PAR1 contributes to influenza A virus pathogenicity in mice
Identifieur interne : 000442 ( Hal/Curation ); précédent : 000441; suivant : 000443PAR1 contributes to influenza A virus pathogenicity in mice
Auteurs : Khaled Khoufache [France] ; Fatma Berri [France] ; Wolfgang Nacken [Allemagne] ; Annette B. Vogel [Allemagne] ; Marie Delenne [France] ; Eric Camerer [France] ; Shaun R. Coughlin [États-Unis] ; Peter Carmeliet [Belgique] ; Bruno Lina [France] ; Guus F. Rimmelzwaan [Pays-Bas] ; Oliver Planz [Allemagne] ; Stephan Ludwig [Allemagne] ; Beatrice Riteau [France]Source :
- Journal of Clinical Investigation [ 0021-9738 ] ; 2013.
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Abstract
Influenza causes substantial morbidity and mortality, and highly pathogenic and drug-resistant strains are likely to emerge in the future. Protease-activated receptor 1 (PAR1) is a thrombin-activated receptor that contributes to inflammatory responses at mucosal surfaces. The role of PAR1 in pathogenesis of virus infections is unknown. Here, we demonstrate that PAR1 contributed to the deleterious inflammatory response after influenza virus infection in mice. Activating PAR1 by administering the agonist TFLLR-NH2 decreased survival and increased lung inflammation after influenza infection. Importantly, both administration of a PAR1 antagonist and PAR1 deficiency protected mice from infection with influenza A viruses (IAVs). Treatment with the PAR1 agonist did not alter survival of mice deficient in plasminogen (PLG), which suggests that PLG permits and/or interacts with a PAR1 function in this model. PARE antagonists are in human trials for other indications. Our findings suggest that PAR1 antagonism might be explored as a treatment for influenza, including that caused by highly pathogenic H5N1 and oseltamivir-resistant H1N1 viruses.
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DOI: 10.1172/JCI61667
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</placeName>
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</author>
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<author><name sortKey="Camerer, Eric" sort="Camerer, Eric" uniqKey="Camerer E" first="Eric" last="Camerer">Eric Camerer</name>
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</address>
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<desc> <address> <addrLine>12, rue de l'École de Médecine - 75270 Paris cedex 06</addrLine>
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</address>
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</desc>
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<tutelle name="U970" active="#struct-300119" type="direct"><org type="institution" xml:id="struct-300119" status="VALID"> <orgName>Hôpital Européen Georges Pompidou [APHP]</orgName>
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<desc> <address> <addrLine>20, rue Leblanc, 75015 Paris</addrLine>
<country key="FR"></country>
</address>
<ref type="url">http://hopital-georgespompidou.aphp.fr/</ref>
</desc>
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<tutelle active="#struct-300068" type="indirect"><org type="regroupinstitution" xml:id="struct-300068" status="VALID"> <orgName>Assistance publique - Hôpitaux de Paris (AP-HP)</orgName>
<orgName type="acronym">APHP</orgName>
<desc> <address> <country key="FR"></country>
</address>
</desc>
</org>
</tutelle>
<tutelle active="#struct-353414" type="indirect"><org type="regroupinstitution" xml:id="struct-353414" status="VALID"> <orgName>Hôpitaux Universitaires Paris Ouest - Hôpitaux Universitaires Île de France Ouest</orgName>
<orgName type="acronym">HUPO</orgName>
<desc> <address> <country key="FR"></country>
</address>
<ref type="url">http://hopitaux-parisouest.aphp.fr/</ref>
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<tutelle name="U970" 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>
