Eurasian-Origin Gene Segments Contribute to the Transmissibility, Aerosol Release, and Morphology of the 2009 Pandemic H1N1 Influenza Virus
Identifieur interne : 000730 ( Ncbi/Merge ); précédent : 000729; suivant : 000731Eurasian-Origin Gene Segments Contribute to the Transmissibility, Aerosol Release, and Morphology of the 2009 Pandemic H1N1 Influenza Virus
Auteurs : Seema S. Lakdawala [États-Unis] ; Elaine W. Lamirande [États-Unis] ; Amorsolo L. Suguitan [États-Unis] ; Weijia Wang [États-Unis] ; Celia P. Santos [États-Unis] ; Leatrice Vogel [États-Unis] ; Yumiko Matsuoka [États-Unis] ; William G. Lindsley [États-Unis] ; Hong Jin [États-Unis] ; Kanta Subbarao [États-Unis]Source :
- PLoS Pathogens [ 1553-7366 ] ; 2011.
Abstract
The epidemiological success of pandemic and epidemic influenza A viruses relies on the ability to transmit efficiently from person-to-person via respiratory droplets. Respiratory droplet (RD) transmission of influenza viruses requires efficient replication and release of infectious influenza particles into the air. The 2009 pandemic H1N1 (pH1N1) virus originated by reassortment of a North American triple reassortant swine (TRS) virus with a Eurasian swine virus that contributed the neuraminidase (NA) and M gene segments. Both the TRS and Eurasian swine viruses caused sporadic infections in humans, but failed to spread from person-to-person, unlike the pH1N1 virus. We evaluated the pH1N1 and its precursor viruses in a ferret model to determine the contribution of different viral gene segments on the release of influenza virus particles into the air and on the transmissibility of the pH1N1 virus. We found that the Eurasian-origin gene segments contributed to efficient RD transmission of the pH1N1 virus likely by modulating the release of influenza viral RNA-containing particles into the air. All viruses replicated well in the upper respiratory tract of infected ferrets, suggesting that factors other than viral replication are important for the release of influenza virus particles and transmission. Our studies demonstrate that the release of influenza viral RNA-containing particles into the air correlates with increased NA activity. Additionally, the pleomorphic phenotype of the pH1N1 virus is dependent upon the Eurasian-origin gene segments, suggesting a link between transmission and virus morphology. We have demonstrated that the viruses are released into exhaled air to varying degrees and a constellation of genes influences the transmissibility of the pH1N1 virus.
Url:
DOI: 10.1371/journal.ppat.1002443
PubMed: 22241979
PubMed Central: 3248560
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<front><div type="abstract" xml:lang="en"><p>The epidemiological success of pandemic and epidemic influenza A viruses relies on the ability to transmit efficiently from person-to-person via respiratory droplets. Respiratory droplet (RD) transmission of influenza viruses requires efficient replication and release of infectious influenza particles into the air. The 2009 pandemic H1N1 (pH1N1) virus originated by reassortment of a North American triple reassortant swine (TRS) virus with a Eurasian swine virus that contributed the neuraminidase (NA) and M gene segments. Both the TRS and Eurasian swine viruses caused sporadic infections in humans, but failed to spread from person-to-person, unlike the pH1N1 virus. We evaluated the pH1N1 and its precursor viruses in a ferret model to determine the contribution of different viral gene segments on the release of influenza virus particles into the air and on the transmissibility of the pH1N1 virus. We found that the Eurasian-origin gene segments contributed to efficient RD transmission of the pH1N1 virus likely by modulating the release of influenza viral RNA-containing particles into the air. All viruses replicated well in the upper respiratory tract of infected ferrets, suggesting that factors other than viral replication are important for the release of influenza virus particles and transmission. Our studies demonstrate that the release of influenza viral RNA-containing particles into the air correlates with increased NA activity. Additionally, the pleomorphic phenotype of the pH1N1 virus is dependent upon the Eurasian-origin gene segments, suggesting a link between transmission and virus morphology. We have demonstrated that the viruses are released into exhaled air to varying degrees and a constellation of genes influences the transmissibility of the pH1N1 virus.</p>
