Cross-Species Transmission and Differential Fate of an Endogenous Retrovirus in Three Mammal Lineages
Identifieur interne : 000E78 ( Pmc/Checkpoint ); précédent : 000E77; suivant : 000E79Cross-Species Transmission and Differential Fate of an Endogenous Retrovirus in Three Mammal Lineages
Auteurs : Xiaoyu Zhuo ; Cédric FeschotteSource :
- PLoS Pathogens [ 1553-7366 ] ; 2015.
Abstract
Endogenous retroviruses (ERVs) arise from retroviruses chromosomally integrated in the host germline. ERVs are common in vertebrate genomes and provide a valuable fossil record of past retroviral infections to investigate the biology and evolution of retroviruses over a deep time scale, including cross-species transmission events. Here we took advantage of a catalog of ERVs we recently produced for the bat
Url:
DOI: 10.1371/journal.ppat.1005279
PubMed: 26562410
PubMed Central: 4643047
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Cross-Species Transmission and Differential Fate of an Endogenous Retrovirus in Three Mammal Lineages</title><author><name sortKey="Zhuo, Xiaoyu" sort="Zhuo, Xiaoyu" uniqKey="Zhuo X" first="Xiaoyu" last="Zhuo">Xiaoyu Zhuo</name><affiliation><nlm:aff id="aff001"></nlm:aff></affiliation></author><author><name sortKey="Feschotte, Cedric" sort="Feschotte, Cedric" uniqKey="Feschotte C" first="Cédric" last="Feschotte">Cédric Feschotte</name><affiliation><nlm:aff id="aff001"></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">26562410</idno><idno type="pmc">4643047</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4643047</idno><idno type="RBID">PMC:4643047</idno><idno type="doi">10.1371/journal.ppat.1005279</idno><date when="2015">2015</date><idno type="wicri:Area/Pmc/Corpus">001096</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">001096</idno><idno type="wicri:Area/Pmc/Curation">001096</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">001096</idno><idno type="wicri:Area/Pmc/Checkpoint">000E78</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Checkpoint">000E78</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Cross-Species Transmission and Differential Fate of an Endogenous Retrovirus in Three Mammal Lineages</title><author><name sortKey="Zhuo, Xiaoyu" sort="Zhuo, Xiaoyu" uniqKey="Zhuo X" first="Xiaoyu" last="Zhuo">Xiaoyu Zhuo</name><affiliation><nlm:aff id="aff001"></nlm:aff></affiliation></author><author><name sortKey="Feschotte, Cedric" sort="Feschotte, Cedric" uniqKey="Feschotte C" first="Cédric" last="Feschotte">Cédric Feschotte</name><affiliation><nlm:aff id="aff001"></nlm:aff></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="2015">2015</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Endogenous retroviruses (ERVs) arise from retroviruses chromosomally integrated in the host germline. ERVs are common in vertebrate genomes and provide a valuable fossil record of past retroviral infections to investigate the biology and evolution of retroviruses over a deep time scale, including cross-species transmission events. Here we took advantage of a catalog of ERVs we recently produced for the bat <italic>Myotis lucifugus</italic> to seek evidence for infiltration of these retroviruses in other mammalian species (>100) currently represented in the genome sequence database. We provide multiple lines of evidence for the cross-ordinal transmission of a gammaretrovirus endogenized independently in the lineages of vespertilionid bats, felid cats and pangolin ~13–25 million years ago. Following its initial introduction, the ERV amplified extensively in parallel in both bat and cat lineages, generating hundreds of species-specific insertions throughout evolution. However, despite being derived from the same viral species, phylogenetic and selection analyses suggest that the ERV experienced different amplification dynamics in the two mammalian lineages. In the cat lineage, the ERV appears to have expanded primarily by retrotransposition of a single proviral progenitor that lost infectious capacity shortly after endogenization. In the bat lineage, the ERV followed a more complex path of germline invasion characterized by both retrotransposition and multiple infection events. The results also suggest that some of the bat ERVs have maintained infectious capacity for extended period of time and may be still infectious today. This study provides one of the most rigorously documented cases of cross-ordinal transmission of a mammalian retrovirus. It also illustrates how the same retrovirus species has transitioned multiple times from an infectious pathogen to a genomic parasite (i.e. retrotransposon), yet experiencing different invasion dynamics in different mammalian hosts.