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</address>
<ref type="url">http://www.inserm.fr</ref>
</desc>
</org>
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</hal:affiliation>
<country>France</country>
</affiliation>
</author>
<author><name sortKey="Coughlin, Shaun R" sort="Coughlin, Shaun R" uniqKey="Coughlin S" first="Shaun R." last="Coughlin">Shaun R. Coughlin</name>
<affiliation wicri:level="1"><hal:affiliation type="institution" xml:id="struct-190541" status="VALID"> <orgName>University of California [San Francisco]</orgName>
<orgName type="acronym">UCSF</orgName>
<desc> <address> <addrLine>505 Parnassus Ave, San Francisco, CA 94143</addrLine>
<country key="US"></country>
</address>
<ref type="url">https://www.ucsf.edu/</ref>
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<tutelles><tutelle active="#struct-471291" type="direct"><org type="regroupinstitution" xml:id="struct-471291" status="VALID"> <orgName>University of California</orgName>
<desc> <address> <country key="US"></country>
</address>
</desc>
</org>
</tutelle>
</tutelles>
</hal:affiliation>
<country>États-Unis</country>
</affiliation>
</author>
<author><name sortKey="Carmeliet, Peter" sort="Carmeliet, Peter" uniqKey="Carmeliet P" first="Peter" last="Carmeliet">Peter Carmeliet</name>
<affiliation wicri:level="1"><hal:affiliation type="institution" xml:id="struct-357456" status="INCOMING"> <orgName>Flanders Institute for Biotechnology</orgName>
<desc> <address> <country key="BE"></country>
</address>
</desc>
</hal:affiliation>
<country>Belgique</country>
</affiliation>
</author>
<author><name sortKey="Lina, Bruno" sort="Lina, Bruno" uniqKey="Lina B" first="Bruno" last="Lina">Bruno Lina</name>
<affiliation wicri:level="1"><hal:affiliation type="laboratory" xml:id="struct-508819" status="OLD"> <idno type="RNSR">201119499B</idno>
<orgName>Virologie et pathologie humaine</orgName>
<orgName type="acronym">VirPath</orgName>
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<desc> <address> <country key="FR"></country>
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<orgName>Université Claude Bernard Lyon 1</orgName>
<orgName type="acronym">UCBL</orgName>
<desc> <address> <addrLine>43, boulevard du 11 novembre 1918, 69622 Villeurbanne cedex</addrLine>
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</address>
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<tutelle active="#struct-301088" type="indirect"><org type="regroupinstitution" xml:id="struct-301088" status="VALID"> <orgName>Université de Lyon</orgName>
<desc> <address> <addrLine>92 rue Pasteur - CS 30122, 69361 Lyon Cedex 07</addrLine>
<country key="FR"></country>
</address>
<ref type="url">https://www.universite-lyon.fr/</ref>
</desc>
</org>
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</hal:affiliation>
<country>France</country>
<placeName><settlement type="city">Lyon</settlement>
<region type="region" nuts="2">Auvergne-Rhône-Alpes</region>
<region type="old region" nuts="2">Rhône-Alpes</region>
</placeName>
<orgName type="university">Université Claude Bernard Lyon 1</orgName>
<orgName type="institution" wicri:auto="newGroup">Université de Lyon</orgName>
</affiliation>
</author>
<author><name sortKey="Rimmelzwaan, Guus F" sort="Rimmelzwaan, Guus F" uniqKey="Rimmelzwaan G" first="Guus F." last="Rimmelzwaan">Guus F. Rimmelzwaan</name>
<affiliation wicri:level="1"><hal:affiliation type="institution" xml:id="struct-485122" status="VALID"> <orgName>Erasmus University Rotterdam</orgName>
<date type="start">2017-02-16</date>
<desc> <address> <country key="NL"></country>
</address>
<ref type="url">https://www.eur.nl/</ref>
</desc>
</hal:affiliation>
<country>Pays-Bas</country>
</affiliation>
</author>
<author><name sortKey="Planz, Oliver" sort="Planz, Oliver" uniqKey="Planz O" first="Oliver" last="Planz">Oliver Planz</name>
<affiliation wicri:level="1"><hal:affiliation type="institution" xml:id="struct-322700" status="VALID"> <orgName>Friedrich-Loeffler-Institut</orgName>
