Structural and Functional Analysis of Laninamivir and its Octanoate Prodrug Reveals Group Specific Mechanisms for Influenza NA Inhibition
Identifieur interne : 000C10 ( Main/Exploration ); précédent : 000C09; suivant : 000C11Structural and Functional Analysis of Laninamivir and its Octanoate Prodrug Reveals Group Specific Mechanisms for Influenza NA Inhibition
Auteurs : Christopher J. Vavricka [République populaire de Chine] ; Qing Li [République populaire de Chine] ; Yan Wu [République populaire de Chine] ; Jianxun Qi [République populaire de Chine] ; Mingyang Wang [République populaire de Chine] ; Yue Liu [République populaire de Chine] ; Feng Gao [République populaire de Chine] ; Jun Liu [République populaire de Chine] ; Enguang Feng [République populaire de Chine] ; Jianhua He [République populaire de Chine] ; Jinfang Wang [République populaire de Chine] ; Hong Liu [République populaire de Chine] ; Hualiang Jiang [République populaire de Chine] ; George F. Gao [République populaire de Chine]Source :
- PLoS Pathogens [ 1553-7366 ] ; 2011.
Descripteurs français
- KwdFr :
- Antienzymes (), Antienzymes (pharmacologie), Antiviraux (), Antiviraux (pharmacologie), Caprylates (), Caprylates (pharmacologie), Concentration inhibitrice 50, Domaine catalytique (), Domaine catalytique (physiologie), Humains, Oséltamivir (), Oséltamivir (pharmacologie), Promédicaments (), Promédicaments (pharmacologie), Résistance virale aux médicaments (), Sialidase (antagonistes et inhibiteurs), Sous-type H1N1 du virus de la grippe A (), Sous-type H1N1 du virus de la grippe A (enzymologie), Zanamivir (), Zanamivir (analogues et dérivés), Zanamivir (pharmacologie).
- MESH :
- analogues et dérivés : Zanamivir.
- antagonistes et inhibiteurs : Sialidase.
- enzymologie : Sous-type H1N1 du virus de la grippe A.
- pharmacologie : Antienzymes, Antiviraux, Caprylates, Oséltamivir, Promédicaments, Zanamivir.
- physiologie : Domaine catalytique.
- Antienzymes, Antiviraux, Caprylates, Concentration inhibitrice 50, Domaine catalytique, Humains, Oséltamivir, Promédicaments, Résistance virale aux médicaments, Sous-type H1N1 du virus de la grippe A, Zanamivir.
English descriptors
- KwdEn :
- Antiviral Agents (chemistry), Antiviral Agents (pharmacology), Caprylates (chemistry), Caprylates (pharmacology), Catalytic Domain (drug effects), Catalytic Domain (physiology), Drug Resistance, Viral (drug effects), Enzyme Inhibitors (chemistry), Enzyme Inhibitors (pharmacology), Humans, Influenza A Virus, H1N1 Subtype (drug effects), Influenza A Virus, H1N1 Subtype (enzymology), Inhibitory Concentration 50, Neuraminidase (antagonists & inhibitors), Oseltamivir (chemistry), Oseltamivir (pharmacology), Prodrugs (chemistry), Prodrugs (pharmacology), Zanamivir (analogs & derivatives), Zanamivir (chemistry), Zanamivir (pharmacology).
- MESH :
- chemical , analogs & derivatives : Zanamivir.
- chemical , antagonists & inhibitors : Neuraminidase.
- chemical , chemistry : Antiviral Agents, Caprylates, Enzyme Inhibitors, Oseltamivir, Prodrugs, Zanamivir.
- chemical , pharmacology : Antiviral Agents, Caprylates, Enzyme Inhibitors, Oseltamivir, Prodrugs, Zanamivir.
- drug effects : Catalytic Domain, Drug Resistance, Viral, Influenza A Virus, H1N1 Subtype.
- enzymology : Influenza A Virus, H1N1 Subtype.
- physiology : Catalytic Domain.
- Humans, Inhibitory Concentration 50.
