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Uncompetitive nanomolar dimeric indenoindole inhibitors of the human breast cancer resistance pump ABCG2.

Identifieur interne : 000746 ( Main/Exploration ); précédent : 000745; suivant : 000747

Uncompetitive nanomolar dimeric indenoindole inhibitors of the human breast cancer resistance pump ABCG2.

Auteurs : Nathalie Guragossian [France] ; Billel Belhani [Algérie] ; Alexis Moreno [France] ; Magda Teixeira Nunes [France] ; Lucia Gonzalez-Lobato [France] ; Christelle Marminon [France] ; Laurent Berthier [France] ; Amanda Do Rocio Andrade Pires [Brésil] ; Csilla Özvegy-Laczka [Hongrie] ; Balázs Sarkadi [Hongrie] ; Raphaël Terreux [France] ; Zouhair Bouaziz [France] ; Malika Berredjem [Algérie] ; Joachim Jose [Allemagne] ; Attilio Di Pietro [France] ; Pierre Falson [France] ; Marc Le Borgne [France]

Source :

RBID : pubmed:33223263

Descripteurs français

English descriptors

Abstract

Multidrug resistance membrane pumps reduce the efficacy of chemotherapies by exporting a wide panel of structurally-divergent drugs. Here, to take advantage of the polyspecificity of the human Breast Cancer Resistance Protein (BCRP/ABCG2) and the dimeric nature of this pump, new dimeric indenoindole-based inhibitors from the monomeric α,β-unsaturated ketone 4b and phenolic derivative 5a were designed. A library of 18 homo/hetero-dimers was synthesised. Homo-dimerization shifted the inhibition efficacy from sub-micromolar to nanomolar range, correlated with the presence of 5a, linked by a 2-6 methylene-long linker. Non-toxic, the best dimers displayed a therapeutic ratio as high as 70,000. It has been found that the high potency of the best compound 7b that displays a KI of 17 nM is due to an uncompetitive behavior toward mitoxantrone efflux and specific for that drug, compared to Hoechst 33342 efflux. Such property may be useful to target such anticancer drug efflux mediated by ABCG2. Finally, at a molecular level, an uncompetitive mechanism by which substrate promotes inhibitor binding implies that at least 2 ligands should bind simultaneously to the drug-binding pocket of ABCG2.

DOI: 10.1016/j.ejmech.2020.113017
PubMed: 33223263


Affiliations:

