Early endonuclease-mediated evasion of RNA sensing ensures efficient coronavirus replication
Identifieur interne : 000878 ( Pmc/Checkpoint ); précédent : 000877; suivant : 000879Early endonuclease-mediated evasion of RNA sensing ensures efficient coronavirus replication
Auteurs : Eveline Kindler [Suisse] ; Cristina Gil-Cruz [Suisse] ; Julia Spanier [Allemagne] ; Yize Li [États-Unis] ; Jochen Wilhelm [Allemagne] ; Huib H. Rabouw [Pays-Bas] ; Roland Züst [Singapour] ; Mihyun Hwang [États-Unis] ; Philip V Ovski [Suisse] ; Hanspeter Stalder [Suisse] ; Sabrina Marti [Suisse] ; Matthias Habjan [Allemagne] ; Luisa Cervantes-Barragan [États-Unis] ; Ruth Elliot [États-Unis] ; Nadja Karl [Allemagne] ; Christina Gaughan [États-Unis] ; Frank J. M. Van Kuppeveld [Pays-Bas] ; Robert H. Silverman [États-Unis] ; Markus Keller [Allemagne] ; Burkhard Ludewig [Suisse] ; Cornelia C. Bergmann [États-Unis] ; John Ziebuhr [Allemagne] ; Susan R. Weiss [États-Unis] ; Ulrich Kalinke [Allemagne] ; Volker Thiel [Suisse]Source :
- PLoS Pathogens [ 1553-7366 ] ; 2017.
Abstract
Coronaviruses are of veterinary and medical importance and include highly pathogenic zoonotic viruses, such as SARS-CoV and MERS-CoV. They are known to efficiently evade early innate immune responses, manifesting in almost negligible expression of type-I interferons (IFN-I). This evasion strategy suggests an evolutionary conserved viral function that has evolved to prevent RNA-based sensing of infection in vertebrate hosts. Here we show that the coronavirus endonuclease (EndoU) activity is key to prevent early induction of double-stranded RNA (dsRNA) host cell responses. Replication of EndoU-deficient coronaviruses is greatly attenuated
Url:
DOI: 10.1371/journal.ppat.1006195
PubMed: 28158275
PubMed Central: 5310923
Affiliations:
- Allemagne, Pays-Bas, Singapour, Suisse, États-Unis
- Basse-Saxe, Canton de Berne, Missouri (État), Ohio, Pennsylvanie, Utrecht (province)
- Berne, Hanovre, Saint-Louis (Missouri), Utrecht
- Université d'Utrecht, Université de Berne, École de médecine (Université Washington de Saint-Louis)
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PMC:5310923Le document en format XML
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Early endonuclease-mediated evasion of RNA sensing ensures efficient coronavirus replication</title>
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</author>
<author><name sortKey="Spanier, Julia" sort="Spanier, Julia" uniqKey="Spanier J" first="Julia" last="Spanier">Julia Spanier</name>
<affiliation wicri:level="3"><nlm:aff id="aff004"><addr-line>Institute for Experimental Infection Research, TWINCORE, Centre for Experimental and Clinical Infection Research, a joint venture between the Helmholtz Centre for Infection Research and the Hannover Medical School, Hannover, Germany</addr-line>
</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Institute for Experimental Infection Research, TWINCORE, Centre for Experimental and Clinical Infection Research, a joint venture between the Helmholtz Centre for Infection Research and the Hannover Medical School, Hannover</wicri:regionArea>
<placeName><region type="land" nuts="2">Basse-Saxe</region>
<settlement type="city">Hanovre</settlement>
</placeName>
</affiliation>
</author>
<author><name sortKey="Li, Yize" sort="Li, Yize" uniqKey="Li Y" first="Yize" last="Li">Yize Li</name>
<affiliation wicri:level="2"><nlm:aff id="aff005"><addr-line>Department of Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, United States of America</addr-line>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA</wicri:regionArea>
<placeName><region type="state">Pennsylvanie</region>
</placeName>
</affiliation>
</author>
<author><name sortKey="Wilhelm, Jochen" sort="Wilhelm, Jochen" uniqKey="Wilhelm J" first="Jochen" last="Wilhelm">Jochen Wilhelm</name>
<affiliation wicri:level="1"><nlm:aff id="aff006"><addr-line>Universities Giessen & Marburg Lung Center (UGMLC), Deutsches Zentrum für Lungenforschung (DZL), Giessen, Germany</addr-line>
</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Universities Giessen & Marburg Lung Center (UGMLC), Deutsches Zentrum für Lungenforschung (DZL), Giessen</wicri:regionArea>
<wicri:noRegion>Giessen</wicri:noRegion>
<wicri:noRegion>Giessen</wicri:noRegion>
<wicri:noRegion>Giessen</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Rabouw, Huib H" sort="Rabouw, Huib H" uniqKey="Rabouw H" first="Huib H." last="Rabouw">Huib H. Rabouw</name>
<affiliation wicri:level="4"><nlm:aff id="aff007"><addr-line>Virology Division, Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands</addr-line>
</nlm:aff>
<country xml:lang="fr">Pays-Bas</country>
<wicri:regionArea>Virology Division, Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, Utrecht</wicri:regionArea>
<placeName><settlement type="city">Utrecht</settlement>
<region nuts="2" type="province">Utrecht (province)</region>
</placeName>
<orgName type="university">Université d'Utrecht</orgName>
</affiliation>
</author>
<author><name sortKey="Zust, Roland" sort="Zust, Roland" uniqKey="Zust R" first="Roland" last="Züst">Roland Züst</name>
<affiliation wicri:level="1"><nlm:aff id="aff008"><addr-line>Singapore Immunology Network, Singapore</addr-line>
</nlm:aff>
<country xml:lang="fr">Singapour</country>
<wicri:regionArea>Singapore Immunology Network</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Hwang, Mihyun" sort="Hwang, Mihyun" uniqKey="Hwang M" first="Mihyun" last="Hwang">Mihyun Hwang</name>
<affiliation wicri:level="2"><nlm:aff id="aff009"><addr-line>Department of Neurosciences, Lerner Research Institute, Cleveland Clinic Foundation, Cleveland, Ohio, United States of America</addr-line>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Neurosciences, Lerner Research Institute, Cleveland Clinic Foundation, Cleveland, Ohio</wicri:regionArea>
<placeName><region type="state">Ohio</region>
</placeName>
</affiliation>
</author>
<author><name sortKey="V Ovski, Philip" sort="V Ovski, Philip" uniqKey="V Ovski P" first="Philip" last="V Ovski">Philip V Ovski</name>
