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1918 H1N1 Influenza Virus Replicates and Induces Proinflammatory Cytokine Responses in Extrarespiratory Tissues of Ferrets

Identifieur interne : 000722 ( Pmc/Corpus ); précédent : 000721; suivant : 000723

1918 H1N1 Influenza Virus Replicates and Induces Proinflammatory Cytokine Responses in Extrarespiratory Tissues of Ferrets

Auteurs : Emmie De Wit ; Jurre Y. Siegers ; Jacqueline M. Cronin ; Sarah Weatherman ; Judith M. Van Den Brand ; Lonneke M. Leijten ; Peter Van Run ; Lineke Begeman ; Henk-Jan Van Den Ham ; Arno C. Andeweg ; Trenton Bushmaker ; Dana P. Scott ; Greg Saturday ; Vincent J. Munster ; Heinz Feldmann ; Debby Van Riel

Source :

RBID : PMC:6018876

Abstract

This study reveals that 1918 H1N1 influenza virus spreads to and induces proinflammatory cytokine responses in extrarespiratory tissues, including the nervous system, liver, and heart. This likely contributes to the development of severe disease, including diseases of the nervous system.


Url:
DOI: 10.1093/infdis/jiy003
PubMed: 29329410
PubMed Central: 6018876

Links to Exploration step

PMC:6018876

Le document en format XML

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<name sortKey="Bushmaker, Trenton" sort="Bushmaker, Trenton" uniqKey="Bushmaker T" first="Trenton" last="Bushmaker">Trenton Bushmaker</name>
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<name sortKey="Scott, Dana P" sort="Scott, Dana P" uniqKey="Scott D" first="Dana P" last="Scott">Dana P. Scott</name>
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<name sortKey="Munster, Vincent J" sort="Munster, Vincent J" uniqKey="Munster V" first="Vincent J" last="Munster">Vincent J. Munster</name>
<affiliation>
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</affiliation>
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<author>
<name sortKey="Feldmann, Heinz" sort="Feldmann, Heinz" uniqKey="Feldmann H" first="Heinz" last="Feldmann">Heinz Feldmann</name>
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<nlm:aff id="AF0001">Laboratory of Virology, National Institutes of Health, Hamilton, Montana</nlm:aff>
</affiliation>
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<title xml:lang="en" level="a" type="main">1918 H1N1 Influenza Virus Replicates and Induces Proinflammatory Cytokine Responses in Extrarespiratory Tissues of Ferrets</title>
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<name sortKey="De Wit, Emmie" sort="De Wit, Emmie" uniqKey="De Wit E" first="Emmie" last="De Wit">Emmie De Wit</name>
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<nlm:aff id="AF0001">Laboratory of Virology, National Institutes of Health, Hamilton, Montana</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Siegers, Jurre Y" sort="Siegers, Jurre Y" uniqKey="Siegers J" first="Jurre Y" last="Siegers">Jurre Y. Siegers</name>
<affiliation>
<nlm:aff id="AF0003">Department of Viroscience, Erasmus MC, Rotterdam, The Netherlands</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Cronin, Jacqueline M" sort="Cronin, Jacqueline M" uniqKey="Cronin J" first="Jacqueline M" last="Cronin">Jacqueline M. Cronin</name>
<affiliation>
<nlm:aff id="AF0001">Laboratory of Virology, National Institutes of Health, Hamilton, Montana</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Weatherman, Sarah" sort="Weatherman, Sarah" uniqKey="Weatherman S" first="Sarah" last="Weatherman">Sarah Weatherman</name>
<affiliation>
<nlm:aff id="AF0001">Laboratory of Virology, National Institutes of Health, Hamilton, Montana</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Van Den Brand, Judith M" sort="Van Den Brand, Judith M" uniqKey="Van Den Brand J" first="Judith M" last="Van Den Brand">Judith M. Van Den Brand</name>
<affiliation>
<nlm:aff id="AF0003">Department of Viroscience, Erasmus MC, Rotterdam, The Netherlands</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Leijten, Lonneke M" sort="Leijten, Lonneke M" uniqKey="Leijten L" first="Lonneke M" last="Leijten">Lonneke M. Leijten</name>
