological states. We examined the role of glucocorticoid receptors (GRs), activated by glucocorticoids released in response to stress and known to regulate inflammation, in DN survival. Overall GR level was decreased in substantia nigra of PD patients and 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-intoxicated mice. GR changes, specifically in the microglia after MPTP treatment, revealed a rapid augmentation in the number of microglia displaying nuclear localization of GR. Mice with selective inactivation of the GR gene in macrophages/microglia (GR<sup>LysMCre</sup>
) but not in DNs (GR<sup>DATCre</sup>
) showed increased loss of DNs after MPTP intoxication. This DN loss in GR<sup>LysMCre</sup>
mice was not prevented by corticosterone treatment, in contrast to the protection observed in control littermates. Moreover, absence of microglial GRs augmented microglial reactivity and led to their persistent activation. Analysis of inflammatory genes revealed an up-regulation of Toll-like receptors (TLRs) by MPTP treatment, particularly TLR9, the level of which was high in postmortem parkinsonian brains. The regulatory control of GR was reflected by higher expression of proinflammatory genes (e.g., TNF-α) with a concomitant decrease in anti-inflammatory genes (e.g., IL-1R2) in GR<sup>LysMCre</sup>
mice. Indeed, in GR<sup>LysMCre</sup>
mice, alterations in phosphorylated NF-κB levels indicated its protracted activation. Together, our data indicate that GR is important in curtailing microglial reactivity, and its deregulation in PD could lead to sustained inflammation-mediated DN injury.</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="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">21467220</article-id>
<article-id pub-id-type="pmc">3080980</article-id>
<article-id pub-id-type="publisher-id">201017820</article-id>
<article-id pub-id-type="doi">10.1073/pnas.1017820108</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Biological Sciences</subject>
<subj-group><subject>Neuroscience</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group><article-title>Microglial glucocorticoid receptors play a pivotal role in regulating dopaminergic neurodegeneration in parkinsonism</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Ros-Bernal</surname>
<given-names>Francisco</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="aff3"><sup>c</sup>
</xref>
<xref ref-type="aff" rid="aff4"><sup>d</sup>
</xref>
<xref ref-type="aff" rid="aff5"><sup>e</sup>
</xref>
<xref ref-type="author-notes" rid="fn1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Hunot</surname>
<given-names>Stéphane</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>c</sup>
</xref>
<xref ref-type="aff" rid="aff6"><sup>f</sup>
</xref>
<xref ref-type="aff" rid="aff7"><sup>g</sup>
</xref>
<xref ref-type="author-notes" rid="fn1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Herrero</surname>
<given-names>Maria Trinidad</given-names>
</name>
<xref ref-type="aff" rid="aff5"><sup>e</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Parnadeau</surname>
<given-names>Sebastien</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="aff3"><sup>c</sup>
</xref>
<xref ref-type="aff" rid="aff4"><sup>d</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Corvol</surname>
<given-names>Jean-Christophe</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>c</sup>
</xref>
<xref ref-type="aff" rid="aff6"><sup>f</sup>
</xref>
<xref ref-type="aff" rid="aff7"><sup>g</sup>
</xref>
<xref ref-type="aff" rid="aff8"><sup>h</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Lu</surname>
<given-names>Lixia</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>c</sup>
</xref>
<xref ref-type="aff" rid="aff6"><sup>f</sup>
</xref>
<xref ref-type="aff" rid="aff7"><sup>g</sup>
</xref>
<xref ref-type="aff" rid="aff9"><sup>i</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Alvarez-Fischer</surname>
<given-names>Daniel</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>c</sup>
</xref>
<xref ref-type="aff" rid="aff6"><sup>f</sup>