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Le document en format XML

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<nlm:affiliation>Laboratoire de Biologie Tissulaire et Ingénierie, CNRS-UCBL1 UMR 5305, IBCP, 69367, Lyon, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
<wicri:regionArea>Laboratoire de Biologie Tissulaire et Ingénierie, CNRS-UCBL1 UMR 5305, IBCP, 69367, Lyon</wicri:regionArea>
<placeName>
<region type="region" nuts="2">Auvergne-Rhône-Alpes</region>
<region type="old region" nuts="2">Rhône-Alpes</region>
<settlement type="city">Lyon</settlement>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Rocio Andrade Pires, Amanda Do" sort="Rocio Andrade Pires, Amanda Do" uniqKey="Rocio Andrade Pires A" first="Amanda Do" last="Rocio Andrade Pires">Amanda Do Rocio Andrade Pires</name>
<affiliation wicri:level="1">
<nlm:affiliation>Drug Resistance & Membrane Proteins Group - Molecular Microbiology and Structural Biochemistry Laboratory, CNRS-UCBL1 UMR 5086, IBCP, 69367, Lyon, France; Departamento de Bioquímica e Biologia Molecular, Universidade Federal Do Paraná, Curitiba, Brazil.</nlm:affiliation>
<country xml:lang="fr">Brésil</country>
<wicri:regionArea>Drug Resistance & Membrane Proteins Group - Molecular Microbiology and Structural Biochemistry Laboratory, CNRS-UCBL1 UMR 5086, IBCP, 69367, Lyon, France; Departamento de Bioquímica e Biologia Molecular, Universidade Federal Do Paraná, Curitiba</wicri:regionArea>
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</affiliation>
</author>
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<name sortKey="Ozvegy Laczka, Csilla" sort="Ozvegy Laczka, Csilla" uniqKey="Ozvegy Laczka C" first="Csilla" last="Özvegy-Laczka">Csilla Özvegy-Laczka</name>
<affiliation wicri:level="3">
<nlm:affiliation>Lnstitute of Enzymology, Research Centre for Natural Sciences, Hungarian Academy of Sciences, 1117, Budapest, Hungary.</nlm:affiliation>
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<wicri:regionArea>Lnstitute of Enzymology, Research Centre for Natural Sciences, Hungarian Academy of Sciences, 1117, Budapest</wicri:regionArea>
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<settlement type="city">Budapest</settlement>
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</affiliation>
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<affiliation wicri:level="3">
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<country xml:lang="fr">Hongrie</country>
<wicri:regionArea>Lnstitute of Enzymology, Research Centre for Natural Sciences, Hungarian Academy of Sciences, 1117, Budapest</wicri:regionArea>
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<settlement type="city">Budapest</settlement>
<region nuts="2">Hongrie centrale</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Terreux, Raphael" sort="Terreux, Raphael" uniqKey="Terreux R" first="Raphaël" last="Terreux">Raphaël Terreux</name>
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<nlm:affiliation>Laboratoire de Biologie Tissulaire et Ingénierie, CNRS-UCBL1 UMR 5305, IBCP, 69367, Lyon, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
<wicri:regionArea>Laboratoire de Biologie Tissulaire et Ingénierie, CNRS-UCBL1 UMR 5305, IBCP, 69367, Lyon</wicri:regionArea>
<placeName>
<region type="region" nuts="2">Auvergne-Rhône-Alpes</region>
<region type="old region" nuts="2">Rhône-Alpes</region>
<settlement type="city">Lyon</settlement>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Bouaziz, Zouhair" sort="Bouaziz, Zouhair" uniqKey="Bouaziz Z" first="Zouhair" last="Bouaziz">Zouhair Bouaziz</name>
<affiliation wicri:level="4">
<nlm:affiliation>EA 4446 Bioactive Molecules and Medicinal Chemistry, Université Claude Bernard Lyon 1, 69373, Lyon, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
<wicri:regionArea>EA 4446 Bioactive Molecules and Medicinal Chemistry, Université Claude Bernard Lyon 1, 69373, Lyon</wicri:regionArea>
