Targeting the Endocytic Pathway and Autophagy Process as a Novel Therapeutic Strategy in COVID-19
Identifieur interne : 000020 ( Pmc/Checkpoint ); précédent : 000019; suivant : 000021Targeting the Endocytic Pathway and Autophagy Process as a Novel Therapeutic Strategy in COVID-19
Auteurs : Naidi Yang [République populaire de Chine] ; Han-Ming Shen [République populaire de Chine]Source :
- International Journal of Biological Sciences [ 1449-2288 ] ; 2020.
Abstract
Coronaviruses (CoVs) are a group of enveloped, single-stranded positive genomic RNA viruses and some of them are known to cause severe respiratory diseases in human, including Severe Acute Respiratory Syndrome (SARS), Middle East Respiratory Syndrome (MERS) and the ongoing coronavirus disease-19 (COVID-19). One key element in viral infection is the process of viral entry into the host cells. In the last two decades, there is increasing understanding on the importance of the endocytic pathway and the autophagy process in viral entry and replication. As a result, the endocytic pathway including endosome and lysosome has become important targets for development of therapeutic strategies in combating diseases caused by CoVs. In this mini-review, we will focus on the importance of the endocytic pathway as well as the autophagy process in viral infection of several pathogenic CoVs inclusive of SARS-CoV, MERS-CoV and the new CoV named as severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), and discuss the development of therapeutic agents by targeting these processes. Such knowledge will provide important clues for control of the ongoing epidemic of SARS-CoV-2 infection and treatment of COVID-19.
Url:
DOI: 10.7150/ijbs.45498
PubMed: 32226290
PubMed Central: 7098027
Affiliations:
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PMC:7098027Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Targeting the Endocytic Pathway and Autophagy Process as a Novel Therapeutic Strategy in COVID-19</title><author><name sortKey="Yang, Naidi" sort="Yang, Naidi" uniqKey="Yang N" first="Naidi" last="Yang">Naidi Yang</name><affiliation wicri:level="1"><nlm:aff id="A1">Key Laboratory of Flexible Electronics (KLOFE) & Institute of Advanced Materials (IAM), Nanjing Tech University (NanjingTech), 30 South Puzhu Road, Nanjing, Jiangsu Province 211800, China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Flexible Electronics (KLOFE) & Institute of Advanced Materials (IAM), Nanjing Tech University (NanjingTech), 30 South Puzhu Road, Nanjing, Jiangsu Province 211800</wicri:regionArea><wicri:noRegion>Jiangsu Province 211800</wicri:noRegion></affiliation></author><author><name sortKey="Shen, Han Ming" sort="Shen, Han Ming" uniqKey="Shen H" first="Han-Ming" last="Shen">Han-Ming Shen</name><affiliation wicri:level="1"><nlm:aff id="A2">Faculty of Health Sciences, University of Macau, Macau SAR, China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Faculty of Health Sciences, University of Macau, Macau SAR</wicri:regionArea><wicri:noRegion>Macau SAR</wicri:noRegion></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">32226290</idno><idno type="pmc">7098027</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7098027</idno><idno type="RBID">PMC:7098027</idno><idno type="doi">10.7150/ijbs.45498</idno><date when="2020">2020</date><idno type="wicri:Area/Pmc/Corpus">001349</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">001349</idno><idno type="wicri:Area/Pmc/Curation">001349</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">001349</idno><idno type="wicri:Area/Pmc/Checkpoint">000020</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Checkpoint">000020</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Targeting