Toll-like receptor 5 agonist flagellin reduces influenza A virus replication independently of type I interferon and interleukin 22 and improves antiviral efficacy of oseltamivir
Identifieur interne : 000300 ( Hal/Corpus ); précédent : 000299; suivant : 000301Toll-like receptor 5 agonist flagellin reduces influenza A virus replication independently of type I interferon and interleukin 22 and improves antiviral efficacy of oseltamivir
Auteurs : Anne-France Georgel ; Delphine Cayet ; Andrés Pizzorno ; Manuel Rosa-Calatrava ; Christophe Paget ; Valentin Sencio ; Jean Dubuisson ; François Trottein ; Jean Claude Sirard ; Christophe CarnoySource :
- Antiviral Research [ 0166-3542 ] ; 2019-04.
English descriptors
Abstract
Influenza infections remain a burden on health care systems despite vaccination programs and marketed antiviral drugs. Immunomodulation through activation of innate sensors could represent innovative approaches to fight the flu. This study evaluated the ability of flagellin, agonist of Toll-like receptor 5 (TLR5), to control the replication of influenza A virus (IAV) in mice. First, we showed that systemic or intranasal administration of flagellin activated transcription of anti-viral genes in lung tissue. Prophylactic and therapeutic flagellin administration resulted in decreased levels of viral RNA and infectious virus in the lungs of H3N2 IAV-infected mice. The effect of the flagellin on viral replication was also observed in Ifnar-/- and Il22-/- IAV-infected mice, suggesting a mechanism independent of type I interferon and interleukin 22 signaling. In addition, a combination therapy associating the neuraminidase inhibitor oseltamivir and flagellin was more effective than standalone treatments in reducing pulmonary viral replication. Thus, this study highlights the therapeutic potential of the flagellin to control the replication of the influenza virus.
Url:
DOI: 10.1016/j.antiviral.2019.05.002
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Hal:inserm-02144074Le document en format XML
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U1019 - UMR 8204</orgName> <orgName type="acronym">CIIL</orgName> <date type="start">2010-01-01</date> <desc> <address> <addrLine>1 Rue du Professeur Calmette - Lille Cedex - 59019 - BP 245</addrLine> <country key="FR"></country> </address> <ref type="url">http://www.ciil.fr/</ref> </desc> <listRelation> <relation name="UMR8204" active="#struct-300166" type="direct"></relation> <relation active="#struct-301247" type="indirect"></relation> <relation name="U1019" active="#struct-303623" type="direct"></relation> <relation name="UMR9017" active="#struct-374570" type="direct"></relation> <relation name="UMR9017" active="#struct-441569" type="direct"></relation> </listRelation> <tutelles><tutelle name="UMR8204" active="#struct-300166" type="direct"><org type="institution" xml:id="struct-300166" status="VALID"> <orgName>Institut Pasteur de Lille</orgName> <date type="start">1894</date> <desc> <address> <addrLine>1 Rue du Professeur Calmette - Lille Cedex - 59019</addrLine> <country key="FR"></country> </address> <ref type="url">https://www.pasteur-lille.fr/accueil/</ref> </desc> <listRelation> <relation active="#struct-301247" type="direct"></relation> </listRelation> </org></tutelle><tutelle active="#struct-301247" type="indirect"><org type="regroupinstitution" xml:id="struct-301247" status="VALID"> <orgName>Réseau International des Instituts Pasteur</orgName> <orgName type="acronym">RIIP</orgName> <desc> <address> <addrLine>25, rue du Dr Roux 75724 Paris Cedex 15</addrLine> <country key="FR"></country> </address> <ref type="url">https://research.pasteur.fr/ip-network</ref> </desc> </org></tutelle><tutelle name="U1019" active="#struct-303623" type="direct"><org type="institution" xml:id="struct-303623" status="VALID"> <idno type="IdRef">026388278</idno> <orgName>Institut National de la Santé et de la Recherche Médicale</orgName> <orgName type="acronym">INSERM</orgName> <desc> <address> <addrLine>101, rue de Tolbiac, 75013 Paris </addrLine> <country key="FR"></country> </address> <ref type="url">http://www.inserm.fr</ref> </desc> </org></tutelle><tutelle name="UMR9017" active="#struct-374570" type="direct"><org type="institution" xml:id="struct-374570" status="VALID"> <idno