<placeName>
<region type="region" nuts="2">Auvergne-Rhône-Alpes</region>
<region type="old region" nuts="2">Rhône-Alpes</region>
<settlement type="city">Lyon</settlement>
</placeName>
<orgName type="university">Université Claude Bernard Lyon 1</orgName>
</affiliation>
</author>
<author>
<name sortKey="Berredjem, Malika" sort="Berredjem, Malika" uniqKey="Berredjem M" first="Malika" last="Berredjem">Malika Berredjem</name>
<affiliation wicri:level="1">
<nlm:affiliation>Laboratory of Applied Organic Chemistry, Synthesis of Biomolecules and Molecular Modelling Group, Badji Mokhtar - Annaba University, 23000, Annaba, Algeria.</nlm:affiliation>
<country xml:lang="fr">Algérie</country>
<wicri:regionArea>Laboratory of Applied Organic Chemistry, Synthesis of Biomolecules and Molecular Modelling Group, Badji Mokhtar - Annaba University, 23000, Annaba</wicri:regionArea>
<wicri:noRegion>Annaba</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Jose, Joachim" sort="Jose, Joachim" uniqKey="Jose J" first="Joachim" last="Jose">Joachim Jose</name>
<affiliation wicri:level="3">
<nlm:affiliation>Institut für Pharmazeutische und Medizinische Chemie, PharmaCampus - Westfälische Wilhelms-Universität Münster, D-48149, Münster, Germany.</nlm:affiliation>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Institut für Pharmazeutische und Medizinische Chemie, PharmaCampus - Westfälische Wilhelms-Universität Münster, D-48149, Münster</wicri:regionArea>
<placeName>
<region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region>
<region type="district" nuts="2">District de Münster</region>
<settlement type="city">Münster</settlement>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Di Pietro, Attilio" sort="Di Pietro, Attilio" uniqKey="Di Pietro A" first="Attilio" last="Di Pietro">Attilio Di Pietro</name>
<affiliation wicri:level="3">
<nlm:affiliation>Drug Resistance & Membrane Proteins Group - Molecular Microbiology and Structural Biochemistry Laboratory, CNRS-UCBL1 UMR 5086, IBCP, 69367, Lyon, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
<wicri:regionArea>Drug Resistance & Membrane Proteins Group - Molecular Microbiology and Structural Biochemistry Laboratory, CNRS-UCBL1 UMR 5086, IBCP, 69367, Lyon</wicri:regionArea>
<placeName>
<region type="region" nuts="2">Auvergne-Rhône-Alpes</region>
<region type="old region" nuts="2">Rhône-Alpes</region>
<settlement type="city">Lyon</settlement>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Falson, Pierre" sort="Falson, Pierre" uniqKey="Falson P" first="Pierre" last="Falson">Pierre Falson</name>
<affiliation wicri:level="3">
<nlm:affiliation>Drug Resistance & Membrane Proteins Group - Molecular Microbiology and Structural Biochemistry Laboratory, CNRS-UCBL1 UMR 5086, IBCP, 69367, Lyon, France. Electronic address: pierre.falson@univ-lyon1.fr.</nlm:affiliation>
<country xml:lang="fr">France</country>
<wicri:regionArea>Drug Resistance & Membrane Proteins Group - Molecular Microbiology and Structural Biochemistry Laboratory, CNRS-UCBL1 UMR 5086, IBCP, 69367, Lyon</wicri:regionArea>
<placeName>
<region type="region" nuts="2">Auvergne-Rhône-Alpes</region>
<region type="old region" nuts="2">Rhône-Alpes</region>
<settlement type="city">Lyon</settlement>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Le Borgne, Marc" sort="Le Borgne, Marc" uniqKey="Le Borgne M" first="Marc" last="Le Borgne">Marc Le Borgne</name>
<affiliation wicri:level="4">
<nlm:affiliation>EA 4446 Bioactive Molecules and Medicinal Chemistry, Université Claude Bernard Lyon 1, 69373, Lyon, France; Small Molecules for Biological Targets Team, Centre de Recherche en Cancérologie de Lyon, Centre Léon Bérard, CNRS 5286, INSERM 1052, Université Claude Bernard Lyon 1, Univ Lyon, Lyon, 69373, France. Electronic address: marc.le-borgne@univ-lyon1.fr.</nlm:affiliation>
<country xml:lang="fr">France</country>