<orgName type="acronym">FLI</orgName>
<desc> <address> <addrLine>Federal Research Institute for Animal HealthSüdufer 10D-17493 Greifswald - Insel Riems</addrLine>
<country key="DE"></country>
</address>
<ref type="url">https://www.fli.de</ref>
</desc>
</hal:affiliation>
<country>Allemagne</country>
</affiliation>
</author>
<author><name sortKey="Ludwig, Stephan" sort="Ludwig, Stephan" uniqKey="Ludwig S" first="Stephan" last="Ludwig">Stephan Ludwig</name>
<affiliation wicri:level="1"><hal:affiliation type="institution" xml:id="struct-425052" status="VALID"> <orgName>University of Münster</orgName>
<desc> <address> <addrLine>Universität Münster Schlossplatz 2 48149 Münster</addrLine>
<country key="DE"></country>
</address>
<ref type="url">https://www.uni-muenster.de/de/</ref>
</desc>
</hal:affiliation>
<country>Allemagne</country>
</affiliation>
</author>
<author><name sortKey="Riteau, Beatrice" sort="Riteau, Beatrice" uniqKey="Riteau B" first="Beatrice" last="Riteau">Beatrice Riteau</name>
<affiliation wicri:level="1"><hal:affiliation type="laboratory" xml:id="struct-211885" status="OLD"> <orgName>Infectiologie Santé Publique</orgName>
<orgName type="acronym">ISP-311</orgName>
<date type="end">2019-12-31</date>
<desc> <address> <addrLine>37380 Nouzilly</addrLine>
<country key="FR"></country>
</address>
<ref type="url">https://www6.val-de-loire.inra.fr/infectiologie-santepublique</ref>
</desc>
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<orgName type="acronym">INRA</orgName>
<date type="start">1946-05-18</date>
<date type="end">2019-12-31</date>
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</address>
<ref type="url">http://www.inra.fr</ref>
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<tutelle active="#struct-300298" type="direct"><org type="institution" xml:id="struct-300298" status="VALID"> <idno type="IdRef">026404478</idno>
<orgName>Université de Tours</orgName>
<date type="start">1970-12-17</date>
<desc> <address> <addrLine>60 rue du Plat d'Étain, 37020 Tours cedex 1 </addrLine>
<country key="FR"></country>
</address>
<ref type="url">http://www.univ-tours.fr</ref>
</desc>
</org>
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</hal:affiliation>
<country>France</country>
<placeName><settlement type="city">Tours</settlement>
<region type="old region" nuts="2">Région Centre</region>
<region type="region" nuts="2">Centre-Val de Loire</region>
</placeName>
<orgName type="university">Université de Tours</orgName>
<orgName type="institution" wicri:auto="newGroup">Centre Val de Loire Université</orgName>
</affiliation>
</author>
</analytic>
<idno type="DOI">10.1172/JCI61667</idno>
<series><title level="j">Journal of Clinical Investigation</title>
<idno type="ISSN">0021-9738</idno>
<imprint><date type="datePub">2013</date>
</imprint>
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<profileDesc><textClass><keywords scheme="mix" xml:lang="en"><term>ANTAGONIST VORAPAXAR</term>
<term>DEPENDENT PATHWAY</term>
<term>IN-VIVO</term>
<term>LUNG INJURY</term>
<term>PROTEASE-ACTIVATED RECEPTORS</term>
<term>THROMBIN</term>
</keywords>
<keywords scheme="mix" xml:lang="fr"><term>INFECTION</term>
<term>INFLAMMATION</term>
<term>PANDEMIC INFLUENZA</term>
<term>PLASMINOGEN</term>
</keywords>
</textClass>
</profileDesc>
</teiHeader>
