Evolution of an Eurasian Avian-like Influenza Virus in Naïve and Vaccinated Pigs
Identifieur interne : 000774 ( Ncbi/Merge ); précédent : 000773; suivant : 000775Evolution of an Eurasian Avian-like Influenza Virus in Naïve and Vaccinated Pigs
Auteurs : Pablo R. Murcia [Royaume-Uni] ; Joseph Hughes [Royaume-Uni] ; Patrizia Battista [Royaume-Uni] ; Lucy Lloyd [Royaume-Uni] ; Gregory J. Baillie [Royaume-Uni] ; Ricardo H. Ramirez-Gonzalez [Royaume-Uni] ; Doug Ormond [Royaume-Uni] ; Karen Oliver [Royaume-Uni] ; Debra Elton [Royaume-Uni] ; Jennifer A. Mumford [Royaume-Uni] ; Mario Caccamo [Royaume-Uni] ; Paul Kellam [Royaume-Uni] ; Bryan T. Grenfell [États-Unis] ; Edward C. Holmes [États-Unis] ; James L. N. Wood [Royaume-Uni]Source :
- PLoS Pathogens [ 1553-7366 ] ; 2012.
Abstract
Influenza viruses are characterized by an ability to cross species boundaries and evade host immunity, sometimes with devastating consequences. The 2009 pandemic of H1N1 influenza A virus highlights the importance of pigs in influenza emergence, particularly as intermediate hosts by which avian viruses adapt to mammals before emerging in humans. Although segment reassortment has commonly been associated with influenza emergence, an expanded host-range is also likely to be associated with the accumulation of specific beneficial point mutations. To better understand the mechanisms that shape the genetic diversity of avian-like viruses in pigs, we studied the evolutionary dynamics of an Eurasian Avian-like swine influenza virus (EA-SIV) in naïve and vaccinated pigs linked by natural transmission. We analyzed multiple clones of the hemagglutinin 1 (HA1) gene derived from consecutive daily viral populations. Strikingly, we observed both transient and fixed changes in the consensus sequence along the transmission chain. Hence, the mutational spectrum of intra-host EA-SIV populations is highly dynamic and allele fixation can occur with extreme rapidity. In addition, mutations that could potentially alter host-range and antigenicity were transmitted between animals and mixed infections were commonplace, even in vaccinated pigs. Finally, we repeatedly detected distinct stop codons in virus samples from co-housed pigs, suggesting that they persisted within hosts and were transmitted among them. This implies that mutations that reduce viral fitness in one host, but which could lead to fitness benefits in a novel host, can circulate at low frequencies.
Url:
DOI: 10.1371/journal.ppat.1002730
PubMed: 22693449
PubMed Central: 3364949
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</nlm:aff>
<country xml:lang="fr">Royaume-Uni</country>
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</nlm:aff>
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<author><name sortKey="Holmes, Edward C" sort="Holmes, Edward C" uniqKey="Holmes E" first="Edward C." last="Holmes">Edward C. Holmes</name>
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<wicri:regionArea>Center for Infectious Disease Dynamics, Department of Biology, The Pennsylvania State University, Pennsylvania</wicri:regionArea>
<placeName><region type="state">Pennsylvanie</region>
<settlement type="city">University Park (Pennsylvanie)</settlement>
</placeName>
<orgName type="university">Université d'État de Pennsylvanie</orgName>
</affiliation>
<affiliation wicri:level="2"><nlm:aff id="aff8"><addr-line>Fogarty International Center, National Institute of Health, Bethesda, Maryland, United States of America</addr-line>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Fogarty International Center, National Institute of Health, Bethesda, Maryland</wicri:regionArea>
<placeName><region type="state">Maryland</region>
</placeName>
</affiliation>
</author>
<author><name sortKey="Wood, James L N" sort="Wood, James L N" uniqKey="Wood J" first="James L. N." last="Wood">James L. N. Wood</name>
<affiliation wicri:level="4"><nlm:aff id="aff1"><addr-line>Cambridge Infectious Diseases Consortium, Department of Veterinary Medicine, University of Cambridge, Cambridge, United Kingdom</addr-line>
</nlm:aff>
<country xml:lang="fr">Royaume-Uni</country>
<wicri:regionArea>Cambridge Infectious Diseases Consortium, Department of Veterinary Medicine, University of Cambridge, Cambridge</wicri:regionArea>
<orgName type="university">Université de Cambridge</orgName>
<placeName><settlement type="city">Cambridge</settlement>
<region type="country">Angleterre</region>
<region type="région" nuts="1">Angleterre de l'Est</region>
</placeName>
</affiliation>
</author>
</analytic>
<series><title level="j">PLoS Pathogens</title>
<idno type="ISSN">1553-7366</idno>
<idno type="eISSN">1553-7374</idno>
<imprint><date when="2012">2012</date>
