Strain-dependent effects of PB1-F2 of triple-reassortant H3N2 influenza viruses in swine
Identifieur interne : 000793 ( Ncbi/Merge ); précédent : 000792; suivant : 000794Strain-dependent effects of PB1-F2 of triple-reassortant H3N2 influenza viruses in swine
Auteurs : Lindomar Pena [États-Unis] ; Amy L. Vincent [États-Unis] ; Crystal L. Loving [États-Unis] ; Jamie N. Henningson [États-Unis] ; Kelly M. Lager [États-Unis] ; Weizhong Li [États-Unis] ; Daniel R. Perez [États-Unis]Source :
- The Journal of General Virology [ 0022-1317 ] ; 2012.
Abstract
The PB1-F2 protein of the influenza A viruses (IAVs) can act as a virulence factor in mice. Its contribution to the virulence of IAV in swine, however, remains largely unexplored. In this study, we chose two genetically related H3N2 triple-reassortant IAVs to assess the impact of PB1-F2 in virus replication and virulence in pigs. Using reverse genetics, we disrupted the PB1-F2 ORF of A/swine/Wisconsin/14094/99 (H3N2) (Sw/99) and A/turkey/Ohio/313053/04 (H3N2) (Ty/04). Removing the PB1-F2 ORF led to increased expression of PB1-N40 in a strain-dependent manner. Ablation of the PB1-F2 ORF (or incorporation of the N66S mutation in the PB1-F2 ORF, Sw/99 N66S) affected the replication in porcine alveolar macrophages of only the Sw/99 KO (PB1-F2 knockout) and Sw/99 N66S variants. The Ty/04 KO strain showed decreased virus replication in swine respiratory explants, whereas no such effect was observed in Sw/99 KO, compared with the wild-type (WT) counterparts. In pigs, PB1-F2 did not affect virus shedding or viral load in the lungs for any of these strains. Upon necropsy, PB1-F2 had no effect on the lung pathology caused by Sw/99 variants. Interestingly, the Ty/04 KO-infected pigs showed significantly increased lung pathology at 3 days post-infection compared with pigs infected with the Ty/04 WT strain. In addition, the pulmonary levels of interleukin (IL)-6, IL-8 and gamma interferon were regulated differentially by the expression of PB1-F2. Taken together, these results indicate that PB1-F2 modulates virus replication, virulence and innate immune responses in pigs in a strain-dependent fashion.
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DOI: 10.1099/vir.0.045005-0
PubMed: 22815274
PubMed Central: 3541787
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Vincent</name><affiliation wicri:level="2"><nlm:aff id="aff3">Virus and Prion Diseases of Livestock Research Unit, National Animal Disease Center, USDA-ARS, Ames, IA, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Virus and Prion Diseases of Livestock Research Unit, National Animal Disease Center, USDA-ARS, Ames, IA</wicri:regionArea><placeName><region type="state">Iowa</region></placeName></affiliation></author><author><name sortKey="Loving, Crystal L" sort="Loving, Crystal L" uniqKey="Loving C" first="Crystal L." last="Loving">Crystal L. Loving</name><affiliation wicri:level="2"><nlm:aff id="aff3">Virus and Prion Diseases of Livestock Research Unit, National Animal Disease Center, USDA-ARS, Ames, IA, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Virus and Prion Diseases of Livestock Research Unit, National Animal Disease Center, USDA-ARS, Ames, IA</wicri:regionArea><placeName><region type="state">Iowa</region></placeName></affiliation></author><author><name sortKey="Henningson, Jamie N" sort="Henningson, Jamie N" uniqKey="Henningson J" first="Jamie N." last="Henningson">Jamie N. Henningson</name><affiliation wicri:level="2"><nlm:aff id="aff3">Virus and Prion Diseases of Livestock Research Unit, National Animal Disease Center, USDA-ARS, Ames, IA, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Virus and Prion Diseases of Livestock Research Unit, National Animal Disease Center, USDA-ARS, Ames, IA</wicri:regionArea><placeName><region type="state">Iowa</region></placeName></affiliation></author><author><name sortKey="Lager, Kelly M" sort="Lager, Kelly M" uniqKey="Lager K" first="Kelly M." last="Lager">Kelly M. Lager</name><affiliation wicri:level="2"><nlm:aff id="aff3">Virus and Prion