Avian Influenza Virus PB1 Gene in H3N2 Viruses Evolved in Humans To Reduce Interferon Inhibition by Skewing Codon Usage toward Interferon-Altered tRNA Pools
Identifieur interne : 000C57 ( Pmc/Curation ); précédent : 000C56; suivant : 000C58Avian Influenza Virus PB1 Gene in H3N2 Viruses Evolved in Humans To Reduce Interferon Inhibition by Skewing Codon Usage toward Interferon-Altered tRNA Pools
Auteurs : Bartram L. Smith [États-Unis] ; Guifang Chen [États-Unis] ; Claus O. Wilke [États-Unis] ; Robert M. Krug [États-Unis]Source :
- mBio [ 2150-7511 ] ; 2018.
Abstract
Influenza A viruses cause an annual contagious respiratory disease in humans and are responsible for periodic high-mortality human pandemics. Pandemic influenza A viruses usually result from the reassortment of gene segments between human and avian influenza viruses. These avian influenza virus gene segments need to adapt to humans. Here we focus on the human adaptation of the synonymous codons of the avian influenza virus PB1 gene of the 1968 H3N2 pandemic virus. We generated recombinant H3N2 viruses differing only in codon usage of PB1 mRNA and demonstrated that codon usage of the PB1 mRNA of recent H3N2 virus isolates enhances replication in interferon (IFN)-treated human cells without affecting replication in untreated cells, thereby partially alleviating the interferon-induced antiviral state. High-throughput sequencing of tRNA pools explains the reduced inhibition of replication by interferon: the levels of some tRNAs differ between interferon-treated and untreated human cells, and evolution of the codon usage of H3N2 PB1 mRNA is skewed toward interferon-altered human tRNA pools. Consequently, the avian influenza virus-derived PB1 mRNAs of modern H3N2 viruses have acquired codon usages that better reflect tRNA availabilities in IFN-treated cells. Our results indicate that the change in tRNA availabilities resulting from interferon treatment is a previously unknown aspect of the antiviral action of interferon, which has been partially overcome by human-adapted H3N2 viruses.
Url:
DOI: 10.1128/mBio.01222-18
PubMed: 29970470
PubMed Central: 6030557
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Smith</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Department of Molecular Biosciences, John Ring LaMontagne Center for Infectious Disease, Institute for Cellular and Molecular Biology, the University of Texas at Austin, Austin, Texas, USA</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular Biosciences, John Ring LaMontagne Center for Infectious Disease, Institute for Cellular and Molecular Biology, the University of Texas at Austin, Austin, Texas</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff2"><addr-line>Department of Integrative Biology, Center for Computational Biology and Bioinformatics, Institute for Cellular and Molecular Biology, the University of Texas at Austin, Austin, Texas, USA</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Integrative Biology, Center for Computational Biology and Bioinformatics, Institute for Cellular and Molecular Biology, the University of Texas at Austin, Austin, Texas</wicri:regionArea></affiliation></author><author><name sortKey="Chen, Guifang" sort="Chen, Guifang" uniqKey="Chen G" first="Guifang" last="Chen">Guifang Chen</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Department of Molecular Biosciences, John Ring LaMontagne Center for Infectious Disease, Institute for Cellular and Molecular Biology, the University of Texas at Austin, Austin, Texas, USA</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular Biosciences, John Ring LaMontagne Center for Infectious Disease, Institute for Cellular and Molecular Biology, the University of Texas at Austin, Austin, Texas</wicri:regionArea></affiliation></author><author><name sortKey="Wilke, Claus O" sort="Wilke, Claus O" uniqKey="Wilke C" first="Claus O." last="Wilke">Claus O. Wilke</name><affiliation wicri:level="1"><nlm:aff id="aff2"><addr-line>Department of Integrative Biology, Center for Computational Biology and Bioinformatics, Institute for Cellular and Molecular Biology, the University of Texas at Austin, Austin, Texas, USA</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Integrative Biology, Center for Computational Biology and Bioinformatics, Institute for Cellular and Molecular Biology, the University of Texas at Austin, Austin, Texas</wicri:regionArea></affiliation></author><author><name sortKey="Krug, Robert M" sort="Krug, Robert M" uniqKey="Krug R" first="Robert M." last="Krug">Robert M. Krug</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Department of Molecular Biosciences, John Ring LaMontagne Center for Infectious Disease, Institute for Cellular and Molecular Biology, the University of Texas at