Characterization of the Lipidomic Profile of Human Coronavirus-Infected Cells: Implications for Lipid Metabolism Remodeling upon Coronavirus Replication
Identifieur interne : 000665 ( Main/Exploration ); précédent : 000664; suivant : 000666Characterization of the Lipidomic Profile of Human Coronavirus-Infected Cells: Implications for Lipid Metabolism Remodeling upon Coronavirus Replication
Auteurs : Bingpeng Yan ; Hin Chu ; Dong Yang ; Kong-Hung Sze ; Pok-Man Lai ; Shuofeng Yuan ; Huiping Shuai ; Yixin Wang ; Richard Yi-Tsun Kao ; Jasper Fuk-Woo Chan [République populaire de Chine] ; Kwok-Yung Yuen [République populaire de Chine]Source :
- Viruses [ 1999-4915 ] ; 2019.
Descripteurs français
- KwdFr :
- Acide arachidonique (métabolisme), Acide linoléique (métabolisme), Chromatographie en phase liquide, Coronavirus humain 229E (physiologie), Glycérophospholipides (métabolisme), Humains, Interactions hôte-pathogène, Lignée cellulaire, Métabolisme des lipides, Réplication virale, Spectrométrie de masse en tandem.
- MESH :
English descriptors
- KwdEn :
- MESH :
- chemical , metabolism : Arachidonic Acid, Glycerophospholipids, Linoleic Acid.
- physiology : Coronavirus 229E, Human.
- Cell Line, Chromatography, Liquid, Host-Pathogen Interactions, Humans, Lipid Metabolism, Tandem Mass Spectrometry, Virus Replication.
Abstract
Lipids play numerous indispensable cellular functions and are involved in multiple steps in the replication cycle of viruses. Infections by human-pathogenic coronaviruses result in diverse clinical outcomes, ranging from self-limiting flu-like symptoms to severe pneumonia with extrapulmonary manifestations. Understanding how cellular lipids may modulate the pathogenicity of human-pathogenic coronaviruses remains poor. To this end, we utilized the human coronavirus 229E (HCoV-229E) as a model coronavirus to comprehensively characterize the host cell lipid response upon coronavirus infection with an ultra-high performance liquid chromatography-mass spectrometry (UPLC–MS)-based lipidomics approach. Our results revealed that glycerophospholipids and fatty acids (FAs) were significantly elevated in the HCoV-229E-infected cells and the linoleic acid (LA) to arachidonic acid (AA) metabolism axis was markedly perturbed upon HCoV-229E infection. Interestingly, exogenous supplement of LA or AA in HCoV-229E-infected cells significantly suppressed HCoV-229E virus replication. Importantly, the inhibitory effect of LA and AA on virus replication was also conserved for the highly pathogenic Middle East respiratory syndrome coronavirus (MERS-CoV). Taken together, our study demonstrated that host lipid metabolic remodeling was significantly associated with human-pathogenic coronavirus propagation. Our data further suggested that lipid metabolism regulation would be a common and druggable target for coronavirus infections.