<affiliation wicri:level="4"><nlm:aff id="aff001"><addr-line>Department of Infectious Diseases and Pathobiology, University of Bern, Bern, Switzerland</addr-line>
</nlm:aff>
<country xml:lang="fr">Suisse</country>
<wicri:regionArea>Department of Infectious Diseases and Pathobiology, University of Bern, Bern</wicri:regionArea>
<placeName><settlement type="city">Berne</settlement>
<region type="région" nuts="3">Canton de Berne</region>
</placeName>
<orgName type="university">Université de Berne</orgName>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff002"><addr-line>Federal Department of Home Affairs, Institute of Virology and Immunology, Bern and Mittelhäusern, Switzerland</addr-line>
</nlm:aff>
<country xml:lang="fr">Suisse</country>
<wicri:regionArea>Federal Department of Home Affairs, Institute of Virology and Immunology, Bern and Mittelhäusern</wicri:regionArea>
<wicri:noRegion>Bern and Mittelhäusern</wicri:noRegion>
</affiliation>
<affiliation wicri:level="4"><nlm:aff id="aff010"><addr-line>Graduate School for Biomedical Science, University of Bern, Bern, Switzerland</addr-line>
</nlm:aff>
<country xml:lang="fr">Suisse</country>
<wicri:regionArea>Graduate School for Biomedical Science, University of Bern, Bern</wicri:regionArea>
<placeName><settlement type="city">Berne</settlement>
<region type="région" nuts="3">Canton de Berne</region>
</placeName>
<orgName type="university">Université de Berne</orgName>
</affiliation>
</author>
<author><name sortKey="Stalder, Hanspeter" sort="Stalder, Hanspeter" uniqKey="Stalder H" first="Hanspeter" last="Stalder">Hanspeter Stalder</name>
<affiliation wicri:level="4"><nlm:aff id="aff001"><addr-line>Department of Infectious Diseases and Pathobiology, University of Bern, Bern, Switzerland</addr-line>
</nlm:aff>
<country xml:lang="fr">Suisse</country>
<wicri:regionArea>Department of Infectious Diseases and Pathobiology, University of Bern, Bern</wicri:regionArea>
<placeName><settlement type="city">Berne</settlement>
<region type="région" nuts="3">Canton de Berne</region>
</placeName>
<orgName type="university">Université de Berne</orgName>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff002"><addr-line>Federal Department of Home Affairs, Institute of Virology and Immunology, Bern and Mittelhäusern, Switzerland</addr-line>
</nlm:aff>
<country xml:lang="fr">Suisse</country>
<wicri:regionArea>Federal Department of Home Affairs, Institute of Virology and Immunology, Bern and Mittelhäusern</wicri:regionArea>
<wicri:noRegion>Bern and Mittelhäusern</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Marti, Sabrina" sort="Marti, Sabrina" uniqKey="Marti S" first="Sabrina" last="Marti">Sabrina Marti</name>
<affiliation wicri:level="4"><nlm:aff id="aff001"><addr-line>Department of Infectious Diseases and Pathobiology, University of Bern, Bern, Switzerland</addr-line>
</nlm:aff>
<country xml:lang="fr">Suisse</country>
<wicri:regionArea>Department of Infectious Diseases and Pathobiology, University of Bern, Bern</wicri:regionArea>
<placeName><settlement type="city">Berne</settlement>
<region type="région" nuts="3">Canton de Berne</region>
</placeName>
<orgName type="university">Université de Berne</orgName>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff002"><addr-line>Federal Department of Home Affairs, Institute of Virology and Immunology, Bern and Mittelhäusern, Switzerland</addr-line>
</nlm:aff>
<country xml:lang="fr">Suisse</country>
<wicri:regionArea>Federal Department of Home Affairs, Institute of Virology and Immunology, Bern and Mittelhäusern</wicri:regionArea>
<wicri:noRegion>Bern and Mittelhäusern</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Habjan, Matthias" sort="Habjan, Matthias" uniqKey="Habjan M" first="Matthias" last="Habjan">Matthias Habjan</name>
<affiliation wicri:level="1"><nlm:aff id="aff011"><addr-line>Max-Planck-Institute of Biochemistry, Martinsried, Germany</addr-line>
</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Max-Planck-Institute of Biochemistry, Martinsried</wicri:regionArea>
<wicri:noRegion>Martinsried</wicri:noRegion>
<wicri:noRegion>Martinsried</wicri:noRegion>
<wicri:noRegion>Martinsried</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Cervantes Barragan, Luisa" sort="Cervantes Barragan, Luisa" uniqKey="Cervantes Barragan L" first="Luisa" last="Cervantes-Barragan">Luisa Cervantes-Barragan</name>
<affiliation wicri:level="4"><nlm:aff id="aff012"><addr-line>Washington University School of Medicine, St. Louis, MO, USA</addr-line>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Washington University School of Medicine, St. Louis, MO</wicri:regionArea>
<placeName><region type="state">Missouri (État)</region>
<settlement type="city">Saint-Louis (Missouri)</settlement>
</placeName>
<orgName type="university">École de médecine (Université Washington de Saint-Louis)</orgName>
</affiliation>
</author>
<author><name sortKey="Elliot, Ruth" sort="Elliot, Ruth" uniqKey="Elliot R" first="Ruth" last="Elliot">Ruth Elliot</name>
<affiliation wicri:level="2"><nlm:aff id="aff005"><addr-line>Department of Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, United States of America</addr-line>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA</wicri:regionArea>
<placeName><region type="state">Pennsylvanie</region>
</placeName>
</affiliation>
</author>
<author><name sortKey="Karl, Nadja" sort="Karl, Nadja" uniqKey="Karl N" first="Nadja" last="Karl">Nadja Karl</name>
<affiliation wicri:level="1"><nlm:aff id="aff013"><addr-line>Institute for Medical Virology, Justus-Liebig-University, Giessen, Germany</addr-line>
</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Institute for Medical Virology, Justus-Liebig-University, Giessen</wicri:regionArea>
<wicri:noRegion>Giessen</wicri:noRegion>
<wicri:noRegion>Giessen</wicri:noRegion>
<wicri:noRegion>Giessen</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Gaughan, Christina" sort="Gaughan, Christina" uniqKey="Gaughan C" first="Christina" last="Gaughan">Christina Gaughan</name>
