Adaptive Gene Amplification As an Intermediate Step in the Expansion of Virus Host Range
Identifieur interne : 001708 ( Main/Exploration ); précédent : 001707; suivant : 001709Adaptive Gene Amplification As an Intermediate Step in the Expansion of Virus Host Range
Auteurs : Greg Brennan [États-Unis] ; Jacob O. Kitzman [États-Unis] ; Stefan Rothenburg [États-Unis] ; Jay Shendure [États-Unis] ; Adam P. Geballe [États-Unis]Source :
- PLoS Pathogens [ 1553-7366 ] ; 2014.
Abstract
The majority of recently emerging infectious diseases in humans is due to cross-species pathogen transmissions from animals. To establish a productive infection in new host species, viruses must overcome barriers to replication mediated by diverse and rapidly evolving host restriction factors such as protein kinase R (PKR). Many viral antagonists of these restriction factors are species specific. For example, the rhesus cytomegalovirus PKR antagonist, RhTRS1, inhibits PKR in some African green monkey (AGM) cells, but does not inhibit human or rhesus macaque PKR. To model the evolutionary changes necessary for cross-species transmission, we generated a recombinant vaccinia virus that expresses RhTRS1 in a strain that lacks PKR inhibitors E3L and K3L (VVΔEΔK+RhTRS1). Serially passaging VVΔEΔK+RhTRS1 in minimally-permissive AGM cells increased viral replication 10- to 100-fold. Notably, adaptation in these AGM cells also improved virus replication 1000- to 10,000-fold in human and rhesus cells. Genetic analyses including deep sequencing revealed amplification of the
Url:
DOI: 10.1371/journal.ppat.1004002
PubMed: 24626510
PubMed Central: 3953438
Affiliations:
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Kitzman</name><affiliation wicri:level="4"><nlm:aff id="aff2"><addr-line>Department of Genome Sciences, University of Washington, Seattle, Washington, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Genome Sciences, University of Washington, Seattle, Washington</wicri:regionArea><placeName><region type="state">Washington (État)</region><settlement type="city">Seattle</settlement></placeName><orgName type="university">Université de Washington</orgName></affiliation></author><author><name sortKey="Rothenburg, Stefan" sort="Rothenburg, Stefan" uniqKey="Rothenburg S" first="Stefan" last="Rothenburg">Stefan Rothenburg</name><affiliation wicri:level="2"><nlm:aff id="aff3"><addr-line>Division of Biology, Kansas State University, Manhattan, Kansas, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Division of Biology, Kansas State University, Manhattan, Kansas</wicri:regionArea><placeName><region type="state">Kansas</region></placeName></affiliation></author><author><name sortKey="Shendure, Jay" sort="Shendure, Jay" uniqKey="Shendure J" first="Jay" last="Shendure">Jay Shendure</name><affiliation wicri:level="4"><nlm:aff id="aff2"><addr-line>Department of Genome Sciences, University of Washington, Seattle, Washington, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Genome Sciences, University of Washington, Seattle, Washington</wicri:regionArea><placeName><region type="state">Washington (État)</region><settlement type="city">Seattle</settlement></placeName><orgName type="university">Université de Washington</orgName></affiliation></author><author><name sortKey="Geballe, Adam P" sort="Geballe, Adam P" uniqKey="Geballe A" first="Adam P." last="Geballe">Adam P. Geballe</name><affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Division of Human Biology, Fred Hutchinson Cancer Research Center, Seattle, Washington, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Division of Human Biology, Fred Hutchinson Cancer Research Center, Seattle, Washington</wicri:regionArea><placeName><region type="state">Washington (État)</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="aff4"><addr-line>Division of Clinical Research, Fred Hutchinson Cancer Research Center, Seattle, Washington, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Division of Clinical Research, Fred Hutchinson Cancer Research Center, Seattle, Washington</wicri:regionArea><placeName><region type="state">Washington (État)</region></placeName></affiliation><affiliation wicri:level="4"><nlm:aff id="aff5"><addr-line>Departments of Microbiology and Medicine, University of Washington, Seattle, Washington, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Departments of Microbiology and Medicine, University of Washington, Seattle, Washington</wicri:regionArea><placeName><region type="state">Washington (État)</region><settlement type="city">Seattle</settlement></placeName><orgName type="university">Université de Washington</orgName></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="2014">2014</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>The majority of recently emerging infectious diseases in humans is due to cross-species pathogen transmissions from animals. To establish a productive infection in new host species, viruses must overcome barriers to replication mediated by diverse and rapidly evolving host restriction factors such as protein kinase R (PKR). Many viral antagonists of these restriction factors are species specific. For example, the rhesus cytomegalovirus PKR antagonist, RhTRS1, inhibits PKR in some African green monkey (AGM) cells, but does not inhibit human or rhesus macaque PKR. To model the evolutionary changes necessary for cross-species transmission, we generated a recombinant vaccinia virus that expresses RhTRS1 in a strain that lacks PKR inhibitors