Url:
DOI: 10.3390/v11010073
PubMed: 30654597
PubMed Central: 6357182
Affiliations:
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Le document en format XML
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Characterization of the Lipidomic Profile of Human Coronavirus-Infected Cells: Implications for Lipid Metabolism Remodeling upon Coronavirus Replication</title>
<author><name sortKey="Yan, Bingpeng" sort="Yan, Bingpeng" uniqKey="Yan B" first="Bingpeng" last="Yan">Bingpeng Yan</name>
<affiliation><nlm:aff id="af1-viruses-11-00073">State Key Laboratory of Emerging Infectious Diseases, The University of Hong Kong, Pokfulam, Hong Kong Special Administrative Region, China;<email>ybp1205@hku.hk</email>
(B.Y.);<email>hinchu@hku.hk</email>
(H.C.);<email>khsze@hku.hk</email>
(K.-H.S.);<email>yuansf@hku.hk</email>
(S.Y.);<email>rytkao@hku.hk</email>
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<affiliation><nlm:aff id="af2-viruses-11-00073">Department of Microbiology, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Hong Kong Special Administrative Region, China;<email>u3005140@connect.hku.hk</email>
(D.Y.);<email>vangor@hku.hk</email>
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<author><name sortKey="Chu, Hin" sort="Chu, Hin" uniqKey="Chu H" first="Hin" last="Chu">Hin Chu</name>
<affiliation><nlm:aff id="af1-viruses-11-00073">State Key Laboratory of Emerging Infectious Diseases, The University of Hong Kong, Pokfulam, Hong Kong Special Administrative Region, China;<email>ybp1205@hku.hk</email>
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<affiliation><nlm:aff id="af2-viruses-11-00073">Department of Microbiology, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Hong Kong Special Administrative Region, China;<email>u3005140@connect.hku.hk</email>
(D.Y.);<email>vangor@hku.hk</email>
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<author><name sortKey="Yang, Dong" sort="Yang, Dong" uniqKey="Yang D" first="Dong" last="Yang">Dong Yang</name>
<affiliation><nlm:aff id="af2-viruses-11-00073">Department of Microbiology, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Hong Kong Special Administrative Region, China;<email>u3005140@connect.hku.hk</email>
(D.Y.);<email>vangor@hku.hk</email>
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<author><name sortKey="Sze, Kong Hung" sort="Sze, Kong Hung" uniqKey="Sze K" first="Kong-Hung" last="Sze">Kong-Hung Sze</name>
<affiliation><nlm:aff id="af1-viruses-11-00073">State Key Laboratory of Emerging Infectious Diseases, The University of Hong Kong, Pokfulam, Hong Kong Special Administrative Region, China;<email>ybp1205@hku.hk</email>
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<affiliation><nlm:aff id="af2-viruses-11-00073">Department of Microbiology, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Hong Kong Special Administrative Region, China;<email>u3005140@connect.hku.hk</email>
(D.Y.);<email>vangor@hku.hk</email>
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<author><name sortKey="Lai, Pok Man" sort="Lai, Pok Man" uniqKey="Lai P" first="Pok-Man" last="Lai">Pok-Man Lai</name>
<affiliation><nlm:aff id="af2-viruses-11-00073">Department of Microbiology, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Hong Kong Special Administrative Region, China;<email>u3005140@connect.hku.hk</email>
(D.Y.);<email>vangor@hku.hk</email>
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</author>
<author><name sortKey="Yuan, Shuofeng" sort="Yuan, Shuofeng" uniqKey="Yuan S" first="Shuofeng" last="Yuan">Shuofeng Yuan</name>
<affiliation><nlm:aff id="af1-viruses-11-00073">State Key Laboratory of Emerging Infectious Diseases, The University of Hong Kong, Pokfulam, Hong Kong Special Administrative Region, China;<email>ybp1205@hku.hk</email>
(B.Y.);<email>hinchu@hku.hk</email>
(H.C.);<email>khsze@hku.hk</email>
(K.-H.S.);<email>yuansf@hku.hk</email>
(S.Y.);<email>rytkao@hku.hk</email>
(R.Y.-T.K.)</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="af2-viruses-11-00073">Department of Microbiology, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Hong Kong Special Administrative Region, China;<email>u3005140@connect.hku.hk</email>