type="IdRef">223446556</idno> <orgName>Université de Lille</orgName> <date type="start">2018-01-01</date> <desc> <address> <addrLine>Lille</addrLine> <country key="FR"></country> </address> <ref type="url">https://www.univ-lille.fr/</ref> </desc> </org></tutelle><tutelle name="UMR9017" active="#struct-441569" type="direct"><org type="institution" xml:id="struct-441569" status="VALID"> <idno type="IdRef">02636817X</idno> <idno type="ISNI">0000000122597504</idno> <orgName>Centre National de la Recherche Scientifique</orgName> <orgName type="acronym">CNRS</orgName> <date type="start">1939-10-19</date> <desc> <address> <country key="FR"></country> </address> <ref type="url">http://www.cnrs.fr/</ref> </desc> </org></tutelle></tutelles></hal:affiliation></affiliation></author><author><name sortKey="Carnoy, Christophe" sort="Carnoy, Christophe" uniqKey="Carnoy C" first="Christophe" last="Carnoy">Christophe Carnoy</name><affiliation><hal:affiliation type="laboratory" xml:id="struct-106189" status="VALID"> <idno type="IdRef">190712678</idno> <idno type="ISNI">0000 0004 0386 3856</idno> <idno type="RNSR">201019101Y</idno> <orgName>Centre d’Infection et d’Immunité de Lille (CIIL) - U1019 - UMR 8204</orgName> <orgName type="acronym">CIIL</orgName> <date type="start">2010-01-01</date> <desc> <address> <addrLine>1 Rue du Professeur Calmette - Lille Cedex - 59019 - BP 245</addrLine> <country key="FR"></country> </address> <ref type="url">http://www.ciil.fr/</ref> </desc> <listRelation> <relation name="UMR8204" active="#struct-300166" type="direct"></relation> <relation active="#struct-301247" type="indirect"></relation> <relation name="U1019" active="#struct-303623" type="direct"></relation> <relation name="UMR9017" active="#struct-374570" type="direct"></relation> <relation name="UMR9017" active="#struct-441569" type="direct"></relation> </listRelation> <tutelles><tutelle name="UMR8204" active="#struct-300166" type="direct"><org type="institution" xml:id="struct-300166" status="VALID"> <orgName>Institut Pasteur de Lille</orgName> <date type="start">1894</date> <desc> <address> <addrLine>1 Rue du Professeur Calmette - Lille Cedex - 59019</addrLine> <country key="FR"></country> </address> <ref type="url">https://www.pasteur-lille.fr/accueil/</ref> </desc> <listRelation> <relation active="#struct-301247" type="direct"></relation> </listRelation> </org></tutelle><tutelle active="#struct-301247" type="indirect"><org type="regroupinstitution" xml:id="struct-301247" status="VALID"> <orgName>Réseau International des Instituts Pasteur</orgName> <orgName type="acronym">RIIP</orgName> <desc> <address> <addrLine>25, rue du Dr Roux 75724 Paris Cedex 15</addrLine> <country key="FR"></country> </address> <ref type="url">https://research.pasteur.fr/ip-network</ref> </desc> </org></tutelle><tutelle name="U1019" active="#struct-303623" type="direct"><org type="institution" xml:id="struct-303623" status="VALID"> <idno type="IdRef">026388278</idno> <orgName>Institut National de la Santé et de la Recherche Médicale</orgName> <orgName type="acronym">INSERM</orgName> <desc> <address> <addrLine>101, rue de Tolbiac, 75013 Paris </addrLine> <country key="FR"></country> </address> <ref type="url">http://www.inserm.fr</ref> </desc> </org></tutelle><tutelle name="UMR9017" active="#struct-374570" type="direct"><org type="institution" xml:id="struct-374570" status="VALID"> <idno type="IdRef">223446556</idno> <orgName>Université de Lille</orgName> <date type="start">2018-01-01</date> <desc> <address> <addrLine>Lille</addrLine> <country key="FR"></country> </address> <ref type="url">https://www.univ-lille.fr/</ref> </desc> </org></tutelle><tutelle name="UMR9017" active="#struct-441569" type="direct"><org type="institution" xml:id="struct-441569" status="VALID"> <idno type="IdRef">02636817X</idno> <idno type="ISNI">0000000122597504</idno> <orgName>Centre National de la Recherche Scientifique</orgName> <orgName type="acronym">CNRS</orgName> <date type="start">1939-10-19</date> <desc> <address> <country key="FR"></country> </address> <ref type="url">http://www.cnrs.fr/</ref> </desc> </org></tutelle></tutelles></hal:affiliation></affiliation></author></analytic><idno type="DOI">10.1016/j.antiviral.2019.05.002</idno><series><title level="j">Antiviral Research</title><idno