<affiliation wicri:level="2"><nlm:aff id="aff014"><addr-line>Department of Cancer Biology, Lerner Research Institute, Cleveland, Ohio, United States of America</addr-line>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Cancer Biology, Lerner Research Institute, Cleveland, Ohio</wicri:regionArea>
<placeName><region type="state">Ohio</region>
</placeName>
</affiliation>
</author>
<author><name sortKey="Van Kuppeveld, Frank J M" sort="Van Kuppeveld, Frank J M" uniqKey="Van Kuppeveld F" first="Frank J. M." last="Van Kuppeveld">Frank J. M. Van Kuppeveld</name>
<affiliation wicri:level="4"><nlm:aff id="aff007"><addr-line>Virology Division, Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands</addr-line>
</nlm:aff>
<country xml:lang="fr">Pays-Bas</country>
<wicri:regionArea>Virology Division, Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, Utrecht</wicri:regionArea>
<placeName><settlement type="city">Utrecht</settlement>
<region nuts="2" type="province">Utrecht (province)</region>
</placeName>
<orgName type="university">Université d'Utrecht</orgName>
</affiliation>
</author>
<author><name sortKey="Silverman, Robert H" sort="Silverman, Robert H" uniqKey="Silverman R" first="Robert H." last="Silverman">Robert H. Silverman</name>
<affiliation wicri:level="2"><nlm:aff id="aff014"><addr-line>Department of Cancer Biology, Lerner Research Institute, Cleveland, Ohio, United States of America</addr-line>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Cancer Biology, Lerner Research Institute, Cleveland, Ohio</wicri:regionArea>
<placeName><region type="state">Ohio</region>
</placeName>
</affiliation>
</author>
<author><name sortKey="Keller, Markus" sort="Keller, Markus" uniqKey="Keller M" first="Markus" last="Keller">Markus Keller</name>
<affiliation wicri:level="1"><nlm:aff id="aff015"><addr-line>Institute of Novel and Emerging Infectious Diseases, Friedrich-Loeffler-Institut, Greifswald-Insel Riems, Germany</addr-line>
</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Institute of Novel and Emerging Infectious Diseases, Friedrich-Loeffler-Institut, Greifswald-Insel Riems</wicri:regionArea>
<wicri:noRegion>Greifswald-Insel Riems</wicri:noRegion>
<wicri:noRegion>Greifswald-Insel Riems</wicri:noRegion>
<wicri:noRegion>Greifswald-Insel Riems</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Ludewig, Burkhard" sort="Ludewig, Burkhard" uniqKey="Ludewig B" first="Burkhard" last="Ludewig">Burkhard Ludewig</name>
<affiliation wicri:level="1"><nlm:aff id="aff003"><addr-line>Institute of Immunobiology, Kantonsspital St.Gallen, St.Gallen, Switzerland</addr-line>
</nlm:aff>
<country xml:lang="fr">Suisse</country>
<wicri:regionArea>Institute of Immunobiology, Kantonsspital St.Gallen, St.Gallen</wicri:regionArea>
<wicri:noRegion>St.Gallen</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Bergmann, Cornelia C" sort="Bergmann, Cornelia C" uniqKey="Bergmann C" first="Cornelia C." last="Bergmann">Cornelia C. Bergmann</name>
<affiliation wicri:level="2"><nlm:aff id="aff009"><addr-line>Department of Neurosciences, Lerner Research Institute, Cleveland Clinic Foundation, Cleveland, Ohio, United States of America</addr-line>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Neurosciences, Lerner Research Institute, Cleveland Clinic Foundation, Cleveland, Ohio</wicri:regionArea>
<placeName><region type="state">Ohio</region>
</placeName>
</affiliation>
</author>
<author><name sortKey="Ziebuhr, John" sort="Ziebuhr, John" uniqKey="Ziebuhr J" first="John" last="Ziebuhr">John Ziebuhr</name>
<affiliation wicri:level="1"><nlm:aff id="aff013"><addr-line>Institute for Medical Virology, Justus-Liebig-University, Giessen, Germany</addr-line>
</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Institute for Medical Virology, Justus-Liebig-University, Giessen</wicri:regionArea>
<wicri:noRegion>Giessen</wicri:noRegion>
<wicri:noRegion>Giessen</wicri:noRegion>
<wicri:noRegion>Giessen</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Weiss, Susan R" sort="Weiss, Susan R" uniqKey="Weiss S" first="Susan R." last="Weiss">Susan R. Weiss</name>
<affiliation wicri:level="2"><nlm:aff id="aff005"><addr-line>Department of Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, United States of America</addr-line>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA</wicri:regionArea>
<placeName><region type="state">Pennsylvanie</region>
</placeName>
</affiliation>
</author>
<author><name sortKey="Kalinke, Ulrich" sort="Kalinke, Ulrich" uniqKey="Kalinke U" first="Ulrich" last="Kalinke">Ulrich Kalinke</name>
<affiliation wicri:level="3"><nlm:aff id="aff004"><addr-line>Institute for Experimental Infection Research, TWINCORE, Centre for Experimental and Clinical Infection Research, a joint venture between the Helmholtz Centre for Infection Research and the Hannover Medical School, Hannover, Germany</addr-line>
</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Institute for Experimental Infection Research, TWINCORE, Centre for Experimental and Clinical Infection Research, a joint venture between the Helmholtz Centre for Infection Research and the Hannover Medical School, Hannover</wicri:regionArea>
<placeName><region type="land" nuts="2">Basse-Saxe</region>
<settlement type="city">Hanovre</settlement>
</placeName>
</affiliation>
</author>
<author><name sortKey="Thiel, Volker" sort="Thiel, Volker" uniqKey="Thiel V" first="Volker" last="Thiel">Volker Thiel</name>
<affiliation wicri:level="4"><nlm:aff id="aff001"><addr-line>Department of Infectious Diseases and Pathobiology, University of Bern, Bern, Switzerland</addr-line>
</nlm:aff>
<country xml:lang="fr">Suisse</country>
<wicri:regionArea>Department of Infectious Diseases and Pathobiology, University of Bern, Bern</wicri:regionArea>
<placeName><settlement type="city">Berne</settlement>
<region type="région" nuts="3">Canton de Berne</region>
</placeName>
<orgName type="university">Université de Berne</orgName>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff002"><addr-line>Federal Department of Home Affairs, Institute of Virology and Immunology, Bern and Mittelhäusern, Switzerland</addr-line>
</nlm:aff>
<country xml:lang="fr">Suisse</country>
<wicri:regionArea>Federal Department of Home Affairs, Institute of Virology and Immunology, Bern and Mittelhäusern</wicri:regionArea>