the Endocytic Pathway and Autophagy Process as a Novel Therapeutic Strategy in COVID-19</title><author><name sortKey="Yang, Naidi" sort="Yang, Naidi" uniqKey="Yang N" first="Naidi" last="Yang">Naidi Yang</name><affiliation wicri:level="1"><nlm:aff id="A1">Key Laboratory of Flexible Electronics (KLOFE) & Institute of Advanced Materials (IAM), Nanjing Tech University (NanjingTech), 30 South Puzhu Road, Nanjing, Jiangsu Province 211800, China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Flexible Electronics (KLOFE) & Institute of Advanced Materials (IAM), Nanjing Tech University (NanjingTech), 30 South Puzhu Road, Nanjing, Jiangsu Province 211800</wicri:regionArea><wicri:noRegion>Jiangsu Province 211800</wicri:noRegion></affiliation></author><author><name sortKey="Shen, Han Ming" sort="Shen, Han Ming" uniqKey="Shen H" first="Han-Ming" last="Shen">Han-Ming Shen</name><affiliation wicri:level="1"><nlm:aff id="A2">Faculty of Health Sciences, University of Macau, Macau SAR, China</nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Faculty of Health Sciences, University of Macau, Macau SAR</wicri:regionArea><wicri:noRegion>Macau SAR</wicri:noRegion></affiliation></author></analytic><series><title level="j">International Journal of Biological Sciences</title><idno type="eISSN">1449-2288</idno><imprint><date when="2020">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Coronaviruses (CoVs) are a group of enveloped, single-stranded positive genomic RNA viruses and some of them are known to cause severe respiratory diseases in human, including Severe Acute Respiratory Syndrome (SARS), Middle East Respiratory Syndrome (MERS) and the ongoing coronavirus disease-19 (COVID-19). One key element in viral infection is the process of viral entry into the host cells. In the last two decades, there is increasing understanding on the importance of the endocytic pathway and the autophagy process in viral entry and replication. As a result, the endocytic pathway including endosome and lysosome has become important targets for development of therapeutic strategies in combating diseases caused by CoVs. In this mini-review, we will focus on the importance of the endocytic pathway as well as the autophagy process in viral infection of several pathogenic CoVs inclusive of SARS-CoV, MERS-CoV and the new CoV named as severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), and discuss the development of therapeutic agents by targeting these processes. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Int J Biol Sci</journal-id><journal-id journal-id-type="iso-abbrev">Int. J. Biol. Sci</journal-id><journal-id journal-id-type="publisher-id">ijbs</journal-id><journal-title-group><journal-title>International Journal of Biological Sciences</journal-title></journal-title-group><issn pub-type="epub">1449-2288</issn><publisher><publisher-name>Ivyspring International Publisher</publisher-name><publisher-loc>Sydney</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">32226290</article-id><article-id pub-id-type="pmc">7098027</article-id><article-id pub-id-type="doi">10.7150/ijbs.45498</article-id><article-id pub-id-type="publisher-id">ijbsv16p1724</article-id><article-categories><subj-group subj-group-type="heading"><subject>Review</subject></subj-group></article-categories><title-group><article-title>Targeting the Endocytic Pathway and Autophagy Process as a Novel Therapeutic Strategy in COVID-19</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Yang</surname><given-names>Naidi</given-names></name><xref ref-type="aff" rid="A1">1</xref></contrib><contrib