<front><div type="abstract" xml:lang="en"> <p>Influenza causes substantial morbidity and mortality, and highly pathogenic and drug-resistant strains are likely to emerge in the future. Protease-activated receptor 1 (PAR1) is a thrombin-activated receptor that contributes to inflammatory responses at mucosal surfaces. The role of PAR1 in pathogenesis of virus infections is unknown. Here, we demonstrate that PAR1 contributed to the deleterious inflammatory response after influenza virus infection in mice. Activating PAR1 by administering the agonist TFLLR-NH2 decreased survival and increased lung inflammation after influenza infection. Importantly, both administration of a PAR1 antagonist and PAR1 deficiency protected mice from infection with influenza A viruses (IAVs). Treatment with the PAR1 agonist did not alter survival of mice deficient in plasminogen (PLG), which suggests that PLG permits and/or interacts with a PAR1 function in this model. PARE antagonists are in human trials for other indications. Our findings suggest that PAR1 antagonism might be explored as a treatment for influenza, including that caused by highly pathogenic H5N1 and oseltamivir-resistant H1N1 viruses.</p>
</div>
</front>
</TEI>
<hal api="V3"> <titleStmt> <title xml:lang="en">PAR1 contributes to influenza A virus pathogenicity in mice</title>
<author role="aut"> <persName> <forename type="first">Khaled</forename>
<surname>Khoufache</surname>
</persName>
<email type="md5">547e112479f45f8da81c026caad07355</email>
<email type="domain">yahoo.fr</email>
<idno type="halauthorid">197742</idno>
<affiliation ref="#struct-211885"></affiliation>
<affiliation ref="#struct-508819"></affiliation>
</author>
<author role="aut"> <persName> <forename type="first">Fatma</forename>
<surname>Berri</surname>
</persName>
<idno type="halauthorid">1003479</idno>
<affiliation ref="#struct-508819"></affiliation>
</author>
<author role="aut"> <persName> <forename type="first">Wolfgang</forename>
<surname>Nacken</surname>
</persName>
<idno type="halauthorid">548374</idno>
<affiliation ref="#struct-425052"></affiliation>
</author>
<author role="aut"> <persName> <forename type="first">Annette B.</forename>
<surname>Vogel</surname>
</persName>
<idno type="halauthorid">11877131</idno>
<affiliation ref="#struct-322700"></affiliation>
</author>
<author role="aut"> <persName> <forename type="first">Marie</forename>
<surname>Delenne</surname>
</persName>
<idno type="halauthorid">11877132</idno>
<affiliation ref="#struct-508819"></affiliation>
</author>
<author role="aut"> <persName> <forename type="first">Eric</forename>
<surname>Camerer</surname>
</persName>
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<affiliation ref="#struct-81503"></affiliation>
<affiliation ref="#struct-301664"></affiliation>
</author>
<author role="aut"> <persName> <forename type="first">Shaun R.</forename>
<surname>Coughlin</surname>
</persName>
<idno type="halauthorid">11726681</idno>
<affiliation ref="#struct-190541"></affiliation>
</author>
<author role="aut"> <persName> <forename type="first">Peter</forename>
<surname>Carmeliet</surname>
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<idno type="halauthorid">193904</idno>
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<affiliation ref="#struct-92863"></affiliation>
</author>
<author role="aut"> <persName> <forename type="first">Bruno</forename>
<surname>Lina</surname>
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<idno type="halauthorid">400981</idno>
<affiliation ref="#struct-508819"></affiliation>
</author>
<author role="aut"> <persName> <forename type="first">Guus F.</forename>
<surname>Rimmelzwaan</surname>
</persName>
<idno type="halauthorid">11877133</idno>
<affiliation ref="#struct-485122"></affiliation>
</author>
<author role="aut"> <persName> <forename type="first">Oliver</forename>
<surname>Planz</surname>
</persName>
<idno type="halauthorid">11877134</idno>
<affiliation ref="#struct-322700"></affiliation>
</author>
<author role="aut"> <persName> <forename type="first">Stephan</forename>
<surname>Ludwig</surname>
</persName>
<idno type="halauthorid">11870369</idno>
<affiliation ref="#struct-425052"></affiliation>
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<author role="aut"> <persName> <forename type="first">Beatrice</forename>
<surname>Riteau</surname>
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<email type="md5">3e2374cca8aec85f239e07ef3201be28</email>
