Pharmacological mechanisms of the anticancer action of sodium selenite against peritoneal cancer in mice.
Identifieur interne : 000137 ( Main/Exploration ); précédent : 000136; suivant : 000138Pharmacological mechanisms of the anticancer action of sodium selenite against peritoneal cancer in mice.
Auteurs : Ximing Wu [République populaire de Chine] ; Guangshan Zhao [République populaire de Chine] ; Yufeng He [République populaire de Chine] ; Wenping Wang [République populaire de Chine] ; Chung S. Yang [États-Unis] ; Jinsong Zhang [République populaire de Chine]Source :
- Pharmacological research [ 1096-1186 ] ; 2019.
Descripteurs français
- KwdFr :
- Animaux (MeSH), Antinéoplasiques (pharmacologie), Cycle cellulaire (effets des médicaments et des substances chimiques), Espèces réactives de l'oxygène (métabolisme), Lignée cellulaire tumorale (MeSH), Mâle (MeSH), Nanoparticules (administration et posologie), Souris (MeSH), Sélénite de sodium (pharmacologie), Tumeurs du péritoine (traitement médicamenteux).
- MESH :
- administration et posologie : Nanoparticules.
- effets des médicaments et des substances chimiques : Cycle cellulaire.
- métabolisme : Espèces réactives de l'oxygène.
- pharmacologie : Antinéoplasiques, Sélénite de sodium.
- traitement médicamenteux : Tumeurs du péritoine.
- Animaux, Lignée cellulaire tumorale, Mâle, Souris.
English descriptors
- KwdEn :
- MESH :
- chemical , metabolism : Reactive Oxygen Species.
- chemical , pharmacology : Antineoplastic Agents, Sodium Selenite.
- administration & dosage : Nanoparticles.
- drug effects : Cell Cycle.
- drug therapy : Peritoneal Neoplasms.
- Animals, Cell Line, Tumor, Male, Mice.
Abstract
Peritoneal carcinomatosis has an extremely poor overall prognosis and remains one of the greatest oncologic challenges. Prior studies in mice show that sodium selenite administered intraperitoneally is highly effective in inhibiting cancer cells implanted in the peritoneal cavity. However, the pharmacological mechanism remains unclear. The present study revisited the therapeutic effect of selenite and elucidated its mechanism of action. We found that intraperitoneal delivery of selenite to cancer cells in the peritoneal cavity of mice rapidly and robustly killed the cancer cells, with a therapeutic efficacy higher than that of cisplatin. The action of selenite was associated with the following pharmacological mechanisms. 1) Favorable drug distribution: selenite increased selenium levels in the cancer cells by 250-fold, while in normal tissues only by 7-fold. 2) Optimal selenium form: selenite was converted in the cancer cells mainly into selenium nanoparticles (SeNPs), which are more efficient than selenite in producing reactive oxygen species (ROS). 3) Persistent hijacking of two pro-survival systems to generate ROS: selenite did not impair thioredoxin- and glutaredoxin-coupled glutathione systems, which facilitate SeNPs to generate ROS and caused severe organelle injury and apoptotic response in the cancer cells. Overall, these mechanisms tend to maximize the potential of selenite in producing ROS in cancer cells and underlie selenite as a candidate therapeutic agent for peritoneal carcinomatosis.