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<front><div type="abstract" xml:lang="en"><p>Influenza viruses are characterized by an ability to cross species boundaries and evade host immunity, sometimes with devastating consequences. The 2009 pandemic of H1N1 influenza A virus highlights the importance of pigs in influenza emergence, particularly as intermediate hosts by which avian viruses adapt to mammals before emerging in humans. Although segment reassortment has commonly been associated with influenza emergence, an expanded host-range is also likely to be associated with the accumulation of specific beneficial point mutations. To better understand the mechanisms that shape the genetic diversity of avian-like viruses in pigs, we studied the evolutionary dynamics of an Eurasian Avian-like swine influenza virus (EA-SIV) in naïve and vaccinated pigs linked by natural transmission. We analyzed multiple clones of the hemagglutinin 1 (HA1) gene derived from consecutive daily viral populations. Strikingly, we observed both transient and fixed changes in the consensus sequence along the transmission chain. Hence, the mutational spectrum of intra-host EA-SIV populations is highly dynamic and allele fixation can occur with extreme rapidity. In addition, mutations that could potentially alter host-range and antigenicity were transmitted between animals and mixed infections were commonplace, even in vaccinated pigs. Finally, we repeatedly detected distinct stop codons in virus samples from co-housed pigs, suggesting that they persisted within hosts and were transmitted among them. This implies that mutations that reduce viral fitness in one host, but which could lead to fitness benefits in a novel host, can circulate at low frequencies.</p>
</div>
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<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<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>
</journal-title-group>
<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>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">22693449</article-id>
<article-id pub-id-type="pmc">3364949</article-id>
<article-id pub-id-type="publisher-id">PPATHOGENS-D-12-00315</article-id>
<article-id pub-id-type="doi">10.1371/journal.ppat.1002730</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
</subj-group>
<subj-group subj-group-type="Discipline-v2"><subject>Biology</subject>
<subj-group><subject>Evolutionary Biology</subject>
<subj-group><subject>Evolutionary Processes</subject>
<subj-group><subject>Emergence</subject>
</subj-group>
</subj-group>
</subj-group>
<subj-group><subject>Microbiology</subject>
<subj-group><subject>Virology</subject>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v2"><subject>Medicine</subject>
<subj-group><subject>Infectious Diseases</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group><article-title>Evolution of an Eurasian Avian-like Influenza Virus in Naïve and Vaccinated Pigs</article-title>
<alt-title alt-title-type="running-head">Swine Influenza Evolution</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Murcia</surname>
<given-names>Pablo R.</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>Hughes</surname>
<given-names>Joseph</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Battista</surname>
<given-names>Patrizia</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Lloyd</surname>
<given-names>Lucy</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Baillie</surname>
<given-names>Gregory J.</given-names>
</name>
<xref ref-type="aff" rid="aff4"><sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Ramirez-Gonzalez</surname>
<given-names>Ricardo H.</given-names>
</name>
<xref ref-type="aff" rid="aff5"><sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Ormond</surname>
<given-names>Doug</given-names>
</name>
<xref ref-type="aff" rid="aff4"><sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Oliver</surname>
<given-names>Karen</given-names>
</name>
<xref ref-type="aff" rid="aff4"><sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Elton</surname>
<given-names>Debra</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Mumford</surname>
<given-names>Jennifer A.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Caccamo</surname>
<given-names>Mario</given-names>
</name>
<xref ref-type="aff" rid="aff5"><sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Kellam</surname>
<given-names>Paul</given-names>
</name>
<xref ref-type="aff" rid="aff4"><sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Grenfell</surname>
<given-names>Bryan T.</given-names>
</name>
<xref ref-type="aff" rid="aff6"><sup>6</sup>
</xref>
