The mTOR inhibitor manassantin B reveals a crucial role of mTORC2 signaling in Epstein-Barr virus reactivation.
Identifieur interne : 000028 ( Main/Exploration ); précédent : 000027; suivant : 000029The mTOR inhibitor manassantin B reveals a crucial role of mTORC2 signaling in Epstein-Barr virus reactivation.
Auteurs : Qian Wang [République populaire de Chine] ; Nannan Zhu [République populaire de Chine] ; Jiayuan Hu [République populaire de Chine] ; Yan Wang [République populaire de Chine] ; Jun Xu [République populaire de Chine] ; Qiong Gu [République populaire de Chine] ; Paul M. Lieberman [États-Unis] ; Yan Yuan [États-Unis]Source :
- The Journal of biological chemistry [ 1083-351X ] ; 2020.
Abstract
Lytic replication of Epstein-Barr virus (EBV) is not only essential for its cell-to-cell spread and host-to-host transmission, but it also contributes to EBV-induced oncogenesis. Thus, blocking EBV lytic replication could be a strategy for managing EBV-associated diseases. Previously, we identified a series of natural lignans isolated from the roots of Saururus chinensis (Asian lizard's tail) that efficiently block EBV lytic replication and virion production with low cytotoxicity. In this study, we attempted to elucidate the molecular mechanism by which these lignans inhibit EBV lytic replication. We found that a representative compound, CSC27 (manassantin B), inhibits EBV lytic replication by suppressing the expression of EBV immediate-early gene BZLF1 via disruption of AP-1 signal transduction. Further analysis revealed that manassantin B specifically blocks the mammalian target of rapamycin complex 2 (mTORC2)-mediated phosphorylation of AKT Ser/Thr protein kinase at Ser-473 and protein kinase Cα (PKCα) at Ser-657. Using phosphoinositide 3-kinase-AKT-specific inhibitors for kinase mapping and shRNA-mediated gene silencing, we validated that manassantin B abrogates EBV lytic replication by inhibiting mTORC2 activity and thereby blocking the mTORC2-PKC/AKT-signaling pathway. These results suggest that mTORC2 may have utility as an antiviral drug target against EBV infections and also reveal that manassantin B has potential therapeutic value for managing cancers that depend on mTORC2 signaling for survival.
DOI: 10.1074/jbc.RA120.012645
PubMed: 32312752
PubMed Central: PMC7247311
Affiliations:
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role of mTORC2 signaling in Epstein-Barr virus reactivation.</title><author><name sortKey="Wang, Qian" sort="Wang, Qian" uniqKey="Wang Q" first="Qian" last="Wang">Qian Wang</name><affiliation wicri:level="1"><nlm:affiliation>Institute of Human Virology, Sun Yat-sen University, Guangzhou, Guangdong 510080, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Institute of Human Virology, Sun Yat-sen University, Guangzhou, Guangdong 510080</wicri:regionArea><wicri:noRegion>Guangdong 510080</wicri:noRegion></affiliation></author><author><name sortKey="Zhu, Nannan" sort="Zhu, Nannan" uniqKey="Zhu N" first="Nannan" last="Zhu">Nannan Zhu</name><affiliation wicri:level="1"><nlm:affiliation>Institute of Human Virology, Sun Yat-sen University, Guangzhou, Guangdong 510080, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Institute of Human Virology, Sun Yat-sen University, Guangzhou, Guangdong 510080</wicri:regionArea><wicri:noRegion>Guangdong 510080</wicri:noRegion></affiliation></author><author><name sortKey="Hu, Jiayuan" sort="Hu, Jiayuan" uniqKey="Hu J" first="Jiayuan" last="Hu">Jiayuan Hu</name><affiliation wicri:level="1"><nlm:affiliation>Institute of Human Virology, Sun Yat-sen University, Guangzhou, Guangdong 510080, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Institute of Human Virology, Sun Yat-sen University, Guangzhou, Guangdong 510080</wicri:regionArea><wicri:noRegion>Guangdong 510080</wicri:noRegion></affiliation></author><author><name sortKey="Wang, Yan" sort="Wang, Yan" uniqKey="Wang Y" first="Yan" last="Wang">Yan Wang</name><affiliation wicri:level="1"><nlm:affiliation>Guanghua School of Stomatology, Sun Yat-sen University, Guangzhou, Guangdong 510080, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Guanghua School of Stomatology, Sun Yat-sen University, Guangzhou, Guangdong 510080</wicri:regionArea><wicri:noRegion>Guangdong 510080</wicri:noRegion></affiliation></author><author><name sortKey="Xu, Jun" sort="Xu, Jun" uniqKey="Xu J" first="Jun" last="Xu">Jun Xu</name><affiliation wicri:level="1"><nlm:affiliation>School of Pharmacy, Sun Yat-sen University, Guangzhou, Guangdong 510080, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>School of Pharmacy, Sun Yat-sen University, Guangzhou, Guangdong 510080</wicri:regionArea><wicri:noRegion>Guangdong 510080</wicri:noRegion></affiliation></author><author><name sortKey="Gu, Qiong" sort="Gu, Qiong" uniqKey="Gu Q" first="Qiong" last="Gu">Qiong Gu</name><affiliation wicri:level="1"><nlm:affiliation>School of Pharmacy, Sun Yat-sen University, Guangzhou, Guangdong 510080, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>School of Pharmacy, Sun Yat-sen University, Guangzhou, Guangdong 510080</wicri:regionArea><wicri:noRegion>Guangdong 510080</wicri:noRegion></affiliation></author><author><name sortKey="Lieberman, Paul M" sort="Lieberman, Paul M" uniqKey="Lieberman P" first="Paul M" last="Lieberman">Paul M. Lieberman</name><affiliation wicri:level="2"><nlm:affiliation>The Wistar Institute, Philadelphia, Pennsylvania 19104.