DOI: 10.1016/j.phrs.2019.104360
PubMed: 31326526
Affiliations:
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Yang</name><affiliation wicri:level="2"><nlm:affiliation>Department of Chemical Biology, Ernest Mario School of Pharmacy, Rutgers, The State University of New Jersey, Piscataway, NJ, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Chemical Biology, Ernest Mario School of Pharmacy, Rutgers, The State University of New Jersey, Piscataway, NJ</wicri:regionArea><placeName><region type="state">New Jersey</region></placeName></affiliation></author><author><name sortKey="Zhang, Jinsong" sort="Zhang, Jinsong" uniqKey="Zhang J" first="Jinsong" last="Zhang">Jinsong Zhang</name><affiliation wicri:level="1"><nlm:affiliation>Laboratory of Redox Biology, School of Tea& Food Science and State Key Laboratory of Tea Plant Biology and Utilization, Anhui Agricultural University, Hefei, Anhui, China. Electronic address: zjs@ahau.edu.cn.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Laboratory of Redox Biology, School of Tea& Food Science and State Key Laboratory of Tea Plant Biology and Utilization, Anhui Agricultural University, Hefei, Anhui</wicri:regionArea><wicri:noRegion>Anhui</wicri:noRegion></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2019">2019</date><idno type="RBID">pubmed:31326526</idno><idno type="pmid">31326526</idno><idno type="doi">10.1016/j.phrs.2019.104360</idno><idno type="wicri:Area/Main/Corpus">000126</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Corpus" wicri:corpus="PubMed">000126</idno><idno type="wicri:Area/Main/Curation">000126</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Curation">000126</idno><idno type="wicri:Area/Main/Exploration">000126</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">Pharmacological mechanisms of the anticancer action of sodium selenite against peritoneal cancer in mice.</title><author><name sortKey="Wu, Ximing" sort="Wu, Ximing" uniqKey="Wu X" first="Ximing" last="Wu">Ximing Wu</name><affiliation wicri:level="1"><nlm:affiliation>Laboratory of Redox Biology, School of Tea& Food Science and State Key Laboratory of Tea Plant Biology and Utilization, Anhui Agricultural University, Hefei, Anhui, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Laboratory of Redox Biology, School of Tea& Food Science and State Key Laboratory of Tea Plant Biology and Utilization, Anhui Agricultural University, Hefei, Anhui</wicri:regionArea><wicri:noRegion>Anhui</wicri:noRegion></affiliation></author><author><name sortKey="Zhao, Guangshan" sort="Zhao, Guangshan" uniqKey="Zhao G" first="Guangshan" last="Zhao">Guangshan Zhao</name><affiliation wicri:level="1"><nlm:affiliation>Laboratory of Redox Biology, School of Tea& Food Science and State Key Laboratory of Tea Plant Biology and Utilization, Anhui Agricultural University, Hefei, Anhui, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Laboratory of Redox Biology, School of Tea& Food Science and State Key Laboratory of Tea Plant Biology and Utilization, Anhui Agricultural University, Hefei, Anhui</wicri:regionArea><wicri:noRegion>Anhui</wicri:noRegion></affiliation></author><author><name sortKey="He, Yufeng" sort="He, Yufeng" uniqKey="He Y" first="Yufeng" last="He">Yufeng He</name><affiliation wicri:level="1"><nlm:affiliation>Laboratory of Redox Biology, School of Tea& Food Science and State Key Laboratory of Tea Plant Biology and Utilization, Anhui Agricultural University, Hefei, Anhui, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Laboratory of Redox Biology, School of Tea& Food Science and State Key Laboratory of Tea Plant Biology and Utilization, Anhui Agricultural University, Hefei, Anhui</wicri:regionArea><wicri:noRegion>Anhui</wicri:noRegion></affiliation></author><author><name sortKey="Wang, Wenping" sort="Wang, Wenping" uniqKey="Wang W" first="Wenping" last="Wang">Wenping Wang</name><affiliation wicri:level="1"><nlm:affiliation>Laboratory of Redox Biology, School of Tea& Food Science and State Key Laboratory of Tea Plant Biology and Utilization, Anhui Agricultural University, Hefei, Anhui, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Laboratory of Redox Biology, School of Tea& Food Science and State Key Laboratory of Tea Plant Biology and Utilization, Anhui Agricultural University, Hefei, Anhui</wicri:regionArea><wicri:noRegion>Anhui</wicri:noRegion></affiliation></author><author><name sortKey="Yang, Chung S" sort="Yang, Chung S" uniqKey="Yang C" first="Chung S" last="Yang">Chung