</xref>
<xref ref-type="aff" rid="aff7"><sup>g</sup>
</xref>
<xref ref-type="aff" rid="aff10"><sup>j</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Carrillo-de Sauvage</surname>
<given-names>María Angeles</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="aff3"><sup>c</sup>
</xref>
<xref ref-type="aff" rid="aff4"><sup>d</sup>
</xref>
<xref ref-type="aff" rid="aff5"><sup>e</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Saurini</surname>
<given-names>Françoise</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>c</sup>
</xref>
<xref ref-type="aff" rid="aff11"><sup>k</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Coussieu</surname>
<given-names>Christiane</given-names>
</name>
<xref ref-type="aff" rid="aff12"><sup>l</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Kinugawa</surname>
<given-names>Kiyoka</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>c</sup>
</xref>
<xref ref-type="aff" rid="aff6"><sup>f</sup>
</xref>
<xref ref-type="aff" rid="aff7"><sup>g</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Prigent</surname>
<given-names>Annick</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>c</sup>
</xref>
<xref ref-type="aff" rid="aff6"><sup>f</sup>
</xref>
<xref ref-type="aff" rid="aff7"><sup>g</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Höglinger</surname>
<given-names>Günter</given-names>
</name>
<xref ref-type="aff" rid="aff10"><sup>j</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Hamon</surname>
<given-names>Michel</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>c</sup>
</xref>
<xref ref-type="aff" rid="aff11"><sup>k</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Tronche</surname>
<given-names>François</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="aff3"><sup>c</sup>
</xref>
<xref ref-type="aff" rid="aff4"><sup>d</sup>
</xref>
<xref ref-type="corresp" rid="cor1"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Hirsch</surname>
<given-names>Etienne C.</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>c</sup>
</xref>
<xref ref-type="aff" rid="aff6"><sup>f</sup>
</xref>
<xref ref-type="aff" rid="aff7"><sup>g</sup>
</xref>
<xref ref-type="corresp" rid="cor1"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Vyas</surname>
<given-names>Sheela</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="aff3"><sup>c</sup>
</xref>
<xref ref-type="aff" rid="aff4"><sup>d</sup>
</xref>
<xref ref-type="corresp" rid="cor1"><sup>2</sup>
</xref>
</contrib>
<aff id="aff1"><sup>a</sup>
<institution>Centre National de la Recherche Scientifique (CNRS)</institution>
, Unité Mixte de Recherche (UMR) 7224, F-75005 Paris,<country>France</country>
;</aff>
<aff id="aff2"><sup>b</sup>
<institution>Institut National de la Santé et de la Recherche Médicale</institution>
(INSERM), Unité 952, F-75005 Paris,<country>France</country>
;</aff>
<aff id="aff3"><sup>c</sup>
<institution>Université Pierre et Marie Curie–Paris 06</institution>
, F-75252 Paris Cedex 5,<country>France</country>
;</aff>
<aff id="aff4"><sup>d</sup>
Institute of Biology,<institution>Collège de France</institution>
, F-75505 Paris,<country>France</country>
;</aff>
<aff id="aff5"><sup>e</sup>
Clinical and Experimental Neuroscience, Centro de Investigación Biomedica en Red de Enfermedades Neurodegenerativas (CIBERNED), School of Medicine,<institution>University of Murcia</institution>
, 30100 Murcia,<country>Spain</country>
;</aff>
<aff id="aff6"><sup>f</sup>
Institut National de la Santé et de la Recherche Médicale, Unité Mixte de Recherche U975,<institution>Hôpital de la Salpêtrière</institution>
, F-75013 Paris,<country>France</country>
;</aff>
<aff id="aff7"><sup>g</sup>
Centre National de la Recherche Scientifique, Unité Mixte de Recherche 7225,<institution>Centre de Recherche de l'Institut du Cerveau et de la Moëlle Épinière</institution>
, F-75013 Paris,<country>France</country>
;</aff>
<aff id="aff8"><sup>h</sup>
Assistance-Publique Hôpitaux de Paris, Clinical Investigation Center CIC-9503, Department of Neurology,<institution>Hôpital Salpêtrière</institution>
