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Cationic penetrating antioxidants switch off Mn cluster of photosystem II in situ.

Identifieur interne : 000149 ( Main/Exploration ); précédent : 000148; suivant : 000150

Cationic penetrating antioxidants switch off Mn cluster of photosystem II in situ.

Auteurs : Vasily V. Ptushenko [Russie] ; Alexei E. Solovchenko ; Andrew Y. Bychkov ; Olga B. Chivkunova ; Andrey V. Golovin ; Olga A. Gorelova ; Tatiana T. Ismagulova ; Leonid V. Kulik ; Elena S. Lobakova ; Alexandr A. Lukyanov ; Rima I. Samoilova ; Pavel N. Scherbakov ; Irina O. Selyakh ; Larisa R. Semenova ; Svetlana G. Vasilieva ; Olga I. Baulina ; Maxim V. Skulachev ; Mikhail P. Kirpichnikov

Source :

RBID : pubmed:31302832

Descripteurs français

English descriptors

Abstract

Mitochondria-targeted antioxidants (also known as 'Skulachev Ions' electrophoretically accumulated by mitochondria) exert anti-ageing and ROS-protecting effects well documented in animal and human cells. However, their effects on chloroplast in photosynthetic cells and corresponding mechanisms are scarcely known. For the first time, we describe a dramatic quenching effect of (10-(6-plastoquinonyl)decyl triphenylphosphonium (SkQ1) on chlorophyll fluorescence, apparently mediated by redox interaction of SkQ1 with Mn cluster in Photosystem II (PSII) of chlorophyte microalga Chlorella vulgaris and disabling the oxygen-evolving complex (OEC). Microalgal cells displayed a vigorous uptake of SkQ1 which internal concentration built up to a very high level. Using optical and EPR spectroscopy, as well as electron donors and in silico molecular simulation techniques, we found that SkQ1 molecule can interact with Mn atoms of the OEC in PSII. This stops water splitting giving rise to potent quencher(s), e.g. oxidized reaction centre of PSII. Other components of the photosynthetic apparatus proved to be mostly intact. This effect of the Skulachev ions might help to develop in vivo models of photosynthetic cells with impaired OEC function but essentially intact otherwise. The observed phenomenon suggests that SkQ1 can be applied to study stress-induced damages to OEC in photosynthetic organisms.

