The Nucleocapsid Protein of Coronaviruses Acts as a Viral Suppressor of RNA Silencing in Mammalian Cells
Identifieur interne : 000756 ( Pmc/Checkpoint ); précédent : 000755; suivant : 000757The Nucleocapsid Protein of Coronaviruses Acts as a Viral Suppressor of RNA Silencing in Mammalian Cells
Auteurs : Lei Cui ; Haiying Wang ; Yanxi Ji ; Jie Yang ; Shan Xu ; Xingyu Huang ; Zidao Wang ; Lei Qin ; Po Tien ; Xi Zhou ; Deyin Guo ; Yu ChenSource :
- Journal of Virology [ 0022-538X ] ; 2015.
Abstract
RNA interference (RNAi) is a process of eukaryotic posttranscriptional gene silencing that functions in antiviral immunity in plants, nematodes, and insects. However, recent studies provided strong supports that RNAi also plays a role in antiviral mechanism in mammalian cells. To combat RNAi-mediated antiviral responses, many viruses encode viral suppressors of RNA silencing (VSR) to facilitate their replication. VSRs have been widely studied for plant and insect viruses, but only a few have been defined for mammalian viruses currently. We identified a novel VSR from coronaviruses, a group of medically important mammalian viruses including Severe acute respiratory syndrome coronavirus (SARS-CoV), and showed that the nucleocapsid protein (N protein) of coronaviruses suppresses RNAi triggered by either short hairpin RNAs or small interfering RNAs in mammalian cells. Mouse hepatitis virus (MHV) is closely related to SARS-CoV in the family
Url:
DOI: 10.1128/JVI.01331-15
PubMed: 26085159
PubMed Central: 4524063
Affiliations:
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<author><name sortKey="Yang, Jie" sort="Yang, Jie" uniqKey="Yang J" first="Jie" last="Yang">Jie Yang</name>
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<author><name sortKey="Xu, Shan" sort="Xu, Shan" uniqKey="Xu S" first="Shan" last="Xu">Shan Xu</name>
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<author><name sortKey="Huang, Xingyu" sort="Huang, Xingyu" uniqKey="Huang X" first="Xingyu" last="Huang">Xingyu Huang</name>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">The Nucleocapsid Protein of Coronaviruses Acts as a Viral Suppressor of RNA Silencing in Mammalian Cells</title>
<author><name sortKey="Cui, Lei" sort="Cui, Lei" uniqKey="Cui L" first="Lei" last="Cui">Lei Cui</name>
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<author><name sortKey="Wang, Haiying" sort="Wang, Haiying" uniqKey="Wang H" first="Haiying" last="Wang">Haiying Wang</name>
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<author><name sortKey="Ji, Yanxi" sort="Ji, Yanxi" uniqKey="Ji Y" first="Yanxi" last="Ji">Yanxi Ji</name>
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<author><name sortKey="Yang, Jie" sort="Yang, Jie" uniqKey="Yang J" first="Jie" last="Yang">Jie Yang</name>
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<author><name sortKey="Xu, Shan" sort="Xu, Shan" uniqKey="Xu S" first="Shan" last="Xu">Shan Xu</name>
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<author><name sortKey="Huang, Xingyu" sort="Huang, Xingyu" uniqKey="Huang X" first="Xingyu" last="Huang">Xingyu Huang</name>
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<author><name sortKey="Wang, Zidao" sort="Wang, Zidao" uniqKey="Wang Z" first="Zidao" last="Wang">Zidao Wang</name>
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<author><name sortKey="Qin, Lei" sort="Qin, Lei" uniqKey="Qin L" first="Lei" last="Qin">Lei Qin</name>
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<author><name sortKey="Tien, Po" sort="Tien, Po" uniqKey="Tien P" first="Po" last="Tien">Po Tien</name>
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<author><name sortKey="Zhou, Xi" sort="Zhou, Xi" uniqKey="Zhou X" first="Xi" last="Zhou">Xi Zhou</name>