<wicri:noRegion>Bern and Mittelhäusern</wicri:noRegion>
</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="2017">2017</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
</fileDesc>
<profileDesc><textClass></textClass>
</profileDesc>
</teiHeader>
<front><div type="abstract" xml:lang="en"><p>Coronaviruses are of veterinary and medical importance and include highly pathogenic zoonotic viruses, such as SARS-CoV and MERS-CoV. They are known to efficiently evade early innate immune responses, manifesting in almost negligible expression of type-I interferons (IFN-I). This evasion strategy suggests an evolutionary conserved viral function that has evolved to prevent RNA-based sensing of infection in vertebrate hosts. Here we show that the coronavirus endonuclease (EndoU) activity is key to prevent early induction of double-stranded RNA (dsRNA) host cell responses. Replication of EndoU-deficient coronaviruses is greatly attenuated <italic>in vivo</italic>
and severely restricted in primary cells even during the early phase of the infection. In macrophages we found immediate induction of IFN-I expression and RNase L-mediated breakdown of ribosomal RNA. Accordingly, EndoU-deficient viruses can retain replication only in cells that are deficient in IFN-I expression or sensing, and in cells lacking both RNase L and PKR. Collectively our results demonstrate that the coronavirus EndoU efficiently prevents simultaneous activation of host cell dsRNA sensors, such as Mda5, OAS and PKR. The localization of the EndoU activity at the site of viral RNA synthesis–within the replicase complex—suggests that coronaviruses have evolved a viral RNA decay pathway to evade early innate and intrinsic antiviral host cell responses.</p>
</div>
</front>
<back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Tenoever, Br" uniqKey="Tenoever B">BR tenOever</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Schneider, Wm" uniqKey="Schneider W">WM Schneider</name>
</author>
<author><name sortKey="Chevillotte, Md" uniqKey="Chevillotte M">MD Chevillotte</name>
</author>
<author><name sortKey="Rice, Cm" uniqKey="Rice C">CM Rice</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Channappanavar, R" uniqKey="Channappanavar R">R Channappanavar</name>
</author>
<author><name sortKey="Fehr, Ar" uniqKey="Fehr A">AR Fehr</name>
</author>
<author><name sortKey="Vijay, R" uniqKey="Vijay R">R Vijay</name>
</author>
<author><name sortKey="Mack, M" uniqKey="Mack M">M Mack</name>
</author>
<author><name sortKey="Zhao, J" uniqKey="Zhao J">J Zhao</name>
</author>
<author><name sortKey="Meyerholz, Dk" uniqKey="Meyerholz D">DK Meyerholz</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Zhou, H" uniqKey="Zhou H">H Zhou</name>
</author>
<author><name sortKey="Perlman, S" uniqKey="Perlman S">S Perlman</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Kindler, E" uniqKey="Kindler E">E Kindler</name>
</author>
<author><name sortKey="Jonsdottir, Hr" uniqKey="Jonsdottir H">HR Jonsdottir</name>
</author>
<author><name sortKey="Muth, D" uniqKey="Muth D">D Muth</name>
</author>
<author><name sortKey="Hamming, Oj" uniqKey="Hamming O">OJ Hamming</name>
</author>
<author><name sortKey="Hartmann, R" uniqKey="Hartmann R">R Hartmann</name>
</author>
<author><name sortKey="Rodriguez, R" uniqKey="Rodriguez R">R Rodriguez</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Roth Cross, Jk" uniqKey="Roth Cross J">JK Roth-Cross</name>
</author>
<author><name sortKey="Martinez Sobrido, L" uniqKey="Martinez Sobrido L">L Martinez-Sobrido</name>
</author>
<author><name sortKey="Scott, Ep" uniqKey="Scott E">EP Scott</name>
</author>
<author><name sortKey="Garcia Sastre, A" uniqKey="Garcia Sastre A">A Garcia-Sastre</name>
</author>
<author><name sortKey="Weiss, Sr" uniqKey="Weiss S">SR Weiss</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Daffis, S" uniqKey="Daffis S">S Daffis</name>
</author>
<author><name sortKey="Szretter, K" uniqKey="Szretter K">K Szretter</name>
</author>
<author><name sortKey="Schriewer, J" uniqKey="Schriewer J">J Schriewer</name>
</author>
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</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Knoops, K" uniqKey="Knoops K">K Knoops</name>
</author>
<author><name sortKey="Kikkert, M" uniqKey="Kikkert M">M Kikkert</name>
</author>
<author><name sortKey="Worm, Sh" uniqKey="Worm S">SH Worm</name>
</author>
<author><name sortKey="Zevenhoven Dobbe, Jc" uniqKey="Zevenhoven Dobbe J">JC Zevenhoven-Dobbe</name>
</author>
<author><name sortKey="Van Der Meer, Y" uniqKey="Van Der Meer Y">Y van der Meer</name>
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<author><name sortKey="Koster, Aj" uniqKey="Koster A">AJ Koster</name>
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</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Zust, R" uniqKey="Zust R">R Zust</name>
</author>
<author><name sortKey="Cervantes Barragan, L" uniqKey="Cervantes Barragan L">L Cervantes-Barragan</name>
</author>
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</author>
<author><name sortKey="Maier, R" uniqKey="Maier R">R Maier</name>
</author>
<author><name sortKey="Neuman, Bw" uniqKey="Neuman B">BW Neuman</name>
</author>
<author><name sortKey="Ziebuhr, J" uniqKey="Ziebuhr J">J Ziebuhr</name>
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</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Kamitani, W" uniqKey="Kamitani W">W Kamitani</name>
</author>
<author><name sortKey="Narayanan, K" uniqKey="Narayanan K">K Narayanan</name>
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</author>
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</author>
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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, CA USA</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">28158275</article-id>
<article-id pub-id-type="pmc">5310923</article-id>
<article-id pub-id-type="doi">10.1371/journal.ppat.1006195</article-id>
<article-id pub-id-type="publisher-id">PPATHOGENS-D-16-01691</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Cell Biology</subject>