DOI: 10.1007/s11120-019-00657-2
PubMed: 31302832


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Le document en format XML

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<nlm:affiliation>Institute of Mitoengineering, M.V. Lomonosov Moscow State University, Moscow, Russia, 119234.</nlm:affiliation>
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<name sortKey="Chivkunova, Olga B" sort="Chivkunova, Olga B" uniqKey="Chivkunova O" first="Olga B" last="Chivkunova">Olga B. Chivkunova</name>
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<nlm:affiliation>Faculty of Biology, M.V. Lomonosov Moscow State University, Moscow, Russia, 119234.</nlm:affiliation>
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<name sortKey="Golovin, Andrey V" sort="Golovin, Andrey V" uniqKey="Golovin A" first="Andrey V" last="Golovin">Andrey V. Golovin</name>
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<nlm:affiliation>Faculty of Bioengineering and Bioinformatics, M.V. Lomonosov Moscow State University, Moscow, Russia, 119234.</nlm:affiliation>
<wicri:noCountry code="subField">119234</wicri:noCountry>
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<nlm:affiliation>Institute of Molecular Medicine, Sechenov First Moscow State Medical University, Moscow, Russia, 119991.</nlm:affiliation>
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<name sortKey="Gorelova, Olga A" sort="Gorelova, Olga A" uniqKey="Gorelova O" first="Olga A" last="Gorelova">Olga A. Gorelova</name>
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<nlm:affiliation>Faculty of Biology, M.V. Lomonosov Moscow State University, Moscow, Russia, 119234.</nlm:affiliation>
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<name sortKey="Ismagulova, Tatiana T" sort="Ismagulova, Tatiana T" uniqKey="Ismagulova T" first="Tatiana T" last="Ismagulova">Tatiana T. Ismagulova</name>
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<nlm:affiliation>Faculty of Biology, M.V. Lomonosov Moscow State University, Moscow, Russia, 119234.</nlm:affiliation>
<wicri:noCountry code="subField">119234</wicri:noCountry>
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<name sortKey="Kulik, Leonid V" sort="Kulik, Leonid V" uniqKey="Kulik L" first="Leonid V" last="Kulik">Leonid V. Kulik</name>
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<nlm:affiliation>Novosibirsk State University, Pirogova Street 2, Novosibirsk, Russia, 630090.</nlm:affiliation>
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<name sortKey="Lobakova, Elena S" sort="Lobakova, Elena S" uniqKey="Lobakova E" first="Elena S" last="Lobakova">Elena S. Lobakova</name>
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<nlm:affiliation>Faculty of Biology, M.V. Lomonosov Moscow State University, Moscow, Russia, 119234.</nlm:affiliation>
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<name sortKey="Samoilova, Rima I" sort="Samoilova, Rima I" uniqKey="Samoilova R" first="Rima I" last="Samoilova">Rima I. Samoilova</name>
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<nlm:affiliation>V.V. Voevodsky Institute of Chemical Kinetics and Combustion of SB RAS, Novosibirsk, Russia, 630090.</nlm:affiliation>
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<name sortKey="Scherbakov, Pavel N" sort="Scherbakov, Pavel N" uniqKey="Scherbakov P" first="Pavel N" last="Scherbakov">Pavel N. Scherbakov</name>
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<name sortKey="Selyakh, Irina O" sort="Selyakh, Irina O" uniqKey="Selyakh I" first="Irina O" last="Selyakh">Irina O. Selyakh</name>
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<wicri:noCountry code="subField">119234</wicri:noCountry>
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<name sortKey="Semenova, Larisa R" sort="Semenova, Larisa R" uniqKey="Semenova L" first="Larisa R" last="Semenova">Larisa R. Semenova</name>
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<nlm:affiliation>Faculty of Biology, M.V. Lomonosov Moscow State University, Moscow, Russia, 119234.</nlm:affiliation>
<wicri:noCountry code="subField">119234</wicri:noCountry>
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<name sortKey="Vasilieva, Svetlana G" sort="Vasilieva, Svetlana G" uniqKey="Vasilieva S" first="Svetlana G" last="Vasilieva">Svetlana G. Vasilieva</name>
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<nlm:affiliation>Faculty of Biology, M.V. Lomonosov Moscow State University, Moscow, Russia, 119234.</nlm:affiliation>
<wicri:noCountry code="subField">119234</wicri:noCountry>
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<wicri:noCountry code="subField">119234</wicri:noCountry>
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<wicri:noCountry code="subField">119234</wicri:noCountry>
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<nlm:affiliation>Institute of Mitoengineering, M.V. Lomonosov Moscow State University, Moscow, Russia, 119234.</nlm:affiliation>
<wicri:noCountry code="subField">119234</wicri:noCountry>
</affiliation>
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<title level="j">Photosynthesis research</title>
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<term>Antioxidants (metabolism)</term>
<term>Cations (MeSH)</term>
<term>Chlorella vulgaris (drug effects)</term>
<term>Chlorella vulgaris (metabolism)</term>
<term>Chlorophyll (metabolism)</term>
<term>Fluorescence (MeSH)</term>
<term>Hydrophobic and Hydrophilic Interactions (MeSH)</term>
<term>Kinetics (MeSH)</term>
<term>Light (MeSH)</term>
<term>Manganese (metabolism)</term>
<term>Molecular Docking Simulation (MeSH)</term>
<term>Oxygen (metabolism)</term>
<term>Photosystem II Protein Complex (metabolism)</term>
<term>Plastoquinone (analogs & derivatives)</term>
