Effects of PB1-F2 on the pathogenicity of H1N1 swine influenza virus in mice and pigs
Identifieur interne : 000245 ( Pmc/Checkpoint ); précédent : 000244; suivant : 000246Effects of PB1-F2 on the pathogenicity of H1N1 swine influenza virus in mice and pigs
Auteurs : Jinhwa Lee ; Jamie Henningson ; Jingjiao Ma ; Michael Duff ; Yuekun Lang ; Yonghai Li ; Yuhao Li ; Abdou Nagy ; Sunyoung Sunwoo ; Bhupinder Bawa ; Jianmei Yang ; Dingping Bai ; Juergen A. Richt ; Wenjun MaSource :
- The Journal of General Virology [ 0022-1317 ] ; 2017.
Abstract
Although several studies have exploited the effects of PB1-F2 in swine influenza viruses, its contribution to the pathogenicity of swine influenza viruses remains unclear. Herein, we investigated the effects of PB1-F2 on the pathogenicity of influenza virus using a virulent H1N1 A/swine/Kansas/77778/2007 (KS07) virus, which expresses a full-length PB1-F2, in mice and pigs. Using reverse genetics, we generated the wild-type KS07 (KS07_WT), a PB1-F2 knockout mutant (KS07_K/O) and its N66S variant (KS07_N66S). KS07_K/O showed similar pathogenicity in mice to the KS07_WT, whereas KS07_N66S displayed enhanced virulence when compared to the other two viruses. KS07_WT exhibited more efficient replication in lungs and nasal shedding in infected pigs than the other two viruses. Pigs infected with the KS07_WT had higher pulmonary levels of granulocyte-macrophage colony-stimulating factor, IFN-γ, IL-6 and IL-8 at 3 and 5 days post-infection, as well as lower levels of IL-2, IL-4 and IL-12 at 1 day post-infection compared to those infected with the KS07_K/O. These results indicate that PB1-F2 modulates KS07 H1N1 virus replication, pathogenicity and innate immune responses in pigs and the single substitution at position 66 (N/S) in the PB1-F2 plays a critical role in virulence in mice. Taken together, our results provide new insights into the effects of PB1-F2 on the virulence of influenza virus in swine and support PB1-F2 as a virulence factor of influenza A virus in a strain- and host-dependent manner.
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DOI: 10.1099/jgv.0.000695
PubMed: 28008819
PubMed Central: 5797944
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Richt</name><affiliation><nlm:aff id="aff1"></nlm:aff></affiliation></author><author><name sortKey="Ma, Wenjun" sort="Ma, Wenjun" uniqKey="Ma W" first="Wenjun" last="Ma">Wenjun Ma</name><affiliation><nlm:aff id="aff1"></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">28008819</idno><idno type="pmc">5797944</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5797944</idno><idno type="RBID">PMC:5797944</idno><idno type="doi">10.1099/jgv.0.000695</idno><date when="2017">2017</date><idno type="wicri:Area/Pmc/Corpus">000627</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000627</idno><idno type="wicri:Area/Pmc/Curation">000627</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">000627</idno><idno type="wicri:Area/Pmc/Checkpoint">000245</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Checkpoint">000245</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Effects of PB1-F2 on the pathogenicity of H1N1 swine influenza virus in mice and pigs</title><author><name sortKey="Lee, Jinhwa" sort="Lee, Jinhwa" uniqKey="Lee J" first="Jinhwa" last="Lee">Jinhwa Lee</name><affiliation><nlm:aff id="aff1"></nlm:aff></affiliation></author><author><name sortKey="Henningson, Jamie" sort="Henningson, Jamie" uniqKey="Henningson J" first="Jamie" last="Henningson">Jamie Henningson</name><affiliation><nlm:aff id="aff1"></nlm:aff></affiliation></author><author><name sortKey="Ma, Jingjiao" sort="Ma, Jingjiao" uniqKey="Ma J" first="Jingjiao" last="Ma">Jingjiao Ma</name><affiliation><nlm:aff id="aff1"></nlm:aff></affiliation></author><author><name sortKey="Duff, Michael" sort="Duff, Michael" uniqKey="Duff M" first="Michael" last="Duff">Michael Duff</name><affiliation><nlm:aff id="aff1"></nlm:aff></affiliation></author><author><name