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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 : 000207 ( France/Analysis ); précédent : 000206; suivant : 000208

Mutations 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 :

RBID : Hal:hal-02351139

English descriptors

Abstract

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.


Url:
DOI: 10.1128/mSphere.00110-18


Affiliations:


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Hal:hal-02351139

Le document en format XML

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<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>
<affiliations>
<list>
<country>
<li>France</li>
<li>Italie</li>
</country>
</list>
<tree>
<country name="Italie">
<noRegion>
<name sortKey="Pagani, Isabel" sort="Pagani, Isabel" uniqKey="Pagani I" first="Isabel" last="Pagani">Isabel Pagani</name>
</noRegion>
<name sortKey="Di Pietro, Andrea" sort="Di Pietro, Andrea" uniqKey="Di Pietro A" first="Andrea" last="Di Pietro">Andrea Di Pietro</name>
<name sortKey="Ghitti, Michela" sort="Ghitti, Michela" uniqKey="Ghitti M" first="Michela" last="Ghitti">Michela Ghitti</name>
<name sortKey="Vicenzi, Elisa" sort="Vicenzi, Elisa" uniqKey="Vicenzi E" first="Elisa" last="Vicenzi">Elisa Vicenzi</name>
</country>
<country name="France">
<noRegion>
<name sortKey="Oteiza, Alexandra" sort="Oteiza, Alexandra" uniqKey="Oteiza A" first="Alexandra" last="Oteiza">Alexandra Oteiza</name>
</noRegion>
<name sortKey="Mechti, Nadir" sort="Mechti, Nadir" uniqKey="Mechti N" first="Nadir" last="Mechti">Nadir Mechti</name>
<name sortKey="Naffakh, Nadia" sort="Naffakh, Nadia" uniqKey="Naffakh N" first="Nadia" last="Naffakh">Nadia Naffakh</name>
</country>
</tree>
</affiliations>
</record>

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