S. Yang</name><affiliation wicri:level="2"><nlm:affiliation>Department of Chemical Biology, Ernest Mario School of Pharmacy, Rutgers, The State University of New Jersey, Piscataway, NJ, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Chemical Biology, Ernest Mario School of Pharmacy, Rutgers, The State University of New Jersey, Piscataway, NJ</wicri:regionArea><placeName><region type="state">New Jersey</region></placeName></affiliation></author><author><name sortKey="Zhang, Jinsong" sort="Zhang, Jinsong" uniqKey="Zhang J" first="Jinsong" last="Zhang">Jinsong Zhang</name><affiliation wicri:level="1"><nlm:affiliation>Laboratory of Redox Biology, School of Tea& Food Science and State Key Laboratory of Tea Plant Biology and Utilization, Anhui Agricultural University, Hefei, Anhui, China. Electronic address: zjs@ahau.edu.cn.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Laboratory of Redox Biology, School of Tea& Food Science and State Key Laboratory of Tea Plant Biology and Utilization, Anhui Agricultural University, Hefei, Anhui</wicri:regionArea><wicri:noRegion>Anhui</wicri:noRegion></affiliation></author></analytic><series><title level="j">Pharmacological research</title><idno type="eISSN">1096-1186</idno><imprint><date when="2019" type="published">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Animals (MeSH)</term><term>Antineoplastic Agents (pharmacology)</term><term>Cell Cycle (drug effects)</term><term>Cell Line, Tumor (MeSH)</term><term>Male (MeSH)</term><term>Mice (MeSH)</term><term>Nanoparticles (administration & dosage)</term><term>Peritoneal Neoplasms (drug therapy)</term><term>Reactive Oxygen Species (metabolism)</term><term>Sodium Selenite (pharmacology)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Animaux (MeSH)</term><term>Antinéoplasiques (pharmacologie)</term><term>Cycle cellulaire (effets des médicaments et des substances chimiques)</term><term>Espèces réactives de l'oxygène (métabolisme)</term><term>Lignée cellulaire tumorale (MeSH)</term><term>Mâle (MeSH)</term><term>Nanoparticules (administration et posologie)</term><term>Souris (MeSH)</term><term>Sélénite de sodium (pharmacologie)</term><term>Tumeurs du péritoine (traitement médicamenteux)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Reactive Oxygen Species</term></keywords><keywords scheme="MESH" type="chemical" qualifier="pharmacology" xml:lang="en"><term>Antineoplastic Agents</term><term>Sodium Selenite</term></keywords><keywords scheme="MESH" qualifier="administration & dosage" xml:lang="en"><term>Nanoparticles</term></keywords><keywords scheme="MESH" qualifier="administration et posologie" xml:lang="fr"><term>Nanoparticules</term></keywords><keywords scheme="MESH" qualifier="drug effects" xml:lang="en"><term>Cell Cycle</term></keywords><keywords scheme="MESH" qualifier="drug therapy" xml:lang="en"><term>Peritoneal Neoplasms</term></keywords><keywords scheme="MESH" qualifier="effets des médicaments et des substances chimiques" xml:lang="fr"><term>Cycle cellulaire</term></keywords><keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Espèces réactives de l'oxygène</term></keywords><keywords scheme="MESH" qualifier="pharmacologie" xml:lang="fr"><term>Antinéoplasiques</term><term>Sélénite de sodium</term></keywords><keywords scheme="MESH" qualifier="traitement médicamenteux" xml:lang="fr"><term>Tumeurs du péritoine</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Animals</term><term>Cell Line, Tumor</term><term>Male</term><term>Mice</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Animaux</term><term>Lignée cellulaire tumorale</term><term>Mâle</term><term>Souris</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Peritoneal carcinomatosis has an extremely poor overall prognosis and remains one of the greatest oncologic challenges. Prior studies in mice show that sodium selenite administered intraperitoneally is highly effective in inhibiting cancer cells implanted in the peritoneal cavity. However, the pharmacological mechanism remains unclear. The present study revisited the therapeutic effect of selenite and elucidated its mechanism of action. We found that intraperitoneal delivery of selenite to cancer cells in the peritoneal cavity of mice rapidly and robustly killed the cancer cells, with a therapeutic efficacy higher than that of cisplatin. The action of selenite was associated with the following pharmacological mechanisms. 