<affiliation>
<nlm:aff id="AF0003">Department of Viroscience, Erasmus MC, Rotterdam, The Netherlands</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Van Run, Peter" sort="Van Run, Peter" uniqKey="Van Run P" first="Peter" last="Van Run">Peter Van Run</name>
<affiliation>
<nlm:aff id="AF0003">Department of Viroscience, Erasmus MC, Rotterdam, The Netherlands</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Begeman, Lineke" sort="Begeman, Lineke" uniqKey="Begeman L" first="Lineke" last="Begeman">Lineke Begeman</name>
<affiliation>
<nlm:aff id="AF0003">Department of Viroscience, Erasmus MC, Rotterdam, The Netherlands</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Van Den Ham, Henk Jan" sort="Van Den Ham, Henk Jan" uniqKey="Van Den Ham H" first="Henk-Jan" last="Van Den Ham">Henk-Jan Van Den Ham</name>
<affiliation>
<nlm:aff id="AF0003">Department of Viroscience, Erasmus MC, Rotterdam, The Netherlands</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Andeweg, Arno C" sort="Andeweg, Arno C" uniqKey="Andeweg A" first="Arno C" last="Andeweg">Arno C. Andeweg</name>
<affiliation>
<nlm:aff id="AF0003">Department of Viroscience, Erasmus MC, Rotterdam, The Netherlands</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Bushmaker, Trenton" sort="Bushmaker, Trenton" uniqKey="Bushmaker T" first="Trenton" last="Bushmaker">Trenton Bushmaker</name>
<affiliation>
<nlm:aff id="AF0001">Laboratory of Virology, National Institutes of Health, Hamilton, Montana</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Scott, Dana P" sort="Scott, Dana P" uniqKey="Scott D" first="Dana P" last="Scott">Dana P. Scott</name>
<affiliation>
<nlm:aff id="AF0002">Rocky Mountain Veterinary Branch, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, Montana</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Saturday, Greg" sort="Saturday, Greg" uniqKey="Saturday G" first="Greg" last="Saturday">Greg Saturday</name>
<affiliation>
<nlm:aff id="AF0002">Rocky Mountain Veterinary Branch, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, Montana</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Munster, Vincent J" sort="Munster, Vincent J" uniqKey="Munster V" first="Vincent J" last="Munster">Vincent J. Munster</name>
<affiliation>
<nlm:aff id="AF0001">Laboratory of Virology, National Institutes of Health, Hamilton, Montana</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Feldmann, Heinz" sort="Feldmann, Heinz" uniqKey="Feldmann H" first="Heinz" last="Feldmann">Heinz Feldmann</name>
<affiliation>
<nlm:aff id="AF0001">Laboratory of Virology, National Institutes of Health, Hamilton, Montana</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Van Riel, Debby" sort="Van Riel, Debby" uniqKey="Van Riel D" first="Debby" last="Van Riel">Debby Van Riel</name>
<affiliation>
<nlm:aff id="AF0003">Department of Viroscience, Erasmus MC, Rotterdam, The Netherlands</nlm:aff>
</affiliation>
</author>
</analytic>
<series>
<title level="j">The Journal of Infectious Diseases</title>
<idno type="ISSN">0022-1899</idno>
<idno type="eISSN">1537-6613</idno>
<imprint>
<date when="2018">2018</date>
</imprint>
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<front>
<div type="abstract" xml:lang="en">
<p>This study reveals that 1918 H1N1 influenza virus spreads to and induces proinflammatory cytokine responses in extrarespiratory tissues, including the nervous system, liver, and heart. This likely contributes to the development of severe disease, including diseases of the nervous system.</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 Infect Dis</journal-id>
<journal-id journal-id-type="iso-abbrev">J. Infect. Dis</journal-id>
<journal-id journal-id-type="publisher-id">jid</journal-id>
<journal-title-group>
<journal-title>The Journal of Infectious Diseases</journal-title>
</journal-title-group>
<issn pub-type="ppub">0022-1899</issn>