, F-75013 Paris,<country>France</country>
;</aff>
<aff id="aff9"><sup>i</sup>
Department of Regenerative Medicine, School of Medicine,<institution>Tongi University</institution>
, Shanghai 200092,<country>China</country>
;</aff>
<aff id="aff10"><sup>j</sup>
Experimental Neurology, Philipps University, D-35033 Marburg,<country>Germany</country>
;</aff>
<aff id="aff11"><sup>k</sup>
Institut National de la Santé et de la Recherche Médicale/Le Centre de Psychiatrie et Neurosciences, Unité Mixte de Recherche 894,<institution>Faculté de Médicine Pierre et Marie Curie</institution>
, F-75013 Paris,<country>France</country>
; and</aff>
<aff id="aff12"><sup>l</sup>
Biochemistry Laboratory,<institution>Hôpital de la Salpêtrière</institution>
, F-75013 Paris,<country>France</country>
</aff>
</contrib-group>
<author-notes><corresp id="cor1"><sup>2</sup>
To whom correspondence may be addressed. E-mail: <email>francois.tronche@upmc.fr</email>
, <email>etienne.hirsch@upmc.fr</email>
, or <email>sheela.vyas@snv.jussieu.fr</email>
.</corresp>
<fn fn-type="edited-by"><p>Edited by Fred H. Gage, The Salk Institute, San Diego, CA, and approved February 24, 2011 (received for review December 2, 2010)</p>
</fn>
<fn fn-type="con"><p>Author contributions: S.H., M.T.H., F.T., E.C.H., and S.V. designed research; F.R.-B., S.H., S.P., J.-C.C., L.L., D.A.-F., M.A.C.-d.S., F.S., C.C., K.K., A.P., and S.V. performed research; G.H., M.H., and F.T. contributed new reagents/analytic tools; F.R.-B., J.-C.C., L.L., D.A.-F., and S.V. analyzed data; and S.H., E.C.H., and S.V. wrote the paper.</p>
</fn>
<fn id="fn1" fn-type="equal"><p><sup>1</sup>
F.R.-B. and S.H. contributed equally to this work.</p>
</fn>
</author-notes>
<pub-date pub-type="ppub"><day>19</day>
<month>4</month>
<year>2011</year>
</pub-date>
<pub-date pub-type="epub"><day>5</day>
<month>4</month>
<year>2011</year>
</pub-date>
<volume>108</volume>
<issue>16</issue>
<fpage>6632</fpage>
<lpage>6637</lpage>
<self-uri xlink:title="pdf" xlink:type="simple" xlink:href="pnas.201017820.pdf"></self-uri>
<abstract><p>Among the pathogenic processes contributing to dopaminergic neuron (DN) death in Parkinson disease (PD), evidence points to non–cell-autonomous mechanisms, particularly chronic inflammation mounted by activated microglia. Yet little is known about endogenous regulatory processes that determine microglial actions in pathological states. We examined the role of glucocorticoid receptors (GRs), activated by glucocorticoids released in response to stress and known to regulate inflammation, in DN survival. Overall GR level was decreased in substantia nigra of PD patients and 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-intoxicated mice. GR changes, specifically in the microglia after MPTP treatment, revealed a rapid augmentation in the number of microglia displaying nuclear localization of GR. Mice with selective inactivation of the GR gene in macrophages/microglia (GR<sup>LysMCre</sup>
) but not in DNs (GR<sup>DATCre</sup>
) showed increased loss of DNs after MPTP intoxication. This DN loss in GR<sup>LysMCre</sup>
mice was not prevented by corticosterone treatment, in contrast to the protection observed in control littermates. Moreover, absence of microglial GRs augmented microglial reactivity and led to their persistent activation. Analysis of inflammatory genes revealed an up-regulation of Toll-like receptors (TLRs) by MPTP treatment, particularly TLR9, the level of which was high in postmortem parkinsonian brains. The regulatory control of GR was reflected by higher expression of proinflammatory genes (e.g., TNF-α) with a concomitant decrease in anti-inflammatory genes (e.g., IL-1R2) in GR<sup>LysMCre</sup>
mice. Indeed, in GR<sup>LysMCre</sup>
mice, alterations in phosphorylated NF-κB levels indicated its protracted activation. Together, our data indicate that GR is important in curtailing microglial reactivity, and its deregulation in PD could lead to sustained inflammation-mediated DN injury.</p>
</abstract>
</article-meta>
</front>
</pmc>
