Mutations Conferring Increased Sensitivity to Tripartite Motif 22 Restriction Accumulated Progressively in the Nucleoprotein of Seasonal Influenza A (H1N1) Viruses between 1918 and 2009
Identifieur interne : 000175 ( Main/Merge ); précédent : 000174; suivant : 000176Mutations Conferring Increased Sensitivity to Tripartite Motif 22 Restriction Accumulated Progressively in the Nucleoprotein of Seasonal Influenza A (H1N1) Viruses between 1918 and 2009
Auteurs : Isabel Pagani [Italie] ; Andrea Di Pietro [Italie] ; Alexandra Oteiza [France] ; Michela Ghitti [Italie] ; Nadir Mechti [France] ; Nadia Naffakh [France] ; Elisa Vicenzi [Italie]Source :
- mSphere [ 2379-5042 ] ; 2018.
English descriptors
- mix :
Abstract
We have uncovered that long-term circulation of seasonal influenza A viruses (IAV) in the human population resulted in the progressive acquisition of increased sensitivity to a component of the innate immune response: the type I interferon-inducible TRIM22 protein, which acts as a restriction factor by inducing the polyubiquitination of the IAV nucleoprotein (NP). We show that four arginine residues present in the NP of the 1918 H1N1 pandemic strain and early postpandemic strains were progressively substituted for by lysines between 1918 and 2009, rendering NP more susceptible to TRIM22-mediated ubiquitination. Our observations suggest that during long-term evolution of IAVs in humans, variants endowed with increased susceptibility to TRIM22 restriction emerge, highlighting the complexity of selection pressures acting on the NP.
Url:
DOI: 10.1128/mSphere.00110-18
PubMed: 29624498
PubMed Central: 5885024
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PMC:5885024Le document en format XML
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type="region">Île-de-France</region><region type="old region">Île-de-France</region><settlement type="city">Paris</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:aff id="aff4"><addr-line>CNRS, UMR3569, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>CNRS, UMR3569, Paris</wicri:regionArea><placeName><region type="region">Île-de-France</region><region type="old region">Île-de-France</region><settlement type="city">Paris</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:aff id="aff5"><addr-line>Université Paris Diderot, Sorbonne Paris Cité, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Université Paris Diderot, Sorbonne Paris Cité, Paris</wicri:regionArea><placeName><region type="region">Île-de-France</region><region type="old region">Île-de-France</region><settlement type="city">Paris</settlement></placeName></affiliation></author><author><name sortKey="Vicenzi, Elisa" sort="Vicenzi, Elisa" uniqKey="Vicenzi E" first="Elisa" last="Vicenzi">Elisa Vicenzi</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>San Raffaele Scientific Institute, Milan, Italy</addr-line></nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>San Raffaele Scientific Institute, Milan</wicri:regionArea><placeName><settlement type="city">Milan</settlement><region nuts="2">Lombardie</region></placeName></affiliation></author></analytic><series><title level="j">mSphere</title><idno type="eISSN">2379-5042</idno><imprint><date when="2018">2018</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="mix" xml:lang="en"><term>TRIM22</term><term>evolution</term><term>influenza A virus</term><term>nucleoprotein</term><term>restriction</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>We have uncovered that long-term circulation of seasonal influenza A viruses (IAV) in the human population resulted in the progressive acquisition of increased sensitivity to a component of the innate immune response: the type I interferon-inducible TRIM22 protein, which acts as a restriction factor by inducing the polyubiquitination of the IAV nucleoprotein (NP). We show that four arginine residues present in the NP of the 1918 H1N1 pandemic strain and early postpandemic strains were progressively substituted for by lysines between 1918 and 2009, rendering NP more susceptible to TRIM22-mediated ubiquitination. Our observations suggest that during long-term evolution of IAVs in humans, variants endowed with increased susceptibility to TRIM22 restriction emerge, highlighting the complexity of selection pressures acting on the NP.