Austin, Austin, Texas, USA</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular Biosciences, John Ring LaMontagne Center for Infectious Disease, Institute for Cellular and Molecular Biology, the University of Texas at Austin, Austin, Texas</wicri:regionArea></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">29970470</idno><idno type="pmc">6030557</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6030557</idno><idno type="RBID">PMC:6030557</idno><idno type="doi">10.1128/mBio.01222-18</idno><date when="2018">2018</date><idno type="wicri:Area/Pmc/Corpus">000C57</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000C57</idno><idno type="wicri:Area/Pmc/Curation">000C57</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">000C57</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Avian Influenza Virus PB1 Gene in H3N2 Viruses Evolved in Humans To Reduce Interferon Inhibition by Skewing Codon Usage toward Interferon-Altered tRNA Pools</title><author><name sortKey="Smith, Bartram L" sort="Smith, Bartram L" uniqKey="Smith B" first="Bartram L." last="Smith">Bartram L. Smith</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Department of Molecular Biosciences, John Ring LaMontagne Center for Infectious Disease, Institute for Cellular and Molecular Biology, the University of Texas at Austin, Austin, Texas, USA</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular Biosciences, John Ring LaMontagne Center for Infectious Disease, Institute for Cellular and Molecular Biology, the University of Texas at Austin, Austin, Texas</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff2"><addr-line>Department of Integrative Biology, Center for Computational Biology and Bioinformatics, Institute for Cellular and Molecular Biology, the University of Texas at Austin, Austin, Texas, USA</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Integrative Biology, Center for Computational Biology and Bioinformatics, Institute for Cellular and Molecular Biology, the University of Texas at Austin, Austin, Texas</wicri:regionArea></affiliation></author><author><name sortKey="Chen, Guifang" sort="Chen, Guifang" uniqKey="Chen G" first="Guifang" last="Chen">Guifang Chen</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Department of Molecular Biosciences, John Ring LaMontagne Center for Infectious Disease, Institute for Cellular and Molecular Biology, the University of Texas at Austin, Austin, Texas, USA</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular Biosciences, John Ring LaMontagne Center for Infectious Disease, Institute for Cellular and Molecular Biology, the University of Texas at Austin, Austin, Texas</wicri:regionArea></affiliation></author><author><name sortKey="Wilke, Claus O" sort="Wilke, Claus O" uniqKey="Wilke C" first="Claus O." last="Wilke">Claus O. Wilke</name><affiliation wicri:level="1"><nlm:aff id="aff2"><addr-line>Department of Integrative Biology, Center for Computational Biology and Bioinformatics, Institute for Cellular and Molecular Biology, the University of Texas at Austin, Austin, Texas, USA</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Integrative Biology, Center for Computational Biology and Bioinformatics, Institute for Cellular and Molecular Biology, the University of Texas at Austin, Austin, Texas</wicri:regionArea></affiliation></author><author><name sortKey="Krug, Robert M" sort="Krug, Robert M" uniqKey="Krug R" first="Robert M." last="Krug">Robert M. Krug</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Department of Molecular Biosciences, John Ring LaMontagne Center for Infectious Disease, Institute for Cellular and Molecular Biology, the University of Texas at Austin, Austin, Texas, USA</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular Biosciences, John Ring LaMontagne Center for Infectious Disease, Institute for Cellular and Molecular Biology, the University of Texas at Austin, Austin, Texas</wicri:regionArea></affiliation></author></analytic><series><title level="j">mBio</title><idno type="eISSN">2150-7511</idno><imprint><date when="2018">2018</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><title>ABSTRACT</title><p>Influenza A viruses cause an annual contagious respiratory disease in humans and are responsible for periodic high-mortality human pandemics. Pandemic influenza A viruses usually result from the reassortment of gene segments between human and avian influenza viruses. These avian influenza virus gene segments need to adapt to humans. Here we focus on the human adaptation of the synonymous codons of the avian influenza virus PB1 gene of the 1968 H3N2 pandemic virus. We generated recombinant H3N2 viruses differing only in codon usage of PB1 mRNA and demonstrated that codon usage of the PB1 mRNA of recent H3N2 virus isolates enhances replication