contrib-type="author"><name><surname>Shen</surname><given-names>Han-Ming</given-names></name><xref ref-type="aff" rid="A2">2</xref><xref ref-type="corresp" rid="FNA_envelop">✉</xref></contrib></contrib-group><aff id="A1"><label>1</label>Key Laboratory of Flexible Electronics (KLOFE) & Institute of Advanced Materials (IAM), Nanjing Tech University (NanjingTech), 30 South Puzhu Road, Nanjing, Jiangsu Province 211800, China</aff><aff id="A2"><label>2</label>Faculty of Health Sciences, University of Macau, Macau SAR, China</aff><author-notes><corresp id="FNA_envelop">✉ Corresponding authors: Naidi Yang: <email>iamndyang@njtech.edu.cn</email> or Han-Ming Shen: <email>hmshen@um.edu.mo</email></corresp><fn fn-type="COI-statement"><p>Competing Interests: The authors have declared that no competing interest exists.</p></fn></author-notes><pub-date pub-type="collection"><year>2020</year></pub-date><pub-date pub-type="epub"><day>15</day><month>3</month><year>2020</year></pub-date><volume>16</volume><issue>10</issue><fpage>1724</fpage><lpage>1731</lpage><history><date date-type="received"><day>1</day><month>3</month><year>2020</year></date><date date-type="accepted"><day>3</day><month>3</month><year>2020</year></date></history><permissions><copyright-statement>© The author(s)</copyright-statement><copyright-year>2020</copyright-year><license license-type="open-access"><license-p>This is an open access article distributed under the terms of the Creative Commons Attribution License (<ext-link ext-link-type="uri" xlink:href="https://creativecommons.org/licenses/by/4.0/">https://creativecommons.org/licenses/by/4.0/</ext-link>). See <ext-link ext-link-type="uri" xlink:href="http://ivyspring.com/terms">http://ivyspring.com/terms</ext-link> for full terms and conditions.</license-p></license></permissions><abstract><p>Coronaviruses (CoVs) are a group of enveloped, single-stranded positive genomic RNA viruses and some of them are known to cause severe respiratory diseases in human, including Severe Acute Respiratory Syndrome (SARS), Middle East Respiratory Syndrome (MERS) and the ongoing coronavirus disease-19 (COVID-19). One key element in viral infection is the process of viral entry into the host cells. In the last two decades, there is increasing understanding on the importance of the endocytic pathway and the autophagy process in viral entry and replication. As a result, the endocytic pathway including endosome and lysosome has become important targets for development of therapeutic strategies in combating diseases caused by CoVs. In this mini-review, we will focus on the importance of the endocytic pathway as well as the autophagy process in viral infection of several pathogenic CoVs inclusive of SARS-CoV, MERS-CoV and the new CoV named as severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), and discuss the development of therapeutic agents by targeting these processes. Such knowledge will provide important clues for control of the ongoing epidemic of SARS-CoV-2 infection and treatment of COVID-19.</p></abstract><kwd-group><kwd>Coronaviruses</kwd><kwd>endocytic pathway</kwd><kwd>autophagy</kwd><kwd>SARS-CoV-2</kwd><kwd>COVID-19</kwd></kwd-group></article-meta></front><floats-group><fig id="F1" position="float"><label>Figure 1</label><caption><p><bold> Involvement of the endocytic pathway and autophagy in the entry and replication of CoVs in host cells.</bold> Entry of CoVs into the host cells is mainly mediated by the endocytic pathway, meanwhile the autophagy has also been implicated in the viral replication in the cells, a process partly related to the formation of DMV in the host cells. As a result, several groups of inhibitors including the lysosomotropic agents such as CQ and inhibitors for clathrin-mediated endocytosis such as chlorpromazine have been proposed to have therapeutic efficacy against CoVs-induced diseases including COVID-19.