<subj-group><subject>Cellular Types</subject>
<subj-group><subject>Animal Cells</subject>
<subj-group><subject>Blood Cells</subject>
<subj-group><subject>White Blood Cells</subject>
<subj-group><subject>Macrophages</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Cell Biology</subject>
<subj-group><subject>Cellular Types</subject>
<subj-group><subject>Animal Cells</subject>
<subj-group><subject>Immune Cells</subject>
<subj-group><subject>White Blood Cells</subject>
<subj-group><subject>Macrophages</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Immunology</subject>
<subj-group><subject>Immune Cells</subject>
<subj-group><subject>White Blood Cells</subject>
<subj-group><subject>Macrophages</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject>
<subj-group><subject>Immunology</subject>
<subj-group><subject>Immune Cells</subject>
<subj-group><subject>White Blood Cells</subject>
<subj-group><subject>Macrophages</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Microbiology</subject>
<subj-group><subject>Virology</subject>
<subj-group><subject>Viral Replication</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject>
<subj-group><subject>Biochemistry</subject>
<subj-group><subject>Proteins</subject>
<subj-group><subject>DNA-binding proteins</subject>
<subj-group><subject>Nucleases</subject>
<subj-group><subject>Ribonucleases</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Biochemistry</subject>
<subj-group><subject>Enzymology</subject>
<subj-group><subject>Enzymes</subject>
<subj-group><subject>Hydrolases</subject>
<subj-group><subject>Nucleases</subject>
<subj-group><subject>Ribonucleases</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Biochemistry</subject>
<subj-group><subject>Proteins</subject>
<subj-group><subject>Enzymes</subject>
<subj-group><subject>Hydrolases</subject>
<subj-group><subject>Nucleases</subject>
<subj-group><subject>Ribonucleases</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject>
<subj-group><subject>Organisms</subject>
<subj-group><subject>Viruses</subject>
<subj-group><subject>RNA viruses</subject>
<subj-group><subject>Coronaviruses</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Microbiology</subject>
<subj-group><subject>Medical Microbiology</subject>
<subj-group><subject>Microbial Pathogens</subject>
<subj-group><subject>Viral Pathogens</subject>
<subj-group><subject>Coronaviruses</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject>
<subj-group><subject>Pathology and Laboratory Medicine</subject>
<subj-group><subject>Pathogens</subject>
<subj-group><subject>Microbial Pathogens</subject>
<subj-group><subject>Viral Pathogens</subject>
<subj-group><subject>Coronaviruses</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Organisms</subject>
<subj-group><subject>Viruses</subject>
<subj-group><subject>Viral Pathogens</subject>
<subj-group><subject>Coronaviruses</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Research and analysis methods</subject>
<subj-group><subject>Chemical synthesis</subject>
<subj-group><subject>Biosynthetic techniques</subject>
<subj-group><subject>Nucleic acid synthesis</subject>
<subj-group><subject>RNA synthesis</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject>
<subj-group><subject>Biochemistry</subject>
<subj-group><subject>Nucleic acids</subject>
<subj-group><subject>RNA</subject>
<subj-group><subject>RNA synthesis</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Microbiology</subject>
<subj-group><subject>Virology</subject>
<subj-group><subject>Viral Transmission and Infection</subject>
<subj-group><subject>Host Cells</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject>
<subj-group><subject>Biochemistry</subject>
<subj-group><subject>Nucleic acids</subject>
<subj-group><subject>RNA</subject>
<subj-group><subject>Non-coding RNA</subject>
<subj-group><subject>Ribosomal RNA</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject>
<subj-group><subject>Biochemistry</subject>
<subj-group><subject>Ribosomes</subject>
<subj-group><subject>Ribosomal RNA</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject>
<subj-group><subject>Cell biology</subject>
<subj-group><subject>Cellular structures and organelles</subject>
<subj-group><subject>Ribosomes</subject>
<subj-group><subject>Ribosomal RNA</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Research and Analysis Methods</subject>
<subj-group><subject>Biological Cultures</subject>
<subj-group><subject>Cell Lines</subject>
<subj-group><subject>L929 Cells</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</article-categories>
<title-group><article-title>Early endonuclease-mediated evasion of RNA sensing ensures efficient coronavirus replication</article-title>
<alt-title alt-title-type="running-head">Viral endonuclease and innate immunity</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Kindler</surname>
<given-names>Eveline</given-names>
</name>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff002"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Gil-Cruz</surname>
<given-names>Cristina</given-names>
</name>
<xref ref-type="aff" rid="aff003"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Spanier</surname>
<given-names>Julia</given-names>
</name>
<xref ref-type="aff" rid="aff004"><sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Li</surname>
<given-names>Yize</given-names>
</name>
<xref ref-type="aff" rid="aff005"><sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Wilhelm</surname>
<given-names>Jochen</given-names>
</name>
<xref ref-type="aff" rid="aff006"><sup>6</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Rabouw</surname>
<given-names>Huib H.</given-names>
</name>
<xref ref-type="aff" rid="aff007"><sup>7</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Züst</surname>
<given-names>Roland</given-names>
</name>
<xref ref-type="aff" rid="aff008"><sup>8</sup>
</xref>
</contrib>
<contrib contrib-type="author"><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0003-2639-0265</contrib-id>
<name><surname>Hwang</surname>
<given-names>Mihyun</given-names>
</name>