in interferon (IFN)-treated human cells without affecting replication in untreated cells, thereby partially alleviating the interferon-induced antiviral state. High-throughput sequencing of tRNA pools explains the reduced inhibition of replication by interferon: the levels of some tRNAs differ between interferon-treated and untreated human cells, and evolution of the codon usage of H3N2 PB1 mRNA is skewed toward interferon-altered human tRNA pools. Consequently, the avian influenza virus-derived PB1 mRNAs of modern H3N2 viruses have acquired codon usages that better reflect tRNA availabilities in IFN-treated cells. Our results indicate that the change in tRNA availabilities resulting from interferon treatment is a previously unknown aspect of the antiviral action of interferon, which has been partially overcome by human-adapted H3N2 viruses.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Cauldwell, Av" uniqKey="Cauldwell A">AV Cauldwell</name></author><author><name sortKey="Long, Js" uniqKey="Long J">JS Long</name></author><author><name sortKey="Moncorge, O" uniqKey="Moncorge O">O Moncorgé</name></author><author><name sortKey="Barclay, Ws" uniqKey="Barclay W">WS Barclay</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Kanaya, S" uniqKey="Kanaya S">S Kanaya</name></author><author><name sortKey="Kinouchi, M" uniqKey="Kinouchi M">M Kinouchi</name></author><author><name sortKey="Abe, T" uniqKey="Abe T">T Abe</name></author><author><name sortKey="Kudo, Y" uniqKey="Kudo Y">Y Kudo</name></author><author><name 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<front><journal-meta><journal-id journal-id-type="nlm-ta">mBio</journal-id><journal-id journal-id-type="iso-abbrev">MBio</journal-id><journal-id journal-id-type="hwp">mbio</journal-id><journal-id journal-id-type="pmc">mbio</journal-id><journal-id journal-id-type="publisher-id">mBio</journal-id><journal-title-group><journal-title>mBio</journal-title></journal-title-group><issn pub-type="epub">2150-7511</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">29970470</article-id><article-id pub-id-type="pmc">6030557</article-id><article-id pub-id-type="publisher-id">mBio01222-18</article-id><article-id pub-id-type="doi">10.1128/mBio.01222-18</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group></article-categories><title-group><article-title>Avian Influenza Virus PB1 Gene in H3N2 Viruses Evolved in Humans To Reduce Interferon Inhibition by Skewing Codon Usage toward Interferon-Altered tRNA Pools</article-title><alt-title alt-title-type="running-head">Avian Influenza PB1 Gene Evolution in Humans</alt-title><alt-title alt-title-type="short-authors">Smith et al.</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Smith</surname><given-names>Bartram L.</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref><xref ref-type="aff" rid="aff2"><sup>b</sup></xref></contrib><contrib contrib-type="author"><name><surname>Chen</surname><given-names>Guifang</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0002-7470-9261</contrib-id><name><surname>Wilke</surname><given-names>Claus O.</given-names></name><xref ref-type="aff" rid="aff2"><sup>b</sup></xref></contrib><contrib contrib-type="author" corresp="yes"><name><surname>Krug</surname><given-names>Robert M.</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><aff id="aff1"><label>a</label><addr-line>Department of Molecular Biosciences, John Ring LaMontagne Center for Infectious Disease, Institute for Cellular and Molecular Biology, the University of Texas at Austin, Austin, Texas, USA</addr-line></aff><aff id="aff2"><label>b</label><addr-line>Department of Integrative Biology, Center for Computational Biology and Bioinformatics, Institute for Cellular and Molecular Biology, the University of Texas at Austin, Austin, Texas, USA</addr-line></aff></contrib-group><contrib-group><contrib contrib-type="editor"><name><surname>Bennink</surname><given-names>Jack R.</given-names></name><role>Editor</role><aff>National Institute of Allergy and Infectious Diseases</aff></contrib></contrib-group><author-notes><corresp id="cor1">Address correspondence to Robert M. Krug, <email>rkrug@austin.utexas.edu</email>.</corresp><fn fn-type="other"><p>This article is a direct contribution from a Fellow of the American Academy of Microbiology. Solicited external reviewers: Wendy Barclay, Imperial College London; Richard Webby, St. Jude Children's Research Hospital.</p></fn></author-notes><pub-date pub-type="epub"><day>3</day><month>7</month><year>2018</year></pub-date><pub-date pub-type="collection"><season>Jul-Aug</season><year>2018</year></pub-date><volume>9</volume><issue>4</issue><elocation-id>e01222-18</elocation-id><history><date date-type="received"><day>5</day><month>6</month><year>2018</year></date><date date-type="accepted"><day>8</day><month>6</month><year>2018</year></date></history><permissions><copyright-statement>Copyright © 2018 Smith et al.