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Taubenberger, Jk" uniqKey="Taubenberger J">JK Taubenberger</name></author><author><name sortKey="Kash, Jc" uniqKey="Kash J">JC Kash</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Capua, I" uniqKey="Capua I">I Capua</name></author><author><name sortKey="Kajaste Rudnitski, A" uniqKey="Kajaste Rudnitski A">A Kajaste-Rudnitski</name></author><author><name sortKey="Bertoli, E" uniqKey="Bertoli E">E Bertoli</name></author><author><name sortKey="Vicenzi, E" uniqKey="Vicenzi E">E Vicenzi</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Sangster, My" uniqKey="Sangster M">MY 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Naffakh</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Eldin, P" uniqKey="Eldin P">P Eldin</name></author><author><name sortKey="Papon, L" uniqKey="Papon L">L Papon</name></author><author><name sortKey="Oteiza, A" uniqKey="Oteiza A">A Oteiza</name></author><author><name sortKey="Brocchi, E" uniqKey="Brocchi E">E Brocchi</name></author><author><name sortKey="Lawson, Tg" uniqKey="Lawson T">TG Lawson</name></author><author><name sortKey="Mechti, N" uniqKey="Mechti N">N Mechti</name></author></analytic></biblStruct></listBibl></div1></back></TEI><double doi="10.1128/mSphere.00110-18"><HAL><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Mutations Conferring Increased Sensitivity to Tripartite Motif 22 Restriction Accumulated Progressively in the Nucleoprotein of Seasonal Influenza A (H1N1) Viruses between 1918 and 2009</title><author><name sortKey="Pagani, Isabel" sort="Pagani, Isabel" uniqKey="Pagani I" first="Isabel" last="Pagani">Isabel Pagani</name><affiliation wicri:level="1"><hal:affiliation type="institution" xml:id="struct-523246" status="VALID"> <orgName>IRCSS San Raffaele Scientific Institute [Milan, Italie]</orgName> <desc> <address> <addrLine>Ospedale San Raffaele - Milano, via Olgettina 60, 20132 Milano, Italia</addrLine> <country key="IT"></country> </address> <ref type="url">http://www.hsr.it/research/about-us/</ref> </desc> </hal:affiliation><country>Italie</country></affiliation></author><author><name sortKey="Di Pietro, Andrea" sort="Di Pietro, Andrea" uniqKey="Di Pietro A" first="Andrea" last="Di Pietro">Andrea Di Pietro</name><affiliation wicri:level="1"><hal:affiliation type="institution" xml:id="struct-523246" status="VALID"> <orgName>IRCSS San Raffaele Scientific Institute [Milan, Italie]</orgName> <desc> <address> <addrLine>Ospedale San Raffaele - Milano, via Olgettina 60, 20132 Milano, Italia</addrLine> <country key="IT"></country> </address> <ref type="url">http://www.hsr.it/research/about-us/</ref> </desc> </hal:affiliation><country>Italie</country></affiliation></author><author><name sortKey="Oteiza, Alexandra" sort="Oteiza, Alexandra" uniqKey="Oteiza A" first="Alexandra" last="Oteiza">Alexandra Oteiza</name><affiliation wicri:level="1"><hal:affiliation type="laboratory" xml:id="struct-500452" status="VALID"> <idno type="RNSR">201722408M</idno> <orgName>Institut de Recherche en Infectiologie de Montpellier</orgName> <orgName type="acronym">IRIM</orgName> <desc> <address> <addrLine>UMR 9004, 1919 Route de Mende - 34293 Montpellier</addrLine> <country key="FR"></country> </address> <ref type="url">http://www.irim.cnrs.fr/</ref> </desc> <listRelation> <relation active="#struct-410122" type="direct"></relation> <relation name="UMR9004" active="#struct-441569" type="direct"></relation> </listRelation> <tutelles><tutelle active="#struct-410122" type="direct"><org type="institution" xml:id="struct-410122" status="VALID"> <idno type="ISNI">0000000120970141</idno> <orgName>Université de Montpellier</orgName> <orgName type="acronym">UM</orgName> <desc> <address> <addrLine>163 rue Auguste Broussonnet - 34090 Montpellier</addrLine> <country key="FR"></country> </address> <ref type="url">http://www.umontpellier.fr/</ref> </desc> </org></tutelle><tutelle name="UMR9004" 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><country>France</country></affiliation></author><author><name sortKey="Ghitti, Michela" sort="Ghitti, Michela" uniqKey="Ghitti M" first="Michela" last="Ghitti">Michela Ghitti</name><affiliation wicri:level="1"><hal:affiliation type="institution" xml:id="struct-523246" status="VALID"> <orgName>IRCSS San Raffaele Scientific Institute [Milan, Italie]</orgName> <desc> <address> <addrLine>Ospedale San Raffaele - Milano, via Olgettina 60, 20132 Milano, Italia</addrLine> <country key="IT"></country> </address> <ref type="url">http://www.hsr.it/research/about-us/</ref> </desc> </hal:affiliation><country>Italie</country></affiliation></author><author><name