Diseases of Livestock Research Unit, National Animal Disease Center, USDA-ARS, Ames, IA, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Virus and Prion Diseases of Livestock Research Unit, National Animal Disease Center, USDA-ARS, Ames, IA</wicri:regionArea><placeName><region type="state">Iowa</region></placeName></affiliation></author><author><name sortKey="Li, Weizhong" sort="Li, Weizhong" uniqKey="Li W" first="Weizhong" last="Li">Weizhong Li</name><affiliation wicri:level="4"><nlm:aff id="aff1">Department of Veterinary Medicine, University of Maryland, College Park, MD, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Veterinary Medicine, University of Maryland, College Park, MD</wicri:regionArea><placeName><region type="state">Maryland</region><settlement type="city">College Park (Maryland)</settlement></placeName><orgName type="university">Université du Maryland</orgName></affiliation><affiliation wicri:level="2"><nlm:aff id="aff2">Virginia–Maryland Regional College of Veterinary Medicine, College Park, MD, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Virginia–Maryland Regional College of Veterinary Medicine, College Park, MD</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author><author><name sortKey="Perez, Daniel R" sort="Perez, Daniel R" uniqKey="Perez D" first="Daniel R." last="Perez">Daniel R. Perez</name><affiliation wicri:level="4"><nlm:aff id="aff1">Department of Veterinary Medicine, University of Maryland, College Park, MD, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Veterinary Medicine, University of Maryland, College Park, MD</wicri:regionArea><placeName><region type="state">Maryland</region><settlement type="city">College Park (Maryland)</settlement></placeName><orgName type="university">Université du Maryland</orgName></affiliation><affiliation wicri:level="2"><nlm:aff id="aff2">Virginia–Maryland Regional College of Veterinary Medicine, College Park, MD, USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Virginia–Maryland Regional College of Veterinary Medicine, College Park, MD</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author></analytic><series><title level="j">The Journal of General Virology</title><idno type="ISSN">0022-1317</idno><idno type="eISSN">1465-2099</idno><imprint><date when="2012">2012</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>The PB1-F2 protein of the influenza A viruses (IAVs) can act as a virulence factor in mice. Its contribution to the virulence of IAV in swine, however, remains largely unexplored. In this study, we chose two genetically related H3N2 triple-reassortant IAVs to assess the impact of PB1-F2 in virus replication and virulence in pigs. Using reverse genetics, we disrupted the PB1-F2 ORF of A/swine/Wisconsin/14094/99 (H3N2) (Sw/99) and A/turkey/Ohio/313053/04 (H3N2) (Ty/04). Removing the PB1-F2 ORF led to increased expression of PB1-N40 in a strain-dependent manner. Ablation of the PB1-F2 ORF (or incorporation of the N66S mutation in the PB1-F2 ORF, Sw/99 N66S) affected the replication in porcine alveolar macrophages of only the Sw/99 KO (PB1-F2 knockout) and Sw/99 N66S variants. The Ty/04 KO strain showed decreased virus replication in swine respiratory explants, whereas no such effect was observed in Sw/99 KO, compared with the wild-type (WT) counterparts. In pigs, PB1-F2 did not affect virus shedding or viral load in the lungs for any of these strains. Upon necropsy, PB1-F2 had no effect on the lung pathology caused by Sw/99 variants. Interestingly, the Ty/04 KO-infected pigs showed significantly increased lung pathology at 3 days post-infection compared with pigs infected with the Ty/04 WT strain. In addition, the pulmonary levels of interleukin (IL)-6, IL-8 and gamma interferon were regulated differentially by the expression of PB1-F2. Taken together, these results indicate that PB1-F2 modulates virus replication, virulence and innate immune responses in pigs in a strain-dependent fashion.