sortKey="Lang, Yuekun" sort="Lang, Yuekun" uniqKey="Lang Y" first="Yuekun" last="Lang">Yuekun Lang</name><affiliation><nlm:aff id="aff1"></nlm:aff></affiliation></author><author><name sortKey="Li, Yonghai" sort="Li, Yonghai" uniqKey="Li Y" first="Yonghai" last="Li">Yonghai Li</name><affiliation><nlm:aff id="aff1"></nlm:aff></affiliation></author><author><name sortKey="Li, Yuhao" sort="Li, Yuhao" uniqKey="Li Y" first="Yuhao" last="Li">Yuhao Li</name><affiliation><nlm:aff id="aff1"></nlm:aff></affiliation></author><author><name sortKey="Nagy, Abdou" sort="Nagy, Abdou" uniqKey="Nagy A" first="Abdou" last="Nagy">Abdou Nagy</name><affiliation><nlm:aff id="aff1"></nlm:aff></affiliation><affiliation><nlm:aff id="aff4"></nlm:aff></affiliation></author><author><name sortKey="Sunwoo, Sunyoung" sort="Sunwoo, Sunyoung" uniqKey="Sunwoo S" first="Sunyoung" last="Sunwoo">Sunyoung Sunwoo</name><affiliation><nlm:aff id="aff1"></nlm:aff></affiliation></author><author><name sortKey="Bawa, Bhupinder" sort="Bawa, Bhupinder" uniqKey="Bawa B" first="Bhupinder" last="Bawa">Bhupinder Bawa</name><affiliation><nlm:aff id="aff1"></nlm:aff></affiliation></author><author><name sortKey="Yang, Jianmei" sort="Yang, Jianmei" uniqKey="Yang J" first="Jianmei" last="Yang">Jianmei Yang</name><affiliation><nlm:aff id="aff1"></nlm:aff></affiliation><affiliation><nlm:aff id="aff2"></nlm:aff></affiliation></author><author><name sortKey="Bai, Dingping" sort="Bai, Dingping" uniqKey="Bai D" first="Dingping" last="Bai">Dingping Bai</name><affiliation><nlm:aff id="aff1"></nlm:aff></affiliation><affiliation><nlm:aff id="aff3"></nlm:aff></affiliation></author><author><name sortKey="Richt, Juergen A" sort="Richt, Juergen A" uniqKey="Richt J" first="Juergen A." last="Richt">Juergen A. Richt</name><affiliation><nlm:aff id="aff1"></nlm:aff></affiliation></author><author><name sortKey="Ma, Wenjun" sort="Ma, Wenjun" uniqKey="Ma W" first="Wenjun" last="Ma">Wenjun Ma</name><affiliation><nlm:aff id="aff1"></nlm:aff></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="2017">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Although several studies have exploited the effects of PB1-F2 in swine influenza viruses, its contribution to the pathogenicity of swine influenza viruses remains unclear. Herein, we investigated the effects of PB1-F2 on the pathogenicity of influenza virus using a virulent H1N1 A/swine/Kansas/77778/2007 (KS07) virus, which expresses a full-length PB1-F2, in mice and pigs. Using reverse genetics, we generated the wild-type KS07 (KS07_WT), a PB1-F2 knockout mutant (KS07_K/O) and its N66S variant (KS07_N66S). KS07_K/O showed similar pathogenicity in mice to the KS07_WT, whereas KS07_N66S displayed enhanced virulence when compared to the other two viruses. KS07_WT exhibited more efficient replication in lungs and nasal shedding in infected pigs than the other two viruses. Pigs infected with the KS07_WT had higher pulmonary levels of granulocyte-macrophage colony-stimulating factor, IFN-γ, IL-6 and IL-8 at 3 and 5 days post-infection, as well as lower levels of IL-2, IL-4 and IL-12 at 1 day post-infection compared to those infected with the KS07_K/O. These results indicate that PB1-F2 modulates KS07 H1N1 virus replication, pathogenicity and innate immune responses in pigs and the single substitution at position 66 (N/S) in the PB1-F2 plays a critical role in virulence in mice. Taken together, our results provide new insights into the effects of PB1-F2 on the virulence of influenza virus in swine and support PB1-F2 as a virulence factor of influenza A virus in a strain- and host-dependent manner.