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<author><name sortKey="Guo, Deyin" sort="Guo, Deyin" uniqKey="Guo D" first="Deyin" last="Guo">Deyin Guo</name>
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<author><name sortKey="Chen, Yu" sort="Chen, Yu" uniqKey="Chen Y" first="Yu" last="Chen">Yu Chen</name>
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<series><title level="j">Journal of Virology</title>
<idno type="ISSN">0022-538X</idno>
<idno type="eISSN">1098-5514</idno>
<imprint><date when="2015">2015</date>
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<front><div type="abstract" xml:lang="en"><title>ABSTRACT</title>
<p>RNA interference (RNAi) is a process of eukaryotic posttranscriptional gene silencing that functions in antiviral immunity in plants, nematodes, and insects. However, recent studies provided strong supports that RNAi also plays a role in antiviral mechanism in mammalian cells. To combat RNAi-mediated antiviral responses, many viruses encode viral suppressors of RNA silencing (VSR) to facilitate their replication. VSRs have been widely studied for plant and insect viruses, but only a few have been defined for mammalian viruses currently. We identified a novel VSR from coronaviruses, a group of medically important mammalian viruses including Severe acute respiratory syndrome coronavirus (SARS-CoV), and showed that the nucleocapsid protein (N protein) of coronaviruses suppresses RNAi triggered by either short hairpin RNAs or small interfering RNAs in mammalian cells. Mouse hepatitis virus (MHV) is closely related to SARS-CoV in the family <named-content content-type="genus-species">Coronaviridae</named-content>
and was used as a coronavirus replication model. The replication of MHV increased when the N proteins were expressed <italic>in trans</italic>
, while knockdown of Dicer1 or Ago2 transcripts facilitated the MHV replication in mammalian cells. These results support the hypothesis that RNAi is a part of the antiviral immunity responses in mammalian cells.</p>
<p><bold>IMPORTANCE</bold>
RNAi has been well known to play important antiviral roles from plants to invertebrates. However, recent studies provided strong supports that RNAi is also involved in antiviral response in mammalian cells. An important indication for RNAi-mediated antiviral activity in mammals is the fact that a number of mammalian viruses encode potent suppressors of RNA silencing. Our results demonstrate that coronavirus N protein could function as a VSR through its double-stranded RNA binding activity. Mutational analysis of N protein allowed us to find out the critical residues for the VSR activity. Using the MHV-A59 as the coronavirus replication model, we showed that ectopic expression of SARS-CoV N protein could promote MHV replication in RNAi-active cells but not in RNAi-depleted cells. These results indicate that coronaviruses encode a VSR that functions in the replication cycle and provide further evidence to support that RNAi-mediated antiviral response exists in mammalian cells.</p>
</div>
</front>
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<pmc article-type="research-article"><pmc-comment>The publisher of this article does not allow downloading of the full text in XML form.</pmc-comment>
<front><journal-meta><journal-id journal-id-type="nlm-ta">J Virol</journal-id>
<journal-id journal-id-type="iso-abbrev">J. Virol</journal-id>
<journal-id journal-id-type="hwp">jvi</journal-id>
<journal-id journal-id-type="pmc">jvi</journal-id>
<journal-id journal-id-type="publisher-id">JVI</journal-id>
<journal-title-group><journal-title>Journal of Virology</journal-title>
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<issn pub-type="ppub">0022-538X</issn>
<issn pub-type="epub">1098-5514</issn>
<publisher><publisher-name>American Society for Microbiology</publisher-name>