<issn pub-type="epub">1537-6613</issn>
<publisher>
<publisher-name>Oxford University Press</publisher-name>
<publisher-loc>US</publisher-loc>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">29329410</article-id>
<article-id pub-id-type="pmc">6018876</article-id>
<article-id pub-id-type="doi">10.1093/infdis/jiy003</article-id>
<article-id pub-id-type="publisher-id">jiy003</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Major Articles and Brief Reports</subject>
<subj-group subj-group-type="category-toc-heading">
<subject>Pathogenesis and Host Response</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>1918 H1N1 Influenza Virus Replicates and Induces Proinflammatory Cytokine Responses in Extrarespiratory Tissues of Ferrets</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>de Wit</surname>
<given-names>Emmie</given-names>
</name>
<xref ref-type="aff" rid="AF0001">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Siegers</surname>
<given-names>Jurre Y</given-names>
</name>
<xref ref-type="aff" rid="AF0003">3</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Cronin</surname>
<given-names>Jacqueline M</given-names>
</name>
<xref ref-type="aff" rid="AF0001">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Weatherman</surname>
<given-names>Sarah</given-names>
</name>
<xref ref-type="aff" rid="AF0001">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>van den Brand</surname>
<given-names>Judith M</given-names>
</name>
<xref ref-type="aff" rid="AF0003">3</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Leijten</surname>
<given-names>Lonneke M</given-names>
</name>
<xref ref-type="aff" rid="AF0003">3</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>van Run</surname>
<given-names>Peter</given-names>
</name>
<xref ref-type="aff" rid="AF0003">3</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Begeman</surname>
<given-names>Lineke</given-names>
</name>
<xref ref-type="aff" rid="AF0003">3</xref>
</contrib>
<contrib contrib-type="author">
<contrib-id contrib-id-type="orcid" authenticated="false">http://orcid.org/0000-0001-8582-5404</contrib-id>
<name>
<surname>van den Ham</surname>
<given-names>Henk-Jan</given-names>
</name>
<xref ref-type="aff" rid="AF0003">3</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Andeweg</surname>
<given-names>Arno C</given-names>
</name>
<xref ref-type="aff" rid="AF0003">3</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Bushmaker</surname>
<given-names>Trenton</given-names>
</name>
<xref ref-type="aff" rid="AF0001">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Scott</surname>
<given-names>Dana P</given-names>
</name>
<xref ref-type="aff" rid="AF0002">2</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Saturday</surname>
<given-names>Greg</given-names>
</name>
<xref ref-type="aff" rid="AF0002">2</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Munster</surname>
<given-names>Vincent J</given-names>
</name>
<xref ref-type="aff" rid="AF0001">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Feldmann</surname>
<given-names>Heinz</given-names>
</name>
<xref ref-type="aff" rid="AF0001">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>van Riel</surname>
<given-names>Debby</given-names>
</name>
<xref ref-type="aff" rid="AF0003">3</xref>
<xref ref-type="corresp" rid="c1"></xref>
<pmc-comment>d.vanriel@erasmusmc.nl</pmc-comment>
</contrib>
</contrib-group>
<aff id="AF0001">
<label>1</label>
Laboratory of Virology, National Institutes of Health, Hamilton, Montana</aff>
<aff id="AF0002">
<label>2</label>
Rocky Mountain Veterinary Branch, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, Montana</aff>
<aff id="AF0003">
<label>3</label>
Department of Viroscience, Erasmus MC, Rotterdam, The Netherlands</aff>
<author-notes>
<corresp id="c1">Correspondence: D. van Riel, PhD, Department of Viroscience, Erasmus MC, PO Box 2040, Ee1716, 3000 CA Rotterdam, The Netherlands (
<email>d.vanriel@erasmusmc.nl</email>
).</corresp>
</author-notes>