Abstract
The 2009 H1N1 influenza pandemic (pH1N1) led to record sales of neuraminidase (NA) inhibitors, which has contributed significantly to the recent increase in oseltamivir-resistant viruses. Therefore, development and careful evaluation of novel NA inhibitors is of great interest. Recently, a highly potent NA inhibitor, laninamivir, has been approved for use in Japan. Laninamivir is effective using a single inhaled dose via its octanoate prodrug (CS-8958) and has been demonstrated to be effective against oseltamivir-resistant NA
Url:
DOI: 10.1371/journal.ppat.1002249
PubMed: 22028647
PubMed Central: 3197600
Affiliations:
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Vavricka</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Li, Qing" sort="Li, Qing" uniqKey="Li Q" first="Qing" last="Li">Qing Li</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:aff id="aff2"><addr-line>School of Life Sciences, University of Science and Technology of China, Hefei, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>School of Life Sciences, University of Science and Technology of China, Hefei</wicri:regionArea><placeName><settlement type="city">Hefei</settlement><region type="province">Anhui</region></placeName></affiliation></author><author><name sortKey="Wu, Yan" sort="Wu, Yan" uniqKey="Wu Y" first="Yan" last="Wu">Yan Wu</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Qi, Jianxun" sort="Qi, Jianxun" uniqKey="Qi J" first="Jianxun" last="Qi">Jianxun Qi</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Wang, Mingyang" sort="Wang, Mingyang" uniqKey="Wang M" first="Mingyang" last="Wang">Mingyang Wang</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:aff id="aff3"><addr-line>Graduate University, Chinese Academy of Sciences, Beijing, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Graduate University, Chinese Academy of Sciences, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Liu, Yue" sort="Liu, Yue" uniqKey="Liu Y" first="Yue" last="Liu">Yue Liu</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Gao, Feng" sort="Gao, Feng" uniqKey="Gao F" first="Feng" last="Gao">Feng Gao</name><affiliation wicri:level="3"><nlm:aff id="aff4"><addr-line>National Laboratory of Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences, Beijing, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>National Laboratory of Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Liu, Jun" sort="Liu, Jun" uniqKey="Liu J" first="Jun" last="Liu">Jun Liu</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Feng, Enguang" sort="Feng, Enguang" uniqKey="Feng E" first="Enguang" last="Feng">Enguang Feng</name><affiliation wicri:level="1"><nlm:aff id="aff5"><addr-line>State Key Laboratory of Drug Research, Shanghai Institute of Materia Medica, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Drug Research, Shanghai Institute of Materia Medica, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai</wicri:regionArea><wicri:noRegion>Shanghai</wicri:noRegion></affiliation></author><author><name sortKey="He, Jianhua" sort="He, Jianhua" uniqKey="He J" first="Jianhua" last="He">Jianhua He</name><affiliation wicri:level="1"><nlm:aff id="aff6"><addr-line>Shanghai Institute of Applied Physics, Chinese Academy of Sciences, Shanghai, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Shanghai Institute of Applied Physics, Chinese Academy of Sciences, Shanghai</wicri:regionArea><wicri:noRegion>Shanghai</wicri:noRegion></affiliation></author><author><name sortKey="Wang, Jinfang" sort="Wang, Jinfang" uniqKey="Wang J" first="Jinfang" last="Wang">Jinfang Wang</name><affiliation wicri:level="1"><nlm:aff id="aff5"><addr-line>State Key Laboratory of Drug Research, Shanghai Institute of Materia Medica, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Drug Research, Shanghai Institute of Materia Medica, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai</wicri:regionArea><wicri:noRegion>Shanghai</wicri:noRegion></affiliation></author><author><name sortKey="Liu, Hong" sort="Liu, Hong" uniqKey="Liu H" first="Hong" last="Liu">Hong Liu</name><affiliation wicri:level="1"><nlm:aff id="aff5"><addr-line>State Key Laboratory of Drug Research, Shanghai Institute of Materia Medica, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Drug Research, Shanghai Institute of Materia Medica, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai</wicri:regionArea><wicri:noRegion>Shanghai</wicri:noRegion></affiliation></author><author><name sortKey="Jiang, Hualiang" sort="Jiang, Hualiang" uniqKey="Jiang H" first="Hualiang" last="Jiang">Hualiang Jiang</name><affiliation wicri:level="1"><nlm:aff id="aff5"><addr-line>State Key Laboratory of Drug Research, Shanghai Institute of Materia Medica, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Drug Research, Shanghai Institute of Materia Medica, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai</wicri:regionArea><wicri:noRegion>Shanghai</wicri:noRegion></affiliation></author><author><name