<xref ref-type="aff" rid="aff7"><sup>7</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Holmes</surname>
<given-names>Edward C.</given-names>
</name>
<xref ref-type="aff" rid="aff7"><sup>7</sup>
</xref>
<xref ref-type="aff" rid="aff8"><sup>8</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Wood</surname>
<given-names>James L. N.</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>Cambridge Infectious Diseases Consortium, Department of Veterinary Medicine, University of Cambridge, Cambridge, United Kingdom</addr-line>
</aff>
<aff id="aff2"><label>2</label>
<addr-line>Medical Research Council-University of Glasgow Centre for Virus Research, Institute of Infection, Inflammation and Immunity, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, United Kingdom</addr-line>
</aff>
<aff id="aff3"><label>3</label>
<addr-line>Animal Health Trust, Centre for Preventive Medicine, Lanwades Park, Newmarket, United Kingdom</addr-line>
</aff>
<aff id="aff4"><label>4</label>
<addr-line>Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge, United Kingdom</addr-line>
</aff>
<aff id="aff5"><label>5</label>
<addr-line>The Genome Analysis Centre, Norwich Research Park, Norwich, United Kingdom</addr-line>
</aff>
<aff id="aff6"><label>6</label>
<addr-line>Department of Ecology and Evolutionary Biology, Princeton University, Princeton, New Jersey, United States of America</addr-line>
</aff>
<aff id="aff7"><label>7</label>
<addr-line>Center for Infectious Disease Dynamics, Department of Biology, The Pennsylvania State University, Pennsylvania, United States of America</addr-line>
</aff>
<aff id="aff8"><label>8</label>
<addr-line>Fogarty International Center, National Institute of Health, Bethesda, Maryland, United States of America</addr-line>
</aff>
<contrib-group><contrib contrib-type="editor"><name><surname>Wilke</surname>
<given-names>Claus O.</given-names>
</name>
<role>Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1">University of Texas at Austin, United States of America</aff>
<author-notes><corresp id="cor1">* E-mail: <email>jlnw2@cam.ac.uk</email>
</corresp>
<fn fn-type="con"><p>Conceived and designed the experiments: PRM JAM BTG ECH JLNW. Performed the experiments: PRM PB DO KO JH. Analyzed the data: PRM JH ECH. Contributed reagents/materials/analysis tools: DE PK GJB LL MC RHR-G. Wrote the paper: PRM ECH.</p>
</fn>
</author-notes>
<pub-date pub-type="collection"><month>5</month>
<year>2012</year>
</pub-date>
<pub-date pub-type="epub"><day>31</day>
<month>5</month>
<year>2012</year>
</pub-date>
<volume>8</volume>
<issue>5</issue>
<elocation-id>e1002730</elocation-id>
<history><date date-type="received"><day>31</day>
<month>1</month>
<year>2012</year>
</date>
<date date-type="accepted"><day>19</day>
<month>4</month>
<year>2012</year>
</date>
</history>
<permissions><copyright-statement>Murcia et al.</copyright-statement>
<copyright-year>2012</copyright-year>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.</license-p>
</license>
</permissions>
<abstract><p>Influenza viruses are characterized by an ability to cross species boundaries and evade host immunity, sometimes with devastating consequences. The 2009 pandemic of H1N1 influenza A virus highlights the importance of pigs in influenza emergence, particularly as intermediate hosts by which avian viruses adapt to mammals before emerging in humans. Although segment reassortment has commonly been associated with influenza emergence, an expanded host-range is also likely to be associated with the accumulation of specific beneficial point mutations. To better understand the mechanisms that shape the genetic diversity of avian-like viruses in pigs, we studied the evolutionary dynamics of an Eurasian Avian-like swine influenza virus (EA-SIV) in naïve and vaccinated pigs linked by natural transmission. We analyzed multiple clones of the hemagglutinin 1 (HA1) gene derived from consecutive daily viral populations. Strikingly, we observed both transient and fixed changes in the consensus sequence along the transmission chain. Hence, the mutational spectrum of intra-host EA-SIV populations is highly dynamic and allele fixation can occur with extreme rapidity. In addition, mutations that could potentially alter host-range and antigenicity were transmitted between animals and mixed infections were commonplace, even in vaccinated pigs. Finally, we repeatedly detected distinct stop codons in virus samples from co-housed pigs, suggesting that they persisted within hosts and were transmitted among them. This implies that mutations that reduce viral fitness in one host, but which could lead to fitness benefits in a novel host, can circulate at low frequencies.</p>
