Antagonism of STAT1 by Nipah virus P gene products modulates disease course but not lethal outcome in the ferret model
Identifieur interne : 000193 ( Pmc/Curation ); précédent : 000192; suivant : 000194Antagonism of STAT1 by Nipah virus P gene products modulates disease course but not lethal outcome in the ferret model
Auteurs : Benjamin A. Satterfield [États-Unis] ; Viktoriya Borisevich [États-Unis] ; Stephanie L. Foster [États-Unis] ; Sergio E. Rodriguez [États-Unis] ; Robert W. Cross [États-Unis] ; Karla A. Fenton [États-Unis] ; Krystle N. Agans [États-Unis] ; Christopher F. Basler [États-Unis] ; Thomas W. Geisbert [États-Unis] ; Chad E. Mire [États-Unis]Source :
- Scientific Reports [ 2045-2322 ] ; 2019.
Abstract
Nipah virus (NiV) is a pathogenic paramyxovirus and zoononis with very high human fatality rates. Previous protein over-expression studies have shown that various mutations to the common N-terminal STAT1-binding motif of the NiV P, V, and W proteins affected the STAT1-binding ability of these proteins thus interfering with he JAK/STAT pathway and reducing their ability to inhibit type-I IFN signaling, but due to differing techniques it was unclear which amino acids were most important in this interaction or what impact this had on pathogenesis
Url:
DOI: 10.1038/s41598-019-53037-0
PubMed: 31723221
PubMed Central: 6853903
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Antagonism of STAT1 by Nipah virus P gene products modulates disease course but not lethal outcome in the ferret model</title>
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<series><title level="j">Scientific Reports</title>
<idno type="eISSN">2045-2322</idno>
<imprint><date when="2019">2019</date>
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<front><div type="abstract" xml:lang="en"><p id="Par1">Nipah virus (NiV) is a pathogenic paramyxovirus and zoononis with very high human fatality rates. Previous protein over-expression studies have shown that various mutations to the common N-terminal STAT1-binding motif of the NiV P, V, and W proteins affected the STAT1-binding ability of these proteins thus interfering with he JAK/STAT pathway and reducing their ability to inhibit type-I IFN signaling, but due to differing techniques it was unclear which amino acids were most important in this interaction or what impact this had on pathogenesis <italic>in vivo</italic>
. We compared all previously described mutations in parallel and found the amino acid mutation Y116E demonstrated the greatest reduction in binding to STAT1 and the greatest reduction in interferon antagonism. A similar reduction in binding and activity was seen for a deletion of twenty amino acids constituting the described STAT1-binding domain. To investigate the contribution of this STAT1-binding motif in NiV-mediated disease, we produced rNiVs with complete deletion of the STAT1-binding motif or the Y116E mutation for ferret challenge studies (rNiV<sub>M</sub>
-STAT1<sup>blind</sup>
). Despite the reduced IFN inhibitory function, ferrets challenged with these rNiV<sub>M</sub>
-STAT1<sup>blind</sup>
mutants had a lethal, albeit altered, NiV-mediated disease course. These data, together with our previously published data, suggest that the major role of NiV P, V, and W in NiV-mediated disease in the ferret model are likely to be in the inhibition of viral recognition/innate immune signaling induction with a minor role for inhibition of IFN signaling.</p>
</div>
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<front><journal-meta><journal-id journal-id-type="nlm-ta">Sci Rep</journal-id>
<journal-id journal-id-type="iso-abbrev">Sci Rep</journal-id>
<journal-title-group><journal-title>Scientific Reports</journal-title>
</journal-title-group>
<issn pub-type="epub">2045-2322</issn>
<publisher><publisher-name>Nature Publishing Group UK</publisher-name>
<publisher-loc>London</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">31723221</article-id>
<article-id pub-id-type="pmc">6853903</article-id>
<article-id pub-id-type="publisher-id">53037</article-id>
<article-id pub-id-type="doi">10.1038/s41598-019-53037-0</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>Antagonism of STAT1 by Nipah virus P gene products modulates disease course but not lethal outcome in the ferret model</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Satterfield</surname>
<given-names>Benjamin A.</given-names>
</name>
<xref ref-type="aff" rid="Aff1">1</xref>
<xref ref-type="aff" rid="Aff2">2</xref>
<xref ref-type="aff" rid="Aff3">3</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Borisevich</surname>
<given-names>Viktoriya</given-names>
</name>
<xref ref-type="aff" rid="Aff1">1</xref>
<xref ref-type="aff" rid="Aff2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Foster</surname>
<given-names>Stephanie L.</given-names>
</name>
<xref ref-type="aff" rid="Aff1">1</xref>
<xref ref-type="aff" rid="Aff2">2</xref>
</contrib>
<contrib contrib-type="author"><contrib-id contrib-id-type="orcid">http://orcid.org/0000-0003-4149-7458</contrib-id>
<name><surname>Rodriguez</surname>
<given-names>Sergio E.</given-names>
</name>
<xref ref-type="aff" rid="Aff1">1</xref>
<xref ref-type="aff" rid="Aff2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Cross</surname>
<given-names>Robert W.</given-names>
</name>
<xref ref-type="aff" rid="Aff1">1</xref>
<xref ref-type="aff" rid="Aff2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Fenton</surname>
<given-names>Karla A.</given-names>
</name>