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<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS Pathog</journal-id>
<journal-id journal-id-type="iso-abbrev">PLoS Pathog</journal-id>
<journal-id journal-id-type="publisher-id">plos</journal-id>
<journal-id journal-id-type="pmc">plospath</journal-id>
<journal-title-group><journal-title>PLoS Pathogens</journal-title>
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<issn pub-type="ppub">1553-7366</issn>
<issn pub-type="epub">1553-7374</issn>
<publisher><publisher-name>Public Library of Science</publisher-name>
<publisher-loc>San Francisco, USA</publisher-loc>
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<article-id pub-id-type="pmc">3248560</article-id>
<article-id pub-id-type="publisher-id">PPATHOGENS-D-11-01769</article-id>
<article-id pub-id-type="doi">10.1371/journal.ppat.1002443</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
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<subj-group subj-group-type="Discipline-v2"><subject>Biology</subject>
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<title-group><article-title>Eurasian-Origin Gene Segments Contribute to the Transmissibility, Aerosol Release, and Morphology of the 2009 Pandemic H1N1 Influenza Virus</article-title>
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</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Vogel</surname>
<given-names>Leatrice</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Matsuoka</surname>
<given-names>Yumiko</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Lindsley</surname>
<given-names>William G.</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Jin</surname>
<given-names>Hong</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Subbarao</surname>
<given-names>Kanta</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="corresp" rid="cor1"><sup>*</sup>
</xref>
</contrib>
</contrib-group>
<aff id="aff1"><label>1</label>
<addr-line>Laboratory of Infectious Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, United States of America</addr-line>
</aff>
<aff id="aff2"><label>2</label>
<addr-line>MedImmune, Mountain View, California, United States of America</addr-line>
</aff>
<aff id="aff3"><label>3</label>
<addr-line>National Institute for Occupational Safety and Health, Morgantown, West Virginia, United States of America</addr-line>
</aff>
<contrib-group><contrib contrib-type="editor"><name><surname>Fouchier</surname>
<given-names>Ron A. M.</given-names>
</name>
<role>Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1">Erasmus Medical Center, Netherlands</aff>
<author-notes><corresp id="cor1">* E-mail: <email>kanta.subbarao@nih.gov</email>
</corresp>
<fn fn-type="con"><p>Conceived and designed the experiments: SSL EWL ALS YM KS. Performed the experiments: SSL EWL ALS WW CPS LV. Analyzed the data: SSL ALS. Contributed reagents/materials/analysis tools: ALS WGL HJ. Wrote the paper: SSL.</p>
</fn>
</author-notes>
<pub-date pub-type="collection"><month>12</month>
<year>2011</year>
</pub-date>
<pub-date pub-type="epub"><day>29</day>
<month>12</month>
<year>2011</year>
</pub-date>
<volume>7</volume>
<issue>12</issue>
<elocation-id>e1002443</elocation-id>
<history><date date-type="received"><day>10</day>
<month>8</month>
<year>2011</year>
</date>
<date date-type="accepted"><day>2</day>
<month>11</month>
<year>2011</year>
</date>
</history>
<permissions><copyright-statement>This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.</copyright-statement>
<copyright-year>2011</copyright-year>
<license xlink:href="https://creativecommons.org/publicdomain/zero/1.0/"><license-p>This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration, which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose.</license-p>
</license>
</permissions>