<term>Plastoquinone (pharmacology)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Antioxydants (métabolisme)</term>
<term>Cations (MeSH)</term>
<term>Chlorella vulgaris (effets des médicaments et des substances chimiques)</term>
<term>Chlorella vulgaris (métabolisme)</term>
<term>Chlorophylle (métabolisme)</term>
<term>Cinétique (MeSH)</term>
<term>Complexe protéique du photosystème II (métabolisme)</term>
<term>Fluorescence (MeSH)</term>
<term>Interactions hydrophobes et hydrophiles (MeSH)</term>
<term>Lumière (MeSH)</term>
<term>Manganèse (métabolisme)</term>
<term>Oxygène (métabolisme)</term>
<term>Plastoquinone 9 (analogues et dérivés)</term>
<term>Plastoquinone 9 (pharmacologie)</term>
<term>Simulation de docking moléculaire (MeSH)</term>
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<term>Plastoquinone</term>
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<term>Antioxidants</term>
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<term>Plastoquinone</term>
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<term>Chlorella vulgaris</term>
<term>Chlorophylle</term>
<term>Complexe protéique du photosystème II</term>
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<term>Molecular Docking Simulation</term>
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<term>Cinétique</term>
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<term>Interactions hydrophobes et hydrophiles</term>
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<div type="abstract" xml:lang="en">Mitochondria-targeted antioxidants (also known as 'Skulachev Ions' electrophoretically accumulated by mitochondria) exert anti-ageing and ROS-protecting effects well documented in animal and human cells. However, their effects on chloroplast in photosynthetic cells and corresponding mechanisms are scarcely known. For the first time, we describe a dramatic quenching effect of (10-(6-plastoquinonyl)decyl triphenylphosphonium (SkQ1) on chlorophyll fluorescence, apparently mediated by redox interaction of SkQ1 with Mn cluster in Photosystem II (PSII) of chlorophyte microalga Chlorella vulgaris and disabling the oxygen-evolving complex (OEC). Microalgal cells displayed a vigorous uptake of SkQ1 which internal concentration built up to a very high level. Using optical and EPR spectroscopy, as well as electron donors and in silico molecular simulation techniques, we found that SkQ1 molecule can interact with Mn atoms of the OEC in PSII. This stops water splitting giving rise to potent quencher(s), e.g. oxidized reaction centre of PSII. Other components of the photosynthetic apparatus proved to be mostly intact. This effect of the Skulachev ions might help to develop in vivo models of photosynthetic cells with impaired OEC function but essentially intact otherwise. The observed phenomenon suggests that SkQ1 can be applied to study stress-induced damages to OEC in photosynthetic organisms.</div>
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<Title>Photosynthesis research</Title>
<ISOAbbreviation>Photosynth Res</ISOAbbreviation>
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<ArticleTitle>Cationic penetrating antioxidants switch off Mn cluster of photosystem II in situ.</ArticleTitle>
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<AbstractText>Mitochondria-targeted antioxidants (also known as 'Skulachev Ions' electrophoretically accumulated by mitochondria) exert anti-ageing and ROS-protecting effects well documented in animal and human cells. However, their effects on chloroplast in photosynthetic cells and corresponding mechanisms are scarcely known. For the first time, we describe a dramatic quenching effect of (10-(6-plastoquinonyl)decyl triphenylphosphonium (SkQ1) on chlorophyll fluorescence, apparently mediated by redox interaction of SkQ1 with Mn cluster in Photosystem II (PSII) of chlorophyte microalga Chlorella vulgaris and disabling the oxygen-evolving complex (OEC). Microalgal cells displayed a vigorous uptake of SkQ1 which internal concentration built up to a very high level. Using optical and EPR spectroscopy, as well as electron donors and in silico molecular simulation techniques, we found that SkQ1 molecule can interact with Mn atoms of the OEC in PSII. This stops water splitting giving rise to potent quencher(s), e.g. oxidized reaction centre of PSII. Other components of the photosynthetic apparatus proved to be mostly intact. This effect of the Skulachev ions might help to develop in vivo models of photosynthetic cells with impaired OEC function but essentially intact otherwise. The observed phenomenon suggests that SkQ1 can be applied to study stress-induced damages to OEC in photosynthetic organisms.</AbstractText>
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<ForeName>Vasily V</ForeName>
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<Affiliation>A.N. Belozersky Institute of Physical-Chemical Biology, M.V. Lomonosov Moscow State University, Moscow, Russia, 119234. ptush@belozersky.msu.ru.</Affiliation>
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<AffiliationInfo>
<Affiliation>N.M. Emanuel Institute of Biochemical Physics of RAS, Moscow, Russia, 119334. ptush@belozersky.msu.ru.</Affiliation>
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<LastName>Solovchenko</LastName>
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<Affiliation>Faculty of Biology, M.V. Lomonosov Moscow State University, Moscow, Russia, 119234.</Affiliation>
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<AffiliationInfo>
<Affiliation>Peoples Friendship University of Russia (RUDN University), Moscow, Russia, 117198.</Affiliation>
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<LastName>Bychkov</LastName>
<ForeName>Andrew Y</ForeName>