(D.Y.);<email>vangor@hku.hk</email>
(P.-M.L.);<email>shuaihp@connect.hku.hk</email>
(H.S.);<email>jasyx@connect.hku.hk</email>
(Y.W.)</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Shuai, Huiping" sort="Shuai, Huiping" uniqKey="Shuai H" first="Huiping" last="Shuai">Huiping Shuai</name>
<affiliation><nlm:aff id="af2-viruses-11-00073">Department of Microbiology, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Hong Kong Special Administrative Region, China;<email>u3005140@connect.hku.hk</email>
(D.Y.);<email>vangor@hku.hk</email>
(P.-M.L.);<email>shuaihp@connect.hku.hk</email>
(H.S.);<email>jasyx@connect.hku.hk</email>
(Y.W.)</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Wang, Yixin" sort="Wang, Yixin" uniqKey="Wang Y" first="Yixin" last="Wang">Yixin Wang</name>
<affiliation><nlm:aff id="af2-viruses-11-00073">Department of Microbiology, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Hong Kong Special Administrative Region, China;<email>u3005140@connect.hku.hk</email>
(D.Y.);<email>vangor@hku.hk</email>
(P.-M.L.);<email>shuaihp@connect.hku.hk</email>
(H.S.);<email>jasyx@connect.hku.hk</email>
(Y.W.)</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Kao, Richard Yi Tsun" sort="Kao, Richard Yi Tsun" uniqKey="Kao R" first="Richard Yi-Tsun" last="Kao">Richard Yi-Tsun Kao</name>
<affiliation><nlm:aff id="af1-viruses-11-00073">State Key Laboratory of Emerging Infectious Diseases, The University of Hong Kong, Pokfulam, Hong Kong Special Administrative Region, China;<email>ybp1205@hku.hk</email>
(B.Y.);<email>hinchu@hku.hk</email>
(H.C.);<email>khsze@hku.hk</email>
(K.-H.S.);<email>yuansf@hku.hk</email>
(S.Y.);<email>rytkao@hku.hk</email>
(R.Y.-T.K.)</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="af2-viruses-11-00073">Department of Microbiology, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Hong Kong Special Administrative Region, China;<email>u3005140@connect.hku.hk</email>
(D.Y.);<email>vangor@hku.hk</email>
(P.-M.L.);<email>shuaihp@connect.hku.hk</email>
(H.S.);<email>jasyx@connect.hku.hk</email>
(Y.W.)</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Chan, Jasper Fuk Woo" sort="Chan, Jasper Fuk Woo" uniqKey="Chan J" first="Jasper Fuk-Woo" last="Chan">Jasper Fuk-Woo Chan</name>
<affiliation><nlm:aff id="af1-viruses-11-00073">State Key Laboratory of Emerging Infectious Diseases, The University of Hong Kong, Pokfulam, Hong Kong Special Administrative Region, China;<email>ybp1205@hku.hk</email>
(B.Y.);<email>hinchu@hku.hk</email>
(H.C.);<email>khsze@hku.hk</email>
(K.-H.S.);<email>yuansf@hku.hk</email>
(S.Y.);<email>rytkao@hku.hk</email>
(R.Y.-T.K.)</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="af2-viruses-11-00073">Department of Microbiology, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Hong Kong Special Administrative Region, China;<email>u3005140@connect.hku.hk</email>
(D.Y.);<email>vangor@hku.hk</email>
(P.-M.L.);<email>shuaihp@connect.hku.hk</email>
(H.S.);<email>jasyx@connect.hku.hk</email>
(Y.W.)</nlm:aff>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="af3-viruses-11-00073">Carol Yu Centre for Infection, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Hong Kong Special Administrative Region, China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Carol Yu Centre for Infection, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Hong Kong Special Administrative Region</wicri:regionArea>
<wicri:noRegion>Hong Kong Special Administrative Region</wicri:noRegion>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="af4-viruses-11-00073">Hainan-Medical University-The University of Hong Kong Joint Laboratory of Tropical Infectious Diseases, Hainan Medical University, Haikou 96708, China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Hainan-Medical University-The University of Hong Kong Joint Laboratory of Tropical Infectious Diseases, Hainan Medical University, Haikou 96708</wicri:regionArea>