<publisher-loc>1752 N St., N.W., Washington, DC</publisher-loc>
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<article-meta><article-id pub-id-type="pmid">26085159</article-id>
<article-id pub-id-type="pmc">4524063</article-id>
<article-id pub-id-type="publisher-id">01331-15</article-id>
<article-id pub-id-type="doi">10.1128/JVI.01331-15</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Virus-Cell Interactions</subject>
</subj-group>
<subj-group subj-group-type="editorial-class"><subject>Spotlight</subject>
</subj-group>
</article-categories>
<title-group><article-title>The Nucleocapsid Protein of Coronaviruses Acts as a Viral Suppressor of RNA Silencing in Mammalian Cells</article-title>
<alt-title alt-title-type="running-head">Coronavirus N as a VSR in Mammalian Cells</alt-title>
<alt-title alt-title-type="short-authors">Cui et al.</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Cui</surname>
<given-names>Lei</given-names>
</name>
</contrib>
<contrib contrib-type="author"><name><surname>Wang</surname>
<given-names>Haiying</given-names>
</name>
</contrib>
<contrib contrib-type="author"><name><surname>Ji</surname>
<given-names>Yanxi</given-names>
</name>
</contrib>
<contrib contrib-type="author"><name><surname>Yang</surname>
<given-names>Jie</given-names>
</name>
</contrib>
<contrib contrib-type="author"><name><surname>Xu</surname>
<given-names>Shan</given-names>
</name>
</contrib>
<contrib contrib-type="author"><name><surname>Huang</surname>
<given-names>Xingyu</given-names>
</name>
</contrib>
<contrib contrib-type="author"><name><surname>Wang</surname>
<given-names>Zidao</given-names>
</name>
</contrib>
<contrib contrib-type="author"><name><surname>Qin</surname>
<given-names>Lei</given-names>
</name>
</contrib>
<contrib contrib-type="author"><name><surname>Tien</surname>
<given-names>Po</given-names>
</name>
</contrib>
<contrib contrib-type="author"><name><surname>Zhou</surname>
<given-names>Xi</given-names>
</name>
</contrib>
<contrib contrib-type="author" corresp="yes"><name><surname>Guo</surname>
<given-names>Deyin</given-names>
</name>
</contrib>
<contrib contrib-type="author" corresp="yes"><name><surname>Chen</surname>
<given-names>Yu</given-names>
</name>
</contrib>
<aff>State Key Laboratory of Virology, College of Life Sciences, Wuhan University, Wuhan, Hubei, China</aff>
</contrib-group>
<contrib-group><contrib contrib-type="editor"><name><surname>Perlman</surname>
<given-names>S.</given-names>
</name>
<role>Editor</role>
</contrib>
</contrib-group>
<author-notes><corresp id="cor1">Address correspondence to Deyin Guo, <email>dguo@whu.edu.cn</email>
, or Yu Chen, <email>chenyu@whu.edu.cn</email>
.</corresp>
<fn fn-type="other"><p><bold>Citation</bold>
Cui L, Wang H, Ji Y, Yang J, Xu S, Huang X, Wang Z, Qin L, Tien P, Zhou X, Guo D, Chen Y. 2015. The nucleocapsid protein of coronaviruses acts as a viral suppressor of RNA silencing in mammalian cells. J Virol 89:9029–9043. doi:<ext-link ext-link-type="uri" xlink:href="http://dx.doi.org/10.1128/JVI.01331-15">10.1128/JVI.01331-15</ext-link>
.</p>
</fn>
</author-notes>
<pub-date pub-type="epub"><day>17</day>
<month>6</month>
<year>2015</year>
</pub-date>
<pub-date pub-type="collection"><day>1</day>
<month>9</month>
<year>2015</year>
</pub-date>
<volume>89</volume>
<issue>17</issue>
<fpage>9029</fpage>
<lpage>9043</lpage>
<history><date date-type="received"><day>21</day>
<month>5</month>
<year>2015</year>
</date>
<date date-type="accepted"><day>11</day>
<month>6</month>
<year>2015</year>
</date>
</history>
<permissions><copyright-statement>Copyright © 2015, American Society for Microbiology. All Rights Reserved.</copyright-statement>
<copyright-year>2015</copyright-year>
<copyright-holder>American Society for Microbiology</copyright-holder>
</permissions>
<self-uri content-type="pdf" xlink:href="zjv01715009029.pdf"></self-uri>