<affiliations><list><country><li>Allemagne</li>
<li>Espagne</li>
<li>France</li>
<li>République populaire de Chine</li>
</country>
</list>
<tree><country name="France"><noRegion><name sortKey="Ros Bernal, Francisco" sort="Ros Bernal, Francisco" uniqKey="Ros Bernal F" first="Francisco" last="Ros-Bernal">Francisco Ros-Bernal</name>
</noRegion>
<name sortKey="Alvarez Fischer, Daniel" sort="Alvarez Fischer, Daniel" uniqKey="Alvarez Fischer D" first="Daniel" last="Alvarez-Fischer">Daniel Alvarez-Fischer</name>
<name sortKey="Alvarez Fischer, Daniel" sort="Alvarez Fischer, Daniel" uniqKey="Alvarez Fischer D" first="Daniel" last="Alvarez-Fischer">Daniel Alvarez-Fischer</name>
<name sortKey="Alvarez Fischer, Daniel" sort="Alvarez Fischer, Daniel" uniqKey="Alvarez Fischer D" first="Daniel" last="Alvarez-Fischer">Daniel Alvarez-Fischer</name>
<name sortKey="Carrillo De Sauvage, Maria Angeles" sort="Carrillo De Sauvage, Maria Angeles" uniqKey="Carrillo De Sauvage M" first="María Angeles" last="Carrillo-De Sauvage">María Angeles Carrillo-De Sauvage</name>
<name sortKey="Carrillo De Sauvage, Maria Angeles" sort="Carrillo De Sauvage, Maria Angeles" uniqKey="Carrillo De Sauvage M" first="María Angeles" last="Carrillo-De Sauvage">María Angeles Carrillo-De Sauvage</name>
<name sortKey="Carrillo De Sauvage, Maria Angeles" sort="Carrillo De Sauvage, Maria Angeles" uniqKey="Carrillo De Sauvage M" first="María Angeles" last="Carrillo-De Sauvage">María Angeles Carrillo-De Sauvage</name>
<name sortKey="Carrillo De Sauvage, Maria Angeles" sort="Carrillo De Sauvage, Maria Angeles" uniqKey="Carrillo De Sauvage M" first="María Angeles" last="Carrillo-De Sauvage">María Angeles Carrillo-De Sauvage</name>
<name sortKey="Corvol, Jean Christophe" sort="Corvol, Jean Christophe" uniqKey="Corvol J" first="Jean-Christophe" last="Corvol">Jean-Christophe Corvol</name>
<name sortKey="Corvol, Jean Christophe" sort="Corvol, Jean Christophe" uniqKey="Corvol J" first="Jean-Christophe" last="Corvol">Jean-Christophe Corvol</name>
<name sortKey="Corvol, Jean Christophe" sort="Corvol, Jean Christophe" uniqKey="Corvol J" first="Jean-Christophe" last="Corvol">Jean-Christophe Corvol</name>
<name sortKey="Corvol, Jean Christophe" sort="Corvol, Jean Christophe" uniqKey="Corvol J" first="Jean-Christophe" last="Corvol">Jean-Christophe Corvol</name>
<name sortKey="Coussieu, Christiane" sort="Coussieu, Christiane" uniqKey="Coussieu C" first="Christiane" last="Coussieu">Christiane Coussieu</name>
<name sortKey="Hamon, Michel" sort="Hamon, Michel" uniqKey="Hamon M" first="Michel" last="Hamon">Michel Hamon</name>
<name sortKey="Hamon, Michel" sort="Hamon, Michel" uniqKey="Hamon M" first="Michel" last="Hamon">Michel Hamon</name>
<name sortKey="Hirsch, Etienne C" sort="Hirsch, Etienne C" uniqKey="Hirsch E" first="Etienne C." last="Hirsch">Etienne C. Hirsch</name>
<name sortKey="Hirsch, Etienne C" sort="Hirsch, Etienne C" uniqKey="Hirsch E" first="Etienne C." last="Hirsch">Etienne C. Hirsch</name>
<name sortKey="Hirsch, Etienne C" sort="Hirsch, Etienne C" uniqKey="Hirsch E" first="Etienne C." last="Hirsch">Etienne C. Hirsch</name>
<name sortKey="Hunot, Stephane" sort="Hunot, Stephane" uniqKey="Hunot S" first="Stéphane" last="Hunot">Stéphane Hunot</name>
<name sortKey="Hunot, Stephane" sort="Hunot, Stephane" uniqKey="Hunot S" first="Stéphane" last="Hunot">Stéphane Hunot</name>
<name sortKey="Hunot, Stephane" sort="Hunot, Stephane" uniqKey="Hunot S" first="Stéphane" last="Hunot">Stéphane Hunot</name>
<name sortKey="Kinugawa, Kiyoka" sort="Kinugawa, Kiyoka" uniqKey="Kinugawa K" first="Kiyoka" last="Kinugawa">Kiyoka Kinugawa</name>
<name sortKey="Kinugawa, Kiyoka" sort="Kinugawa, Kiyoka" uniqKey="Kinugawa K" first="Kiyoka" last="Kinugawa">Kiyoka Kinugawa</name>
<name sortKey="Kinugawa, Kiyoka" sort="Kinugawa, Kiyoka" uniqKey="Kinugawa K" first="Kiyoka" last="Kinugawa">Kiyoka Kinugawa</name>
<name sortKey="Lu, Lixia" sort="Lu, Lixia" uniqKey="Lu L" first="Lixia" last="Lu">Lixia Lu</name>
<name sortKey="Lu, Lixia" sort="Lu, Lixia" uniqKey="Lu L" first="Lixia" last="Lu">Lixia Lu</name>