</abstract>
<abstract abstract-type="summary"><title>Author Summary</title>
<p>The latest human influenza pandemic highlights the ability of influenza viruses to jump species barriers and emerge in new hosts, as well as the role of pigs in generating viruses with pandemic potential. The mutational power of influenza virus, caused by intrinsically error-prone viral polymerases, has been directly linked to viral emergence, as adaptive mutations present in the reservoir host are likely to be key to the evolution of sustained transmission in new hosts. Hence, studying how mutations are generated, maintained and transmitted in and among pigs is critical to understanding how novel viruses could emerge. Here we characterized the evolution and mutational spectra of influenza virus populations within naïve and vaccinated pigs linked by natural transmission, by analyzing multiple viral sequences obtained at different times post-infection. We show that the genetic make-up of influenza viruses in pigs is highly dynamic: the frequency of particular mutations, including those that could potentially alter host specificity or result in vaccine escape, fluctuated markedly, including one rapid fixation event. We also show that co-infections are common and multiple viruses – even defective ones – were transmitted between pigs despite being vaccinated. Our results provide empirical evidence of the complex dynamics of influenza viral populations in pigs and provide insight on the evolutionary basis of RNA viral emergence.</p>
</abstract>
<counts><page-count count="12"></page-count>
</counts>
</article-meta>
</front>
</pmc>
<affiliations><list><country><li>Royaume-Uni</li>
<li>États-Unis</li>
</country>
<region><li>Angleterre</li>
<li>Angleterre de l'Est</li>
<li>Maryland</li>
<li>New Jersey</li>
<li>Pennsylvanie</li>
</region>
<settlement><li>Cambridge</li>
<li>Princeton (New Jersey)</li>
<li>University Park (Pennsylvanie)</li>
</settlement>
<orgName><li>Université d'État de Pennsylvanie</li>
<li>Université de Cambridge</li>
<li>Université de Princeton</li>
</orgName>
</list>
<tree><country name="Royaume-Uni"><region name="Angleterre"><name sortKey="Murcia, Pablo R" sort="Murcia, Pablo R" uniqKey="Murcia P" first="Pablo R." last="Murcia">Pablo R. Murcia</name>
</region>
<name sortKey="Baillie, Gregory J" sort="Baillie, Gregory J" uniqKey="Baillie G" first="Gregory J." last="Baillie">Gregory J. Baillie</name>
<name sortKey="Battista, Patrizia" sort="Battista, Patrizia" uniqKey="Battista P" first="Patrizia" last="Battista">Patrizia Battista</name>
<name sortKey="Caccamo, Mario" sort="Caccamo, Mario" uniqKey="Caccamo M" first="Mario" last="Caccamo">Mario Caccamo</name>
<name sortKey="Elton, Debra" sort="Elton, Debra" uniqKey="Elton D" first="Debra" last="Elton">Debra Elton</name>
<name sortKey="Hughes, Joseph" sort="Hughes, Joseph" uniqKey="Hughes J" first="Joseph" last="Hughes">Joseph Hughes</name>
<name sortKey="Kellam, Paul" sort="Kellam, Paul" uniqKey="Kellam P" first="Paul" last="Kellam">Paul Kellam</name>
<name sortKey="Lloyd, Lucy" sort="Lloyd, Lucy" uniqKey="Lloyd L" first="Lucy" last="Lloyd">Lucy Lloyd</name>
<name sortKey="Mumford, Jennifer A" sort="Mumford, Jennifer A" uniqKey="Mumford J" first="Jennifer A." last="Mumford">Jennifer A. Mumford</name>
<name sortKey="Murcia, Pablo R" sort="Murcia, Pablo R" uniqKey="Murcia P" first="Pablo R." last="Murcia">Pablo R. Murcia</name>
<name sortKey="Oliver, Karen" sort="Oliver, Karen" uniqKey="Oliver K" first="Karen" last="Oliver">Karen Oliver</name>
<name sortKey="Ormond, Doug" sort="Ormond, Doug" uniqKey="Ormond D" first="Doug" last="Ormond">Doug Ormond</name>
<name sortKey="Ramirez Gonzalez, Ricardo H" sort="Ramirez Gonzalez, Ricardo H" uniqKey="Ramirez Gonzalez R" first="Ricardo H." last="Ramirez-Gonzalez">Ricardo H. Ramirez-Gonzalez</name>
<name sortKey="Wood, James L N" sort="Wood, James L N" uniqKey="Wood J" first="James L. N." last="Wood">James L. N. Wood</name>
</country>
<country name="États-Unis"><region name="New Jersey"><name sortKey="Grenfell, Bryan T" sort="Grenfell, Bryan T" uniqKey="Grenfell B" first="Bryan T." last="Grenfell">Bryan T. Grenfell</name>
</region>
<name sortKey="Grenfell, Bryan T" sort="Grenfell, Bryan T" uniqKey="Grenfell B" first="Bryan T." last="Grenfell">Bryan T. Grenfell</name>
<name sortKey="Holmes, Edward C" sort="Holmes, Edward C" uniqKey="Holmes E" first="Edward C." last="Holmes">Edward C. Holmes</name>
<name sortKey="Holmes, Edward C" sort="Holmes, Edward C" uniqKey="Holmes E" first="Edward C." last="Holmes">Edward C. Holmes</name>
</country>
</tree>
</affiliations>
</record>
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