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Antiviral activity of human OASL protein is mediated by enhancing signaling of the RIG-I RNA sensor.

Identifieur interne : 003C17 ( PubMed/Checkpoint ); précédent : 003C16; suivant : 003C18

Antiviral activity of human OASL protein is mediated by enhancing signaling of the RIG-I RNA sensor.

Auteurs : Jianzhong Zhu [États-Unis] ; Yugen Zhang [États-Unis] ; Arundhati Ghosh [États-Unis] ; Rolando A. Cuevas [États-Unis] ; Adriana Forero [États-Unis] ; Jayeeta Dhar [États-Unis] ; Mikkel S Es Ibsen [Danemark] ; Jonathan Leo Schmid-Burgk [Allemagne] ; Tobias Schmidt [Allemagne] ; Madhavi K. Ganapathiraju [États-Unis] ; Takashi Fujita [Japon] ; Rune Hartmann [Danemark] ; Sailen Barik [États-Unis] ; Veit Hornung [Allemagne] ; Carolyn B. Coyne [États-Unis] ; Saumendra N. Sarkar [États-Unis]

Source :

RBID : pubmed:24931123

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English descriptors

Abstract

Virus infection is sensed in the cytoplasm by retinoic acid-inducible gene I (RIG-I, also known as DDX58), which requires RNA and polyubiquitin binding to induce type I interferon (IFN) and activate cellular innate immunity. We show that the human IFN-inducible oligoadenylate synthetases-like (OASL) protein has antiviral activity and mediates RIG-I activation by mimicking polyubiquitin. Loss of OASL expression reduced RIG-I signaling and enhanced virus replication in human cells. Conversely, OASL expression suppressed replication of a number of viruses in a RIG-I-dependent manner and enhanced RIG-I-mediated IFN induction. OASL interacted and colocalized with RIG-I, and through its C-terminal ubiquitin-like domain specifically enhanced RIG-I signaling. Bone-marrow-derived macrophages from mice deficient for Oasl2 showed that among the two mouse orthologs of human OASL, Oasl2 is functionally similar to human OASL. Our findings show a mechanism by which human OASL contributes to host antiviral responses by enhancing RIG-I activation.