1) Favorable drug distribution: selenite increased selenium levels in the cancer cells by 250-fold, while in normal tissues only by 7-fold. 2) Optimal selenium form: selenite was converted in the cancer cells mainly into selenium nanoparticles (SeNPs), which are more efficient than selenite in producing reactive oxygen species (ROS). 3) Persistent hijacking of two pro-survival systems to generate ROS: selenite did not impair thioredoxin- and glutaredoxin-coupled glutathione systems, which facilitate SeNPs to generate ROS and caused severe organelle injury and apoptotic response in the cancer cells. Overall, these mechanisms tend to maximize the potential of selenite in producing ROS in cancer cells and underlie selenite as a candidate therapeutic agent for peritoneal carcinomatosis.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">31326526</PMID><DateCompleted><Year>2020</Year><Month>06</Month><Day>17</Day></DateCompleted><DateRevised><Year>2020</Year><Month>06</Month><Day>17</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1096-1186</ISSN><JournalIssue CitedMedium="Internet"><Volume>147</Volume><PubDate><Year>2019</Year><Month>09</Month></PubDate></JournalIssue><Title>Pharmacological research</Title><ISOAbbreviation>Pharmacol Res</ISOAbbreviation></Journal><ArticleTitle>Pharmacological mechanisms of the anticancer action of sodium selenite against peritoneal cancer in mice.</ArticleTitle><Pagination><MedlinePgn>104360</MedlinePgn></Pagination><ELocationID EIdType="pii" ValidYN="Y">S1043-6618(19)30556-0</ELocationID><ELocationID EIdType="doi" ValidYN="Y">10.1016/j.phrs.2019.104360</ELocationID><Abstract><AbstractText>Peritoneal carcinomatosis has an extremely poor overall prognosis and remains one of the greatest oncologic challenges. Prior studies in mice show that sodium selenite administered intraperitoneally is highly effective in inhibiting cancer cells implanted in the peritoneal cavity. However, the pharmacological mechanism remains unclear. The present study revisited the therapeutic effect of selenite and elucidated its mechanism of action. We found that intraperitoneal delivery of selenite to cancer cells in the peritoneal cavity of mice rapidly and robustly killed the cancer cells, with a therapeutic efficacy higher than that of cisplatin. The action of selenite was associated with the following pharmacological mechanisms. 1) Favorable drug distribution: selenite increased selenium levels in the cancer cells by 250-fold, while in normal tissues only by 7-fold. 2) Optimal selenium form: selenite was converted in the cancer cells mainly into selenium nanoparticles (SeNPs), which are more efficient than selenite in producing reactive oxygen species (ROS). 3) Persistent hijacking of two pro-survival systems to generate ROS: selenite did not impair thioredoxin- and glutaredoxin-coupled glutathione systems, which facilitate SeNPs to generate ROS and caused severe organelle injury and apoptotic response in the cancer cells. Overall, these mechanisms tend to maximize the potential of selenite in producing ROS in cancer cells and underlie selenite as a candidate therapeutic agent for peritoneal carcinomatosis.</AbstractText><CopyrightInformation>Copyright © 2019 Elsevier Ltd. All rights reserved.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Wu</LastName><ForeName>Ximing</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>Laboratory of Redox Biology, School of Tea& Food Science and State Key Laboratory of Tea Plant Biology and Utilization, Anhui Agricultural University, Hefei, Anhui, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhao</LastName><ForeName>Guangshan</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>Laboratory of Redox Biology, School of Tea& Food Science and State Key Laboratory of Tea Plant Biology and Utilization, Anhui Agricultural University, Hefei, Anhui, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>He</LastName><ForeName>Yufeng</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>Laboratory of Redox Biology, School of Tea& Food Science and State Key Laboratory of Tea Plant Biology and Utilization, Anhui Agricultural University, Hefei, Anhui, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Wenping</ForeName><Initials>W</Initials><AffiliationInfo><Affiliation>Laboratory of Redox Biology, School of Tea& Food Science and State Key Laboratory of Tea Plant Biology and Utilization, Anhui Agricultural University, Hefei, Anhui, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Yang</LastName><ForeName>Chung S</ForeName><Initials>CS</Initials><AffiliationInfo><Affiliation>Department of Chemical Biology, Ernest Mario School of Pharmacy, Rutgers, The State University of New Jersey, Piscataway, NJ, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhang</LastName><ForeName>Jinsong</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Laboratory of Redox Biology, School of Tea& Food Science and State Key Laboratory of Tea Plant Biology and Utilization, Anhui Agricultural University, Hefei, Anhui, China. Electronic address: zjs@ahau.edu.cn.