</p></caption><graphic xlink:href="ijbsv16p1724g001"></graphic></fig><table-wrap id="T1" position="float"><label>Table 1</label><caption><p>Implication of autophagy in the infection of CoVs</p></caption><table frame="hsides" rules="groups"><thead valign="top"><tr><th rowspan="1" colspan="1">Type of Coronavirus tested</th><th rowspan="1" colspan="1">Autophagy machinery tested</th><th rowspan="1" colspan="1">Infected Cells/Organs</th><th rowspan="1" colspan="1">Main findings</th><th rowspan="1" colspan="1">Refs</th></tr></thead><tbody valign="top"><tr><td rowspan="1" colspan="1"><bold>Mousehepatitis virus (MHV)</bold></td><td rowspan="1" colspan="1">LC3<break></break>ATG12</td><td rowspan="1" colspan="1">DBT cells<break></break>Mouse embryonic stem cell</td><td rowspan="1" colspan="1">Autophagy machinery are required for MHV replication</td><td rowspan="1" colspan="1"><xref rid="B24" ref-type="bibr">24</xref></td></tr><tr><td rowspan="1" colspan="1"><bold>SARS-CoV</bold></td><td rowspan="1" colspan="1">Endogenous LC3</td><td rowspan="1" colspan="1">Vero E6 cells</td><td rowspan="1" colspan="1">Viral replication-transcription complexes (RTCs) are co-localizing with endogenous LC3</td><td rowspan="1" colspan="1"><xref rid="B25" ref-type="bibr">25</xref></td></tr><tr><td rowspan="1" colspan="1"><bold>SARS-CoV</bold></td><td rowspan="1" colspan="1">Both Endogenous LC3 and GFP-LC3</td><td rowspan="1" colspan="1">Vero E6 cells</td><td rowspan="1" colspan="1">No evidence are observed for colocalization of LC3 or GFP-LC3 with the SARS-CoV RTCs</td><td rowspan="1" colspan="1"><xref rid="B27" ref-type="bibr">27</xref></td></tr><tr><td rowspan="1" colspan="1"><bold>Mousehepatitis virus (MHV)</bold></td><td rowspan="1" colspan="1">ATG5</td><td rowspan="1" colspan="1">Mouse embryonic fibroblasts (MEFs)</td><td rowspan="1" colspan="1">Deletion of ATG5 does not affect MHV replication</td><td rowspan="1" colspan="1"><xref rid="B28" ref-type="bibr">28</xref></td></tr><tr><td rowspan="1" colspan="1"><bold>Mouse hepatitis virus (MHV)</bold></td><td rowspan="1" colspan="1">ATG7</td><td rowspan="1" colspan="1">Mouse embryonic fibroblasts (MEFs)</td><td rowspan="1" colspan="1">Deletion of ATG7 does not affect MHV replication</td><td rowspan="1" colspan="1"><xref rid="B29" ref-type="bibr">29</xref></td></tr><tr><td rowspan="1" colspan="1"><bold>Bronchitis virus (IBV)</bold></td><td rowspan="1" colspan="1">ATG5<break></break>LC3</td><td rowspan="1" colspan="1">CHO cell line<break></break>MEFs</td><td rowspan="1" colspan="1">Coronavirus replicase nsp6 protein induces autophagy</td><td rowspan="1" colspan="1"><xref rid="B26" ref-type="bibr">26</xref></td></tr><tr><td rowspan="1" colspan="1"><bold>SARS-CoV</bold></td><td rowspan="1" colspan="1">ATG5</td><td rowspan="1" colspan="1">Mouse embryonic fibroblasts (MEFs)</td><td rowspan="1" colspan="1">SARS-CoV replication is not affected in ATG5 KO MEFs</td><td rowspan="1" colspan="1"><xref rid="B30" ref-type="bibr">30</xref></td></tr><tr><td rowspan="1" colspan="1"><bold>Overexpression of membrane- associated papain-like protease PLP2 (PLP2-TM) of SARS-CoV and MERS-CoV</bold></td><td rowspan="1" colspan="1">LC3<break></break>Beclin1</td><td rowspan="1" colspan="1">HEK293T, HeLa and MCF-7 cells</td><td rowspan="1" colspan="1">Overexpression of PLP2-TM blocks autophagosomes-lysosomes fusion<break></break>Beclin1 KD partially decreases coronavirus replication</td><td rowspan="1" colspan="1"><xref