DOI: 10.1016/j.immuni.2014.05.007
PubMed: 24931123


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pubmed:24931123

Le document en format XML

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<name sortKey="Ganapathiraju, Madhavi K" sort="Ganapathiraju, Madhavi K" uniqKey="Ganapathiraju M" first="Madhavi K" last="Ganapathiraju">Madhavi K. Ganapathiraju</name>
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<name sortKey="Hartmann, Rune" sort="Hartmann, Rune" uniqKey="Hartmann R" first="Rune" last="Hartmann">Rune Hartmann</name>
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<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Center for Gene Regulation in Health and Disease, and Department of Biological, Geological and Environmental Sciences, Cleveland State University, Cleveland, OH 44115</wicri:regionArea>
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<name sortKey="Hornung, Veit" sort="Hornung, Veit" uniqKey="Hornung V" first="Veit" last="Hornung">Veit Hornung</name>
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<nlm:affiliation>Institute for Clinical Chemistry and Clinical Pharmacology, University of Bonn, Bonn 53127, Germany.</nlm:affiliation>
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<name sortKey="Coyne, Carolyn B" sort="Coyne, Carolyn B" uniqKey="Coyne C" first="Carolyn B" last="Coyne">Carolyn B. Coyne</name>
<affiliation wicri:level="2">
<nlm:affiliation>Cancer Virology Program, University of Pittsburgh Cancer Institute, University of Pittsburgh School of Medicine, Pittsburgh, PA 15213, USA; Department of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh, PA 15213, USA.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
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<placeName>
<region type="state">Pennsylvanie</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Sarkar, Saumendra N" sort="Sarkar, Saumendra N" uniqKey="Sarkar S" first="Saumendra N" last="Sarkar">Saumendra N. Sarkar</name>
<affiliation wicri:level="2">
<nlm:affiliation>Cancer Virology Program, University of Pittsburgh Cancer Institute, University of Pittsburgh School of Medicine, Pittsburgh, PA 15213, USA; Department of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh, PA 15213, USA. Electronic address: saumen@pitt.edu.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
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<region type="state">Pennsylvanie</region>
</placeName>
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</analytic>
<series>
<title level="j">Immunity</title>
<idno type="eISSN">1097-4180</idno>
<imprint>
<date when="2014" type="published">2014</date>
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<term>2',5'-Oligoadenylate Synthetase (genetics)</term>
<term>2',5'-Oligoadenylate Synthetase (immunology)</term>
<term>Animals</term>
<term>DEAD Box Protein 58</term>
<term>DEAD-box RNA Helicases (immunology)</term>
<term>DNA Virus Infections (immunology)</term>
<term>HCT116 Cells</term>
<term>HEK293 Cells</term>
<term>Humans</term>
<term>Immunity, Innate</term>
<term>Interferon Regulatory Factor-7 (metabolism)</term>
<term>Interferon Type I (immunology)</term>
<term>Mice</term>
<term>Mice, Inbred C57BL</term>
<term>Mice, Knockout</term>
<term>Polyubiquitin</term>
<term>Protein Binding (immunology)</term>
<term>RNA Interference</term>
<term>RNA Virus Infections (immunology)</term>
<term>RNA, Small Interfering</term>
<term>Signal Transduction (immunology)</term>
<term>Virus Replication (immunology)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>2',5'-Oligoadenylate synthetase (génétique)</term>
<term>2',5'-Oligoadenylate synthetase (immunologie)</term>
<term>Animaux</term>
<term>Cellules HCT116</term>
<term>Cellules HEK293</term>
<term>DEAD-box RNA helicases (immunologie)</term>
<term>Facteur-7 de régulation d'interféron (métabolisme)</term>
<term>Humains</term>
<term>Immunité innée</term>
<term>Infections à virus à ADN (immunologie)</term>
<term>Infections à virus à ARN (immunologie)</term>
<term>Interférence par ARN</term>
<term>Interféron de type I (immunologie)</term>
<term>Liaison aux protéines (immunologie)</term>
<term>Petit ARN interférent</term>
<term>Polyubiquitine</term>
<term>Protéine-58 à domaine DEAD</term>
<term>Réplication virale (immunologie)</term>
<term>Souris</term>
<term>Souris de lignée C57BL</term>
<term>Souris knockout</term>
<term>Transduction du signal (immunologie)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en">
<term>2',5'-Oligoadenylate Synthetase</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="immunology" xml:lang="en">
<term>2',5'-Oligoadenylate Synthetase</term>
<term>DEAD-box RNA Helicases</term>
<term>Interferon Type I</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr">
<term>2',5'-Oligoadenylate synthetase</term>
</keywords>
<keywords scheme="MESH" qualifier="immunologie" xml:lang="fr">
<term>2',5'-Oligoadenylate synthetase</term>
<term>DEAD-box RNA helicases</term>
<term>Infections à virus à ADN</term>
<term>Infections à virus à ARN</term>
<term>Interféron de type I</term>
<term>Liaison aux protéines</term>
<term>Réplication virale</term>
<term>Transduction du signal</term>
</keywords>
<keywords scheme="MESH" qualifier="immunology" xml:lang="en">
<term>DNA Virus Infections</term>
<term>Protein Binding</term>
<term>RNA Virus Infections</term>
<term>Signal Transduction</term>
<term>Virus Replication</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en">
<term>Interferon Regulatory Factor-7</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Facteur-7 de régulation d'interféron</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Animals</term>
