The Severe Acute Respiratory Syndrome Coronavirus Nucleocapsid Inhibits Type I Interferon Production by Interfering with TRIM25-Mediated RIG-I Ubiquitination
Identifieur interne : 000C92 ( Pmc/Curation ); précédent : 000C91; suivant : 000C93The Severe Acute Respiratory Syndrome Coronavirus Nucleocapsid Inhibits Type I Interferon Production by Interfering with TRIM25-Mediated RIG-I Ubiquitination
Auteurs : Yong Hu ; Wei Li ; Ting Gao ; Yan Cui ; Yanwen Jin ; Ping Li ; Qingjun Ma ; Xuan Liu ; Cheng CaoSource :
- Journal of Virology [ 0022-538X ] ; 2017.
Abstract
Severe acute respiratory syndrome (SARS) is a respiratory disease, caused by a coronavirus (SARS-CoV), that is characterized by atypical pneumonia. The nucleocapsid protein (N protein) of SARS-CoV plays an important role in inhibition of type I interferon (IFN) production via an unknown mechanism. In this study, the SARS-CoV N protein was found to bind to the SPRY domain of the tripartite motif protein 25 (TRIM25) E3 ubiquitin ligase, thereby interfering with the association between TRIM25 and retinoic acid-inducible gene I (RIG-I) and inhibiting TRIM25-mediated RIG-I ubiquitination and activation. Type I IFN production induced by poly I·C or Sendai virus (SeV) was suppressed by the SARS-CoV N protein. SARS-CoV replication was increased by overexpression of the full-length N protein but not N amino acids 1 to 361, which could not interact with TRIM25. These findings provide an insightful interpretation of the SARS-CoV-mediated host innate immune suppression caused by the N protein.
Url:
DOI: 10.1128/JVI.02143-16
PubMed: 28148787
PubMed Central: 5375661
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">The Severe Acute Respiratory Syndrome Coronavirus Nucleocapsid Inhibits Type I Interferon Production by Interfering with TRIM25-Mediated RIG-I Ubiquitination</title>
<author><name sortKey="Hu, Yong" sort="Hu, Yong" uniqKey="Hu Y" first="Yong" last="Hu">Yong Hu</name>
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<author><name sortKey="Li, Wei" sort="Li, Wei" uniqKey="Li W" first="Wei" last="Li">Wei Li</name>
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<author><name sortKey="Gao, Ting" sort="Gao, Ting" uniqKey="Gao T" first="Ting" last="Gao">Ting Gao</name>
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<author><name sortKey="Cui, Yan" sort="Cui, Yan" uniqKey="Cui Y" first="Yan" last="Cui">Yan Cui</name>
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<author><name sortKey="Jin, Yanwen" sort="Jin, Yanwen" uniqKey="Jin Y" first="Yanwen" last="Jin">Yanwen Jin</name>
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<author><name sortKey="Li, Ping" sort="Li, Ping" uniqKey="Li P" first="Ping" last="Li">Ping Li</name>
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<author><name sortKey="Ma, Qingjun" sort="Ma, Qingjun" uniqKey="Ma Q" first="Qingjun" last="Ma">Qingjun Ma</name>
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<author><name sortKey="Liu, Xuan" sort="Liu, Xuan" uniqKey="Liu X" first="Xuan" last="Liu">Xuan Liu</name>
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<author><name sortKey="Cao, Cheng" sort="Cao, Cheng" uniqKey="Cao C" first="Cheng" last="Cao">Cheng Cao</name>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">The Severe Acute Respiratory Syndrome Coronavirus Nucleocapsid Inhibits Type I Interferon Production by Interfering with TRIM25-Mediated RIG-I Ubiquitination</title>
<author><name sortKey="Hu, Yong" sort="Hu, Yong" uniqKey="Hu Y" first="Yong" last="Hu">Yong Hu</name>
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<author><name sortKey="Li, Wei" sort="Li, Wei" uniqKey="Li W" first="Wei" last="Li">Wei Li</name>
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<author><name sortKey="Gao, Ting" sort="Gao, Ting" uniqKey="Gao T" first="Ting" last="Gao">Ting Gao</name>
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<author><name sortKey="Cui, Yan" sort="Cui, Yan" uniqKey="Cui Y" first="Yan" last="Cui">Yan Cui</name>
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<author><name sortKey="Jin, Yanwen" sort="Jin, Yanwen" uniqKey="Jin Y" first="Yanwen" last="Jin">Yanwen Jin</name>
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<author><name sortKey="Li, Ping" sort="Li, Ping" uniqKey="Li P" first="Ping" last="Li">Ping Li</name>
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<author><name sortKey="Ma, Qingjun" sort="Ma, Qingjun" uniqKey="Ma Q" first="Qingjun" last="Ma">Qingjun Ma</name>