rid="B31" ref-type="bibr">31</xref></td></tr><tr><td rowspan="1" colspan="1"><bold>MERS-CoV</bold></td><td rowspan="1" colspan="1">Beclin1</td><td rowspan="1" colspan="1">Vero B4</td><td rowspan="1" colspan="1">MERS-CoV) blocks the fusion of autophagosomes and lysosomes<break></break>Enhanced autophagy reduces the replication of MERS-CoV</td><td rowspan="1" colspan="1"><xref rid="B32" ref-type="bibr">32</xref></td></tr></tbody></table></table-wrap><table-wrap id="T2" position="float"><label>Table 2</label><caption><p>Involvement of the endocytic pathway and the respective inhibitors in CoV infection</p></caption><table frame="hsides" rules="groups"><thead valign="top"><tr><th rowspan="1" colspan="1">Virus and cells tested</th><th rowspan="1" colspan="1">Part of endocytic pathway studied</th><th rowspan="1" colspan="1">Main findings</th><th rowspan="1" colspan="1">Effective inhibitors tested</th><th rowspan="1" colspan="1">Refs</th></tr></thead><tbody valign="top"><tr><td rowspan="1" colspan="1">MHV/ Mouse L cells, Sac2 cells, and DBT cells</td><td rowspan="1" colspan="1">Late endosome</td><td rowspan="1" colspan="1">MHV replication machinery co-localizes with late endosomal membranes</td><td rowspan="1" colspan="1">NA</td><td rowspan="1" colspan="1"><xref rid="B44" ref-type="bibr">44</xref></td></tr><tr><td rowspan="1" colspan="1">SARS-CoV/Vero E6 cells</td><td rowspan="1" colspan="1">S protein-mediated entry</td><td rowspan="1" colspan="1">SARS-CoV entry requires acidification of endosomes</td><td rowspan="1" colspan="1">Balfilomycin A1, CQ, NH4Cl</td><td rowspan="1" colspan="1"><xref rid="B45" ref-type="bibr">45</xref></td></tr><tr><td rowspan="1" colspan="1">SARS-CoV S glycoprotein/Vero cells</td><td rowspan="1" colspan="1">S-protein mediated entry</td><td rowspan="1" colspan="1">S-protein mediated entry is pH-dependent</td><td rowspan="1" colspan="1">Bafilomycin A1, NH4Cl</td><td rowspan="1" colspan="1"><xref rid="B46" ref-type="bibr">46</xref></td></tr><tr><td rowspan="1" colspan="1">SARS-CoV /Vero E6 cells</td><td rowspan="1" colspan="1">Endo-lysosomal pH/cysteine protease</td><td rowspan="1" colspan="1">SARS-CoV entry requires acidification of endosomes</td><td rowspan="1" colspan="1">CQ, NH4Cl</td><td rowspan="1" colspan="1"><xref rid="B47" ref-type="bibr">47</xref></td></tr><tr><td rowspan="1" colspan="1">SARS-CoV/Vero cells, 293T cells</td><td rowspan="1" colspan="1">Endo-lysosomal cysteine protease Cathepsin L</td><td rowspan="1" colspan="1">Cathepsin L is required for infection of cells with ACE2 expression</td><td rowspan="1" colspan="1">E64d, Z-FY-DMK</td><td rowspan="1" colspan="1"><xref rid="B48" ref-type="bibr">48</xref></td></tr><tr><td rowspan="1" colspan="1">MHV/Murine fibroblast L2 and 17CL-1 cells</td><td rowspan="1" colspan="1">Endo-lysosomal cysteine protease Cathepsins</td><td rowspan="1" colspan="1">Endosomal proteolysis by cathepsins are required for viral entry</td><td rowspan="1" colspan="1">NH4Cl, CQ, Bafilomycin A1</td><td rowspan="1" colspan="1"><xref rid="B49" ref-type="bibr">49</xref></td></tr><tr><td rowspan="1" colspan="1">MHV/ 17Cl-1 cells, LR-7 cells and DBT cells</td><td rowspan="1" colspan="1">Clathrin-dependent endocytosis</td><td rowspan="1" colspan="1">Infection by MHV is sensitive to lysosomotropic agents and inhibitors of endocytosis</td><td rowspan="1" colspan="1">Chlorpromazine, Bafilomycin A1, Concanamycin A, NH4Cl, Monensin</td><td rowspan="1" colspan="1"><xref rid="B50" ref-type="bibr">50</xref></td></tr><tr><td rowspan="1" colspan="1">SARS-CoV/HepG2 cells</td><td rowspan="1" colspan="1">Clathrin-dependent endocytosis</td><td rowspan="1" colspan="1">Virus entry is mediated by clathrin-dependent