<email type="domain">univ-lyon1.fr</email>
<idno type="halauthorid">1208506</idno>
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</author>
<editor role="depositor"> <persName> <forename>Migration</forename>
<surname>ProdInra</surname>
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<email type="domain">inrae.fr</email>
</editor>
<funder>Agence Nationale de la Recherche (ANR); Inserm Avenir; Marie Curie actions; Long-term structural funding-Methusalem by the Flemish government</funder>
</titleStmt>
<editionStmt> <edition n="v1" type="current"> <date type="whenSubmitted">2020-05-28 20:54:51</date>
<date type="whenModified">2020-05-30 03:42:50</date>
<date type="whenReleased">2020-05-28 20:54:51</date>
<date type="whenProduced">2013</date>
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<idno type="halRefHtml">Journal of Clinical Investigation, American Society for Clinical Investigation, 2013, 123 (1), pp.206 - 214. ⟨10.1172/JCI61667⟩</idno>
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<seriesStmt> <idno type="stamp" n="INRAE">Institut National de Recherche en Agriculture, Alimentation et Environnement</idno>
<idno type="stamp" n="INRA">INRA - Institut national de la recherche agronomique</idno>
<idno type="stamp" n="APHP" corresp="INSERM">AP-HP</idno>
<idno type="stamp" n="UNIV-LYON1">Université Claude Bernard - Lyon I</idno>
<idno type="stamp" n="CHU-UNIV-PARIS5">Les centres hospitaliers de Paris Descartes</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>
<idno type="stamp" n="UNIV-PARIS5" corresp="UNIV-PARIS">Université Paris Descartes (Paris 5)</idno>
<idno type="stamp" n="UP-SANTE">Université de Paris - Faculté de Santé</idno>
<idno type="stamp" n="INSERM">INSERM - Institut national de la santé et de la recherche médicale</idno>
<idno type="stamp" n="USPC">Université Sorbonne Paris Cité</idno>
<idno type="stamp" n="UNIV-PARIS">Université de Paris</idno>
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<note type="peer" n="1">Yes</note>
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<sourceDesc> <biblStruct> <analytic> <title xml:lang="en">PAR1 contributes to influenza A virus pathogenicity in mice</title>
<author role="aut"> <persName> <forename type="first">Khaled</forename>
<surname>Khoufache</surname>
</persName>
<email type="md5">547e112479f45f8da81c026caad07355</email>
<email type="domain">yahoo.fr</email>
<idno type="halauthorid">197742</idno>
<affiliation ref="#struct-211885"></affiliation>
<affiliation ref="#struct-508819"></affiliation>
</author>
<author role="aut"> <persName> <forename type="first">Fatma</forename>
<surname>Berri</surname>
</persName>
<idno type="halauthorid">1003479</idno>
<affiliation ref="#struct-508819"></affiliation>
</author>
<author role="aut"> <persName> <forename type="first">Wolfgang</forename>
<surname>Nacken</surname>
</persName>
<idno type="halauthorid">548374</idno>
<affiliation ref="#struct-425052"></affiliation>
</author>
<author role="aut"> <persName> <forename type="first">Annette B.</forename>
<surname>Vogel</surname>
</persName>
<idno type="halauthorid">11877131</idno>
<affiliation ref="#struct-322700"></affiliation>
</author>
<author role="aut"> <persName> <forename type="first">Marie</forename>
<surname>Delenne</surname>
</persName>
<idno type="halauthorid">11877132</idno>
<affiliation ref="#struct-508819"></affiliation>
</author>
<author role="aut"> <persName> <forename type="first">Eric</forename>
<surname>Camerer</surname>
</persName>
<idno type="halauthorid">1557508</idno>
<affiliation ref="#struct-81503"></affiliation>
<affiliation ref="#struct-301664"></affiliation>
</author>
<author role="aut"> <persName> <forename type="first">Shaun R.</forename>
<surname>Coughlin</surname>
</persName>
<idno type="halauthorid">11726681</idno>
<affiliation ref="#struct-190541"></affiliation>
</author>
<author role="aut"> <persName> <forename type="first">Peter</forename>