<xref ref-type="aff" rid="aff009"><sup>9</sup>
</xref>
</contrib>
<contrib contrib-type="author"><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-8366-1220</contrib-id>
<name><surname>V’kovski</surname>
<given-names>Philip</given-names>
</name>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff002"><sup>2</sup>
</xref>
<xref ref-type="aff" rid="aff010"><sup>10</sup>
</xref>
</contrib>
<contrib contrib-type="author"><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0003-0763-6469</contrib-id>
<name><surname>Stalder</surname>
<given-names>Hanspeter</given-names>
</name>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff002"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Marti</surname>
<given-names>Sabrina</given-names>
</name>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff002"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Habjan</surname>
<given-names>Matthias</given-names>
</name>
<xref ref-type="aff" rid="aff011"><sup>11</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Cervantes-Barragan</surname>
<given-names>Luisa</given-names>
</name>
<xref ref-type="aff" rid="aff012"><sup>12</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Elliot</surname>
<given-names>Ruth</given-names>
</name>
<xref ref-type="aff" rid="aff005"><sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Karl</surname>
<given-names>Nadja</given-names>
</name>
<xref ref-type="aff" rid="aff013"><sup>13</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Gaughan</surname>
<given-names>Christina</given-names>
</name>
<xref ref-type="aff" rid="aff014"><sup>14</sup>
</xref>
</contrib>
<contrib contrib-type="author"><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0001-5800-749X</contrib-id>
<name><surname>van Kuppeveld</surname>
<given-names>Frank J. M.</given-names>
</name>
<xref ref-type="aff" rid="aff007"><sup>7</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Silverman</surname>
<given-names>Robert H.</given-names>
</name>
<xref ref-type="aff" rid="aff014"><sup>14</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Keller</surname>
<given-names>Markus</given-names>
</name>
<xref ref-type="aff" rid="aff015"><sup>15</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Ludewig</surname>
<given-names>Burkhard</given-names>
</name>
<xref ref-type="aff" rid="aff003"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Bergmann</surname>
<given-names>Cornelia C.</given-names>
</name>
<xref ref-type="aff" rid="aff009"><sup>9</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Ziebuhr</surname>
<given-names>John</given-names>
</name>
<xref ref-type="aff" rid="aff013"><sup>13</sup>
</xref>
</contrib>
<contrib contrib-type="author"><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-8155-4528</contrib-id>
<name><surname>Weiss</surname>
<given-names>Susan R.</given-names>
</name>
<xref ref-type="aff" rid="aff005"><sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Kalinke</surname>
<given-names>Ulrich</given-names>
</name>
<xref ref-type="aff" rid="aff004"><sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author"><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-5783-0887</contrib-id>
<name><surname>Thiel</surname>
<given-names>Volker</given-names>
</name>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff002"><sup>2</sup>
</xref>
<xref ref-type="corresp" rid="cor001">*</xref>
</contrib>
</contrib-group>
<aff id="aff001"><label>1</label>
<addr-line>Department of Infectious Diseases and Pathobiology, University of Bern, Bern, Switzerland</addr-line>
</aff>
<aff id="aff002"><label>2</label>
<addr-line>Federal Department of Home Affairs, Institute of Virology and Immunology, Bern and Mittelhäusern, Switzerland</addr-line>
</aff>
<aff id="aff003"><label>3</label>
<addr-line>Institute of Immunobiology, Kantonsspital St.Gallen, St.Gallen, Switzerland</addr-line>
</aff>
<aff id="aff004"><label>4</label>
<addr-line>Institute for Experimental Infection Research, TWINCORE, Centre for Experimental and Clinical Infection Research, a joint venture between the Helmholtz Centre for Infection Research and the Hannover Medical School, Hannover, Germany</addr-line>
</aff>
<aff id="aff005"><label>5</label>
<addr-line>Department of Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, United States of America</addr-line>
</aff>
<aff id="aff006"><label>6</label>
<addr-line>Universities Giessen & Marburg Lung Center (UGMLC), Deutsches Zentrum für Lungenforschung (DZL), Giessen, Germany</addr-line>
</aff>
<aff id="aff007"><label>7</label>
<addr-line>Virology Division, Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands</addr-line>
</aff>
<aff id="aff008"><label>8</label>
<addr-line>Singapore Immunology Network, Singapore</addr-line>
</aff>
<aff id="aff009"><label>9</label>
<addr-line>Department of Neurosciences, Lerner Research Institute, Cleveland Clinic Foundation, Cleveland, Ohio, United States of America</addr-line>
</aff>
<aff id="aff010"><label>10</label>
<addr-line>Graduate School for Biomedical Science, University of Bern, Bern, Switzerland</addr-line>
</aff>
<aff id="aff011"><label>11</label>
<addr-line>Max-Planck-Institute of Biochemistry, Martinsried, Germany</addr-line>
</aff>
<aff id="aff012"><label>12</label>
<addr-line>Washington University School of Medicine, St. Louis, MO, USA</addr-line>
</aff>
<aff id="aff013"><label>13</label>
<addr-line>Institute for Medical Virology, Justus-Liebig-University, Giessen, Germany</addr-line>
</aff>
<aff id="aff014"><label>14</label>
<addr-line>Department of Cancer Biology, Lerner Research Institute, Cleveland, Ohio, United States of America</addr-line>
</aff>
<aff id="aff015"><label>15</label>
<addr-line>Institute of Novel and Emerging Infectious Diseases, Friedrich-Loeffler-Institut, Greifswald-Insel Riems, Germany</addr-line>
</aff>
<contrib-group><contrib contrib-type="editor"><name><surname>Perlman</surname>
<given-names>Stanley</given-names>
</name>
<role>Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1"><addr-line>University of Iowa, UNITED STATES</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"><p><list list-type="simple"><list-item><p><bold>Conceptualization:</bold>