sortKey="Mechti, Nadir" sort="Mechti, Nadir" uniqKey="Mechti N" first="Nadir" last="Mechti">Nadir Mechti</name><affiliation wicri:level="1"><hal:affiliation type="laboratory" xml:id="struct-417138" status="OLD"> <idno type="IdRef">235658278</idno> <idno type="RNSR">200818198A</idno> <orgName>Génétique Moléculaire des Virus à ARN - Molecular Genetics of RNA Viruses</orgName> <orgName type="acronym">GMV-ARN (UMR_3569 / U-Pasteur_2)</orgName> <date type="end">2019-12-31</date> <desc> <address> <addrLine>Département de Virologie, 25-28 rue du docteur Roux, 75724 Paris cedex 15</addrLine> <country key="FR"></country> </address> <ref type="url">https://research.pasteur.fr/en/team/molecular-genetics-of-rna-viruses/</ref> </desc> <listRelation> <relation name="UMR_3569" active="#struct-441569" type="direct"></relation> <relation name="U-Pasteur_2" active="#struct-300301" type="direct"></relation> <relation active="#struct-300027" type="direct"></relation> </listRelation> <tutelles><tutelle name="UMR_3569" 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><tutelle name="U-Pasteur_2" 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</org></tutelle></tutelles></hal:affiliation><country>France</country></affiliation></author><author><name sortKey="Naffakh, Nadia" sort="Naffakh, Nadia" uniqKey="Naffakh N" first="Nadia" last="Naffakh">Nadia Naffakh</name><affiliation wicri:level="1"><hal:affiliation type="laboratory" xml:id="struct-417138" status="OLD"> <idno type="IdRef">235658278</idno> <idno type="RNSR">200818198A</idno> <orgName>Génétique Moléculaire des Virus à ARN - Molecular Genetics of RNA Viruses</orgName> <orgName type="acronym">GMV-ARN (UMR_3569 / U-Pasteur_2)</orgName> <date type="end">2019-12-31</date> <desc> <address> <addrLine>Département de Virologie, 25-28 rue du docteur Roux, 75724 Paris cedex 15</addrLine> <country key="FR"></country> </address> <ref type="url">https://research.pasteur.fr/en/team/molecular-genetics-of-rna-viruses/</ref> </desc> <listRelation> <relation name="UMR_3569" active="#struct-441569" type="direct"></relation> <relation name="U-Pasteur_2" active="#struct-300301" type="direct"></relation> <relation active="#struct-300027" type="direct"></relation> </listRelation> <tutelles><tutelle name="UMR_3569" 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><tutelle name="U-Pasteur_2" active="#struct-300301" type="direct"><org type="institution" xml:id="struct-300301" status="OLD"> <idno type="ISNI">0000000121514068</idno> <idno type="IdRef">027542084</idno> <orgName>Université Paris Diderot - Paris 7</orgName> <orgName type="acronym">UPD7</orgName> <date type="end">2019-12-31</date> <desc> <address> <addrLine>5 rue Thomas-Mann - 75205 Paris cedex 13</addrLine> <country key="FR"></country> </address> <ref type="url">http://www.univ-paris-diderot.fr</ref> </desc> </org></tutelle><tutelle active="#struct-300027" type="direct"><org type="institution" xml:id="struct-300027" status="VALID"> <idno type="IdRef">027936643</idno> <idno type="ISNI">0000 0001 2353 6535</idno> <orgName>Institut Pasteur [Paris]</orgName> <date type="start">1887-06-04</date> <desc> <address> <addrLine>25-28, rue du docteur Roux, 75724 Paris cedex 15</addrLine> <country key="FR"></country> </address> <ref type="url">https://www.pasteur.fr</ref> </desc> </org></tutelle></tutelles></hal:affiliation><country>France</country></affiliation></author><author><name sortKey="Vicenzi, Elisa" sort="Vicenzi, Elisa" uniqKey="Vicenzi E" first="Elisa" last="Vicenzi">Elisa Vicenzi</name><affiliation wicri:level="1"><hal:affiliation type="institution" xml:id="struct-523246" status="VALID"> <orgName>IRCSS San Raffaele Scientific Institute [Milan, Italie]</orgName> <desc> <address> <addrLine>Ospedale San Raffaele - Milano, via Olgettina 60, 20132 Milano, Italia</addrLine> <country key="IT"></country> </address> <ref type="url">http://www.hsr.it/research/about-us/</ref> </desc> </hal:affiliation><country>Italie</country></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">HAL</idno><idno type="RBID">Hal:hal-02351139</idno><idno type="halId">hal-02351139</idno><idno type="halUri">https://hal.archives-ouvertes.fr/hal-02351139</idno><idno type="url">https://hal.archives-ouvertes.fr/hal-02351139</idno><idno type="doi">10.1128/mSphere.00110-18</idno><date when="2018-04-25">2018-04-25</date><idno type="wicri:Area/Hal/Corpus">000218</idno><idno type="wicri:Area/Hal/Curation">000218</idno><idno type="wicri:Area/Hal/Checkpoint">000026</idno><idno