</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-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>Microbiology Society</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">28008819</article-id><article-id pub-id-type="pmc">5797944</article-id><article-id pub-id-type="publisher-id">000695</article-id><article-id pub-id-type="doi">10.1099/jgv.0.000695</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject><subj-group subj-group-type="heading"><subject>Animal</subject><subj-group subj-group-type="heading"><subject>Negative-strand RNA Viruses</subject></subj-group></subj-group></subj-group></article-categories><title-group><article-title>Effects of PB1-F2 on the pathogenicity of H1N1 swine influenza virus in mice and pigs</article-title><alt-title alt-title-type="recto-page-foot"><ext-link ext-link-type="uri" xlink:href="http://jgv.microbiologyresearch.org">http://jgv.microbiologyresearch.org</ext-link></alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Lee</surname><given-names>Jinhwa</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Henningson</surname><given-names>Jamie</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Ma</surname><given-names>Jingjiao</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Duff</surname><given-names>Michael</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Lang</surname><given-names>Yuekun</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Li</surname><given-names>Yonghai</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Li</surname><given-names>Yuhao</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Nagy</surname><given-names>Abdou</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff4"><sup>†</sup></xref></contrib><contrib contrib-type="author"><name><surname>Sunwoo</surname><given-names>Sunyoung</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Bawa</surname><given-names>Bhupinder</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Yang</surname><given-names>Jianmei</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"><name><surname>Bai</surname><given-names>Dingping</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff3"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Richt</surname><given-names>Juergen A.</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author" corresp="yes"><name><surname>Ma</surname><given-names>Wenjun</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="corresp" rid="cor1"></xref></contrib><aff id="aff1"><label><sup>1</sup></label><institution>Department of Diagnostic Medicine/Pathobiology, Kansas State University</institution>,<addr-line>Manhattan, KS</addr-line>,<country>USA</country></aff><aff id="aff2"><label><sup>2</sup></label><institution>Innovation Team for Pathogen Ecology Research on Animal Influenza Virus, Department of Avian Infectious Disease, Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences</institution>,<addr-line>Shanghai</addr-line>,<country>PR China</country></aff><aff id="aff3"><label><sup>3</sup></label><institution>School of Animal Science, Fujian Agriculture and Forestry University</institution>,<addr-line>Fuzhou</addr-line>,<country>PR China</country></aff><aff id="aff4"><label><sup>†</sup></label>Present address: Department of Virology, Faculty of Veterinary Medicine, Zagazig University, Zagazig 44519, Egypt.</aff></contrib-group><author-notes><corresp id="cor1"><bold>*Correspondence:</bold> Wenjun Ma, <email xlink:href="wma@vet.k-state.edu">wma@vet.k-state.edu</email></corresp></author-notes><pub-date pub-type="ppub"><month>1</month><year>2017</year></pub-date><pub-date pub-type="epub"><day>20</day><month>2</month><year>2017</year></pub-date><pub-date pub-type="pmc-release"><day>20</day><month>2</month><year>2017</year></pub-date><pmc-comment> PMC Release delay is 0 months and 0 days and was based on the