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2019</Year><Month>07</Month><Day>18</Day></ArticleDate></Article><MedlineJournalInfo><Country>Netherlands</Country><MedlineTA>Pharmacol Res</MedlineTA><NlmUniqueID>8907422</NlmUniqueID><ISSNLinking>1043-6618</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D000970">Antineoplastic Agents</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D017382">Reactive Oxygen Species</NameOfSubstance></Chemical><Chemical><RegistryNumber>HIW548RQ3W</RegistryNumber><NameOfSubstance UI="D018038">Sodium Selenite</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D000818" MajorTopicYN="N">Animals</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D000970" MajorTopicYN="N">Antineoplastic Agents</DescriptorName><QualifierName UI="Q000494" MajorTopicYN="Y">pharmacology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D002453" MajorTopicYN="N">Cell Cycle</DescriptorName><QualifierName UI="Q000187" MajorTopicYN="N">drug effects</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D045744" MajorTopicYN="N">Cell Line, Tumor</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D008297" MajorTopicYN="N">Male</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D051379" MajorTopicYN="N">Mice</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D053758" MajorTopicYN="N">Nanoparticles</DescriptorName><QualifierName UI="Q000008" MajorTopicYN="Y">administration & dosage</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D010534" MajorTopicYN="N">Peritoneal Neoplasms</DescriptorName><QualifierName UI="Q000188" MajorTopicYN="Y">drug therapy</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D017382" MajorTopicYN="N">Reactive Oxygen Species</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D018038" MajorTopicYN="N">Sodium Selenite</DescriptorName><QualifierName UI="Q000494" MajorTopicYN="Y">pharmacology</QualifierName></MeshHeading></MeshHeadingList><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="Y">Peritoneal carcinomatosis</Keyword><Keyword MajorTopicYN="Y">Reactive oxygen species</Keyword><Keyword MajorTopicYN="Y">Selenium nanoparticles</Keyword><Keyword MajorTopicYN="Y">Sodium selenite</Keyword><Keyword MajorTopicYN="Y">Thioredoxin and glutaredoxin-coupled glutathione systems</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2019</Year><Month>04</Month><Day>26</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2019</Year><Month>07</Month><Day>15</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2019</Year><Month>07</Month><Day>17</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2019</Year><Month>7</Month><Day>22</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>6</Month><Day>18</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2019</Year><Month>7</Month><Day>22</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">31326526</ArticleId><ArticleId IdType="pii">S1043-6618(19)30556-0</ArticleId><ArticleId IdType="doi">10.1016/j.phrs.2019.104360</ArticleId></ArticleIdList></PubmedData></pubmed><affiliations><list><country><li>République populaire de Chine</li><li>États-Unis</li></country><region><li>New Jersey</li></region></list><tree><country name="République populaire de Chine"><noRegion><name sortKey="Wu, Ximing" sort="Wu, Ximing" uniqKey="Wu X" first="Ximing" last="Wu">Ximing Wu</name></noRegion><name sortKey="He, Yufeng" sort="He, Yufeng" uniqKey="He Y" first="Yufeng" last="He">Yufeng He</name><name sortKey="Wang, Wenping" sort="Wang, Wenping" uniqKey="Wang W" first="Wenping" last="Wang">Wenping Wang</name><name sortKey="Zhang, Jinsong" sort="Zhang, Jinsong" uniqKey="Zhang J" first="Jinsong" last="Zhang">Jinsong Zhang</name><name sortKey="Zhao, Guangshan" sort="Zhao, Guangshan" uniqKey="Zhao G" first="Guangshan" last="Zhao">Guangshan Zhao</name></country><country name="États-Unis"><region name="New Jersey"><name sortKey="Yang, Chung S" sort="Yang, Chung S" uniqKey="Yang C" first="Chung S" last="Yang">Chung S. 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