type="wicri:explorRef" wicri:stream="Hal" wicri:step="Checkpoint">000026</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">Mutations Conferring Increased Sensitivity to Tripartite Motif 22 Restriction Accumulated Progressively in the Nucleoprotein of Seasonal Influenza A (H1N1) Viruses between 1918 and 2009</title><author><name sortKey="Pagani, Isabel" sort="Pagani, Isabel" uniqKey="Pagani I" first="Isabel" last="Pagani">Isabel Pagani</name><affiliation wicri:level="1"><hal:affiliation type="institution" xml:id="struct-523246" status="VALID"> <orgName>IRCSS San Raffaele Scientific Institute [Milan, Italie]</orgName> <desc> <address> <addrLine>Ospedale San Raffaele - Milano, via Olgettina 60, 20132 Milano, Italia</addrLine> <country key="IT"></country> </address> <ref type="url">http://www.hsr.it/research/about-us/</ref> </desc> </hal:affiliation><country>Italie</country></affiliation></author><author><name sortKey="Di Pietro, Andrea" sort="Di Pietro, Andrea" uniqKey="Di Pietro A" first="Andrea" last="Di Pietro">Andrea Di Pietro</name><affiliation wicri:level="1"><hal:affiliation type="institution" xml:id="struct-523246" status="VALID"> <orgName>IRCSS San Raffaele Scientific Institute [Milan, Italie]</orgName> <desc> <address> <addrLine>Ospedale San Raffaele - Milano, via Olgettina 60, 20132 Milano, Italia</addrLine> <country key="IT"></country> </address> <ref type="url">http://www.hsr.it/research/about-us/</ref> </desc> </hal:affiliation><country>Italie</country></affiliation></author><author><name sortKey="Oteiza, Alexandra" sort="Oteiza, Alexandra" uniqKey="Oteiza A" first="Alexandra" last="Oteiza">Alexandra Oteiza</name><affiliation wicri:level="1"><hal:affiliation type="laboratory" xml:id="struct-500452" status="VALID"> <idno type="RNSR">201722408M</idno> <orgName>Institut de Recherche en Infectiologie de Montpellier</orgName> <orgName type="acronym">IRIM</orgName> <desc> <address> <addrLine>UMR 9004, 1919 Route de Mende - 34293 Montpellier</addrLine> <country key="FR"></country> </address> <ref type="url">http://www.irim.cnrs.fr/</ref> </desc> <listRelation> <relation active="#struct-410122" type="direct"></relation> <relation name="UMR9004" active="#struct-441569" type="direct"></relation> </listRelation> <tutelles><tutelle active="#struct-410122" type="direct"><org type="institution" xml:id="struct-410122" status="VALID"> <idno type="ISNI">0000000120970141</idno> <orgName>Université de Montpellier</orgName> <orgName type="acronym">UM</orgName> <desc> <address> <addrLine>163 rue Auguste Broussonnet - 34090 Montpellier</addrLine> <country key="FR"></country> </address> <ref type="url">http://www.umontpellier.fr/</ref> </desc> </org></tutelle><tutelle name="UMR9004" 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><country>France</country></affiliation></author><author><name sortKey="Ghitti, Michela" sort="Ghitti, Michela" uniqKey="Ghitti M" first="Michela" last="Ghitti">Michela Ghitti</name><affiliation wicri:level="1"><hal:affiliation type="institution" xml:id="struct-523246" status="VALID"> <orgName>IRCSS San Raffaele Scientific Institute [Milan, Italie]</orgName> <desc> <address> <addrLine>Ospedale San Raffaele - Milano, via Olgettina 60, 20132 Milano, Italia</addrLine> <country key="IT"></country> </address> <ref type="url">http://www.hsr.it/research/about-us/</ref> </desc> </hal:affiliation><country>Italie</country></affiliation></author><author><name sortKey="Mechti, Nadir" sort="Mechti, Nadir" uniqKey="Mechti N" first="Nadir" last="Mechti">Nadir Mechti</name><affiliation wicri:level="1"><hal:affiliation type="laboratory" xml:id="struct-417138" status="OLD"> <idno type="IdRef">235658278</idno> <idno type="RNSR">200818198A</idno> <orgName>Génétique Moléculaire des Virus à ARN - Molecular Genetics of RNA Viruses</orgName> <orgName type="acronym">GMV-ARN (UMR_3569 / U-Pasteur_2)</orgName> <date type="end">2019-12-31</date> <desc> <address> <addrLine>Département de Virologie, 25-28 rue du docteur Roux, 75724 Paris cedex 15</addrLine> <country key="FR"></country> </address> <ref type="url">https://research.pasteur.fr/en/team/molecular-genetics-of-rna-viruses/</ref> </desc> <listRelation> <relation name="UMR_3569" active="#struct-441569" type="direct"></relation> <relation name="U-Pasteur_2" active="#struct-300301" type="direct"></relation> <relation active="#struct-300027" type="direct"></relation> </listRelation> <tutelles><tutelle name="UMR_3569" 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><tutelle