<surname>Carmeliet</surname>
</persName>
<idno type="halauthorid">193904</idno>
<affiliation ref="#struct-357456"></affiliation>
<affiliation ref="#struct-92863"></affiliation>
</author>
<author role="aut"> <persName> <forename type="first">Bruno</forename>
<surname>Lina</surname>
</persName>
<idno type="halauthorid">400981</idno>
<affiliation ref="#struct-508819"></affiliation>
</author>
<author role="aut"> <persName> <forename type="first">Guus F.</forename>
<surname>Rimmelzwaan</surname>
</persName>
<idno type="halauthorid">11877133</idno>
<affiliation ref="#struct-485122"></affiliation>
</author>
<author role="aut"> <persName> <forename type="first">Oliver</forename>
<surname>Planz</surname>
</persName>
<idno type="halauthorid">11877134</idno>
<affiliation ref="#struct-322700"></affiliation>
</author>
<author role="aut"> <persName> <forename type="first">Stephan</forename>
<surname>Ludwig</surname>
</persName>
<idno type="halauthorid">11870369</idno>
<affiliation ref="#struct-425052"></affiliation>
</author>
<author role="aut"> <persName> <forename type="first">Beatrice</forename>
<surname>Riteau</surname>
</persName>
<email type="md5">3e2374cca8aec85f239e07ef3201be28</email>
<email type="domain">univ-lyon1.fr</email>
<idno type="halauthorid">1208506</idno>
<affiliation ref="#struct-211885"></affiliation>
<affiliation ref="#struct-194495"></affiliation>
</author>
</analytic>
<monogr> <idno type="halJournalId" status="VALID">1386</idno>
<idno type="issn">0021-9738</idno>
<title level="j">Journal of Clinical Investigation</title>
<imprint> <publisher>American Society for Clinical Investigation</publisher>
<biblScope unit="volume">123</biblScope>
<biblScope unit="issue">1</biblScope>
<biblScope unit="pp">206 - 214</biblScope>
<date type="datePub">2013</date>
</imprint>
</monogr>
<idno type="doi">10.1172/JCI61667</idno>
<idno type="prodinra">211606</idno>
<idno type="wos">000313598500026</idno>
</biblStruct>
</sourceDesc>
<profileDesc> <langUsage> <language ident="en">English</language>
</langUsage>
<textClass> <keywords scheme="author"> <term xml:lang="en">PROTEASE-ACTIVATED RECEPTORS</term>
<term xml:lang="en">ANTAGONIST VORAPAXAR</term>
<term xml:lang="en">DEPENDENT PATHWAY</term>
<term xml:lang="en">LUNG INJURY</term>
<term xml:lang="en">IN-VIVO</term>
<term xml:lang="en">THROMBIN</term>
<term xml:lang="fr">PANDEMIC INFLUENZA</term>
<term xml:lang="fr">PLASMINOGEN</term>
<term xml:lang="fr">INFECTION</term>
<term xml:lang="fr">INFLAMMATION</term>
</keywords>
<classCode scheme="halDomain" n="sdv">Life Sciences [q-bio]</classCode>
<classCode scheme="halTypology" n="ART">Journal articles</classCode>
</textClass>
<abstract xml:lang="en"> <p>Influenza causes substantial morbidity and mortality, and highly pathogenic and drug-resistant strains are likely to emerge in the future. Protease-activated receptor 1 (PAR1) is a thrombin-activated receptor that contributes to inflammatory responses at mucosal surfaces. The role of PAR1 in pathogenesis of virus infections is unknown. Here, we demonstrate that PAR1 contributed to the deleterious inflammatory response after influenza virus infection in mice. Activating PAR1 by administering the agonist TFLLR-NH2 decreased survival and increased lung inflammation after influenza infection. Importantly, both administration of a PAR1 antagonist and PAR1 deficiency protected mice from infection with influenza A viruses (IAVs). Treatment with the PAR1 agonist did not alter survival of mice deficient in plasminogen (PLG), which suggests that PLG permits and/or interacts with a PAR1 function in this model. PARE antagonists are in human trials for other indications. Our findings suggest that PAR1 antagonism might be explored as a treatment for influenza, including that caused by highly pathogenic H5N1 and oseltamivir-resistant H1N1 viruses.</p>
</abstract>
</profileDesc>
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