<volume>98</volume><issue>1</issue><fpage>31</fpage><lpage>42</lpage><history><date date-type="received"><day>09</day><month>10</month><year>2016</year></date><date date-type="accepted"><day>22</day><month>12</month><year>2016</year></date></history><permissions><copyright-statement>© 2017 The Authors</copyright-statement><copyright-year>2017</copyright-year></permissions><self-uri xlink:title="pdf" xlink:type="simple" xlink:href="jgv-98-31.pdf"></self-uri><abstract><p>Although several studies have exploited the effects of PB1-F2 in swine influenza viruses, its contribution to the pathogenicity of swine influenza viruses remains unclear. Herein, we investigated the effects of PB1-F2 on the pathogenicity of influenza virus using a virulent H1N1 A/swine/Kansas/77778/2007 (KS07) virus, which expresses a full-length PB1-F2, in mice and pigs. Using reverse genetics, we generated the wild-type KS07 (KS07_WT), a PB1-F2 knockout mutant (KS07_K/O) and its N66S variant (KS07_N66S). KS07_K/O showed similar pathogenicity in mice to the KS07_WT, whereas KS07_N66S displayed enhanced virulence when compared to the other two viruses. KS07_WT exhibited more efficient replication in lungs and nasal shedding in infected pigs than the other two viruses. Pigs infected with the KS07_WT had higher pulmonary levels of granulocyte-macrophage colony-stimulating factor, IFN-γ, IL-6 and IL-8 at 3 and 5 days post-infection, as well as lower levels of IL-2, IL-4 and IL-12 at 1 day post-infection compared to those infected with the KS07_K/O. These results indicate that PB1-F2 modulates KS07 H1N1 virus replication, pathogenicity and innate immune responses in pigs and the single substitution at position 66 (N/S) in the PB1-F2 plays a critical role in virulence in mice. Taken together, our results provide new insights into the effects of PB1-F2 on the virulence of influenza virus in swine and support PB1-F2 as a virulence factor of influenza A virus in a strain- and host-dependent manner.</p></abstract><kwd-group><kwd>PB1-F2</kwd><kwd>swine influenza H1N1 virus</kwd><kwd>pathogenicity</kwd><kwd>mouse and pig</kwd></kwd-group><funding-group><award-group><funding-source id="sp1">Kansas State University</funding-source><award-id rid="sp1">SRO# 001</award-id></award-group><award-group><funding-source id="sp2">NIAID funded Center of Excellence for Influenza Research and Surveillance</funding-source><award-id rid="sp2">HHSN266200700006C</award-id></award-group></funding-group><custom-meta-group><custom-meta><meta-name>OpenAccessEmbargo</meta-name><meta-value>12</meta-value></custom-meta></custom-meta-group></article-meta></front></pmc><affiliations><list></list><tree><noCountry><name sortKey="Bai, Dingping" sort="Bai, Dingping" uniqKey="Bai D" first="Dingping" last="Bai">Dingping Bai</name><name sortKey="Bawa, Bhupinder" sort="Bawa, Bhupinder" uniqKey="Bawa B" first="Bhupinder" last="Bawa">Bhupinder Bawa</name><name sortKey="Duff, Michael" sort="Duff, Michael" uniqKey="Duff M" first="Michael" last="Duff">Michael Duff</name><name sortKey="Henningson, Jamie" sort="Henningson, Jamie" uniqKey="Henningson J" first="Jamie" last="Henningson">Jamie Henningson</name><name sortKey="Lang, Yuekun" sort="Lang, Yuekun" uniqKey="Lang Y" first="Yuekun" last="Lang">Yuekun Lang</name><name sortKey="Lee, Jinhwa" sort="Lee, Jinhwa" uniqKey="Lee J" first="Jinhwa" last="Lee">Jinhwa Lee</name><name sortKey="Li, Yonghai" sort="Li, Yonghai" uniqKey="Li Y" first="Yonghai" last="Li">Yonghai Li</name><name sortKey="Li, Yuhao" sort="Li, Yuhao" uniqKey="Li Y" first="Yuhao" last="Li">Yuhao Li</name><name sortKey="Ma, Jingjiao" sort="Ma, Jingjiao" uniqKey="Ma J" first="Jingjiao" last="Ma">Jingjiao Ma</name><name sortKey="Ma, Wenjun" sort="Ma, Wenjun" uniqKey="Ma W" first="Wenjun" last="Ma">Wenjun Ma</name><name sortKey="Nagy, Abdou" sort="Nagy, Abdou" uniqKey="Nagy A" first="Abdou" last="Nagy">Abdou Nagy</name><name sortKey="Richt, Juergen A" sort="Richt, Juergen A" uniqKey="Richt J" first="Juergen A." last="Richt">Juergen A. Richt</name><name sortKey="Sunwoo, Sunyoung" sort="Sunwoo, Sunyoung" uniqKey="Sunwoo S" first="Sunyoung" last="Sunwoo">Sunyoung Sunwoo</name><name sortKey="Yang, Jianmei" sort="Yang, Jianmei" uniqKey="Yang J" first="Jianmei" last="Yang">Jianmei Yang</name></noCountry></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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