name="U-Pasteur_2" active="#struct-300301" type="direct"><org type="institution" xml:id="struct-300301" status="OLD"> <idno type="ISNI">0000000121514068</idno> <idno type="IdRef">027542084</idno> <orgName>Université Paris Diderot - Paris 7</orgName> <orgName type="acronym">UPD7</orgName> <date type="end">2019-12-31</date> <desc> <address> <addrLine>5 rue Thomas-Mann - 75205 Paris cedex 13</addrLine> <country key="FR"></country> </address> <ref type="url">http://www.univ-paris-diderot.fr</ref> </desc> </org></tutelle><tutelle active="#struct-300027" type="direct"><org type="institution" xml:id="struct-300027" status="VALID"> <idno type="IdRef">027936643</idno> <idno type="ISNI">0000 0001 2353 6535</idno> <orgName>Institut Pasteur [Paris]</orgName> <date type="start">1887-06-04</date> <desc> <address> <addrLine>25-28, rue du docteur Roux, 75724 Paris cedex 15</addrLine> <country key="FR"></country> </address> <ref type="url">https://www.pasteur.fr</ref> </desc> </org></tutelle></tutelles></hal:affiliation><country>France</country></affiliation></author><author><name sortKey="Naffakh, Nadia" sort="Naffakh, Nadia" uniqKey="Naffakh N" first="Nadia" last="Naffakh">Nadia Naffakh</name><affiliation wicri:level="1"><hal:affiliation type="laboratory" xml:id="struct-417138" status="OLD"> <idno type="IdRef">235658278</idno> <idno type="RNSR">200818198A</idno> <orgName>Génétique Moléculaire des Virus à ARN - Molecular Genetics of RNA Viruses</orgName> <orgName type="acronym">GMV-ARN (UMR_3569 / U-Pasteur_2)</orgName> <date type="end">2019-12-31</date> <desc> <address> <addrLine>Département de Virologie, 25-28 rue du docteur Roux, 75724 Paris cedex 15</addrLine> <country key="FR"></country> </address> <ref type="url">https://research.pasteur.fr/en/team/molecular-genetics-of-rna-viruses/</ref> </desc> <listRelation> <relation name="UMR_3569" active="#struct-441569" type="direct"></relation> <relation name="U-Pasteur_2" active="#struct-300301" type="direct"></relation> <relation active="#struct-300027" type="direct"></relation> </listRelation> <tutelles><tutelle name="UMR_3569" 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><tutelle name="U-Pasteur_2" active="#struct-300301" type="direct"><org type="institution" xml:id="struct-300301" status="OLD"> <idno type="ISNI">0000000121514068</idno> <idno type="IdRef">027542084</idno> <orgName>Université Paris Diderot - Paris 7</orgName> <orgName type="acronym">UPD7</orgName> <date type="end">2019-12-31</date> <desc> <address> <addrLine>5 rue Thomas-Mann - 75205 Paris cedex 13</addrLine> <country key="FR"></country> </address> <ref type="url">http://www.univ-paris-diderot.fr</ref> </desc> </org></tutelle><tutelle active="#struct-300027" type="direct"><org type="institution" xml:id="struct-300027" status="VALID"> <idno type="IdRef">027936643</idno> <idno type="ISNI">0000 0001 2353 6535</idno> <orgName>Institut Pasteur [Paris]</orgName> <date type="start">1887-06-04</date> <desc> <address> <addrLine>25-28, rue du docteur Roux, 75724 Paris cedex 15</addrLine> <country key="FR"></country> </address> <ref type="url">https://www.pasteur.fr</ref> </desc> </org></tutelle></tutelles></hal:affiliation><country>France</country></affiliation></author><author><name sortKey="Vicenzi, Elisa" sort="Vicenzi, Elisa" uniqKey="Vicenzi E" first="Elisa" last="Vicenzi">Elisa Vicenzi</name><affiliation wicri:level="1"><hal:affiliation type="institution" xml:id="struct-523246" status="VALID"> <orgName>IRCSS San Raffaele Scientific Institute [Milan, Italie]</orgName> <desc> <address> <addrLine>Ospedale San Raffaele - Milano, via Olgettina 60, 20132 Milano, Italia</addrLine> <country key="IT"></country> </address> <ref type="url">http://www.hsr.it/research/about-us/</ref> </desc> </hal:affiliation><country>Italie</country></affiliation></author></analytic><idno type="DOI">10.1128/mSphere.00110-18</idno></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="mix" xml:lang="en"><term>TRIM22</term><term>evolution</term><term>influenza A virus</term><term>nucleoprotein</term><term>restriction</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"> <p>Influenza A viruses (IAVs) can cause zoonotic infections with pandemic potential when most of the human population is immunologically naive. After a pandemic, IAVs evolve to become seasonal in the human host by acquiring adaptive mutations. We have previously reported that the interferon (IFN)-inducible tripartite motif 22 (TRIM22) protein restricts the