<xref ref-type="aff" rid="Aff1">1</xref>
<xref ref-type="aff" rid="Aff2">2</xref>
</contrib>
<contrib contrib-type="author"><contrib-id contrib-id-type="orcid">http://orcid.org/0000-0002-7319-6935</contrib-id>
<name><surname>Agans</surname>
<given-names>Krystle N.</given-names>
</name>
<xref ref-type="aff" rid="Aff1">1</xref>
<xref ref-type="aff" rid="Aff2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Basler</surname>
<given-names>Christopher F.</given-names>
</name>
<xref ref-type="aff" rid="Aff4">4</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Geisbert</surname>
<given-names>Thomas W.</given-names>
</name>
<xref ref-type="aff" rid="Aff1">1</xref>
<xref ref-type="aff" rid="Aff2">2</xref>
</contrib>
<contrib contrib-type="author" corresp="yes"><contrib-id contrib-id-type="orcid">http://orcid.org/0000-0001-7596-1808</contrib-id>
<name><surname>Mire</surname>
<given-names>Chad E.</given-names>
</name>
<address><email>chmire@utmb.edu</email>
</address>
<xref ref-type="aff" rid="Aff1">1</xref>
<xref ref-type="aff" rid="Aff2">2</xref>
</contrib>
<aff id="Aff1"><label>1</label>
<institution-wrap><institution-id institution-id-type="ISNI">0000 0001 1547 9964</institution-id>
<institution-id institution-id-type="GRID">grid.176731.5</institution-id>
<institution>Galveston National Laboratory,</institution>
<institution>University of Texas Medical Branch,</institution>
</institution-wrap>
Galveston, TX USA</aff>
<aff id="Aff2"><label>2</label>
<institution-wrap><institution-id institution-id-type="ISNI">0000 0001 1547 9964</institution-id>
<institution-id institution-id-type="GRID">grid.176731.5</institution-id>
<institution>Department of Microbiology and Immunology,</institution>
<institution>University of Texas Medical Branch,</institution>
</institution-wrap>
Galveston, TX USA</aff>
<aff id="Aff3"><label>3</label>
<institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0459 167X</institution-id>
<institution-id institution-id-type="GRID">grid.66875.3a</institution-id>
<institution>Mayo Clinic, Department of Medicine,</institution>
</institution-wrap>
Rochester, MN USA</aff>
<aff id="Aff4"><label>4</label>
<institution-wrap><institution-id institution-id-type="ISNI">0000 0004 1936 7400</institution-id>
<institution-id institution-id-type="GRID">grid.256304.6</institution-id>
<institution>Center for Microbial Pathogenesis,</institution>
<institution>Institute for Biomedical Sciences, Georgia State University,</institution>
</institution-wrap>
Atlanta, GA USA</aff>
</contrib-group>
<pub-date pub-type="epub"><day>13</day>
<month>11</month>
<year>2019</year>
</pub-date>
<pub-date pub-type="pmc-release"><day>13</day>
<month>11</month>
<year>2019</year>
</pub-date>
<pub-date pub-type="collection"><year>2019</year>
</pub-date>
<volume>9</volume>
<elocation-id>16710</elocation-id>
<history><date date-type="received"><day>9</day>
<month>11</month>
<year>2018</year>
</date>
<date date-type="accepted"><day>22</day>
<month>10</month>
<year>2019</year>
</date>
</history>
<permissions><copyright-statement>© The Author(s) 2019</copyright-statement>
<license license-type="OpenAccess"><license-p><bold>Open Access</bold>
This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>
.</license-p>
</license>
</permissions>
<abstract id="Abs1"><p id="Par1">Nipah virus (NiV) is a pathogenic paramyxovirus and zoononis with very high human fatality rates. Previous protein over-expression studies have shown that various mutations to the common N-terminal STAT1-binding motif of the NiV P, V, and W proteins affected the STAT1-binding ability of these proteins thus interfering with he JAK/STAT pathway and reducing their ability to inhibit type-I IFN signaling, but due to differing techniques it was unclear which amino acids were most important in this interaction or what impact this had on pathogenesis <italic>in vivo</italic>
. We compared all previously described mutations in parallel and found the amino acid mutation Y116E demonstrated the greatest reduction in binding to STAT1 and the greatest reduction in interferon antagonism. A similar reduction in binding and activity was seen for a deletion of twenty amino acids constituting the described STAT1-binding domain. To investigate the contribution of this STAT1-binding motif in NiV-mediated disease, we produced rNiVs with complete deletion of the STAT1-binding motif or the Y116E mutation for ferret challenge studies (rNiV<sub>M</sub>
-STAT1<sup>blind</sup>
). Despite the reduced IFN inhibitory function, ferrets challenged with these rNiV<sub>M</sub>
-STAT1<sup>blind</sup>
mutants had a lethal, albeit altered, NiV-mediated disease course. These data, together with our previously published data, suggest that the major role of NiV P, V, and W in NiV-mediated disease in the ferret model are likely to be in the inhibition of viral recognition/innate immune signaling induction with a minor role for inhibition of IFN signaling.</p>
</abstract>
<kwd-group kwd-group-type="npg-subject"><title>Subject terms</title>
<kwd>Microbiology</kwd>
<kwd>Viral immune evasion</kwd>
</kwd-group>
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<institution>U.S. Department of Health & Human Services | NIH | National Institute of Allergy and Infectious Diseases (NIAID)</institution>
</institution-wrap>
</funding-source>
<award-id>UC7-AI094660</award-id>
<principal-award-recipient><name><surname>Mire</surname>
<given-names>Chad E.</given-names>
</name>
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