<wicri:noRegion>Haikou 96708</wicri:noRegion>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="af5-viruses-11-00073">Hainan-Medical University-The University of Hong Kong Joint Laboratory of Tropical Infectious Diseases, The University of Hong Kong, Pokfulam, Hong Kong Special Administrative Region, China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Hainan-Medical University-The University of Hong Kong Joint Laboratory of Tropical Infectious Diseases, The University of Hong Kong, Pokfulam, Hong Kong Special Administrative Region</wicri:regionArea>
<wicri:noRegion>Hong Kong Special Administrative Region</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Yuen, Kwok Yung" sort="Yuen, Kwok Yung" uniqKey="Yuen K" first="Kwok-Yung" last="Yuen">Kwok-Yung Yuen</name>
<affiliation><nlm:aff id="af1-viruses-11-00073">State Key Laboratory of Emerging Infectious Diseases, The University of Hong Kong, Pokfulam, Hong Kong Special Administrative Region, China;<email>ybp1205@hku.hk</email>
(B.Y.);<email>hinchu@hku.hk</email>
(H.C.);<email>khsze@hku.hk</email>
(K.-H.S.);<email>yuansf@hku.hk</email>
(S.Y.);<email>rytkao@hku.hk</email>
(R.Y.-T.K.)</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="af2-viruses-11-00073">Department of Microbiology, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Hong Kong Special Administrative Region, China;<email>u3005140@connect.hku.hk</email>
(D.Y.);<email>vangor@hku.hk</email>
(P.-M.L.);<email>shuaihp@connect.hku.hk</email>
(H.S.);<email>jasyx@connect.hku.hk</email>
(Y.W.)</nlm:aff>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="af3-viruses-11-00073">Carol Yu Centre for Infection, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Hong Kong Special Administrative Region, China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Carol Yu Centre for Infection, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Hong Kong Special Administrative Region</wicri:regionArea>
<wicri:noRegion>Hong Kong Special Administrative Region</wicri:noRegion>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="af4-viruses-11-00073">Hainan-Medical University-The University of Hong Kong Joint Laboratory of Tropical Infectious Diseases, Hainan Medical University, Haikou 96708, China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Hainan-Medical University-The University of Hong Kong Joint Laboratory of Tropical Infectious Diseases, Hainan Medical University, Haikou 96708</wicri:regionArea>
<wicri:noRegion>Haikou 96708</wicri:noRegion>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="af5-viruses-11-00073">Hainan-Medical University-The University of Hong Kong Joint Laboratory of Tropical Infectious Diseases, The University of Hong Kong, Pokfulam, Hong Kong Special Administrative Region, China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Hainan-Medical University-The University of Hong Kong Joint Laboratory of Tropical Infectious Diseases, The University of Hong Kong, Pokfulam, Hong Kong Special Administrative Region</wicri:regionArea>
<wicri:noRegion>Hong Kong Special Administrative Region</wicri:noRegion>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="af6-viruses-11-00073">The Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, The University of Hong Kong, Pokfulam, Hong Kong Special Administrative Region, China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>The Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, The University of Hong Kong, Pokfulam, Hong Kong Special Administrative Region</wicri:regionArea>
<wicri:noRegion>Hong Kong Special Administrative Region</wicri:noRegion>
</affiliation>
</author>
</analytic>
<series><title level="j">Viruses</title>
<idno type="eISSN">1999-4915</idno>
<imprint><date when="2019">2019</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
</fileDesc>
<profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Arachidonic Acid (metabolism)</term>
<term>Cell Line</term>
<term>Chromatography, Liquid</term>
<term>Coronavirus 229E, Human (physiology)</term>
<term>Glycerophospholipids (metabolism)</term>