replication of seasonal IAVs by direct interaction with the viral nucleoprotein (NP), leading to its polyubiquitination and protea-somal degradation. Here we show that, in contrast to seasonal H1N1 IAVs, the 2009 pandemic H1N1 strain as well as H1N1 strains from the 1930s are resistant to TRIM22 restriction. We demonstrate that arginine-to-lysine substitutions conferring an increased sensitivity to TRIM22-dependent ubiquitination accumulated progressively in the NP of seasonal influenza A (H1N1) viruses between 1918 and 2009. Our findings suggest that during long-term circulation and evolution of IAVs in humans, adaptive mutations are favored at the expense of an increased sensitivity to some components of the innate immune response. IMPORTANCE We have uncovered that long-term circulation of seasonal influenza A viruses (IAV) in the human population resulted in the progressive acquisition of increased sensitivity to a component of the innate immune response: the type I interferon-inducible TRIM22 protein, which acts as a restriction factor by inducing the polyubiquiti-nation of the IAV nucleoprotein (NP). We show that four arginine residues present in the NP of the 1918 H1N1 pandemic strain and early postpandemic strains were progressively substituted for by lysines between 1918 and 2009, rendering NP more susceptible to TRIM22-mediated ubiquitination. Our observations suggest that during long-term evolution of IAVs in humans, variants endowed with increased susceptibility to TRIM22 restriction emerge, highlighting the complexity of selection pressures acting on the NP.</p> </div></front></TEI></HAL><PMC><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Mutations Conferring Increased Sensitivity to Tripartite Motif 22 Restriction Accumulated Progressively in the Nucleoprotein of Seasonal Influenza A (H1N1) Viruses between 1918 and 2009</title><author><name sortKey="Pagani, Isabel" sort="Pagani, Isabel" uniqKey="Pagani I" first="Isabel" last="Pagani">Isabel Pagani</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>San Raffaele Scientific Institute, Milan, Italy</addr-line></nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>San Raffaele Scientific Institute, Milan</wicri:regionArea><placeName><settlement type="city">Milan</settlement><region nuts="2">Lombardie</region></placeName></affiliation></author><author><name sortKey="Di Pietro, Andrea" sort="Di Pietro, Andrea" uniqKey="Di Pietro A" first="Andrea" last="Di Pietro">Andrea Di Pietro</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>San Raffaele Scientific Institute, Milan, Italy</addr-line></nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>San Raffaele Scientific Institute, Milan</wicri:regionArea><placeName><settlement type="city">Milan</settlement><region nuts="2">Lombardie</region></placeName></affiliation></author><author><name sortKey="Oteiza, Alexandra" sort="Oteiza, Alexandra" uniqKey="Oteiza A" first="Alexandra" last="Oteiza">Alexandra Oteiza</name><affiliation wicri:level="3"><nlm:aff id="aff2"><addr-line>CNRS UMR 5235, DIMNP, University of Montpellier, Montpellier, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>CNRS UMR 5235, DIMNP, University of Montpellier, Montpellier</wicri:regionArea><placeName><region type="region">Occitanie (région administrative)</region><region type="old region">Languedoc-Roussillon</region><settlement type="city">Montpellier</settlement></placeName></affiliation></author><author><name sortKey="Ghitti, Michela" sort="Ghitti, Michela" uniqKey="Ghitti M" first="Michela" last="Ghitti">Michela Ghitti</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>San Raffaele Scientific Institute, Milan, Italy</addr-line></nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>San Raffaele Scientific Institute, Milan</wicri:regionArea><placeName><settlement type="city">Milan</settlement><region nuts="2">Lombardie</region></placeName></affiliation></author><author><name sortKey="Mechti, Nadir" sort="Mechti, Nadir" uniqKey="Mechti N" first="Nadir" last="Mechti">Nadir Mechti</name><affiliation wicri:level="3"><nlm:aff id="aff2"><addr-line>CNRS UMR 5235, DIMNP, University of Montpellier, Montpellier, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>CNRS UMR 5235, DIMNP, University of Montpellier, Montpellier</wicri:regionArea><placeName><region type="region">Occitanie (région administrative)</region><region type="old region">Languedoc-Roussillon</region><settlement