type="ISSN">0166-3542</idno><imprint><date type="datePub">2019-04</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="mix" xml:lang="en"><term>Influenza A virus</term><term>TLR5</term><term>flagellin</term><term>interleukin 22</term><term>type I interferon</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"> <p>Influenza infections remain a burden on health care systems despite vaccination programs and marketed antiviral drugs. Immunomodulation through activation of innate sensors could represent innovative approaches to fight the flu. This study evaluated the ability of flagellin, agonist of Toll-like receptor 5 (TLR5), to control the replication of influenza A virus (IAV) in mice. First, we showed that systemic or intranasal administration of flagellin activated transcription of anti-viral genes in lung tissue. Prophylactic and therapeutic flagellin administration resulted in decreased levels of viral RNA and infectious virus in the lungs of H3N2 IAV-infected mice. The effect of the flagellin on viral replication was also observed in Ifnar-/- and Il22-/- IAV-infected mice, suggesting a mechanism independent of type I interferon and interleukin 22 signaling. In addition, a combination therapy associating the neuraminidase inhibitor oseltamivir and flagellin was more effective than standalone treatments in reducing pulmonary viral replication. Thus, this study highlights the therapeutic potential of the flagellin to control the replication of the influenza virus.</p> </div></front></TEI><hal api="V3"> <titleStmt> <title xml:lang="en">Toll-like receptor 5 agonist flagellin reduces influenza A virus replication independently of type I interferon and interleukin 22 and improves antiviral efficacy of oseltamivir</title> <author role="aut"> <persName> <forename type="first">Anne-France</forename> <surname>Georgel</surname> </persName> <idno type="halauthorid">1194704</idno> <affiliation ref="#struct-561025"></affiliation> <affiliation ref="#struct-106189"></affiliation> </author> <author role="aut"> <persName> <forename type="first">Delphine</forename> <surname>Cayet</surname> </persName> <idno type="halauthorid">335432</idno> <affiliation ref="#struct-106189"></affiliation> </author> <author role="aut"> <persName> <forename type="first">Andrés</forename> <surname>Pizzorno</surname> </persName> <idno type="halauthorid">11309847</idno> <affiliation ref="#struct-543794"></affiliation> </author> <author role="aut"> <persName> <forename type="first">Manuel</forename> <surname>Rosa-Calatrava</surname> </persName> <idno type="halauthorid">412451</idno> <affiliation ref="#struct-543794"></affiliation> </author> <author role="aut"> <persName> <forename type="first">Christophe</forename> <surname>Paget</surname> </persName> <idno type="halauthorid">346651</idno> <affiliation ref="#struct-182226"></affiliation> </author> <author role="aut"> <persName> <forename type="first">Valentin</forename> <surname>Sencio</surname> </persName> <idno type="halauthorid">11443860</idno> <affiliation ref="#struct-106189"></affiliation> </author> <author role="aut"> <persName> <forename type="first">Jean</forename> <surname>Dubuisson</surname> </persName> <idno type="halauthorid">136770</idno> <affiliation ref="#struct-106189"></affiliation> </author> <author role="aut"> <persName> <forename type="first">François</forename> <surname>Trottein</surname> </persName> <email type="md5">fc3a463716e1c271812f3ad12c756bd7</email> <email type="domain">pasteur-lille.fr</email> <idno type="idhal" notation="string">francois-trottein</idno> <idno type="idhal" notation="numeric">175543</idno> <idno type="halauthorid">112793</idno> <idno type="ORCID">https://orcid.org/0000-0003-3373-1814</idno> <affiliation ref="#struct-106189"></affiliation> </author> <author role="crp"> <persName> <forename type="first">Jean Claude</forename> <surname>Sirard</surname> </persName> <email type="md5">342fa9242fa86965b20fb3cc292a98c1</email> <email type="domain">inserm.fr</email> <idno type="idhal" notation="string">jean-claude-sirard</idno> <idno type="idhal" notation="numeric">957</idno> <idno type="halauthorid">964581</idno> <idno type="IdRef">https://www.idref.fr/124317901</idno> <idno type="ORCID">https://orcid.org/0000-0001-9854-4652</idno> <idno type="ResearcherId">http://www.researcherid.com/rid/B-5932-2011</idno> <affiliation