<term>Host-Pathogen Interactions</term>
<term>Humans</term>
<term>Linoleic Acid (metabolism)</term>
<term>Lipid Metabolism</term>
<term>Tandem Mass Spectrometry</term>
<term>Virus Replication</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr"><term>Acide arachidonique (métabolisme)</term>
<term>Acide linoléique (métabolisme)</term>
<term>Chromatographie en phase liquide</term>
<term>Coronavirus humain 229E (physiologie)</term>
<term>Glycérophospholipides (métabolisme)</term>
<term>Humains</term>
<term>Interactions hôte-pathogène</term>
<term>Lignée cellulaire</term>
<term>Métabolisme des lipides</term>
<term>Réplication virale</term>
<term>Spectrométrie de masse en tandem</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Arachidonic Acid</term>
<term>Glycerophospholipids</term>
<term>Linoleic Acid</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Acide arachidonique</term>
<term>Acide linoléique</term>
<term>Glycérophospholipides</term>
</keywords>
<keywords scheme="MESH" qualifier="physiologie" xml:lang="fr"><term>Coronavirus humain 229E</term>
</keywords>
<keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Coronavirus 229E, Human</term>
</keywords>
<keywords scheme="MESH" xml:lang="en"><term>Cell Line</term>
<term>Chromatography, Liquid</term>
<term>Host-Pathogen Interactions</term>
<term>Humans</term>
<term>Lipid Metabolism</term>
<term>Tandem Mass Spectrometry</term>
<term>Virus Replication</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr"><term>Chromatographie en phase liquide</term>
<term>Humains</term>
<term>Interactions hôte-pathogène</term>
<term>Lignée cellulaire</term>
<term>Métabolisme des lipides</term>
<term>Réplication virale</term>
<term>Spectrométrie de masse en tandem</term>
</keywords>
</textClass>
</profileDesc>
</teiHeader>
<front><div type="abstract" xml:lang="en"><p>Lipids play numerous indispensable cellular functions and are involved in multiple steps in the replication cycle of viruses. Infections by human-pathogenic coronaviruses result in diverse clinical outcomes, ranging from self-limiting flu-like symptoms to severe pneumonia with extrapulmonary manifestations. Understanding how cellular lipids may modulate the pathogenicity of human-pathogenic coronaviruses remains poor. To this end, we utilized the human coronavirus 229E (HCoV-229E) as a model coronavirus to comprehensively characterize the host cell lipid response upon coronavirus infection with an ultra-high performance liquid chromatography-mass spectrometry (UPLC–MS)-based lipidomics approach. Our results revealed that glycerophospholipids and fatty acids (FAs) were significantly elevated in the HCoV-229E-infected cells and the linoleic acid (LA) to arachidonic acid (AA) metabolism axis was markedly perturbed upon HCoV-229E infection. Interestingly, exogenous supplement of LA or AA in HCoV-229E-infected cells significantly suppressed HCoV-229E virus replication. Importantly, the inhibitory effect of LA and AA on virus replication was also conserved for the highly pathogenic Middle East respiratory syndrome coronavirus (MERS-CoV). Taken together, our study demonstrated that host lipid metabolic remodeling was significantly associated with human-pathogenic coronavirus propagation. Our data further suggested that lipid metabolism regulation would be a common and druggable target for coronavirus infections.</p>
</div>
</front>
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<author><name sortKey="Weselake, R J" uniqKey="Weselake R">R.J. Weselake</name>
</author>
<author><name sortKey="Zou, J" uniqKey="Zou J">J. Zou</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Demetz, E" uniqKey="Demetz E">E. Demetz</name>
</author>
<author><name sortKey="Schroll, A" uniqKey="Schroll A">A. Schroll</name>
</author>
<author><name sortKey="Auer, K" uniqKey="Auer K">K. Auer</name>
</author>
<author><name sortKey="Heim, C" uniqKey="Heim C">C. Heim</name>
</author>
<author><name sortKey="Patsch, J R" uniqKey="Patsch J">J.R. Patsch</name>
</author>
<author><name sortKey="Eller, P" uniqKey="Eller P">P. Eller</name>
