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 : 000014 ( 1968/Analysis ); précédent : 000013; suivant : 000015Avian 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
Affiliations:
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PMC:6030557Le document en format XML
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Smith</name><affiliation wicri:level="4"><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><placeName><region type="state">Texas</region><settlement type="city">Austin (Texas)</settlement></placeName><orgName type="university">Université du Texas à Austin</orgName></affiliation><affiliation wicri:level="4"><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><placeName><region type="state">Texas</region><settlement type="city">Austin (Texas)</settlement></placeName><orgName type="university">Université du Texas à Austin</orgName></affiliation></author><author><name sortKey="Chen, Guifang" sort="Chen, Guifang" uniqKey="Chen G" first="Guifang" last="Chen">Guifang Chen</name><affiliation wicri:level="4"><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><placeName><region type="state">Texas</region><settlement type="city">Austin (Texas)</settlement></placeName><orgName type="university">Université du Texas à Austin</orgName></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="4"><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><placeName><region type="state">Texas</region><settlement type="city">Austin (Texas)</settlement></placeName><orgName type="university">Université du Texas à Austin</orgName></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="4"><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><placeName><region type="state">Texas</region><settlement type="city">Austin (Texas)</settlement></placeName><orgName type="university">Université du Texas à Austin</orgName></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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Lebleu</name></author><author><name sortKey="Rebello, Ma" uniqKey="Rebello M">MA Rebello</name></author><author><name sortKey="Lengyel, P" uniqKey="Lengyel P">P Lengyel</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Takeda, Mp" uniqKey="Takeda M">MP Takeda</name></author><author><name sortKey="Pekosz, A" uniqKey="Pekosz A">A Pekosz</name></author><author><name sortKey="Shuck, K" uniqKey="Shuck K">K Shuck</name></author><author><name sortKey="Pinto, Lh" uniqKey="Pinto L">LH Pinto</name></author><author><name sortKey="Lamb, Ra" uniqKey="Lamb R">RA Lamb</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Twu, Ky" uniqKey="Twu K">KY Twu</name></author><author><name sortKey="Noah, Dl" uniqKey="Noah D">DL Noah</name></author><author><name sortKey="Rao, P" uniqKey="Rao P">P Rao</name></author><author><name sortKey="Kuo, Rl" uniqKey="Kuo R">RL Kuo</name></author><author><name sortKey="Krug, Rm" uniqKey="Krug R">RM Krug</name></author></analytic></biblStruct></listBibl></div1></back></TEI><affiliations><list><country><li>États-Unis</li></country><region><li>Texas</li></region><settlement><li>Austin (Texas)</li></settlement><orgName><li>Université du Texas à Austin</li></orgName></list><tree><country name="États-Unis"><region name="Texas"><name sortKey="Smith, Bartram L" sort="Smith, Bartram L" uniqKey="Smith B" first="Bartram L." last="Smith">Bartram L. Smith</name></region><name sortKey="Chen, Guifang" sort="Chen, Guifang" uniqKey="Chen G" first="Guifang" last="Chen">Guifang Chen</name><name sortKey="Krug, Robert M" sort="Krug, Robert M" uniqKey="Krug R" first="Robert M." last="Krug">Robert M. Krug</name><name sortKey="Smith, Bartram L" sort="Smith, Bartram L" uniqKey="Smith B" first="Bartram L." last="Smith">Bartram L. Smith</name><name sortKey="Wilke, Claus O" sort="Wilke, Claus O" uniqKey="Wilke C" first="Claus O." last="Wilke">Claus O. Wilke</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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