EK RZ LCB BL VT.</p>
</list-item>
<list-item><p><bold>Formal analysis:</bold>
EK JW MHw HHR PV SM.</p>
</list-item>
<list-item><p><bold>Funding acquisition:</bold>
RHS SRW VT.</p>
</list-item>
<list-item><p><bold>Investigation:</bold>
EK CGC JS YL HHR RZ MHw HS PV RE SM MHa LCB NK CG.</p>
</list-item>
<list-item><p><bold>Project administration:</bold>
VT.</p>
</list-item>
<list-item><p><bold>Resources:</bold>
RHS MK BL CCB FJMvK JZ SRW UK VT.</p>
</list-item>
<list-item><p><bold>Supervision:</bold>
RHS MK BL CCB FJMvK JZ SRW UK VT.</p>
</list-item>
<list-item><p><bold>Visualization:</bold>
EK VT.</p>
</list-item>
<list-item><p><bold>Writing – original draft:</bold>
EK VT.</p>
</list-item>
<list-item><p><bold>Writing – review & editing:</bold>
EK CGC JS YL JW RZ MHw MHa LCB RHS MK BL CCB JZ SRW UK VT.</p>
</list-item>
</list>
</p>
</fn>
<corresp id="cor001">* E-mail: <email>Volker.thiel@vetsuisse.unibe.ch</email>
</corresp>
</author-notes>
<pub-date pub-type="epub"><day>3</day>
<month>2</month>
<year>2017</year>
</pub-date>
<pub-date pub-type="collection"><month>2</month>
<year>2017</year>
</pub-date>
<volume>13</volume>
<issue>2</issue>
<elocation-id>e1006195</elocation-id>
<history><date date-type="received"><day>29</day>
<month>7</month>
<year>2016</year>
</date>
<date date-type="accepted"><day>20</day>
<month>1</month>
<year>2017</year>
</date>
</history>
<permissions><copyright-statement>© 2017 Kindler et al</copyright-statement>
<copyright-year>2017</copyright-year>
<copyright-holder>Kindler et al</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 <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>
, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</license-p>
</license>
</permissions>
<self-uri content-type="pdf" xlink:href="ppat.1006195.pdf"></self-uri>
<abstract><p>Coronaviruses are of veterinary and medical importance and include highly pathogenic zoonotic viruses, such as SARS-CoV and MERS-CoV. They are known to efficiently evade early innate immune responses, manifesting in almost negligible expression of type-I interferons (IFN-I). This evasion strategy suggests an evolutionary conserved viral function that has evolved to prevent RNA-based sensing of infection in vertebrate hosts. Here we show that the coronavirus endonuclease (EndoU) activity is key to prevent early induction of double-stranded RNA (dsRNA) host cell responses. Replication of EndoU-deficient coronaviruses is greatly attenuated <italic>in vivo</italic>
and severely restricted in primary cells even during the early phase of the infection. In macrophages we found immediate induction of IFN-I expression and RNase L-mediated breakdown of ribosomal RNA. Accordingly, EndoU-deficient viruses can retain replication only in cells that are deficient in IFN-I expression or sensing, and in cells lacking both RNase L and PKR. Collectively our results demonstrate that the coronavirus EndoU efficiently prevents simultaneous activation of host cell dsRNA sensors, such as Mda5, OAS and PKR. The localization of the EndoU activity at the site of viral RNA synthesis–within the replicase complex—suggests that coronaviruses have evolved a viral RNA decay pathway to evade early innate and intrinsic antiviral host cell responses.</p>
</abstract>
<abstract abstract-type="summary"><title>Author summary</title>
<p>Coronaviruses are long known to be particularly successful in evading host innate immune responses. This manifests in barely detectable interferon responses during the first hours of infection and greatly facilitates establishment of robust virus replication. This phenotype of early innate immune evasion is common to all coronaviruses and can have detrimental consequences particular for infections with highly pathogenic coronaviruses, such as SARS-CoV and MERS-CoV. We therefore hypothesized that there must be an evolutionary conserved viral function that has evolved to prevent sensing of coronavirus infection by infected host cells. Our study now describes this function, namely the highly conserved coronavirus endoribonuclease activity. We found that coronaviruses that lack this enzymatic activity are readily visible to infected host cells that can now mount a swift and potent host response restricting virus replication within hours. Our study provides a new paradigm of a first layer of RNA virus innate immune evasion during the early phase of infection, that takes place at the site of RNA synthesis, and is based on removal of dsRNA that would otherwise trigger the simultaneous activation of cytoplasmic host cell sensors.</p>
</abstract>
<funding-group><award-group id="award001"><funding-source><institution-wrap><institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/501100001711</institution-id>
<institution>Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung</institution>
</institution-wrap>
</funding-source>
<award-id>149784</award-id>
<principal-award-recipient><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-5783-0887</contrib-id>
<name><surname>Thiel</surname>
<given-names>Volker</given-names>
</name>
</principal-award-recipient>
</award-group>
<award-group id="award002"><funding-source><institution-wrap><institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/100000002</institution-id>
<institution>National Institutes of Health</institution>
</institution-wrap>
</funding-source>
<award-id>R01-AI104887</award-id>
<principal-award-recipient><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-8155-4528</contrib-id>
<name><surname>Weiss</surname>
<given-names>Susan R.</given-names>
</name>
</principal-award-recipient>
</award-group>
<award-group id="award003"><funding-source><institution-wrap><institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/100000002</institution-id>
<institution>National Institutes of Health</institution>
</institution-wrap>
</funding-source>
<award-id>R01-AI104887</award-id>
<principal-award-recipient><name><surname>Silverman</surname>
<given-names>Robert H.</given-names>
</name>
</principal-award-recipient>
</award-group>