ref="#struct-106189"></affiliation> </author> <author role="aut"> <persName> <forename type="first">Christophe</forename> <surname>Carnoy</surname> </persName> <idno type="halauthorid">1194701</idno> <affiliation ref="#struct-106189"></affiliation> </author> <editor role="depositor"> <persName> <forename>Jean-Claude</forename> <surname>Sirard</surname> </persName> <email type="md5">342fa9242fa86965b20fb3cc292a98c1</email> <email type="domain">inserm.fr</email> </editor> <funder>This work was funded by INSERM, CNRS, Institut Pasteur de Lille, University of Lille and Inserm-Transfert (CoPoC grant “Innatebiotic”).</funder> </titleStmt> <editionStmt> <edition n="v1" type="current"> <date type="whenSubmitted">2019-05-29 18:08:21</date> <date type="whenModified">2020-03-30 08:30:03</date> <date type="whenReleased">2019-06-03 09:22:50</date> <date type="whenProduced">2019-04</date> <date type="whenEndEmbargoed">2019-10-02</date> <ref type="file" target="https://www.hal.inserm.fr/inserm-02144074/document"> <date notBefore="2019-10-02"></date> </ref> <ref type="file" subtype="author" n="1" target="https://www.hal.inserm.fr/inserm-02144074/file/POSTPRINT.pdf"> <date notBefore="2019-10-02"></date> </ref> </edition> <respStmt> <resp>contributor</resp> <name key="110101"> <persName> <forename>Jean-Claude</forename> <surname>Sirard</surname> </persName> <email type="md5">342fa9242fa86965b20fb3cc292a98c1</email> <email type="domain">inserm.fr</email> </name> </respStmt> </editionStmt> <publicationStmt> <distributor>CCSD</distributor> <idno type="halId">inserm-02144074</idno> <idno type="halUri">https://www.hal.inserm.fr/inserm-02144074</idno> <idno type="halBibtex">georgel:inserm-02144074</idno> <idno type="halRefHtml">Antiviral Research, Elsevier Masson, 2019, 168, pp.28-35. ⟨10.1016/j.antiviral.2019.05.002⟩</idno> <idno type="halRef">Antiviral Research, Elsevier Masson, 2019, 168, pp.28-35. ⟨10.1016/j.antiviral.2019.05.002⟩</idno> </publicationStmt> <seriesStmt> <idno type="stamp" n="INSERM">INSERM - Institut national de la santé et de la recherche médicale</idno> <idno type="stamp" n="RIIP_LILLE">Institut Pasteur de Lille</idno> <idno type="stamp" n="RIIP">Institut Pasteur RIIP (Réseau International)</idno> <idno type="stamp" n="ENS-LYON">École Normale Supérieure de Lyon</idno> <idno type="stamp" n="CNRS">CNRS - Centre national de la recherche scientifique</idno> <idno type="stamp" n="UNIV-LYON1">Université Claude Bernard - Lyon I</idno> <idno type="stamp" n="UNIV-LILLE">Université de Lille</idno> <idno type="stamp" n="CIRI" corresp="UNIV-LYON1">Centre International de Recherche en Infectiologie</idno> <idno type="stamp" n="VIRPATH-CIRI" corresp="CIRI">Virpath-CIRI- Grippe, de l'émergence au contrôle-Virpath-CIRI- Influenza, from emergence to control?</idno> <idno type="stamp" n="UNIV-TOURS">Université François Rabelais</idno> <idno type="stamp" n="UDL">UDL</idno> <idno type="stamp" n="UNIV-LYON">Université de Lyon</idno> </seriesStmt> <notesStmt> <note type="audience" n="2">International</note> <note type="popular" n="0">No</note> <note type="peer" n="1">Yes</note> </notesStmt> <sourceDesc> <biblStruct> <analytic> <title xml:lang="en">Toll-like receptor 5 agonist flagellin reduces influenza A virus replication independently of type I interferon and interleukin 22 and improves antiviral efficacy of oseltamivir</title> <author role="aut"> <persName> <forename type="first">Anne-France</forename> <surname>Georgel</surname> </persName> <idno type="halauthorid">1194704</idno> <affiliation ref="#struct-561025"></affiliation> <affiliation ref="#struct-106189"></affiliation> </author> <author role="aut"> <persName> <forename type="first">Delphine</forename> <surname>Cayet</surname> </persName> <idno type="halauthorid">335432</idno> <affiliation ref="#struct-106189"></affiliation> </author> <author role="aut"> <persName> <forename type="first">Andrés</forename> <surname>Pizzorno</surname> </persName> <idno type="halauthorid">11309847</idno> <affiliation ref="#struct-543794"></affiliation> </author> <author role="aut"> <persName> <forename type="first">Manuel</forename> <surname>Rosa-Calatrava</surname> </persName> <idno type="halauthorid">412451</idno> <affiliation ref="#struct-543794"></affiliation> </author> <author