</p></div></front></TEI><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 Gen Virol</journal-id><journal-id journal-id-type="iso-abbrev">J. Gen. Virol</journal-id><journal-id journal-id-type="publisher-id">JGV</journal-id><journal-id journal-id-type="hwp">vir</journal-id><journal-title-group><journal-title>The Journal of General Virology</journal-title></journal-title-group><issn pub-type="ppub">0022-1317</issn><issn pub-type="epub">1465-2099</issn><publisher><publisher-name>Society for General Microbiology</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">22815274</article-id><article-id pub-id-type="pmc">3541787</article-id><article-id pub-id-type="publisher-id">045005</article-id><article-id pub-id-type="doi">10.1099/vir.0.045005-0</article-id><article-categories><subj-group subj-group-type="article-type"><subject>Standard</subject></subj-group><subj-group subj-group-type="heading"><subject>Animal</subject><subj-group subj-group-type="heading"><subject>RNA viruses</subject></subj-group></subj-group></article-categories><title-group><article-title>Strain-dependent effects of PB1-F2 of triple-reassortant H3N2 influenza viruses in swine</article-title><alt-title alt-title-type="recto-page-foot"><ext-link ext-link-type="uri" xlink:href="http://vir.sgmjournals.org">http://vir.sgmjournals.org</ext-link></alt-title><alt-title alt-title-type="verso-running-head">L. Pena and others</alt-title><alt-title alt-title-type="recto-running-head">Effects of influenza PB1-F2 in pigs</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Pena</surname><given-names>Lindomar</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff2"><sup>2</sup></xref></contrib><contrib contrib-type="author" corresp="yes"><name><surname>Vincent</surname><given-names>Amy L.</given-names></name><xref ref-type="aff" rid="aff3"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Loving</surname><given-names>Crystal L.</given-names></name><xref ref-type="aff" rid="aff3"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Henningson</surname><given-names>Jamie N.</given-names></name><xref ref-type="aff" rid="aff3"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Lager</surname><given-names>Kelly M.</given-names></name><xref ref-type="aff" rid="aff3"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Li</surname><given-names>Weizhong</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff2"><sup>2</sup></xref></contrib><contrib contrib-type="author" corresp="yes"><name><surname>Perez</surname><given-names>Daniel R.</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff2"><sup>2</sup></xref></contrib><aff id="aff1"><label>1</label>Department of Veterinary Medicine, University of Maryland, College Park, MD, USA</aff><aff id="aff2"><label>2</label>Virginia–Maryland Regional College of Veterinary Medicine, College Park, MD, USA</aff><aff id="aff3"><label>3</label>Virus and Prion Diseases of Livestock Research Unit, National Animal Disease Center, USDA-ARS, Ames, IA, USA</aff></contrib-group><author-notes><corresp id="cor1"><bold>Correspondence</bold> Daniel R. Perez <email xlink:href="dperez1@umd.edu">dperez1@umd.edu</email> Amy L. Vincent <email xlink:href="Amy.Vincent@ars.usda.gov">Amy.Vincent@ars.usda.gov</email></corresp></author-notes><pub-date pub-type="ppub"><month>10</month><year>2012</year></pub-date><pub-date pub-type="pmc-release"><day>1</day><month>10</month><year>2013</year></pub-date><pmc-comment> PMC Release delay is 12 months and 0 days and was based on the
<volume>93</volume><issue>Pt 10</issue><fpage>2204</fpage><lpage>2214</lpage><history><date date-type="received"><day>06</day><month>6</month><year>2012</year></date><date date-type="accepted"><day>17</day><month>7</month><year>2012</year></date></history><permissions><copyright-statement>© 2012 SGM</copyright-statement></permissions><self-uri xlink:title="pdf" xlink:type="simple" xlink:href="2204_vir045005.pdf"></self-uri><abstract><p>The PB1-F2 protein of the influenza A viruses (IAVs) can act as a virulence factor in mice. Its contribution to the virulence of IAV in swine, however, remains largely unexplored. In this study, we chose two genetically