type="city">Montpellier</settlement></placeName></affiliation></author><author><name sortKey="Naffakh, Nadia" sort="Naffakh, Nadia" uniqKey="Naffakh N" first="Nadia" last="Naffakh">Nadia Naffakh</name><affiliation wicri:level="3"><nlm:aff id="aff3"><addr-line>Institut Pasteur, Unité de Génétique Moléculaire des Virus à ARN, Département de Virologie, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Institut Pasteur, Unité de Génétique Moléculaire des Virus à ARN, Département de Virologie, Paris</wicri:regionArea><placeName><region type="region">Île-de-France</region><region type="old region">Île-de-France</region><settlement type="city">Paris</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:aff id="aff4"><addr-line>CNRS, UMR3569, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>CNRS, UMR3569, Paris</wicri:regionArea><placeName><region type="region">Île-de-France</region><region type="old region">Île-de-France</region><settlement type="city">Paris</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:aff id="aff5"><addr-line>Université Paris Diderot, Sorbonne Paris Cité, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Université Paris Diderot, Sorbonne Paris Cité, Paris</wicri:regionArea><placeName><region type="region">Île-de-France</region><region type="old region">Île-de-France</region><settlement type="city">Paris</settlement></placeName></affiliation></author><author><name sortKey="Vicenzi, Elisa" sort="Vicenzi, Elisa" uniqKey="Vicenzi E" first="Elisa" last="Vicenzi">Elisa Vicenzi</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>San Raffaele Scientific Institute, Milan, Italy</addr-line></nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>San Raffaele Scientific Institute, Milan</wicri:regionArea><placeName><settlement type="city">Milan</settlement><region nuts="2">Lombardie</region></placeName></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">29624498</idno><idno type="pmc">5885024</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5885024</idno><idno type="RBID">PMC:5885024</idno><idno type="doi">10.1128/mSphere.00110-18</idno><date when="2018">2018</date><idno type="wicri:Area/Pmc/Corpus">000C64</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000C64</idno><idno type="wicri:Area/Pmc/Curation">000C64</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">000C64</idno><idno type="wicri:Area/Pmc/Checkpoint">000126</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Checkpoint">000126</idno><idno type="wicri:Area/Ncbi/Merge">000E63</idno><idno type="wicri:Area/Ncbi/Curation">000E63</idno><idno type="wicri:Area/Ncbi/Checkpoint">000E63</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Mutations Conferring Increased Sensitivity to Tripartite Motif 22 Restriction Accumulated Progressively in the Nucleoprotein of Seasonal Influenza A (H1N1) Viruses between 1918 and 2009</title><author><name sortKey="Pagani, Isabel" sort="Pagani, Isabel" uniqKey="Pagani I" first="Isabel" last="Pagani">Isabel Pagani</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>San Raffaele Scientific Institute, Milan, Italy</addr-line></nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>San Raffaele Scientific Institute, Milan</wicri:regionArea><placeName><settlement type="city">Milan</settlement><region nuts="2">Lombardie</region></placeName></affiliation></author><author><name sortKey="Di Pietro, Andrea" sort="Di Pietro, Andrea" uniqKey="Di Pietro A" first="Andrea" last="Di Pietro">Andrea Di Pietro</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>San Raffaele Scientific Institute, Milan, Italy</addr-line></nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>San Raffaele Scientific Institute, Milan</wicri:regionArea><placeName><settlement type="city">Milan</settlement><region nuts="2">Lombardie</region></placeName></affiliation></author><author><name sortKey="Oteiza, Alexandra" sort="Oteiza, Alexandra" uniqKey="Oteiza A" first="Alexandra" last="Oteiza">Alexandra Oteiza</name><affiliation wicri:level="3"><nlm:aff id="aff2"><addr-line>CNRS UMR 5235, DIMNP, University of Montpellier, Montpellier, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>CNRS UMR 5235, DIMNP, University of Montpellier, Montpellier</wicri:regionArea><placeName><region type="region">Occitanie (région administrative)</region><region type="old region">Languedoc-Roussillon</region><settlement type="city">Montpellier</settlement></placeName></affiliation></author><author><name sortKey="Ghitti, Michela" sort="Ghitti, Michela" uniqKey="Ghitti