sortKey="Gao, George F" sort="Gao, George F" uniqKey="Gao G" first="George F." last="Gao">George F. Gao</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:aff id="aff2"><addr-line>School of Life Sciences, University of Science and Technology of China, Hefei, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>School of Life Sciences, University of Science and Technology of China, Hefei</wicri:regionArea><placeName><settlement type="city">Hefei</settlement><region type="province">Anhui</region></placeName></affiliation><affiliation wicri:level="3"><nlm:aff id="aff3"><addr-line>Graduate University, Chinese Academy of Sciences, Beijing, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Graduate University, Chinese Academy of Sciences, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:aff id="aff7"><addr-line>Beijing Institutes of Life Science, Chinese Academy of Sciences, Beijing, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Beijing Institutes of Life Science, Chinese Academy of Sciences, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author></analytic><series><title level="j">PLoS Pathogens</title><idno type="ISSN">1553-7366</idno><idno type="eISSN">1553-7374</idno><imprint><date when="2011">2011</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Antiviral Agents (chemistry)</term><term>Antiviral Agents (pharmacology)</term><term>Caprylates (chemistry)</term><term>Caprylates (pharmacology)</term><term>Catalytic Domain (drug effects)</term><term>Catalytic Domain (physiology)</term><term>Drug Resistance, Viral (drug effects)</term><term>Enzyme Inhibitors (chemistry)</term><term>Enzyme Inhibitors (pharmacology)</term><term>Humans</term><term>Influenza A Virus, H1N1 Subtype (drug effects)</term><term>Influenza A Virus, H1N1 Subtype (enzymology)</term><term>Inhibitory Concentration 50</term><term>Neuraminidase (antagonists & inhibitors)</term><term>Oseltamivir (chemistry)</term><term>Oseltamivir (pharmacology)</term><term>Prodrugs (chemistry)</term><term>Prodrugs (pharmacology)</term><term>Zanamivir (analogs & derivatives)</term><term>Zanamivir (chemistry)</term><term>Zanamivir (pharmacology)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Antienzymes ()</term><term>Antienzymes (pharmacologie)</term><term>Antiviraux ()</term><term>Antiviraux (pharmacologie)</term><term>Caprylates ()</term><term>Caprylates (pharmacologie)</term><term>Concentration inhibitrice 50</term><term>Domaine catalytique ()</term><term>Domaine catalytique (physiologie)</term><term>Humains</term><term>Oséltamivir ()</term><term>Oséltamivir (pharmacologie)</term><term>Promédicaments ()</term><term>Promédicaments (pharmacologie)</term><term>Résistance virale aux médicaments ()</term><term>Sialidase (antagonistes et inhibiteurs)</term><term>Sous-type H1N1 du virus de la grippe A ()</term><term>Sous-type H1N1 du virus de la grippe A (enzymologie)</term><term>Zanamivir ()</term><term>Zanamivir (analogues et dérivés)</term><term>Zanamivir (pharmacologie)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="analogs & derivatives" xml:lang="en"><term>Zanamivir</term></keywords><keywords scheme="MESH" type="chemical" qualifier="antagonists & inhibitors" xml:lang="en"><term>Neuraminidase</term></keywords><keywords scheme="MESH" type="chemical" qualifier="chemistry" xml:lang="en"><term>Antiviral Agents</term><term>Caprylates</term><term>Enzyme Inhibitors</term><term>Oseltamivir</term><term>Prodrugs</term><term>Zanamivir</term></keywords><keywords scheme="MESH" type="chemical" qualifier="pharmacology" xml:lang="en"><term>Antiviral Agents</term><term>Caprylates</term><term>Enzyme Inhibitors</term><term>Oseltamivir</term><term>Prodrugs</term><term>Zanamivir</term></keywords><keywords scheme="MESH" qualifier="analogues et dérivés" xml:lang="fr"><term>Zanamivir</term></keywords><keywords scheme="MESH" qualifier="antagonistes et inhibiteurs" xml:lang="fr"><term>Sialidase</term></keywords><keywords scheme="MESH" qualifier="drug effects" xml:lang="en"><term>Catalytic Domain</term><term>Drug Resistance, Viral</term><term>Influenza A Virus, H1N1 Subtype</term></keywords><keywords scheme="MESH" qualifier="enzymologie" xml:lang="fr"><term>Sous-type H1N1 du virus de la grippe A</term></keywords><keywords scheme="MESH" qualifier="enzymology" xml:lang="en"><term>Influenza A Virus, H1N1 Subtype</term></keywords><keywords scheme="MESH" qualifier="pharmacologie" xml:lang="fr"><term>Antienzymes</term><term>Antiviraux</term><term>Caprylates</term><term>Oséltamivir</term><term>Promédicaments</term><term>Zanamivir</term></keywords><keywords scheme="MESH" qualifier="physiologie" xml:lang="fr"><term>Domaine catalytique</term></keywords><keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Catalytic Domain</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Humans</term><term>Inhibitory Concentration 50</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Antienzymes</term><term>Antiviraux</term><term>Caprylates</term><term>Concentration inhibitrice 