</copyright-statement><copyright-year>2018</copyright-year><copyright-holder>Smith et al.</copyright-holder><license license-type="open-access" xlink:href="https://creativecommons.org/licenses/by/4.0/"><license-p>This is an open-access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="https://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution 4.0 International license</ext-link>.</license-p></license></permissions><self-uri content-type="pdf" xlink:href="mbo004183961001.pdf"></self-uri><abstract><title>ABSTRACT</title><p>Influenza A viruses cause an annual contagious respiratory disease in humans and are responsible for periodic high-mortality human pandemics. Pandemic influenza A viruses usually result from the reassortment of gene segments between human and avian influenza viruses. These avian influenza virus gene segments need to adapt to humans. Here we focus on the human adaptation of the synonymous codons of the avian influenza virus PB1 gene of the 1968 H3N2 pandemic virus. We generated recombinant H3N2 viruses differing only in codon usage of PB1 mRNA and demonstrated that codon usage of the PB1 mRNA of recent H3N2 virus isolates enhances replication in interferon (IFN)-treated human cells without affecting replication in untreated cells, thereby partially alleviating the interferon-induced antiviral state. High-throughput sequencing of tRNA pools explains the reduced inhibition of replication by interferon: the levels of some tRNAs differ between interferon-treated and untreated human cells, and evolution of the codon usage of H3N2 PB1 mRNA is skewed toward interferon-altered human tRNA pools. Consequently, the avian influenza virus-derived PB1 mRNAs of modern H3N2 viruses have acquired codon usages that better reflect tRNA availabilities in IFN-treated cells. Our results indicate that the change in tRNA availabilities resulting from interferon treatment is a previously unknown aspect of the antiviral action of interferon, which has been partially overcome by human-adapted H3N2 viruses.</p></abstract><abstract abstract-type="executive-summary"><title>IMPORTANCE</title><p>Pandemic influenza A viruses that cause high human mortality usually result from reassortment of gene segments between human and avian influenza viruses. These avian influenza virus gene segments need to adapt to humans. Here we focus on the human adaptation of the avian influenza virus PB1 gene that was incorporated into the 1968 H3N2 pandemic virus. We demonstrate that the coding sequence of the PB1 mRNA of modern H3N2 viruses enhances replication in human cells in which interferon has activated a potent antiviral state. Reduced interferon inhibition results from evolution of PB1 mRNA codons skewed toward the pools of tRNAs in interferon-treated human cells, which, as shown here, differ significantly from the tRNA pools in untreated human cells. Consequently, avian influenza virus-derived PB1 mRNAs of modern H3N2 viruses have acquired codon usages that better reflect tRNA availabilities in IFN-treated cells and are translated more efficiently.</p></abstract><kwd-group><title>KEYWORDS</title><kwd>codon usage</kwd><kwd>evolution</kwd><kwd>influenza A virus</kwd><kwd>influenza PB1 protein</kwd><kwd>interferon</kwd></kwd-group><funding-group><award-group id="award1"><funding-source><institution-wrap><institution>HHS | National Institutes of Health (NIH)</institution><institution-id>https://doi.org/10.13039/100000002</institution-id></institution-wrap></funding-source><award-id>AI11772</award-id><principal-award-recipient><name><surname>Krug</surname><given-names>Robert M.</given-names></name></principal-award-recipient></award-group><award-group id="award2"><funding-source><institution-wrap><institution>HHS | National Institutes of Health (NIH)</institution><institution-id>https://doi.org/10.13039/100000002</institution-id></institution-wrap></funding-source><award-id>GM088344</award-id><principal-award-recipient><name><surname>Wilke</surname><given-names>Claus O.</given-names></name></principal-award-recipient></award-group></funding-group><counts><count count="4" count-type="supplementary-material"></count><fig-count count="6"></fig-count><table-count count="0"></table-count><equation-count count="0"></equation-count><ref-count count="39"></ref-count><page-count count="14"></page-count><word-count count="8937"></word-count></counts><custom-meta-group><custom-meta><meta-name>cover-date</meta-name><meta-value>July/August 2018</meta-value></custom-meta></custom-meta-group></article-meta></front></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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