</author>
<author><name sortKey="Theurl, M" uniqKey="Theurl M">M. Theurl</name>
</author>
<author><name sortKey="Theurl, I" uniqKey="Theurl I">I. Theurl</name>
</author>
<author><name sortKey="Theurl, M" uniqKey="Theurl M">M. Theurl</name>
</author>
<author><name sortKey="Seifert, M" uniqKey="Seifert M">M. Seifert</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Persichini, T" uniqKey="Persichini T">T. Persichini</name>
</author>
<author><name sortKey="Mastrantonio, R" uniqKey="Mastrantonio R">R. Mastrantonio</name>
</author>
<author><name sortKey="Del Matto, S" uniqKey="Del Matto S">S. Del Matto</name>
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<author><name sortKey="Palomba, L" uniqKey="Palomba L">L. Palomba</name>
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<author><name sortKey="Cantoni, O" uniqKey="Cantoni O">O. Cantoni</name>
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<author><name sortKey="Colasanti, M" uniqKey="Colasanti M">M. Colasanti</name>
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</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Chandrasekharan, J A" uniqKey="Chandrasekharan J">J.A. Chandrasekharan</name>
</author>
<author><name sortKey="Marginean, A" uniqKey="Marginean A">A. Marginean</name>
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<author><name sortKey="Sharma Walia, N" uniqKey="Sharma Walia N">N. Sharma-Walia</name>
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<biblStruct><analytic><author><name sortKey="Muller, C" uniqKey="Muller C">C. Muller</name>
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<author><name sortKey="Karl, N" uniqKey="Karl N">N. Karl</name>
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</analytic>
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<affiliations><list><country><li>République populaire de Chine</li>
</country>
</list>
<tree><noCountry><name sortKey="Chu, Hin" sort="Chu, Hin" uniqKey="Chu H" first="Hin" last="Chu">Hin Chu</name>
<name sortKey="Kao, Richard Yi Tsun" sort="Kao, Richard Yi Tsun" uniqKey="Kao R" first="Richard Yi-Tsun" last="Kao">Richard Yi-Tsun Kao</name>
<name sortKey="Lai, Pok Man" sort="Lai, Pok Man" uniqKey="Lai P" first="Pok-Man" last="Lai">Pok-Man Lai</name>
<name sortKey="Shuai, Huiping" sort="Shuai, Huiping" uniqKey="Shuai H" first="Huiping" last="Shuai">Huiping Shuai</name>
<name sortKey="Sze, Kong Hung" sort="Sze, Kong Hung" uniqKey="Sze K" first="Kong-Hung" last="Sze">Kong-Hung Sze</name>
<name sortKey="Wang, Yixin" sort="Wang, Yixin" uniqKey="Wang Y" first="Yixin" last="Wang">Yixin Wang</name>
<name sortKey="Yan, Bingpeng" sort="Yan, Bingpeng" uniqKey="Yan B" first="Bingpeng" last="Yan">Bingpeng Yan</name>
<name sortKey="Yang, Dong" sort="Yang, Dong" uniqKey="Yang D" first="Dong" last="Yang">Dong Yang</name>
<name sortKey="Yuan, Shuofeng" sort="Yuan, Shuofeng" uniqKey="Yuan S" first="Shuofeng" last="Yuan">Shuofeng Yuan</name>
</noCountry>
<country name="République populaire de Chine"><noRegion><name sortKey="Chan, Jasper Fuk Woo" sort="Chan, Jasper Fuk Woo" uniqKey="Chan J" first="Jasper Fuk-Woo" last="Chan">Jasper Fuk-Woo Chan</name>
</noRegion>
<name sortKey="Chan, Jasper Fuk Woo" sort="Chan, Jasper Fuk Woo" uniqKey="Chan J" first="Jasper Fuk-Woo" last="Chan">Jasper Fuk-Woo Chan</name>
<name sortKey="Chan, Jasper Fuk Woo" sort="Chan, Jasper Fuk Woo" uniqKey="Chan J" first="Jasper Fuk-Woo" last="Chan">Jasper Fuk-Woo Chan</name>
<name sortKey="Yuen, Kwok Yung" sort="Yuen, Kwok Yung" uniqKey="Yuen K" first="Kwok-Yung" last="Yuen">Kwok-Yung Yuen</name>
<name sortKey="Yuen, Kwok Yung" sort="Yuen, Kwok Yung" uniqKey="Yuen K" first="Kwok-Yung" last="Yuen">Kwok-Yung Yuen</name>
<name sortKey="Yuen, Kwok Yung" sort="Yuen, Kwok Yung" uniqKey="Yuen K" first="Kwok-Yung" last="Yuen">Kwok-Yung Yuen</name>
<name sortKey="Yuen, Kwok Yung" sort="Yuen, Kwok Yung" uniqKey="Yuen K" first="Kwok-Yung" last="Yuen">Kwok-Yung Yuen</name>
</country>
</tree>
</affiliations>
</record>
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