related H3N2 triple-reassortant IAVs to assess the impact of PB1-F2 in virus replication and virulence in pigs. Using reverse genetics, we disrupted the PB1-F2 ORF of A/swine/Wisconsin/14094/99 (H3N2) (Sw/99) and A/turkey/Ohio/313053/04 (H3N2) (Ty/04). Removing the PB1-F2 ORF led to increased expression of PB1-N40 in a strain-dependent manner. Ablation of the PB1-F2 ORF (or incorporation of the N66S mutation in the PB1-F2 ORF, Sw/99 N66S) affected the replication in porcine alveolar macrophages of only the Sw/99 KO (PB1-F2 knockout) and Sw/99 N66S variants. The Ty/04 KO strain showed decreased virus replication in swine respiratory explants, whereas no such effect was observed in Sw/99 KO, compared with the wild-type (WT) counterparts. In pigs, PB1-F2 did not affect virus shedding or viral load in the lungs for any of these strains. Upon necropsy, PB1-F2 had no effect on the lung pathology caused by Sw/99 variants. Interestingly, the Ty/04 KO-infected pigs showed significantly increased lung pathology at 3 days post-infection compared with pigs infected with the Ty/04 WT strain. In addition, the pulmonary levels of interleukin (IL)-6, IL-8 and gamma interferon were regulated differentially by the expression of PB1-F2. Taken together, these results indicate that PB1-F2 modulates virus replication, virulence and innate immune responses in pigs in a strain-dependent fashion.</p></abstract><funding-group><award-group><funding-source id="sp1">CDC-HHS</funding-source><award-id rid="sp1">1U01CI000355</award-id></award-group><award-group><funding-source id="sp2">NIAID-NIH</funding-source><award-id rid="sp2">R01AI052155</award-id></award-group><award-group><funding-source id="sp3">CSREES-USDA</funding-source><award-id rid="sp3">2005-05523</award-id></award-group><award-group><funding-source id="sp4">NIAID-NIH</funding-source><award-id rid="sp4">HHSN266200700010C</award-id></award-group><award-group><funding-source id="sp5">USDA-ARS</funding-source></award-group></funding-group><custom-meta-group><custom-meta><meta-name>CopyEditor</meta-name><meta-value>Natalie Wilder</meta-value></custom-meta><custom-meta><meta-name>Disc-work</meta-name><meta-value>Sarah Ferris</meta-value></custom-meta><custom-meta><meta-name>openaccess</meta-name><meta-value>free</meta-value></custom-meta><custom-meta><meta-name>OpenAccessEmbargo</meta-name><meta-value>12</meta-value></custom-meta></custom-meta-group></article-meta></front></pmc><affiliations><list><country><li>États-Unis</li></country><region><li>Iowa</li><li>Maryland</li></region><settlement><li>College Park (Maryland)</li></settlement><orgName><li>Université du Maryland</li></orgName></list><tree><country name="États-Unis"><region name="Maryland"><name sortKey="Pena, Lindomar" sort="Pena, Lindomar" uniqKey="Pena L" first="Lindomar" last="Pena">Lindomar Pena</name></region><name sortKey="Henningson, Jamie N" sort="Henningson, Jamie N" uniqKey="Henningson J" first="Jamie N." last="Henningson">Jamie N. Henningson</name><name sortKey="Lager, Kelly M" sort="Lager, Kelly M" uniqKey="Lager K" first="Kelly M." last="Lager">Kelly M. Lager</name><name sortKey="Li, Weizhong" sort="Li, Weizhong" uniqKey="Li W" first="Weizhong" last="Li">Weizhong Li</name><name sortKey="Li, Weizhong" sort="Li, Weizhong" uniqKey="Li W" first="Weizhong" last="Li">Weizhong Li</name><name sortKey="Loving, Crystal L" sort="Loving, Crystal L" uniqKey="Loving C" first="Crystal L." last="Loving">Crystal L. Loving</name><name sortKey="Pena, Lindomar" sort="Pena, Lindomar" uniqKey="Pena L" first="Lindomar" last="Pena">Lindomar Pena</name><name sortKey="Perez, Daniel R" sort="Perez, Daniel R" uniqKey="Perez D" first="Daniel R." last="Perez">Daniel R. Perez</name><name sortKey="Perez, Daniel R" sort="Perez, Daniel R" uniqKey="Perez D" first="Daniel R." last="Perez">Daniel R. Perez</name><name sortKey="Vincent, Amy L" sort="Vincent, Amy L" uniqKey="Vincent A" first="Amy L." last="Vincent">Amy L. Vincent</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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