<abstract><p>The epidemiological success of pandemic and epidemic influenza A viruses relies on the ability to transmit efficiently from person-to-person via respiratory droplets. Respiratory droplet (RD) transmission of influenza viruses requires efficient replication and release of infectious influenza particles into the air. The 2009 pandemic H1N1 (pH1N1) virus originated by reassortment of a North American triple reassortant swine (TRS) virus with a Eurasian swine virus that contributed the neuraminidase (NA) and M gene segments. Both the TRS and Eurasian swine viruses caused sporadic infections in humans, but failed to spread from person-to-person, unlike the pH1N1 virus. We evaluated the pH1N1 and its precursor viruses in a ferret model to determine the contribution of different viral gene segments on the release of influenza virus particles into the air and on the transmissibility of the pH1N1 virus. We found that the Eurasian-origin gene segments contributed to efficient RD transmission of the pH1N1 virus likely by modulating the release of influenza viral RNA-containing particles into the air. All viruses replicated well in the upper respiratory tract of infected ferrets, suggesting that factors other than viral replication are important for the release of influenza virus particles and transmission. Our studies demonstrate that the release of influenza viral RNA-containing particles into the air correlates with increased NA activity. Additionally, the pleomorphic phenotype of the pH1N1 virus is dependent upon the Eurasian-origin gene segments, suggesting a link between transmission and virus morphology. We have demonstrated that the viruses are released into exhaled air to varying degrees and a constellation of genes influences the transmissibility of the pH1N1 virus.</p>
</abstract>
<abstract abstract-type="summary"><title>Author Summary</title>
<p>Influenza A viruses spread rapidly from person-to-person via respiratory droplets (RDs). In this study we used a ferret model to explore viral functions involved in RD transmission of influenza viruses. The 2009 pandemic H1N1 (pH1N1) virus originated by reassortment of a North American triple reassortant swine (TRS) virus with a Eurasian swine virus. Both TRS and Eurasian swine viruses had previously caused sporadic infections in humans, but failed to spread from person-to-person, unlike the pH1N1 virus. We evaluated the release of influenza virus-containing aerosols and the transmissibility of the pH1N1, TRS, and Eurasian viruses in ferrets and found that the Eurasian-origin gene segments contributed to efficient RD transmission of the pH1N1 virus by modulating the release of influenza viral RNA-containing particles into the air. The increased release of viral RNA-containing particles correlated with increased viral neuraminidase activity and production of filamentous viral particles. These observations enhance what we currently know about the viral requirements for influenza virus RD transmission and have implications for assessing the potential of novel influenza viruses to spread.</p>
</abstract>
<counts><page-count count="14"></page-count>
</counts>
</article-meta>
</front>
</pmc>
<affiliations><list><country><li>États-Unis</li>
</country>
<region><li>Californie</li>
<li>Maryland</li>
<li>Virginie-Occidentale</li>
</region>
</list>
<tree><country name="États-Unis"><region name="Maryland"><name sortKey="Lakdawala, Seema S" sort="Lakdawala, Seema S" uniqKey="Lakdawala S" first="Seema S." last="Lakdawala">Seema S. Lakdawala</name>
</region>
<name sortKey="Jin, Hong" sort="Jin, Hong" uniqKey="Jin H" first="Hong" last="Jin">Hong Jin</name>
<name sortKey="Lamirande, Elaine W" sort="Lamirande, Elaine W" uniqKey="Lamirande E" first="Elaine W." last="Lamirande">Elaine W. Lamirande</name>
<name sortKey="Lindsley, William G" sort="Lindsley, William G" uniqKey="Lindsley W" first="William G." last="Lindsley">William G. Lindsley</name>
<name sortKey="Matsuoka, Yumiko" sort="Matsuoka, Yumiko" uniqKey="Matsuoka Y" first="Yumiko" last="Matsuoka">Yumiko Matsuoka</name>
<name sortKey="Santos, Celia P" sort="Santos, Celia P" uniqKey="Santos C" first="Celia P." last="Santos">Celia P. Santos</name>
<name sortKey="Subbarao, Kanta" sort="Subbarao, Kanta" uniqKey="Subbarao K" first="Kanta" last="Subbarao">Kanta Subbarao</name>
<name sortKey="Suguitan, Amorsolo L" sort="Suguitan, Amorsolo L" uniqKey="Suguitan A" first="Amorsolo L." last="Suguitan">Amorsolo L. Suguitan</name>
<name sortKey="Vogel, Leatrice" sort="Vogel, Leatrice" uniqKey="Vogel L" first="Leatrice" last="Vogel">Leatrice Vogel</name>
<name sortKey="Wang, Weijia" sort="Wang, Weijia" uniqKey="Wang W" first="Weijia" last="Wang">Weijia Wang</name>
</country>
</tree>
</affiliations>
</record>
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