<abstract><title>ABSTRACT</title>
<p>RNA interference (RNAi) is a process of eukaryotic posttranscriptional gene silencing that functions in antiviral immunity in plants, nematodes, and insects. However, recent studies provided strong supports that RNAi also plays a role in antiviral mechanism in mammalian cells. To combat RNAi-mediated antiviral responses, many viruses encode viral suppressors of RNA silencing (VSR) to facilitate their replication. VSRs have been widely studied for plant and insect viruses, but only a few have been defined for mammalian viruses currently. We identified a novel VSR from coronaviruses, a group of medically important mammalian viruses including Severe acute respiratory syndrome coronavirus (SARS-CoV), and showed that the nucleocapsid protein (N protein) of coronaviruses suppresses RNAi triggered by either short hairpin RNAs or small interfering RNAs in mammalian cells. Mouse hepatitis virus (MHV) is closely related to SARS-CoV in the family <named-content content-type="genus-species">Coronaviridae</named-content>
and was used as a coronavirus replication model. The replication of MHV increased when the N proteins were expressed <italic>in trans</italic>
, while knockdown of Dicer1 or Ago2 transcripts facilitated the MHV replication in mammalian cells. These results support the hypothesis that RNAi is a part of the antiviral immunity responses in mammalian cells.</p>
<p><bold>IMPORTANCE</bold>
RNAi has been well known to play important antiviral roles from plants to invertebrates. However, recent studies provided strong supports that RNAi is also involved in antiviral response in mammalian cells. An important indication for RNAi-mediated antiviral activity in mammals is the fact that a number of mammalian viruses encode potent suppressors of RNA silencing. Our results demonstrate that coronavirus N protein could function as a VSR through its double-stranded RNA binding activity. Mutational analysis of N protein allowed us to find out the critical residues for the VSR activity. Using the MHV-A59 as the coronavirus replication model, we showed that ectopic expression of SARS-CoV N protein could promote MHV replication in RNAi-active cells but not in RNAi-depleted cells. These results indicate that coronaviruses encode a VSR that functions in the replication cycle and provide further evidence to support that RNAi-mediated antiviral response exists in mammalian cells.</p>
</abstract>
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<affiliations><list></list>
<tree><noCountry><name sortKey="Chen, Yu" sort="Chen, Yu" uniqKey="Chen Y" first="Yu" last="Chen">Yu Chen</name>
<name sortKey="Cui, Lei" sort="Cui, Lei" uniqKey="Cui L" first="Lei" last="Cui">Lei Cui</name>
<name sortKey="Guo, Deyin" sort="Guo, Deyin" uniqKey="Guo D" first="Deyin" last="Guo">Deyin Guo</name>
<name sortKey="Huang, Xingyu" sort="Huang, Xingyu" uniqKey="Huang X" first="Xingyu" last="Huang">Xingyu Huang</name>
<name sortKey="Ji, Yanxi" sort="Ji, Yanxi" uniqKey="Ji Y" first="Yanxi" last="Ji">Yanxi Ji</name>
<name sortKey="Qin, Lei" sort="Qin, Lei" uniqKey="Qin L" first="Lei" last="Qin">Lei Qin</name>
<name sortKey="Tien, Po" sort="Tien, Po" uniqKey="Tien P" first="Po" last="Tien">Po Tien</name>
<name sortKey="Wang, Haiying" sort="Wang, Haiying" uniqKey="Wang H" first="Haiying" last="Wang">Haiying Wang</name>
<name sortKey="Wang, Zidao" sort="Wang, Zidao" uniqKey="Wang Z" first="Zidao" last="Wang">Zidao Wang</name>
<name sortKey="Xu, Shan" sort="Xu, Shan" uniqKey="Xu S" first="Shan" last="Xu">Shan Xu</name>
<name sortKey="Yang, Jie" sort="Yang, Jie" uniqKey="Yang J" first="Jie" last="Yang">Jie Yang</name>
<name sortKey="Zhou, Xi" sort="Zhou, Xi" uniqKey="Zhou X" first="Xi" last="Zhou">Xi Zhou</name>
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