<award-group id="award004"><funding-source><institution-wrap><institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/100000002</institution-id>
<institution>National Institutes of Health</institution>
</institution-wrap>
</funding-source>
<award-id>R01-NS081008</award-id>
<principal-award-recipient><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-8155-4528</contrib-id>
<name><surname>Weiss</surname>
<given-names>Susan R.</given-names>
</name>
</principal-award-recipient>
</award-group>
<funding-statement>This work was supported by the Swiss National Science Foundation (SNF project 149784), and by NIH Grants R01-AI104887 (to SRW and RHS), R01-NS081008 (to SRW), and R01-CA044059 (to RHS). 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="8"></fig-count>
<table-count count="0"></table-count>
<page-count count="26"></page-count>
</counts>
<custom-meta-group><custom-meta><meta-name>PLOS Publication Stage</meta-name>
<meta-value>vor-update-to-uncorrected-proof</meta-value>
</custom-meta>
<custom-meta><meta-name>Publication Update</meta-name>
<meta-value>2017-02-15</meta-value>
</custom-meta>
<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><country><li>Allemagne</li>
<li>Pays-Bas</li>
<li>Singapour</li>
<li>Suisse</li>
<li>États-Unis</li>
</country>
<region><li>Basse-Saxe</li>
<li>Canton de Berne</li>
<li>Missouri (État)</li>
<li>Ohio</li>
<li>Pennsylvanie</li>
<li>Utrecht (province)</li>
</region>
<settlement><li>Berne</li>
<li>Hanovre</li>
<li>Saint-Louis (Missouri)</li>
<li>Utrecht</li>
</settlement>
<orgName><li>Université d'Utrecht</li>
<li>Université de Berne</li>
<li>École de médecine (Université Washington de Saint-Louis)</li>
</orgName>
</list>
<tree><country name="Suisse"><region name="Canton de Berne"><name sortKey="Kindler, Eveline" sort="Kindler, Eveline" uniqKey="Kindler E" first="Eveline" last="Kindler">Eveline Kindler</name>
</region>
<name sortKey="Gil Cruz, Cristina" sort="Gil Cruz, Cristina" uniqKey="Gil Cruz C" first="Cristina" last="Gil-Cruz">Cristina Gil-Cruz</name>
<name sortKey="Kindler, Eveline" sort="Kindler, Eveline" uniqKey="Kindler E" first="Eveline" last="Kindler">Eveline Kindler</name>
<name sortKey="Ludewig, Burkhard" sort="Ludewig, Burkhard" uniqKey="Ludewig B" first="Burkhard" last="Ludewig">Burkhard Ludewig</name>
<name sortKey="Marti, Sabrina" sort="Marti, Sabrina" uniqKey="Marti S" first="Sabrina" last="Marti">Sabrina Marti</name>
<name sortKey="Marti, Sabrina" sort="Marti, Sabrina" uniqKey="Marti S" first="Sabrina" last="Marti">Sabrina Marti</name>
<name sortKey="Stalder, Hanspeter" sort="Stalder, Hanspeter" uniqKey="Stalder H" first="Hanspeter" last="Stalder">Hanspeter Stalder</name>
<name sortKey="Stalder, Hanspeter" sort="Stalder, Hanspeter" uniqKey="Stalder H" first="Hanspeter" last="Stalder">Hanspeter Stalder</name>
<name sortKey="Thiel, Volker" sort="Thiel, Volker" uniqKey="Thiel V" first="Volker" last="Thiel">Volker Thiel</name>
<name sortKey="Thiel, Volker" sort="Thiel, Volker" uniqKey="Thiel V" first="Volker" last="Thiel">Volker Thiel</name>
<name sortKey="V Ovski, Philip" sort="V Ovski, Philip" uniqKey="V Ovski P" first="Philip" last="V Ovski">Philip V Ovski</name>
<name sortKey="V Ovski, Philip" sort="V Ovski, Philip" uniqKey="V Ovski P" first="Philip" last="V Ovski">Philip V Ovski</name>
<name sortKey="V Ovski, Philip" sort="V Ovski, Philip" uniqKey="V Ovski P" first="Philip" last="V Ovski">Philip V Ovski</name>
</country>
<country name="Allemagne"><region name="Basse-Saxe"><name sortKey="Spanier, Julia" sort="Spanier, Julia" uniqKey="Spanier J" first="Julia" last="Spanier">Julia Spanier</name>
</region>
<name sortKey="Habjan, Matthias" sort="Habjan, Matthias" uniqKey="Habjan M" first="Matthias" last="Habjan">Matthias Habjan</name>
<name sortKey="Kalinke, Ulrich" sort="Kalinke, Ulrich" uniqKey="Kalinke U" first="Ulrich" last="Kalinke">Ulrich Kalinke</name>
<name sortKey="Karl, Nadja" sort="Karl, Nadja" uniqKey="Karl N" first="Nadja" last="Karl">Nadja Karl</name>
<name sortKey="Keller, Markus" sort="Keller, Markus" uniqKey="Keller M" first="Markus" last="Keller">Markus Keller</name>
<name sortKey="Wilhelm, Jochen" sort="Wilhelm, Jochen" uniqKey="Wilhelm J" first="Jochen" last="Wilhelm">Jochen Wilhelm</name>
<name sortKey="Ziebuhr, John" sort="Ziebuhr, John" uniqKey="Ziebuhr J" first="John" last="Ziebuhr">John Ziebuhr</name>
</country>
<country name="États-Unis"><region name="Pennsylvanie"><name sortKey="Li, Yize" sort="Li, Yize" uniqKey="Li Y" first="Yize" last="Li">Yize Li</name>
</region>
<name sortKey="Bergmann, Cornelia C" sort="Bergmann, Cornelia C" uniqKey="Bergmann C" first="Cornelia C." last="Bergmann">Cornelia C. Bergmann</name>
<name sortKey="Cervantes Barragan, Luisa" sort="Cervantes Barragan, Luisa" uniqKey="Cervantes Barragan L" first="Luisa" last="Cervantes-Barragan">Luisa Cervantes-Barragan</name>
<name sortKey="Elliot, Ruth" sort="Elliot, Ruth" uniqKey="Elliot R" first="Ruth" last="Elliot">Ruth Elliot</name>
<name sortKey="Gaughan, Christina" sort="Gaughan, Christina" uniqKey="Gaughan C" first="Christina" last="Gaughan">Christina Gaughan</name>
<name sortKey="Hwang, Mihyun" sort="Hwang, Mihyun" uniqKey="Hwang M" first="Mihyun" last="Hwang">Mihyun Hwang</name>
<name sortKey="Silverman, Robert H" sort="Silverman, Robert H" uniqKey="Silverman R" first="Robert H." last="Silverman">Robert H. Silverman</name>
<name sortKey="Weiss, Susan R" sort="Weiss, Susan R" uniqKey="Weiss S" first="Susan R." last="Weiss">Susan R. Weiss</name>
</country>
<country name="Pays-Bas"><region name="Utrecht (province)"><name sortKey="Rabouw, Huib H" sort="Rabouw, Huib H" uniqKey="Rabouw H" first="Huib H." last="Rabouw">Huib H. Rabouw</name>
</region>
<name sortKey="Van Kuppeveld, Frank J M" sort="Van Kuppeveld, Frank J M" uniqKey="Van Kuppeveld F" first="Frank J. M." last="Van Kuppeveld">Frank J. M. Van Kuppeveld</name>
</country>
<country name="Singapour"><noRegion><name sortKey="Zust, Roland" sort="Zust, Roland" uniqKey="Zust R" first="Roland" last="Züst">Roland Züst</name>
</noRegion>
</country>
</tree>
</affiliations>
</record>
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