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<Affiliation>Faculty of Geology, M.V. Lomonosov Moscow State University, Moscow, Russia, 119234.</Affiliation>
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<LastName>Chivkunova</LastName>
<ForeName>Olga B</ForeName>
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<LastName>Golovin</LastName>
<ForeName>Andrey V</ForeName>
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<Affiliation>Faculty of Bioengineering and Bioinformatics, M.V. Lomonosov Moscow State University, Moscow, Russia, 119234.</Affiliation>
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<AffiliationInfo>
<Affiliation>Institute of Molecular Medicine, Sechenov First Moscow State Medical University, Moscow, Russia, 119991.</Affiliation>
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<ForeName>Tatiana T</ForeName>
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<LastName>Kulik</LastName>
<ForeName>Leonid V</ForeName>
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<Affiliation>V.V. Voevodsky Institute of Chemical Kinetics and Combustion of SB RAS, Novosibirsk, Russia, 630090.</Affiliation>
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<AffiliationInfo>
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<LastName>Lukyanov</LastName>
<ForeName>Alexandr A</ForeName>
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<ForeName>Rima I</ForeName>
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<LastName>Scherbakov</LastName>
<ForeName>Pavel N</ForeName>
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<LastName>Selyakh</LastName>
<ForeName>Irina O</ForeName>
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<Affiliation>Faculty of Biology, M.V. Lomonosov Moscow State University, Moscow, Russia, 119234.</Affiliation>
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<LastName>Semenova</LastName>
<ForeName>Larisa R</ForeName>
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<Affiliation>Faculty of Biology, M.V. Lomonosov Moscow State University, Moscow, Russia, 119234.</Affiliation>
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<LastName>Vasilieva</LastName>
<ForeName>Svetlana G</ForeName>
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<LastName>Baulina</LastName>
<ForeName>Olga I</ForeName>
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<Affiliation>Faculty of Biology, M.V. Lomonosov Moscow State University, Moscow, Russia, 119234.</Affiliation>
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<LastName>Skulachev</LastName>
<ForeName>Maxim V</ForeName>
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<Affiliation>A.N. Belozersky Institute of Physical-Chemical Biology, M.V. Lomonosov Moscow State University, Moscow, Russia, 119234.</Affiliation>
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<AffiliationInfo>
<Affiliation>Institute of Mitoengineering, M.V. Lomonosov Moscow State University, Moscow, Russia, 119234.</Affiliation>
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<LastName>Kirpichnikov</LastName>
<ForeName>Mikhail P</ForeName>
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<Affiliation>Faculty of Biology, M.V. Lomonosov Moscow State University, Moscow, Russia, 119234.</Affiliation>
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<Country></Country>
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<Citation>Biochim Biophys Acta. 1983 Jul 15;726(2):97-133</Citation>
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<Reference>
<Citation>Biochim Biophys Acta. 2015 Dec;1847(12):1495-508</Citation>
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<name sortKey="Bychkov, Andrew Y" sort="Bychkov, Andrew Y" uniqKey="Bychkov A" first="Andrew Y" last="Bychkov">Andrew Y. Bychkov</name>
<name sortKey="Chivkunova, Olga B" sort="Chivkunova, Olga B" uniqKey="Chivkunova O" first="Olga B" last="Chivkunova">Olga B. Chivkunova</name>
<name sortKey="Golovin, Andrey V" sort="Golovin, Andrey V" uniqKey="Golovin A" first="Andrey V" last="Golovin">Andrey V. Golovin</name>
<name sortKey="Gorelova, Olga A" sort="Gorelova, Olga A" uniqKey="Gorelova O" first="Olga A" last="Gorelova">Olga A. Gorelova</name>
<name sortKey="Ismagulova, Tatiana T" sort="Ismagulova, Tatiana T" uniqKey="Ismagulova T" first="Tatiana T" last="Ismagulova">Tatiana T. Ismagulova</name>
<name sortKey="Kirpichnikov, Mikhail P" sort="Kirpichnikov, Mikhail P" uniqKey="Kirpichnikov M" first="Mikhail P" last="Kirpichnikov">Mikhail P. Kirpichnikov</name>
<name sortKey="Kulik, Leonid V" sort="Kulik, Leonid V" uniqKey="Kulik L" first="Leonid V" last="Kulik">Leonid V. Kulik</name>
<name sortKey="Lobakova, Elena S" sort="Lobakova, Elena S" uniqKey="Lobakova E" first="Elena S" last="Lobakova">Elena S. Lobakova</name>
<name sortKey="Lukyanov, Alexandr A" sort="Lukyanov, Alexandr A" uniqKey="Lukyanov A" first="Alexandr A" last="Lukyanov">Alexandr A. Lukyanov</name>
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<name sortKey="Scherbakov, Pavel N" sort="Scherbakov, Pavel N" uniqKey="Scherbakov P" first="Pavel N" last="Scherbakov">Pavel N. Scherbakov</name>
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<name sortKey="Semenova, Larisa R" sort="Semenova, Larisa R" uniqKey="Semenova L" first="Larisa R" last="Semenova">Larisa R. Semenova</name>
<name sortKey="Skulachev, Maxim V" sort="Skulachev, Maxim V" uniqKey="Skulachev M" first="Maxim V" last="Skulachev">Maxim V. Skulachev</name>
<name sortKey="Solovchenko, Alexei E" sort="Solovchenko, Alexei E" uniqKey="Solovchenko A" first="Alexei E" last="Solovchenko">Alexei E. Solovchenko</name>
<name sortKey="Vasilieva, Svetlana G" sort="Vasilieva, Svetlana G" uniqKey="Vasilieva S" first="Svetlana G" last="Vasilieva">Svetlana G. Vasilieva</name>
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