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Pennsylvanie</region></placeName><wicri:cityArea>The Wistar Institute, Philadelphia</wicri:cityArea></affiliation></author><author><name sortKey="Yuan, Yan" sort="Yuan, Yan" uniqKey="Yuan Y" first="Yan" last="Yuan">Yan Yuan</name><affiliation wicri:level="1"><nlm:affiliation>Institute of Human Virology, Sun Yat-sen University, Guangzhou, Guangdong 510080, China yuan2@upenn.edu.</nlm:affiliation><country wicri:rule="url">États-Unis</country><wicri:regionArea>Institute of Human Virology, Sun Yat-sen University, Guangzhou, Guangdong 510080</wicri:regionArea><wicri:noRegion>Guangdong 510080</wicri:noRegion></affiliation><affiliation wicri:level="2"><nlm:affiliation>Department of Microbiology, University of Pennsylvania School of Dental Medicine, Philadelphia, Pennsylvania 19104.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Pennsylvanie</region></placeName><wicri:cityArea>Department of Microbiology, University of Pennsylvania School of Dental Medicine, Philadelphia</wicri:cityArea></affiliation></author></analytic><series><title level="j">The Journal of biological chemistry</title><idno type="eISSN">1083-351X</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Lytic replication of Epstein-Barr virus (EBV) is not only essential for its cell-to-cell spread and host-to-host transmission, but it also contributes to EBV-induced oncogenesis. Thus, blocking EBV lytic replication could be a strategy for managing EBV-associated diseases. Previously, we identified a series of natural lignans isolated from the roots of <i>Saururus chinensis</i> (Asian lizard's tail) that efficiently block EBV lytic replication and virion production with low cytotoxicity. In this study, we attempted to elucidate the molecular mechanism by which these lignans inhibit EBV lytic replication. We found that a representative compound, CSC27 (manassantin B), inhibits EBV lytic replication by suppressing the expression of EBV immediate-early gene <i>BZLF1</i> via disruption of AP-1 signal transduction. Further analysis revealed that manassantin B specifically blocks the mammalian target of rapamycin complex 2 (mTORC2)-mediated phosphorylation of AKT Ser/Thr protein kinase at Ser-473 and protein kinase Cα (PKCα) at Ser-657. Using phosphoinositide 3-kinase-AKT-specific inhibitors for kinase mapping and shRNA-mediated gene silencing, we validated that manassantin B abrogates EBV lytic replication by inhibiting mTORC2 activity and thereby blocking the mTORC2-PKC/AKT-signaling pathway. These results suggest that mTORC2 may have utility as an antiviral drug target against EBV infections and also reveal that manassantin B has potential therapeutic value for managing cancers that depend on mTORC2 signaling for survival.</div></front></TEI><pubmed><MedlineCitation Status="In-Data-Review" Owner="NLM"><PMID Version="1">32312752</PMID><DateRevised><Year>2020</Year><Month>11</Month><Day>04</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1083-351X</ISSN><JournalIssue CitedMedium="Internet"><Volume>295</Volume><Issue>21</Issue><PubDate><Year>2020</Year><Month>May</Month><Day>22</Day></PubDate></JournalIssue><Title>The Journal of biological chemistry</Title><ISOAbbreviation>J Biol Chem</ISOAbbreviation></Journal><ArticleTitle>The mTOR inhibitor manassantin B reveals a crucial role of mTORC2 signaling in Epstein-Barr virus reactivation.</ArticleTitle><Pagination><MedlinePgn>7431-7441</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1074/jbc.RA120.012645</ELocationID><Abstract><AbstractText>Lytic replication of Epstein-Barr virus (EBV) is not only essential for its cell-to-cell spread and host-to-host transmission, but it also contributes to EBV-induced oncogenesis. Thus, blocking EBV lytic replication could be a strategy for managing EBV-associated diseases. Previously, we identified a series of natural lignans isolated from the roots of <i>Saururus chinensis</i> (Asian lizard's tail) that efficiently block EBV lytic replication and virion production with low cytotoxicity. In this study, we attempted to elucidate the molecular mechanism by which these lignans inhibit EBV lytic replication. We found that a representative compound, CSC27 (manassantin B), inhibits EBV lytic replication by suppressing the expression of EBV immediate-early gene <i>BZLF1</i> via disruption of AP-1 signal transduction. Further analysis revealed that manassantin B specifically blocks the mammalian target of rapamycin complex 2 (mTORC2)-mediated phosphorylation of AKT Ser/Thr protein kinase at Ser-473 and protein kinase Cα (PKCα) at Ser-657. Using phosphoinositide 3-kinase-AKT-specific inhibitors for kinase mapping and shRNA-mediated gene silencing, we validated that manassantin B abrogates EBV lytic replication by inhibiting mTORC2 activity and thereby blocking the mTORC2-PKC/AKT-signaling pathway. These results suggest that mTORC2 may have utility as an antiviral drug target against EBV infections and also reveal that manassantin B has potential therapeutic value for managing cancers that depend on mTORC2 signaling for survival.