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<author><name sortKey="Liu, Xuan" sort="Liu, Xuan" uniqKey="Liu X" first="Xuan" last="Liu">Xuan Liu</name>
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<author><name sortKey="Cao, Cheng" sort="Cao, Cheng" uniqKey="Cao C" first="Cheng" last="Cao">Cheng Cao</name>
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<series><title level="j">Journal of Virology</title>
<idno type="ISSN">0022-538X</idno>
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<imprint><date when="2017">2017</date>
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<front><div type="abstract" xml:lang="en"><title>ABSTRACT</title>
<p>Severe acute respiratory syndrome (SARS) is a respiratory disease, caused by a coronavirus (SARS-CoV), that is characterized by atypical pneumonia. The nucleocapsid protein (N protein) of SARS-CoV plays an important role in inhibition of type I interferon (IFN) production via an unknown mechanism. In this study, the SARS-CoV N protein was found to bind to the SPRY domain of the tripartite motif protein 25 (TRIM25) E3 ubiquitin ligase, thereby interfering with the association between TRIM25 and retinoic acid-inducible gene I (RIG-I) and inhibiting TRIM25-mediated RIG-I ubiquitination and activation. Type I IFN production induced by poly I·C or Sendai virus (SeV) was suppressed by the SARS-CoV N protein. SARS-CoV replication was increased by overexpression of the full-length N protein but not N amino acids 1 to 361, which could not interact with TRIM25. These findings provide an insightful interpretation of the SARS-CoV-mediated host innate immune suppression caused by the N protein.</p>
<p><bold>IMPORTANCE</bold>
The SARS-CoV N protein is essential for the viral life cycle and plays a key role in the virus-host interaction. We demonstrated that the interaction between the C terminus of the N protein and the SPRY domain of TRIM25 inhibited TRIM25-mediated RIG-I ubiquitination, which resulted in the inhibition of IFN production. We also found that the Middle East respiratory syndrome CoV (MERS-CoV) N protein interacted with TRIM25 and inhibited RIG-I signaling. The outcomes of these findings indicate the function of the coronavirus N protein in modulating the host's initial innate immune response.</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>
</journal-title-group>
<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>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">28148787</article-id>
<article-id pub-id-type="pmc">5375661</article-id>
<article-id pub-id-type="publisher-id">02143-16</article-id>
<article-id pub-id-type="doi">10.1128/JVI.02143-16</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Virus-Cell Interactions</subject>
</subj-group>
</article-categories>
<title-group><article-title>The Severe Acute Respiratory Syndrome Coronavirus Nucleocapsid Inhibits Type I Interferon Production by Interfering with TRIM25-Mediated RIG-I Ubiquitination</article-title>
<alt-title alt-title-type="running-head">SARS-CoV N Protein Inhibits Type I Interferon Pathway</alt-title>
<alt-title alt-title-type="short-authors">Hu et al.</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Hu</surname>
<given-names>Yong</given-names>
</name>
</contrib>
<contrib contrib-type="author"><name><surname>Li</surname>
<given-names>Wei</given-names>
</name>
</contrib>
<contrib contrib-type="author"><name><surname>Gao</surname>
<given-names>Ting</given-names>
</name>
</contrib>
<contrib contrib-type="author"><name><surname>Cui</surname>
<given-names>Yan</given-names>
</name>
</contrib>
<contrib contrib-type="author"><name><surname>Jin</surname>
<given-names>Yanwen</given-names>
</name>
</contrib>
<contrib contrib-type="author"><name><surname>Li</surname>
<given-names>Ping</given-names>
</name>
</contrib>
<contrib contrib-type="author"><name><surname>Ma</surname>
<given-names>Qingjun</given-names>
</name>
</contrib>
<contrib contrib-type="author" corresp="yes"><name><surname>Liu</surname>
<given-names>Xuan</given-names>
</name>
</contrib>
<contrib contrib-type="author" corresp="yes"><name><surname>Cao</surname>
<given-names>Cheng</given-names>
</name>
</contrib>
<aff>State Key Laboratory of Pathogen Biosecurity, Beijing Institute of Biotechnology, Beijing, China</aff>
</contrib-group>
<contrib-group><contrib contrib-type="editor"><name><surname>Perlman</surname>
<given-names>Stanley</given-names>
</name>
<role>Editor</role>
<aff>University of Iowa</aff>
</contrib>
</contrib-group>