<name sortKey="Lu, Lixia" sort="Lu, Lixia" uniqKey="Lu L" first="Lixia" last="Lu">Lixia Lu</name>
<name sortKey="Parnadeau, Sebastien" sort="Parnadeau, Sebastien" uniqKey="Parnadeau S" first="Sebastien" last="Parnadeau">Sebastien Parnadeau</name>
<name sortKey="Parnadeau, Sebastien" sort="Parnadeau, Sebastien" uniqKey="Parnadeau S" first="Sebastien" last="Parnadeau">Sebastien Parnadeau</name>
<name sortKey="Parnadeau, Sebastien" sort="Parnadeau, Sebastien" uniqKey="Parnadeau S" first="Sebastien" last="Parnadeau">Sebastien Parnadeau</name>
<name sortKey="Parnadeau, Sebastien" sort="Parnadeau, Sebastien" uniqKey="Parnadeau S" first="Sebastien" last="Parnadeau">Sebastien Parnadeau</name>
<name sortKey="Prigent, Annick" sort="Prigent, Annick" uniqKey="Prigent A" first="Annick" last="Prigent">Annick Prigent</name>
<name sortKey="Prigent, Annick" sort="Prigent, Annick" uniqKey="Prigent A" first="Annick" last="Prigent">Annick Prigent</name>
<name sortKey="Prigent, Annick" sort="Prigent, Annick" uniqKey="Prigent A" first="Annick" last="Prigent">Annick Prigent</name>
<name sortKey="Ros Bernal, Francisco" sort="Ros Bernal, Francisco" uniqKey="Ros Bernal F" first="Francisco" last="Ros-Bernal">Francisco Ros-Bernal</name>
<name sortKey="Ros Bernal, Francisco" sort="Ros Bernal, Francisco" uniqKey="Ros Bernal F" first="Francisco" last="Ros-Bernal">Francisco Ros-Bernal</name>
<name sortKey="Ros Bernal, Francisco" sort="Ros Bernal, Francisco" uniqKey="Ros Bernal F" first="Francisco" last="Ros-Bernal">Francisco Ros-Bernal</name>
<name sortKey="Saurini, Francoise" sort="Saurini, Francoise" uniqKey="Saurini F" first="Françoise" last="Saurini">Françoise Saurini</name>
<name sortKey="Saurini, Francoise" sort="Saurini, Francoise" uniqKey="Saurini F" first="Françoise" last="Saurini">Françoise Saurini</name>
<name sortKey="Tronche, Francois" sort="Tronche, Francois" uniqKey="Tronche F" first="François" last="Tronche">François Tronche</name>
<name sortKey="Tronche, Francois" sort="Tronche, Francois" uniqKey="Tronche F" first="François" last="Tronche">François Tronche</name>
<name sortKey="Tronche, Francois" sort="Tronche, Francois" uniqKey="Tronche F" first="François" last="Tronche">François Tronche</name>
<name sortKey="Tronche, Francois" sort="Tronche, Francois" uniqKey="Tronche F" first="François" last="Tronche">François Tronche</name>
<name sortKey="Vyas, Sheela" sort="Vyas, Sheela" uniqKey="Vyas S" first="Sheela" last="Vyas">Sheela Vyas</name>
<name sortKey="Vyas, Sheela" sort="Vyas, Sheela" uniqKey="Vyas S" first="Sheela" last="Vyas">Sheela Vyas</name>
<name sortKey="Vyas, Sheela" sort="Vyas, Sheela" uniqKey="Vyas S" first="Sheela" last="Vyas">Sheela Vyas</name>
<name sortKey="Vyas, Sheela" sort="Vyas, Sheela" uniqKey="Vyas S" first="Sheela" last="Vyas">Sheela Vyas</name>
</country>
<country name="Espagne"><noRegion><name sortKey="Ros Bernal, Francisco" sort="Ros Bernal, Francisco" uniqKey="Ros Bernal F" first="Francisco" last="Ros-Bernal">Francisco Ros-Bernal</name>
</noRegion>
<name sortKey="Carrillo De Sauvage, Maria Angeles" sort="Carrillo De Sauvage, Maria Angeles" uniqKey="Carrillo De Sauvage M" first="María Angeles" last="Carrillo-De Sauvage">María Angeles Carrillo-De Sauvage</name>
<name sortKey="Herrero, Maria Trinidad" sort="Herrero, Maria Trinidad" uniqKey="Herrero M" first="Maria Trinidad" last="Herrero">Maria Trinidad Herrero</name>
</country>
<country name="République populaire de Chine"><noRegion><name sortKey="Lu, Lixia" sort="Lu, Lixia" uniqKey="Lu L" first="Lixia" last="Lu">Lixia Lu</name>
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<country name="Allemagne"><noRegion><name sortKey="Alvarez Fischer, Daniel" sort="Alvarez Fischer, Daniel" uniqKey="Alvarez Fischer D" first="Daniel" last="Alvarez-Fischer">Daniel Alvarez-Fischer</name>
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<name sortKey="Hoglinger, Gunter" sort="Hoglinger, Gunter" uniqKey="Hoglinger G" first="Günter" last="Höglinger">Günter Höglinger</name>
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