endocytosis</td><td rowspan="1" colspan="1">Chlorpromazine, MβCD</td><td rowspan="1" colspan="1"><xref rid="B39" ref-type="bibr">39</xref></td></tr><tr><td rowspan="1" colspan="1">SARS-CoV/Vero cells</td><td rowspan="1" colspan="1">Late endosome</td><td rowspan="1" colspan="1">Amiodarone inhibits late endosome to suppress SARS-CoV infection</td><td rowspan="1" colspan="1">Amiodarone</td><td rowspan="1" colspan="1"><xref rid="B51" ref-type="bibr">51</xref></td></tr><tr><td rowspan="1" colspan="1">SARS-CoV/HEK293E cells</td><td rowspan="1" colspan="1">Clathrin- and caveolae-mediated endocytic pathway</td><td rowspan="1" colspan="1">Virus entry is mediated by a clathrin- and caveolae-independent endocytic pathway</td><td rowspan="1" colspan="1">NH4Cl, CQ, Bafilomycin A1</td><td rowspan="1" colspan="1"><xref rid="B38" ref-type="bibr">38</xref></td></tr><tr><td rowspan="1" colspan="1">MHV/mouse astrocytoma DHT cells</td><td rowspan="1" colspan="1">Clathrin-or Caveolin-mediated endocytosis</td><td rowspan="1" colspan="1">MHV entry is via clathrin- but not Caveolin-dependent endocytosis</td><td rowspan="1" colspan="1">Chlorpromazine</td><td rowspan="1" colspan="1"><xref rid="B52" ref-type="bibr">52</xref></td></tr><tr><td rowspan="1" colspan="1">MHV and MERS-CoV/ LR7 cells, HEK293T and Vero cells</td><td rowspan="1" colspan="1">Clathrin-mediated endocytosis</td><td rowspan="1" colspan="1">Entry of MHV is mediated by lysosomal proteases, while entry of MERS-CoV is mediated by furin</td><td rowspan="1" colspan="1">NH4Cl, CQ, Bafilomycin A1, Chlorpromazine, Monensin</td><td rowspan="1" colspan="1"><xref rid="B53" ref-type="bibr">53</xref></td></tr><tr><td rowspan="1" colspan="1">MHV and MERS-CoV/ LR7 cells, HEK293T and Vero cells</td><td rowspan="1" colspan="1">Clathrin-mediated endocytosis</td><td rowspan="1" colspan="1">Cardiotonic steroids ouabain and bufalin inhibit infection of cells with MHV and MERS-CoV</td><td rowspan="1" colspan="1">Ouabain, Bufalin</td><td rowspan="1" colspan="1"><xref rid="B54" ref-type="bibr">54</xref></td></tr><tr><td rowspan="1" colspan="1">MERS-CoV, SARS-CoV/HEK293T, A549, HeLa, etc</td><td rowspan="1" colspan="1">Late endosome-lysosome</td><td rowspan="1" colspan="1">Teicoplanin and derivatives inhibit Cathepsin L and block viral entry</td><td rowspan="1" colspan="1">Teicoplanin and derivatives</td><td rowspan="1" colspan="1"><xref rid="B55" ref-type="bibr">55</xref></td></tr><tr><td rowspan="1" colspan="1">MERS-CoV, SARS-CoV/Vero81, Huh7, and Calu3 cells</td><td rowspan="1" colspan="1">Endosomal proteases</td><td rowspan="1" colspan="1">Cathepsin L-mediated S protein cleavage expands virus tropism</td><td rowspan="1" colspan="1">E64d, PCI (a proprotein convertase inhibitor, dec-RVKR-cmk)</td><td rowspan="1" colspan="1"><xref rid="B56" ref-type="bibr">56</xref></td></tr><tr><td rowspan="1" colspan="1">SARS-CoV 2/ Vero E6</td><td rowspan="1" colspan="1">Endosomal pH</td><td rowspan="1" colspan="1">SARS-CoV-2 entry requires acidification of endosomes</td><td rowspan="1" colspan="1">CQ</td><td rowspan="1" colspan="1"><xref rid="B43" ref-type="bibr">43</xref></td></tr></tbody></table></table-wrap></floats-group></pmc><affiliations><list><country><li>République populaire de Chine</li></country></list><tree><country name="République populaire de Chine"><noRegion><name sortKey="Yang, Naidi" sort="Yang, Naidi" uniqKey="Yang N" first="Naidi" last="Yang">Naidi Yang</name></noRegion><name sortKey="Shen, Han Ming" sort="Shen, Han Ming" uniqKey="Shen H" first="Han-Ming" last="Shen">Han-Ming Shen</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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