role="aut"> <persName> <forename type="first">Christophe</forename> <surname>Paget</surname> </persName> <idno type="halauthorid">346651</idno> <affiliation ref="#struct-182226"></affiliation> </author> <author role="aut"> <persName> <forename type="first">Valentin</forename> <surname>Sencio</surname> </persName> <idno type="halauthorid">11443860</idno> <affiliation ref="#struct-106189"></affiliation> </author> <author role="aut"> <persName> <forename type="first">Jean</forename> <surname>Dubuisson</surname> </persName> <idno type="halauthorid">136770</idno> <affiliation ref="#struct-106189"></affiliation> </author> <author role="aut"> <persName> <forename type="first">François</forename> <surname>Trottein</surname> </persName> <email type="md5">fc3a463716e1c271812f3ad12c756bd7</email> <email type="domain">pasteur-lille.fr</email> <idno type="idhal" notation="string">francois-trottein</idno> <idno type="idhal" notation="numeric">175543</idno> <idno type="halauthorid">112793</idno> <idno type="ORCID">https://orcid.org/0000-0003-3373-1814</idno> <affiliation ref="#struct-106189"></affiliation> </author> <author role="crp"> <persName> <forename type="first">Jean Claude</forename> <surname>Sirard</surname> </persName> <email type="md5">342fa9242fa86965b20fb3cc292a98c1</email> <email type="domain">inserm.fr</email> <idno type="idhal" notation="string">jean-claude-sirard</idno> <idno type="idhal" notation="numeric">957</idno> <idno type="halauthorid">964581</idno> <idno type="IdRef">https://www.idref.fr/124317901</idno> <idno type="ORCID">https://orcid.org/0000-0001-9854-4652</idno> <idno type="ResearcherId">http://www.researcherid.com/rid/B-5932-2011</idno> <affiliation ref="#struct-106189"></affiliation> </author> <author role="aut"> <persName> <forename type="first">Christophe</forename> <surname>Carnoy</surname> </persName> <idno type="halauthorid">1194701</idno> <affiliation ref="#struct-106189"></affiliation> </author> </analytic> <monogr> <idno type="halJournalId" status="VALID">10572</idno> <idno type="issn">0166-3542</idno> <title level="j">Antiviral Research</title> <imprint> <publisher>Elsevier Masson</publisher> <biblScope unit="volume">168</biblScope> <biblScope unit="pp">28-35</biblScope> <date type="datePub">2019-04</date> </imprint> </monogr> <idno type="doi">10.1016/j.antiviral.2019.05.002</idno> <idno type="pubmed">31078648</idno> </biblStruct> </sourceDesc> <profileDesc> <langUsage> <language ident="en">English</language> </langUsage> <textClass> <keywords scheme="author"> <term xml:lang="en">Influenza A virus</term> <term xml:lang="en">TLR5</term> <term xml:lang="en">flagellin</term> <term xml:lang="en">type I interferon</term> <term xml:lang="en">interleukin 22</term> </keywords> <classCode scheme="halDomain" n="sdv.mhep.mi">Life Sciences [q-bio]/Human health and pathology/Infectious diseases</classCode> <classCode scheme="halTypology" n="ART">Journal articles</classCode> </textClass> <abstract xml:lang="en"> <p>Influenza infections remain a burden on health care systems despite vaccination programs and marketed antiviral drugs. Immunomodulation through activation of innate sensors could represent innovative approaches to fight the flu. This study evaluated the ability of flagellin, agonist of Toll-like receptor 5 (TLR5), to control the replication of influenza A virus (IAV) in mice. First, we showed that systemic or intranasal administration of flagellin activated transcription of anti-viral genes in lung tissue. Prophylactic and therapeutic flagellin administration resulted in decreased levels of viral RNA and infectious virus in the lungs of H3N2 IAV-infected mice. The effect of the flagellin on viral replication was also observed in Ifnar-/- and Il22-/- IAV-infected mice, suggesting a mechanism independent of type I interferon and interleukin 22 signaling. In addition, a combination therapy associating the neuraminidase inhibitor oseltamivir and flagellin was more effective than standalone treatments in reducing pulmonary viral replication. Thus, this study highlights the therapeutic potential of the flagellin to control the replication of the influenza virus.</p> </abstract> </profileDesc> </hal></record>Pour manipuler ce document sous Unix (Dilib)
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