Effects of PB1-F2 on the pathogenicity of H1N1 swine influenza virus in mice and pigs
Identifieur interne : 000627 ( Pmc/Corpus ); précédent : 000626; suivant : 000628Effects 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.
Url:
DOI: 10.1099/jgv.0.000695
PubMed: 28008819
PubMed Central: 5797944
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PMC:5797944Le document en format XML
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<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>
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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 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>
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<issn pub-type="epub">1465-2099</issn>
<publisher><publisher-name>Microbiology Society</publisher-name>
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<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 . </pmc-comment>
<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>
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<kwd>pathogenicity</kwd>
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<funding-group><award-group><funding-source id="sp1">Kansas State University</funding-source>
<award-id rid="sp1">SRO# 001</award-id>
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<award-group><funding-source id="sp2">NIAID funded Center of Excellence for Influenza Research and Surveillance</funding-source>
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