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Parrish, Cr" uniqKey="Parrish C">CR Parrish</name></author><author><name sortKey="Holmes, Ec" uniqKey="Holmes E">EC Holmes</name></author><author><name sortKey="Morens, Dm" uniqKey="Morens D">DM Morens</name></author><author><name sortKey="Park, E C" uniqKey="Park E">E-C Park</name></author><author><name sortKey="Burke, Ds" uniqKey="Burke D">DS Burke</name></author><author><name sortKey="Calisher, Ch" uniqKey="Calisher C">CH Calisher</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Wolfe, Nd" uniqKey="Wolfe N">ND Wolfe</name></author><author><name sortKey="Dunavan, Cp" uniqKey="Dunavan C">CP 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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></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, CA USA</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">26562410</article-id><article-id pub-id-type="pmc">4643047</article-id><article-id pub-id-type="doi">10.1371/journal.ppat.1005279</article-id><article-id pub-id-type="publisher-id">PPATHOGENS-D-15-01561</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group></article-categories><title-group><article-title>Cross-Species Transmission and Differential Fate of an Endogenous Retrovirus in Three Mammal Lineages</article-title><alt-title alt-title-type="running-head">Cross-Species Transmission and Differential Fate of an ERV</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Zhuo</surname><given-names>Xiaoyu</given-names></name><xref ref-type="aff" rid="aff001"></xref></contrib><contrib contrib-type="author"><name><surname>Feschotte</surname><given-names>Cédric</given-names></name><xref rid="cor001" ref-type="corresp">*</xref><xref ref-type="aff" rid="aff001"></xref></contrib></contrib-group><aff id="aff001"><addr-line>Department of Human Genetics, University of Utah School of Medicine, Salt Lake City, Utah, United States of America</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>Belshaw</surname><given-names>Robert</given-names></name><role>Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1"><addr-line>Plymouth University, UNITED KINGDOM</addr-line></aff><author-notes><fn fn-type="COI-statement" id="coi001"><p>The authors have declared that no competing interests exist.</p></fn><fn fn-type="con" id="contrib001"><p>Conceived and designed the experiments: XZ CF. Performed the experiments: XZ. Analyzed the data: XZ CF. Contributed reagents/materials/analysis tools: XZ. Wrote the paper: XZ CF.</p></fn><corresp id="cor001">* E-mail: <email>cedric@genetics.utah.edu</email></corresp></author-notes><pub-date pub-type="epub"><day>12</day><month>11</month><year>2015</year></pub-date><pub-date pub-type="collection"><month>11</month><year>2015</year></pub-date><volume>11</volume><issue>11</issue><elocation-id>e1005279</elocation-id><history><date date-type="received"><day>5</day><month>7</month><year>2015</year></date><date date-type="accepted"><day>23</day><month>10</month><year>2015</year></date></history><permissions><copyright-statement>© 2015 Zhuo, Feschotte</copyright-statement><copyright-year>2015</copyright-year><copyright-holder>Zhuo, Feschotte</copyright-holder><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><self-uri content-type="pdf" xlink:type="simple" xlink:href="ppat.1005279.pdf"></self-uri><abstract><p>Endogenous retroviruses (ERVs) arise from retroviruses chromosomally integrated in the host germline. ERVs are common in vertebrate genomes and provide a valuable fossil record of past retroviral infections to investigate the biology and evolution of retroviruses over a deep time scale, including cross-species transmission events. Here we took advantage of a catalog of ERVs we recently produced for the bat <italic>Myotis lucifugus</italic> to seek evidence for infiltration of these retroviruses in other mammalian species (>100) currently represented in the genome sequence