M" first="Michela" last="Ghitti">Michela Ghitti</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>San Raffaele Scientific Institute, Milan, Italy</addr-line></nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>San Raffaele Scientific Institute, Milan</wicri:regionArea><placeName><settlement type="city">Milan</settlement><region nuts="2">Lombardie</region></placeName></affiliation></author><author><name sortKey="Mechti, Nadir" sort="Mechti, Nadir" uniqKey="Mechti N" first="Nadir" last="Mechti">Nadir Mechti</name><affiliation wicri:level="3"><nlm:aff id="aff2"><addr-line>CNRS UMR 5235, DIMNP, University of Montpellier, Montpellier, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>CNRS UMR 5235, DIMNP, University of Montpellier, Montpellier</wicri:regionArea><placeName><region type="region">Occitanie (région administrative)</region><region type="old region">Languedoc-Roussillon</region><settlement type="city">Montpellier</settlement></placeName></affiliation></author><author><name sortKey="Naffakh, Nadia" sort="Naffakh, Nadia" uniqKey="Naffakh N" first="Nadia" last="Naffakh">Nadia Naffakh</name><affiliation wicri:level="3"><nlm:aff id="aff3"><addr-line>Institut Pasteur, Unité de Génétique Moléculaire des Virus à ARN, Département de Virologie, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Institut Pasteur, Unité de Génétique Moléculaire des Virus à ARN, Département de Virologie, Paris</wicri:regionArea><placeName><region type="region">Île-de-France</region><region type="old region">Île-de-France</region><settlement type="city">Paris</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:aff id="aff4"><addr-line>CNRS, UMR3569, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>CNRS, UMR3569, Paris</wicri:regionArea><placeName><region type="region">Île-de-France</region><region type="old region">Île-de-France</region><settlement type="city">Paris</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:aff id="aff5"><addr-line>Université Paris Diderot, Sorbonne Paris Cité, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Université Paris Diderot, Sorbonne Paris Cité, Paris</wicri:regionArea><placeName><region type="region">Île-de-France</region><region type="old region">Île-de-France</region><settlement type="city">Paris</settlement></placeName></affiliation></author><author><name sortKey="Vicenzi, Elisa" sort="Vicenzi, Elisa" uniqKey="Vicenzi E" first="Elisa" last="Vicenzi">Elisa Vicenzi</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>San Raffaele Scientific Institute, Milan, Italy</addr-line></nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>San Raffaele Scientific Institute, Milan</wicri:regionArea><placeName><settlement type="city">Milan</settlement><region nuts="2">Lombardie</region></placeName></affiliation></author></analytic><series><title level="j">mSphere</title><idno type="eISSN">2379-5042</idno><imprint><date when="2018">2018</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>We have uncovered that long-term circulation of seasonal influenza A viruses (IAV) in the human population resulted in the progressive acquisition of increased sensitivity to a component of the innate immune response: the type I interferon-inducible TRIM22 protein, which acts as a restriction factor by inducing the polyubiquitination of the IAV nucleoprotein (NP). We show that four arginine residues present in the NP of the 1918 H1N1 pandemic strain and early postpandemic strains were progressively substituted for by lysines between 1918 and 2009, rendering NP more susceptible to TRIM22-mediated ubiquitination. Our observations suggest that during long-term evolution of IAVs in humans, variants endowed with increased susceptibility to TRIM22 restriction emerge, highlighting the complexity of selection pressures acting on the NP.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Taubenberger, Jk" uniqKey="Taubenberger J">JK Taubenberger</name></author><author><name sortKey="Kash, Jc" uniqKey="Kash J">JC Kash</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Capua, I" uniqKey="Capua I">I Capua</name></author><author><name sortKey="Kajaste Rudnitski, A" uniqKey="Kajaste Rudnitski A">A Kajaste-Rudnitski</name></author><author><name sortKey="Bertoli, E" uniqKey="Bertoli E">E Bertoli</name></author><author><name sortKey="Vicenzi, E" uniqKey="Vicenzi E">E Vicenzi</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Sangster, My" uniqKey="Sangster M">MY 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