<term>DEAD Box Protein 58</term>
<term>HCT116 Cells</term>
<term>HEK293 Cells</term>
<term>Humans</term>
<term>Immunity, Innate</term>
<term>Mice</term>
<term>Mice, Inbred C57BL</term>
<term>Mice, Knockout</term>
<term>Polyubiquitin</term>
<term>RNA Interference</term>
<term>RNA, Small Interfering</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>Animaux</term>
<term>Cellules HCT116</term>
<term>Cellules HEK293</term>
<term>Humains</term>
<term>Immunité innée</term>
<term>Interférence par ARN</term>
<term>Petit ARN interférent</term>
<term>Polyubiquitine</term>
<term>Protéine-58 à domaine DEAD</term>
<term>Souris</term>
<term>Souris de lignée C57BL</term>
<term>Souris knockout</term>
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<front>
<div type="abstract" xml:lang="en">Virus infection is sensed in the cytoplasm by retinoic acid-inducible gene I (RIG-I, also known as DDX58), which requires RNA and polyubiquitin binding to induce type I interferon (IFN) and activate cellular innate immunity. We show that the human IFN-inducible oligoadenylate synthetases-like (OASL) protein has antiviral activity and mediates RIG-I activation by mimicking polyubiquitin. Loss of OASL expression reduced RIG-I signaling and enhanced virus replication in human cells. Conversely, OASL expression suppressed replication of a number of viruses in a RIG-I-dependent manner and enhanced RIG-I-mediated IFN induction. OASL interacted and colocalized with RIG-I, and through its C-terminal ubiquitin-like domain specifically enhanced RIG-I signaling. Bone-marrow-derived macrophages from mice deficient for Oasl2 showed that among the two mouse orthologs of human OASL, Oasl2 is functionally similar to human OASL. Our findings show a mechanism by which human OASL contributes to host antiviral responses by enhancing RIG-I activation.</div>
</front>
</TEI>
<pubmed>
<MedlineCitation Status="MEDLINE" Owner="NLM">
<PMID Version="1">24931123</PMID>
<DateCreated>
<Year>2014</Year>
<Month>06</Month>
<Day>21</Day>
</DateCreated>
<DateCompleted>
<Year>2014</Year>
<Month>09</Month>
<Day>05</Day>
</DateCompleted>
<DateRevised>
<Year>2017</Year>
<Month>02</Month>
<Day>20</Day>
</DateRevised>
<Article PubModel="Print-Electronic">
<Journal>
<ISSN IssnType="Electronic">1097-4180</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>40</Volume>
<Issue>6</Issue>
<PubDate>
<Year>2014</Year>
<Month>Jun</Month>
<Day>19</Day>
</PubDate>
</JournalIssue>
<Title>Immunity</Title>
<ISOAbbreviation>Immunity</ISOAbbreviation>
</Journal>
<ArticleTitle>Antiviral activity of human OASL protein is mediated by enhancing signaling of the RIG-I RNA sensor.</ArticleTitle>
<Pagination>
<MedlinePgn>936-48</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1016/j.immuni.2014.05.007</ELocationID>
<ELocationID EIdType="pii" ValidYN="Y">S1074-7613(14)00187-3</ELocationID>
<Abstract>
<AbstractText>Virus infection is sensed in the cytoplasm by retinoic acid-inducible gene I (RIG-I, also known as DDX58), which requires RNA and polyubiquitin binding to induce type I interferon (IFN) and activate cellular innate immunity. We show that the human IFN-inducible oligoadenylate synthetases-like (OASL) protein has antiviral activity and mediates RIG-I activation by mimicking polyubiquitin. Loss of OASL expression reduced RIG-I signaling and enhanced virus replication in human cells. Conversely, OASL expression suppressed replication of a number of viruses in a RIG-I-dependent manner and enhanced RIG-I-mediated IFN induction. OASL interacted and colocalized with RIG-I, and through its C-terminal ubiquitin-like domain specifically enhanced RIG-I signaling. Bone-marrow-derived macrophages from mice deficient for Oasl2 showed that among the two mouse orthologs of human OASL, Oasl2 is functionally similar to human OASL. Our findings show a mechanism by which human OASL contributes to host antiviral responses by enhancing RIG-I activation.</AbstractText>
<CopyrightInformation>Copyright © 2014 Elsevier Inc. All rights reserved.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Zhu</LastName>
<ForeName>Jianzhong</ForeName>
<Initials>J</Initials>
<AffiliationInfo>
<Affiliation>Cancer Virology Program, University of Pittsburgh Cancer Institute, University of Pittsburgh School of Medicine, Pittsburgh, PA 15213, USA; Department of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh, PA 15213, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Zhang</LastName>
<ForeName>Yugen</ForeName>
<Initials>Y</Initials>
<AffiliationInfo>
<Affiliation>Cancer Virology Program, University of Pittsburgh Cancer Institute, University of Pittsburgh School of Medicine, Pittsburgh, PA 15213, USA; Department of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh, PA 15213, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Ghosh</LastName>
<ForeName>Arundhati</ForeName>
<Initials>A</Initials>
<AffiliationInfo>
<Affiliation>Cancer Virology Program, University of Pittsburgh Cancer Institute, University of Pittsburgh School of Medicine, Pittsburgh, PA 15213, USA; Department of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh, PA 15213, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Cuevas</LastName>
<ForeName>Rolando A</ForeName>
<Initials>RA</Initials>
<AffiliationInfo>
<Affiliation>Cancer Virology Program, University of Pittsburgh Cancer Institute, University of Pittsburgh School of Medicine, Pittsburgh, PA 15213, USA; Department of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh, PA 15213, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Forero</LastName>