50</term><term>Domaine catalytique</term><term>Humains</term><term>Oséltamivir</term><term>Promédicaments</term><term>Résistance virale aux médicaments</term><term>Sous-type H1N1 du virus de la grippe A</term><term>Zanamivir</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>The 2009 H1N1 influenza pandemic (pH1N1) led to record sales of neuraminidase (NA) inhibitors, which has contributed significantly to the recent increase in oseltamivir-resistant viruses. Therefore, development and careful evaluation of novel NA inhibitors is of great interest. Recently, a highly potent NA inhibitor, laninamivir, has been approved for use in Japan. Laninamivir is effective using a single inhaled dose via its octanoate prodrug (CS-8958) and has been demonstrated to be effective against oseltamivir-resistant NA <italic>in vitro</italic>. However, effectiveness of laninamivir octanoate prodrug against oseltamivir-resistant influenza infection in adults has not been demonstrated. NA is classified into 2 groups based upon phylogenetic analysis and it is becoming clear that each group has some distinct structural features. Recently, we found that pH1N1 N1 NA (p09N1) is an atypical group 1 NA with some group 2-like features in its active site (lack of a 150-cavity). Furthermore, it has been reported that certain oseltamivir-resistant substitutions in the NA active site are group 1 specific. In order to comprehensively evaluate the effectiveness of laninamivir, we utilized recombinant N5 (typical group 1), p09N1 (atypical group 1) and N2 from the 1957 pandemic H2N2 (p57N2) (typical group 2) to carry out <italic>in vitro</italic> inhibition assays. We found that laninamivir and its octanoate prodrug display group specific preferences to different influenza NAs and provide the structural basis of their specific action based upon their novel complex crystal structures. Our results indicate that laninamivir and zanamivir are more effective against group 1 NA with a 150-cavity than group 2 NA with no 150-cavity. Furthermore, we have found that the laninamivir octanoate prodrug has a unique binding mode in p09N1 that is different from that of group 2 p57N2, but with some similarities to NA-oseltamivir binding, which provides additional insight into group specific differences of oseltamivir binding and resistance.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Dawood, Fs" uniqKey="Dawood F">FS Dawood</name></author><author><name sortKey="Jain, S" uniqKey="Jain S">S Jain</name></author><author><name sortKey="Finelli, L" uniqKey="Finelli L">L Finelli</name></author><author><name sortKey="Shaw, Mw" uniqKey="Shaw M">MW Shaw</name></author><author><name sortKey="Lindstrom, S" uniqKey="Lindstrom S">S Lindstrom</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Wang, Tt" uniqKey="Wang T">TT Wang</name></author><author><name sortKey="Palese, P" uniqKey="Palese P">P 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Vavricka</name></noRegion><name sortKey="Feng, Enguang" sort="Feng, Enguang" uniqKey="Feng E" first="Enguang" last="Feng">Enguang Feng</name><name sortKey="Gao, Feng" sort="Gao, Feng" uniqKey="Gao F" first="Feng" last="Gao">Feng Gao</name><name sortKey="Gao, George F" sort="Gao, George F" uniqKey="Gao G" first="George F." last="Gao">George F. Gao</name><name sortKey="Gao, George F" sort="Gao, George F" uniqKey="Gao G" first="George F." last="Gao">George F. Gao</name><name sortKey="Gao, George F" sort="Gao, George F" uniqKey="Gao G" first="George F." last="Gao">George F. Gao</name><name sortKey="Gao, George F" sort="Gao, George F" uniqKey="Gao G" first="George F." last="Gao">George F. Gao</name><name sortKey="He, Jianhua" sort="He, Jianhua" uniqKey="He J" first="Jianhua" last="He">Jianhua He</name><name sortKey="Jiang, Hualiang" sort="Jiang, Hualiang" uniqKey="Jiang H" first="Hualiang" last="Jiang">Hualiang Jiang</name><name sortKey="Li, Qing" sort="Li, Qing" uniqKey="Li Q" first="Qing" last="Li">Qing Li</name><name sortKey="Li, Qing" sort="Li, Qing" uniqKey="Li Q" first="Qing" last="Li">Qing Li</name><name sortKey="Liu, Hong" sort="Liu, Hong" uniqKey="Liu H" first="Hong" last="Liu">Hong Liu</name><name sortKey="Liu, Jun" sort="Liu, Jun" uniqKey="Liu J" first="Jun" last="Liu">Jun Liu</name><name sortKey="Liu, Yue" sort="Liu, Yue" uniqKey="Liu Y" first="Yue" last="Liu">Yue Liu</name><name sortKey="Qi, Jianxun" sort="Qi, Jianxun" uniqKey="Qi J" first="Jianxun" last="Qi">Jianxun Qi</name><name sortKey="Wang, Jinfang" sort="Wang, Jinfang" uniqKey="Wang J" first="Jinfang" last="Wang">Jinfang Wang</name><name sortKey="Wang, Mingyang" sort="Wang, Mingyang" uniqKey="Wang M" first="Mingyang" last="Wang">Mingyang Wang</name><name sortKey="Wang, Mingyang" sort="Wang, Mingyang" uniqKey="Wang M" first="Mingyang" last="Wang">Mingyang Wang</name><name sortKey="Wu, Yan" sort="Wu, Yan" uniqKey="Wu Y" first="Yan" last="Wu">Yan Wu</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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