<wicri:regionArea>EA 4446 Bioactive Molecules and Medicinal Chemistry, Université Claude Bernard Lyon 1, 69373, Lyon, France; Small Molecules for Biological Targets Team, Centre de Recherche en Cancérologie de Lyon, Centre Léon Bérard, CNRS 5286, INSERM 1052, Université Claude Bernard Lyon 1, Univ Lyon, Lyon, 69373</wicri:regionArea>
<placeName>
<region type="region" nuts="2">Auvergne-Rhône-Alpes</region>
<region type="old region" nuts="2">Rhône-Alpes</region>
</placeName>
<orgName type="university">Université Claude Bernard Lyon 1</orgName>
</affiliation>
</author>
</analytic>
<series>
<title level="j">European journal of medicinal chemistry</title>
<idno type="eISSN">1768-3254</idno>
<imprint>
<date when="2021" type="published">2021</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
</fileDesc>
<profileDesc>
<textClass>
<keywords scheme="KwdEn" xml:lang="en">
<term>ATP Binding Cassette Transporter, Subfamily G, Member 2 (antagonists & inhibitors)</term>
<term>ATP Binding Cassette Transporter, Subfamily G, Member 2 (genetics)</term>
<term>ATP Binding Cassette Transporter, Subfamily G, Member 2 (metabolism)</term>
<term>Antineoplastic Agents (chemical synthesis)</term>
<term>Antineoplastic Agents (chemistry)</term>
<term>Antineoplastic Agents (pharmacology)</term>
<term>Breast Neoplasms (drug therapy)</term>
<term>Breast Neoplasms (metabolism)</term>
<term>Breast Neoplasms (pathology)</term>
<term>Cell Proliferation (drug effects)</term>
<term>Cell Survival (drug effects)</term>
<term>Cells, Cultured (MeSH)</term>
<term>Dose-Response Relationship, Drug (MeSH)</term>
<term>Drug Resistance, Neoplasm (drug effects)</term>
<term>Drug Screening Assays, Antitumor (MeSH)</term>
<term>Female (MeSH)</term>
<term>Humans (MeSH)</term>
<term>Indoles (chemical synthesis)</term>
<term>Indoles (chemistry)</term>
<term>Indoles (pharmacology)</term>
<term>Molecular Dynamics Simulation (MeSH)</term>
<term>Molecular Structure (MeSH)</term>
<term>Neoplasm Proteins (antagonists & inhibitors)</term>
<term>Neoplasm Proteins (genetics)</term>
<term>Neoplasm Proteins (metabolism)</term>
<term>Structure-Activity Relationship (MeSH)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Antinéoplasiques (composition chimique)</term>
<term>Antinéoplasiques (pharmacologie)</term>
<term>Antinéoplasiques (synthèse chimique)</term>
<term>Cellules cultivées (MeSH)</term>
<term>Femelle (MeSH)</term>
<term>Humains (MeSH)</term>
<term>Indoles (composition chimique)</term>
<term>Indoles (pharmacologie)</term>
<term>Indoles (synthèse chimique)</term>
<term>Membre-2 de la sous-famille G des transporteurs à cassette liant l'ATP (antagonistes et inhibiteurs)</term>
<term>Membre-2 de la sous-famille G des transporteurs à cassette liant l'ATP (génétique)</term>
<term>Membre-2 de la sous-famille G des transporteurs à cassette liant l'ATP (métabolisme)</term>
<term>Prolifération cellulaire (effets des médicaments et des substances chimiques)</term>
<term>Protéines tumorales (antagonistes et inhibiteurs)</term>
<term>Protéines tumorales (génétique)</term>
<term>Protéines tumorales (métabolisme)</term>
<term>Relation dose-effet des médicaments (MeSH)</term>
<term>Relation structure-activité (MeSH)</term>
<term>Résistance aux médicaments antinéoplasiques (effets des médicaments et des substances chimiques)</term>
<term>Simulation de dynamique moléculaire (MeSH)</term>
<term>Structure moléculaire (MeSH)</term>
<term>Survie cellulaire (effets des médicaments et des substances chimiques)</term>
<term>Tests de criblage d'agents antitumoraux (MeSH)</term>
<term>Tumeurs du sein (anatomopathologie)</term>
<term>Tumeurs du sein (métabolisme)</term>
<term>Tumeurs du sein (traitement médicamenteux)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="antagonists & inhibitors" xml:lang="en">
<term>ATP Binding Cassette Transporter, Subfamily G, Member 2</term>
<term>Neoplasm Proteins</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="chemical synthesis" xml:lang="en">