<pub-date pub-type="ppub">
<day>15</day>
<month>4</month>
<year>2018</year>
</pub-date>
<pub-date pub-type="epub" iso-8601-date="2018-01-10">
<day>10</day>
<month>1</month>
<year>2018</year>
</pub-date>
<pub-date pub-type="pmc-release">
<day>28</day>
<month>3</month>
<year>2019</year>
</pub-date>
<pmc-comment> PMC Release delay is 12 months and 0 days and was based on the . </pmc-comment>
<volume>217</volume>
<issue>8</issue>
<fpage>1237</fpage>
<lpage>1246</lpage>
<history>
<date date-type="received">
<day>09</day>
<month>11</month>
<year>2017</year>
</date>
<date date-type="accepted">
<day>08</day>
<month>1</month>
<year>2018</year>
</date>
</history>
<permissions>
<copyright-statement>Published by Oxford University Press for the Infectious Diseases Society of America 2018.</copyright-statement>
<copyright-year>2018</copyright-year>
<license license-type="us-gov">
<license-p>This work is written by (a) US Government employee(s) and is in the public domain in the US.</license-p>
</license>
</permissions>
<self-uri xlink:href="jiy003.pdf"></self-uri>
<abstract abstract-type="teaser">
<p>This study reveals that 1918 H1N1 influenza virus spreads to and induces proinflammatory cytokine responses in extrarespiratory tissues, including the nervous system, liver, and heart. This likely contributes to the development of severe disease, including diseases of the nervous system.</p>
</abstract>
<abstract>
<title>Abstract</title>
<sec id="s1">
<title>Background</title>
<p>The 1918 Spanish H1N1 influenza pandemic was the most severe recorded influenza pandemic with an estimated 20–50 million deaths worldwide. Even though it is known that influenza viruses can cause extrarespiratory tract complications—which are often severe or even fatal—the potential contribution of extrarespiratory tissues to the pathogenesis of 1918 H1N1 virus infection has not been studied comprehensively.</p>
</sec>
<sec id="s2">
<title>Methods</title>
<p>Here, we performed a time-course study in ferrets inoculated intranasally with 1918 H1N1 influenza virus, with special emphasis on the involvement of extrarespiratory tissues. Respiratory and extrarespiratory tissues were collected after inoculation for virological, histological, and immunological analysis.</p>
</sec>
<sec id="s3">
<title>Results</title>
<p>Infectious virus was detected at high titers in respiratory tissues and, at lower titers in most extrarespiratory tissues. Evidence for active virus replication, as indicated by the detection of nucleoprotein by immunohistochemistry, was observed in the respiratory tract, peripheral and central nervous system, and liver. Proinflammatory cytokines were up-regulated in respiratory tissues, olfactory bulb, spinal cord, liver, heart, and pancreas.</p>
</sec>
<sec id="s4">
<title>Conclusions</title>
<p>1918 H1N1 virus spread to and induced cytokine responses in tissues outside the respiratory tract, which likely contributed to the severity of infection. Moreover, our data support the suggested link between 1918 H1N1 infection and central nervous system disease.</p>
</sec>
</abstract>
<kwd-group>
<kwd>influenza A virus</kwd>
<kwd>1918 H1N1 virus</kwd>
<kwd>pathogenesis</kwd>
<kwd>CNS disease</kwd>
<kwd>extrarespiratory</kwd>
</kwd-group>
<funding-group>
<award-group award-type="grant">
<funding-source>
<named-content content-type="funder-name">National Institute of Allergy and Infectious Diseases</named-content>
<named-content content-type="funder-identifier">10.13039/100000060</named-content>
</funding-source>
</award-group>
<award-group award-type="grant">
<funding-source>
<named-content content-type="funder-name">National Institutes of Health</named-content>
<named-content content-type="funder-identifier">10.13039/100000002</named-content>
</funding-source>
</award-group>
</funding-group>
<counts>
<page-count count="10"></page-count>
</counts>
</article-meta>
</front>
</pmc>
</record>

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