<ForeName>Adriana</ForeName>
<Initials>A</Initials>
<AffiliationInfo>
<Affiliation>Cancer Virology Program, University of Pittsburgh Cancer Institute, University of Pittsburgh School of Medicine, Pittsburgh, PA 15213, USA; Department of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh, PA 15213, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Dhar</LastName>
<ForeName>Jayeeta</ForeName>
<Initials>J</Initials>
<AffiliationInfo>
<Affiliation>Center for Gene Regulation in Health and Disease, and Department of Biological, Geological and Environmental Sciences, Cleveland State University, Cleveland, OH 44115, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Ibsen</LastName>
<ForeName>Mikkel Søes</ForeName>
<Initials>MS</Initials>
<AffiliationInfo>
<Affiliation>Department of Molecular Biology, Aarhus University, Aarhus 8000, Denmark.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Schmid-Burgk</LastName>
<ForeName>Jonathan Leo</ForeName>
<Initials>JL</Initials>
<AffiliationInfo>
<Affiliation>Institute for Clinical Chemistry and Clinical Pharmacology, University of Bonn, Bonn 53127, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Schmidt</LastName>
<ForeName>Tobias</ForeName>
<Initials>T</Initials>
<AffiliationInfo>
<Affiliation>Institute for Clinical Chemistry and Clinical Pharmacology, University of Bonn, Bonn 53127, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Ganapathiraju</LastName>
<ForeName>Madhavi K</ForeName>
<Initials>MK</Initials>
<AffiliationInfo>
<Affiliation>Department of Biomedical Informatics, University of Pittsburgh School of Medicine, Pittsburgh, PA 15213, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Fujita</LastName>
<ForeName>Takashi</ForeName>
<Initials>T</Initials>
<AffiliationInfo>
<Affiliation>Laboratory of Molecular Genetics, Kyoto University, Kyoto 606-8507, Japan.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Hartmann</LastName>
<ForeName>Rune</ForeName>
<Initials>R</Initials>
<AffiliationInfo>
<Affiliation>Department of Molecular Biology, Aarhus University, Aarhus 8000, Denmark.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Barik</LastName>
<ForeName>Sailen</ForeName>
<Initials>S</Initials>
<AffiliationInfo>
<Affiliation>Center for Gene Regulation in Health and Disease, and Department of Biological, Geological and Environmental Sciences, Cleveland State University, Cleveland, OH 44115, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Hornung</LastName>
<ForeName>Veit</ForeName>
<Initials>V</Initials>
<AffiliationInfo>
<Affiliation>Institute for Clinical Chemistry and Clinical Pharmacology, University of Bonn, Bonn 53127, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Coyne</LastName>
<ForeName>Carolyn B</ForeName>
<Initials>CB</Initials>
<AffiliationInfo>
<Affiliation>Cancer Virology Program, University of Pittsburgh Cancer Institute, University of Pittsburgh School of Medicine, Pittsburgh, PA 15213, USA; Department of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh, PA 15213, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Sarkar</LastName>
<ForeName>Saumendra N</ForeName>
<Initials>SN</Initials>
<AffiliationInfo>
<Affiliation>Cancer Virology Program, University of Pittsburgh Cancer Institute, University of Pittsburgh School of Medicine, Pittsburgh, PA 15213, USA; Department of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh, PA 15213, USA. Electronic address: saumen@pitt.edu.</Affiliation>
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<Language>eng</Language>
<GrantList CompleteYN="Y">
<Grant>
<GrantID>U24 AI082673</GrantID>
<Acronym>AI</Acronym>
<Agency>NIAID NIH HHS</Agency>
<Country>United States</Country>
</Grant>
<Grant>
<GrantID>AI082673</GrantID>
<Acronym>AI</Acronym>
<Agency>NIAID NIH HHS</Agency>
<Country>United States</Country>
</Grant>
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<PublicationType UI="D052061">Research Support, N.I.H., Extramural</PublicationType>
<PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic">
<Year>2014</Year>
<Month>06</Month>
<Day>12</Day>
</ArticleDate>
</Article>
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<Country>United States</Country>
<MedlineTA>Immunity</MedlineTA>
<NlmUniqueID>9432918</NlmUniqueID>
<ISSNLinking>1074-7613</ISSNLinking>
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<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="C494234">IRF7 protein, human</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D050839">Interferon Regulatory Factor-7</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D007370">Interferon Type I</NameOfSubstance>
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<Chemical>
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<Chemical>
<RegistryNumber>120904-94-1</RegistryNumber>
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<Chemical>
<RegistryNumber>EC 2.7.7.-</RegistryNumber>
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<Chemical>
<RegistryNumber>EC 2.7.7.-</RegistryNumber>
<NameOfSubstance UI="C475084">Oasl2 protein, mouse</NameOfSubstance>
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<Chemical>
<RegistryNumber>EC 2.7.7.84</RegistryNumber>
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<Chemical>
<RegistryNumber>EC 3.6.1.-</RegistryNumber>
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<Chemical>
<RegistryNumber>EC 3.6.4.13</RegistryNumber>
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</Chemical>
<Chemical>
<RegistryNumber>EC 3.6.4.13</RegistryNumber>
<NameOfSubstance UI="D053487">DEAD-box RNA Helicases</NameOfSubstance>
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