<author-notes><corresp id="cor1">Address correspondence to Xuan Liu, <email>liux931932@163.com</email>
, or Cheng Cao, <email>cao_c@sohu.com</email>
.</corresp>
<fn fn-type="other"><p><bold>Citation</bold>
Hu Y, Li W, Gao T, Cui Y, Jin Y, Li P, Ma Q, Liu X, Cao C. 2017. The severe acute respiratory syndrome coronavirus nucleocapsid inhibits type I interferon production by interfering with TRIM25-mediated RIG-I ubiquitination. J Virol 91:e02143-16. <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.1128/JVI.02143-16">https://doi.org/10.1128/JVI.02143-16</ext-link>
.</p>
</fn>
</author-notes>
<pub-date pub-type="epreprint"><day>1</day>
<month>2</month>
<year>2017</year>
</pub-date>
<pub-date pub-type="epub"><day>29</day>
<month>3</month>
<year>2017</year>
</pub-date>
<pub-date pub-type="collection"><day>15</day>
<month>4</month>
<year>2017</year>
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<volume>91</volume>
<issue>8</issue>
<elocation-id>e02143-16</elocation-id>
<history><date date-type="received"><day>1</day>
<month>11</month>
<year>2016</year>
</date>
<date date-type="accepted"><day>24</day>
<month>1</month>
<year>2017</year>
</date>
</history>
<permissions><copyright-statement>Copyright © 2017 American Society for Microbiology.</copyright-statement>
<copyright-year>2017</copyright-year>
<copyright-holder>American Society for Microbiology</copyright-holder>
<license license-type="asm" xlink:href="https://doi.org/10.1128/ASMCopyrightv1"><license-p><ext-link ext-link-type="uri" xlink:href="https://doi.org/10.1128/ASMCopyrightv1">All Rights Reserved</ext-link>
.</license-p>
</license>
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<self-uri content-type="pdf" xlink:href="zjv008172487001.pdf"></self-uri>
<abstract><title>ABSTRACT</title>
<p>Severe acute respiratory syndrome (SARS) is a respiratory disease, caused by a coronavirus (SARS-CoV), that is characterized by atypical pneumonia. The nucleocapsid protein (N protein) of SARS-CoV plays an important role in inhibition of type I interferon (IFN) production via an unknown mechanism. In this study, the SARS-CoV N protein was found to bind to the SPRY domain of the tripartite motif protein 25 (TRIM25) E3 ubiquitin ligase, thereby interfering with the association between TRIM25 and retinoic acid-inducible gene I (RIG-I) and inhibiting TRIM25-mediated RIG-I ubiquitination and activation. Type I IFN production induced by poly I·C or Sendai virus (SeV) was suppressed by the SARS-CoV N protein. SARS-CoV replication was increased by overexpression of the full-length N protein but not N amino acids 1 to 361, which could not interact with TRIM25. These findings provide an insightful interpretation of the SARS-CoV-mediated host innate immune suppression caused by the N protein.</p>
<p><bold>IMPORTANCE</bold>
The SARS-CoV N protein is essential for the viral life cycle and plays a key role in the virus-host interaction. We demonstrated that the interaction between the C terminus of the N protein and the SPRY domain of TRIM25 inhibited TRIM25-mediated RIG-I ubiquitination, which resulted in the inhibition of IFN production. We also found that the Middle East respiratory syndrome CoV (MERS-CoV) N protein interacted with TRIM25 and inhibited RIG-I signaling. The outcomes of these findings indicate the function of the coronavirus N protein in modulating the host's initial innate immune response.</p>
</abstract>
<kwd-group><title>KEYWORDS</title>
<kwd>SARS coronavirus</kwd>
<kwd>nucleocapsid</kwd>
<kwd>interferon</kwd>
<kwd>TRIM25</kwd>
<kwd>RIG-I</kwd>
</kwd-group>
<funding-group><award-group id="award1"><funding-source id="gs1">Ministry of science and</funding-source>
<award-id rid="gs1">2012CB518900</award-id>
<award-id rid="gs1">2016YFC1202400</award-id>
</award-group>
<award-group id="award2"><funding-source id="gs2">Natural Science Foundation of China</funding-source>
<award-id rid="gs2">30871240</award-id>
<award-id rid="gs2">81550001</award-id>
</award-group>
</funding-group>
<counts><fig-count count="8"></fig-count>
<table-count count="1"></table-count>
<equation-count count="0"></equation-count>
<ref-count count="61"></ref-count>
<page-count count="15"></page-count>
<word-count count="8723"></word-count>
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<custom-meta-group><custom-meta><meta-name>cover-date</meta-name>
<meta-value>April 2017</meta-value>
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</front>
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