<term>Antineoplastic Agents</term>
<term>Indoles</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="chemistry" xml:lang="en">
<term>Antineoplastic Agents</term>
<term>Indoles</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en">
<term>ATP Binding Cassette Transporter, Subfamily G, Member 2</term>
<term>Neoplasm Proteins</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en">
<term>ATP Binding Cassette Transporter, Subfamily G, Member 2</term>
<term>Neoplasm Proteins</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="pharmacology" xml:lang="en">
<term>Antineoplastic Agents</term>
<term>Indoles</term>
</keywords>
<keywords scheme="MESH" qualifier="anatomopathologie" xml:lang="fr">
<term>Tumeurs du sein</term>
</keywords>
<keywords scheme="MESH" qualifier="antagonistes et inhibiteurs" xml:lang="fr">
<term>Membre-2 de la sous-famille G des transporteurs à cassette liant l'ATP</term>
<term>Protéines tumorales</term>
</keywords>
<keywords scheme="MESH" qualifier="composition chimique" xml:lang="fr">
<term>Antinéoplasiques</term>
<term>Indoles</term>
</keywords>
<keywords scheme="MESH" qualifier="drug effects" xml:lang="en">
<term>Cell Proliferation</term>
<term>Cell Survival</term>
<term>Drug Resistance, Neoplasm</term>
</keywords>
<keywords scheme="MESH" qualifier="drug therapy" xml:lang="en">
<term>Breast Neoplasms</term>
</keywords>
<keywords scheme="MESH" qualifier="effets des médicaments et des substances chimiques" xml:lang="fr">
<term>Prolifération cellulaire</term>
<term>Résistance aux médicaments antinéoplasiques</term>
<term>Survie cellulaire</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr">
<term>Membre-2 de la sous-famille G des transporteurs à cassette liant l'ATP</term>
<term>Protéines tumorales</term>
</keywords>
<keywords scheme="MESH" qualifier="metabolism" xml:lang="en">
<term>Breast Neoplasms</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Membre-2 de la sous-famille G des transporteurs à cassette liant l'ATP</term>
<term>Protéines tumorales</term>
<term>Tumeurs du sein</term>
</keywords>
<keywords scheme="MESH" qualifier="pathology" xml:lang="en">
<term>Breast Neoplasms</term>
</keywords>
<keywords scheme="MESH" qualifier="pharmacologie" xml:lang="fr">
<term>Antinéoplasiques</term>
<term>Indoles</term>
</keywords>
<keywords scheme="MESH" qualifier="synthèse chimique" xml:lang="fr">
<term>Antinéoplasiques</term>
<term>Indoles</term>
</keywords>
<keywords scheme="MESH" qualifier="traitement médicamenteux" xml:lang="fr">
<term>Tumeurs du sein</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Cells, Cultured</term>
<term>Dose-Response Relationship, Drug</term>
<term>Drug Screening Assays, Antitumor</term>
<term>Female</term>
<term>Humans</term>
<term>Molecular Dynamics Simulation</term>
<term>Molecular Structure</term>
<term>Structure-Activity Relationship</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>Cellules cultivées</term>
<term>Femelle</term>
<term>Humains</term>
<term>Relation dose-effet des médicaments</term>
<term>Relation structure-activité</term>
<term>Simulation de dynamique moléculaire</term>
<term>Structure moléculaire</term>
<term>Tests de criblage d'agents antitumoraux</term>
</keywords>
</textClass>
</profileDesc>
</teiHeader>
<front>
<div type="abstract" xml:lang="en">Multidrug resistance membrane pumps reduce the efficacy of chemotherapies by exporting a wide panel of structurally-divergent drugs. Here, to take advantage of the polyspecificity of the human Breast Cancer Resistance Protein (BCRP/ABCG2) and the dimeric nature of this pump, new dimeric indenoindole-based inhibitors from the monomeric α,β-unsaturated ketone 4b and phenolic derivative 5a were designed. A library of 18 homo/hetero-dimers was synthesised. Homo-dimerization shifted the inhibition efficacy from sub-micromolar to nanomolar range, correlated with the presence of 5a, linked by a 2-6 methylene-long linker. Non-toxic, the best dimers displayed a therapeutic ratio as high as 70,000. It has been found that the high potency of the best compound 7b that displays a K