database. We provide multiple lines of evidence for the cross-ordinal transmission of a gammaretrovirus endogenized independently in the lineages of vespertilionid bats, felid cats and pangolin ~13–25 million years ago. Following its initial introduction, the ERV amplified extensively in parallel in both bat and cat lineages, generating hundreds of species-specific insertions throughout evolution. However, despite being derived from the same viral species, phylogenetic and selection analyses suggest that the ERV experienced different amplification dynamics in the two mammalian lineages. In the cat lineage, the ERV appears to have expanded primarily by retrotransposition of a single proviral progenitor that lost infectious capacity shortly after endogenization. In the bat lineage, the ERV followed a more complex path of germline invasion characterized by both retrotransposition and multiple infection events. The results also suggest that some of the bat ERVs have maintained infectious capacity for extended period of time and may be still infectious today. This study provides one of the most rigorously documented cases of cross-ordinal transmission of a mammalian retrovirus. It also illustrates how the same retrovirus species has transitioned multiple times from an infectious pathogen to a genomic parasite (i.e. retrotransposon), yet experiencing different invasion dynamics in different mammalian hosts.</p></abstract><abstract abstract-type="summary"><title>Author Summary</title><p>The cross-species transmission of viruses poses a continuous threat to public health. Bats are increasingly recognized as a major reservoir for zoonotic RNA viruses, including rabies, Ebola, and possibly MERS, but little is known about their capacity to harbor and transmit retroviruses. Here we investigated past incidents of cross-species transmission involving bat retroviruses, by screening for the presence of endogenous retroviruses (ERVs) previously identified in the genome of the little brown bat in more than 100 diverse mammal species. This screen revealed an intriguing case of a gammaretrovirus that independently infiltrated the germ line of species belonging to three mammalian orders: vesper bat, felid cat and pangolin. We found that the ERV initiated its genomic invasion of the three lineages around the same timeframe ~13–25 million years ago, but experienced a different fate in each lineage. In the pangolin lineage, the ERV’s genomic propagation stalled shortly after endogenization, while it amplified continuously throughout felid and vesper bat evolution to generate hundreds of species-specific insertions in each lineage. Furthermore, in the cat lineage genomic amplification appears to have occurred predominantly via retrotransposition; while in bats the ERV has expanded via a mixture of retrotransposition and reinfection activity that may still be ongoing.</p></abstract><funding-group><funding-statement>The work is supported by grant R01-GM077582 from National Institutes of Health (<ext-link ext-link-type="uri" xlink:href="http://www.nih.gov/">http://www.nih.gov/</ext-link>). XZ is also supported by University of Utah graduate research fellowship (<ext-link ext-link-type="uri" xlink:href="https://gradschool.utah.edu/">https://gradschool.utah.edu/</ext-link>). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.</funding-statement></funding-group><counts><fig-count count="5"></fig-count><table-count count="1"></table-count><page-count count="23"></page-count></counts><custom-meta-group><custom-meta id="data-availability"><meta-name>Data Availability</meta-name><meta-value>All relevant data are within the paper and its Supporting Information files.</meta-value></custom-meta></custom-meta-group></article-meta><notes><title>Data Availability</title><p>All relevant data are within the paper and its Supporting Information files.</p></notes></front></pmc><affiliations><list></list><tree><noCountry><name sortKey="Feschotte, Cedric" sort="Feschotte, Cedric" uniqKey="Feschotte C" first="Cédric" last="Feschotte">Cédric Feschotte</name><name sortKey="Zhuo, Xiaoyu" sort="Zhuo, Xiaoyu" uniqKey="Zhuo X" first="Xiaoyu" last="Zhuo">Xiaoyu Zhuo</name></noCountry></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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