E3L and K3L (VVΔEΔK+RhTRS1). Serially passaging VVΔEΔK+RhTRS1 in minimally-permissive AGM cells increased viral replication 10- to 100-fold. Notably, adaptation in these AGM cells also improved virus replication 1000- to 10,000-fold in human and rhesus cells. Genetic analyses including deep sequencing revealed amplification of the <italic>rhtrs1</italic> locus in the adapted viruses. Supplying additional <italic>rhtrs1</italic> in <italic>trans</italic> confirmed that amplification alone was sufficient to improve VVΔEΔK+RhTRS1 replication. Viruses with amplified <italic>rhtrs1</italic> completely blocked AGM PKR, but only partially blocked human PKR, consistent with the replication properties of these viruses in AGM and human cells. Finally, in contrast to AGM-adapted viruses, which could be serially propagated in human cells, VVΔEΔK+RhTRS1 yielded no progeny virus after only three passages in human cells. Thus, <italic>rhtrs1</italic> amplification in a minimally permissive intermediate host was a necessary step, enabling expansion of the virus range to previously nonpermissive hosts. These data support the hypothesis that amplification of a weak viral antagonist may be a general evolutionary mechanism to permit replication in otherwise resistant host species, providing a molecular foothold that could enable further adaptations necessary for efficient replication in the new host.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Yamada, A" uniqKey="Yamada A">A Yamada</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Mahy, Bw" uniqKey="Mahy B">BW Mahy</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Bengis, Rg" uniqKey="Bengis R">RG Bengis</name></author><author><name sortKey="Leighton, Fa" uniqKey="Leighton F">FA Leighton</name></author><author><name sortKey="Fischer, Jr" uniqKey="Fischer J">JR Fischer</name></author><author><name sortKey="Artois, M" uniqKey="Artois M">M Artois</name></author><author><name sortKey="Morner, T" uniqKey="Morner 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Chenna</name></author><author><name sortKey="Sugawara, H" uniqKey="Sugawara H">H Sugawara</name></author><author><name sortKey="Koike, T" uniqKey="Koike T">T Koike</name></author><author><name sortKey="Lopez, R" uniqKey="Lopez R">R Lopez</name></author><author><name sortKey="Gibson, Tj" uniqKey="Gibson T">TJ Gibson</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Esposito, J" uniqKey="Esposito J">J Esposito</name></author><author><name sortKey="Condit, R" uniqKey="Condit R">R Condit</name></author><author><name sortKey="Obijeski, J" uniqKey="Obijeski J">J Obijeski</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Simpson, Jt" uniqKey="Simpson J">JT Simpson</name></author><author><name sortKey="Wong, K" uniqKey="Wong K">K Wong</name></author><author><name sortKey="Jackman, Sd" uniqKey="Jackman S">SD Jackman</name></author><author><name sortKey="Schein, Je" uniqKey="Schein J">JE Schein</name></author><author><name sortKey="Jones, Sj" uniqKey="Jones S">SJ Jones</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Li, H" uniqKey="Li H">H Li</name></author><author><name sortKey="Durbin, R" uniqKey="Durbin R">R Durbin</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Mckenna, A" uniqKey="Mckenna A">A McKenna</name></author><author><name sortKey="Hanna, M" uniqKey="Hanna M">M Hanna</name></author><author><name sortKey="Banks, E" uniqKey="Banks E">E Banks</name></author><author><name sortKey="Sivachenko, A" uniqKey="Sivachenko A">A Sivachenko</name></author><author><name sortKey="Cibulskis, K" uniqKey="Cibulskis K">K Cibulskis</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Li, H" uniqKey="Li H">H Li</name></author><author><name sortKey="Durbin, R" uniqKey="Durbin R">R Durbin</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Kurtz, S" uniqKey="Kurtz S">S Kurtz</name></author><author><name sortKey="Phillippy, A" uniqKey="Phillippy A">A Phillippy</name></author><author><name sortKey="Delcher, Al" uniqKey="Delcher A">AL Delcher</name></author><author><name sortKey="Smoot, M" uniqKey="Smoot M">M Smoot</name></author><author><name sortKey="Shumway, M" uniqKey="Shumway M">M Shumway</name></author></analytic></biblStruct></listBibl></div1></back></TEI><affiliations><list><country><li>États-Unis</li></country><region><li>Kansas</li><li>Washington (État)</li></region><settlement><li>Seattle</li></settlement><orgName><li>Université de Washington</li></orgName></list><tree><country name="États-Unis"><region name="Washington (État)"><name sortKey="Brennan, Greg" sort="Brennan, Greg" uniqKey="Brennan G" first="Greg" last="Brennan">Greg Brennan</name></region><name sortKey="Geballe, Adam P" sort="Geballe, Adam P" uniqKey="Geballe A" first="Adam P." last="Geballe">Adam P. Geballe</name><name sortKey="Geballe, Adam P" sort="Geballe, Adam P" uniqKey="Geballe A" first="Adam P." last="Geballe">Adam P. Geballe</name><name sortKey="Geballe, Adam P" sort="Geballe, Adam P" uniqKey="Geballe A" first="Adam P." last="Geballe">Adam P. Geballe</name><name sortKey="Kitzman, Jacob O" sort="Kitzman, Jacob O" uniqKey="Kitzman J" first="Jacob O." last="Kitzman">Jacob O. Kitzman</name><name sortKey="Rothenburg, Stefan" sort="Rothenburg, Stefan" uniqKey="Rothenburg S" first="Stefan" last="Rothenburg">Stefan Rothenburg</name><name sortKey="Shendure, Jay" sort="Shendure, Jay" uniqKey="Shendure J" first="Jay" last="Shendure">Jay Shendure</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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