<sub>I</sub>
of 17 nM is due to an uncompetitive behavior toward mitoxantrone efflux and specific for that drug, compared to Hoechst 33342 efflux. Such property may be useful to target such anticancer drug efflux mediated by ABCG2. Finally, at a molecular level, an uncompetitive mechanism by which substrate promotes inhibitor binding implies that at least 2 ligands should bind simultaneously to the drug-binding pocket of ABCG2.</div>
</front>
</TEI>
<affiliations>
<list>
<country>
<li>Algérie</li>
<li>Allemagne</li>
<li>Brésil</li>
<li>France</li>
<li>Hongrie</li>
</country>
<region>
<li>Auvergne-Rhône-Alpes</li>
<li>District de Münster</li>
<li>Hongrie centrale</li>
<li>Rhénanie-du-Nord-Westphalie</li>
<li>Rhône-Alpes</li>
</region>
<settlement>
<li>Budapest</li>
<li>Lyon</li>
<li>Münster</li>
</settlement>
<orgName>
<li>Université Claude Bernard Lyon 1</li>
</orgName>
</list>
<tree>
<country name="France">
<region name="Auvergne-Rhône-Alpes">
<name sortKey="Guragossian, Nathalie" sort="Guragossian, Nathalie" uniqKey="Guragossian N" first="Nathalie" last="Guragossian">Nathalie Guragossian</name>
</region>
<name sortKey="Berthier, Laurent" sort="Berthier, Laurent" uniqKey="Berthier L" first="Laurent" last="Berthier">Laurent Berthier</name>
<name sortKey="Bouaziz, Zouhair" sort="Bouaziz, Zouhair" uniqKey="Bouaziz Z" first="Zouhair" last="Bouaziz">Zouhair Bouaziz</name>
<name sortKey="Di Pietro, Attilio" sort="Di Pietro, Attilio" uniqKey="Di Pietro A" first="Attilio" last="Di Pietro">Attilio Di Pietro</name>
<name sortKey="Falson, Pierre" sort="Falson, Pierre" uniqKey="Falson P" first="Pierre" last="Falson">Pierre Falson</name>
<name sortKey="Gonzalez Lobato, Lucia" sort="Gonzalez Lobato, Lucia" uniqKey="Gonzalez Lobato L" first="Lucia" last="Gonzalez-Lobato">Lucia Gonzalez-Lobato</name>
<name sortKey="Le Borgne, Marc" sort="Le Borgne, Marc" uniqKey="Le Borgne M" first="Marc" last="Le Borgne">Marc Le Borgne</name>
<name sortKey="Marminon, Christelle" sort="Marminon, Christelle" uniqKey="Marminon C" first="Christelle" last="Marminon">Christelle Marminon</name>
<name sortKey="Moreno, Alexis" sort="Moreno, Alexis" uniqKey="Moreno A" first="Alexis" last="Moreno">Alexis Moreno</name>
<name sortKey="Nunes, Magda Teixeira" sort="Nunes, Magda Teixeira" uniqKey="Nunes M" first="Magda Teixeira" last="Nunes">Magda Teixeira Nunes</name>
<name sortKey="Terreux, Raphael" sort="Terreux, Raphael" uniqKey="Terreux R" first="Raphaël" last="Terreux">Raphaël Terreux</name>
</country>
<country name="Algérie">
<region name="Auvergne-Rhône-Alpes">
<name sortKey="Belhani, Billel" sort="Belhani, Billel" uniqKey="Belhani B" first="Billel" last="Belhani">Billel Belhani</name>
</region>
<name sortKey="Berredjem, Malika" sort="Berredjem, Malika" uniqKey="Berredjem M" first="Malika" last="Berredjem">Malika Berredjem</name>
</country>
<country name="Brésil">
<noRegion>
<name sortKey="Rocio Andrade Pires, Amanda Do" sort="Rocio Andrade Pires, Amanda Do" uniqKey="Rocio Andrade Pires A" first="Amanda Do" last="Rocio Andrade Pires">Amanda Do Rocio Andrade Pires</name>
</noRegion>
</country>
<country name="Hongrie">
<region name="Hongrie centrale">
<name sortKey="Ozvegy Laczka, Csilla" sort="Ozvegy Laczka, Csilla" uniqKey="Ozvegy Laczka C" first="Csilla" last="Özvegy-Laczka">Csilla Özvegy-Laczka</name>
</region>
<name sortKey="Sarkadi, Balazs" sort="Sarkadi, Balazs" uniqKey="Sarkadi B" first="Balázs" last="Sarkadi">Balázs Sarkadi</name>
</country>
<country name="Allemagne">
<region name="Rhénanie-du-Nord-Westphalie">
<name sortKey="Jose, Joachim" sort="Jose, Joachim" uniqKey="Jose J" first="Joachim" last="Jose">Joachim Jose</name>
</region>
</country>
</tree>
</affiliations>
</record>

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