</AbstractText><CopyrightInformation>© 2020 Wang et al.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Qian</ForeName><Initials>Q</Initials><AffiliationInfo><Affiliation>Institute of Human Virology, Sun Yat-sen University, Guangzhou, Guangdong 510080, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhu</LastName><ForeName>Nannan</ForeName><Initials>N</Initials><Identifier Source="ORCID">https://orcid.org/0000-0001-5497-9400</Identifier><AffiliationInfo><Affiliation>Institute of Human Virology, Sun Yat-sen University, Guangzhou, Guangdong 510080, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hu</LastName><ForeName>Jiayuan</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Institute of Human Virology, Sun Yat-sen University, Guangzhou, Guangdong 510080, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Yan</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>Guanghua School of Stomatology, Sun Yat-sen University, Guangzhou, Guangdong 510080, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Xu</LastName><ForeName>Jun</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>School of Pharmacy, Sun Yat-sen University, Guangzhou, Guangdong 510080, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Gu</LastName><ForeName>Qiong</ForeName><Initials>Q</Initials><Identifier Source="ORCID">https://orcid.org/0000-0001-6011-3697</Identifier><AffiliationInfo><Affiliation>School of Pharmacy, Sun Yat-sen University, Guangzhou, Guangdong 510080, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lieberman</LastName><ForeName>Paul M</ForeName><Initials>PM</Initials><AffiliationInfo><Affiliation>The Wistar Institute, Philadelphia, Pennsylvania 19104.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Yuan</LastName><ForeName>Yan</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>Institute of Human Virology, Sun Yat-sen University, Guangzhou, Guangdong 510080, China yuan2@upenn.edu.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Microbiology, University of Pennsylvania School of Dental Medicine, Philadelphia, Pennsylvania 19104.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>P01 CA174439</GrantID><Acronym>CA</Acronym><Agency>NCI NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>P30 CA010815</GrantID><Acronym>CA</Acronym><Agency>NCI NIH HHS</Agency><Country>United States</Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>04</Month><Day>20</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>J Biol Chem</MedlineTA><NlmUniqueID>2985121R</NlmUniqueID><ISSNLinking>0021-9258</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">EBV reactivation</Keyword><Keyword MajorTopicYN="N">Epstein-Barr virus (EBV)</Keyword><Keyword MajorTopicYN="N">inhibition mechanism</Keyword><Keyword MajorTopicYN="N">inhibitor</Keyword><Keyword MajorTopicYN="N">lignan</Keyword><Keyword MajorTopicYN="N">mTOR complex (mTORC)</Keyword><Keyword MajorTopicYN="N">mTORC2 inhibitor</Keyword><Keyword MajorTopicYN="N">manassantin B</Keyword><Keyword MajorTopicYN="N">protein kinase C (PKC)</Keyword><Keyword MajorTopicYN="N">viral DNA</Keyword><Keyword MajorTopicYN="N">viral replication</Keyword><Keyword MajorTopicYN="N">virology</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2020</Year><Month>01</Month><Day>13</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2020</Year><Month>04</Month><Day>16</Day></PubMedPubDate><PubMedPubDate PubStatus="pmc-release"><Year>2021</Year><Month>05</Month><Day>22</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>4</Month><Day>22</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>4</Month><Day>22</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>4</Month><Day>22</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">32312752</ArticleId><ArticleId 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sortKey="Hu, Jiayuan" sort="Hu, Jiayuan" uniqKey="Hu J" first="Jiayuan" last="Hu">Jiayuan Hu</name><name sortKey="Wang, Yan" sort="Wang, Yan" uniqKey="Wang Y" first="Yan" last="Wang">Yan Wang</name><name sortKey="Xu, Jun" sort="Xu, Jun" uniqKey="Xu J" first="Jun" last="Xu">Jun Xu</name><name sortKey="Zhu, Nannan" sort="Zhu, Nannan" uniqKey="Zhu N" first="Nannan" last="Zhu">Nannan Zhu</name></country><country name="États-Unis"><region name="Pennsylvanie"><name sortKey="Lieberman, Paul M" sort="Lieberman, Paul M" uniqKey="Lieberman P" first="Paul M" last="Lieberman">Paul M. Lieberman</name></region><name sortKey="Yuan, Yan" sort="Yuan, Yan" uniqKey="Yuan Y" first="Yan" last="Yuan">Yan Yuan</name><name sortKey="Yuan, Yan" sort="Yuan, Yan" uniqKey="Yuan Y" first="Yan" last="Yuan">Yan Yuan</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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