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Comparative Profiling of Ubiquitin Proteasome System Interplay with Influenza A Virus PB2 Polymerase Protein Recapitulating Virus Evolution in Humans

Identifieur interne : 000042 ( Hal/Corpus ); précédent : 000041; suivant : 000043

Comparative Profiling of Ubiquitin Proteasome System Interplay with Influenza A Virus PB2 Polymerase Protein Recapitulating Virus Evolution in Humans

Auteurs : Elise Biquand ; Juline Poirson ; Marwah Karim ; Marion Declercq ; Nicolas Malausse ; Patricia Cassonnet ; Cyril Barbezange ; Marie-Laure Straub ; Louis Jones ; Sandie Munier ; Nadia Naffakh ; Sylvie Van Der Werf ; Yves Jacob ; Murielle Masson ; Caroline Demeret

Source :

RBID : Hal:pasteur-01971491

English descriptors

Abstract

The optimized exploitation of cell resources is one cornerstone of a successful infection. Differential mapping of host-pathogen protein-protein interactions (PPIs) on the basis of comparative interactomics of multiple strains is an effective strategy to highlight correlations between host proteome hijacking and biological or pathogenic traits. Here, we developed an interactomic pipeline to deliver high-confidence comparative maps of PPIs between a given pathogen and the human ubiquitin proteasome system (UPS). This subarray of the human proteome represents a range of essential cellular functions and promiscuous targets for many viruses. The screening pipeline was applied to the influenza A virus (IAV) PB2 polymer-ase proteins of five strains representing different levels of virulence in humans. An extensive PB2-UPS interplay has been detected that recapitulates the evolution of IAVs in humans. Functional validation with several IAV strains, including the seasonal H1N1 pdm09 and H3N2 viruses, confirmed the biological relevance of most identified UPS factors and revealed strain-independent and strain-specific effects of UPS factor invalidation on IAV infection. This strategy is applicable to proteins from any other virus or pathogen, providing a valuable resource with which to explore the UPS-pathogen interplay and its relationship with pathogenicity. IMPORTANCE Influenza A viruses (IAVs) are responsible for mild-to-severe seasonal respiratory illness of public health concern worldwide, and the risk of avian strain outbreaks in humans is a constant threat. Elucidating the requisites of IAV adaptation to humans is thus of prime importance. In this study, we explored how PB2 replication proteins of IAV strains with different levels of virulence in humans hijack a major protein modification pathway of the human host cell, the ubiquitin protea-some system (UPS). We found that the PB2 protein engages in an extended interplay with the UPS that evolved along with the virus's adaptation to humans. This suggests that UPS hijacking underlies the efficient infection of humans and can be used as an indicator for evaluation of the potential of avian IAVs to infect humans. Several UPS factors were found to be necessary for infection with circulating IAV strains, pointing to potential targets for therapeutic approaches.


Url:
DOI: 10.1128/mSphere.00330-17

Links to Exploration step

Hal:pasteur-01971491

Le document en format XML

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<idno type="DOI">10.1128/mSphere.00330-17</idno>
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<keywords scheme="mix" xml:lang="en">
<term>comparative interactomics</term>
<term>influenza viruses</term>
<term>ubiquitination</term>
<term>virus-host interactions</term>
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<front>
<div type="abstract" xml:lang="en">
<p>The optimized exploitation of cell resources is one cornerstone of a successful infection. Differential mapping of host-pathogen protein-protein interactions (PPIs) on the basis of comparative interactomics of multiple strains is an effective strategy to highlight correlations between host proteome hijacking and biological or pathogenic traits. Here, we developed an interactomic pipeline to deliver high-confidence comparative maps of PPIs between a given pathogen and the human ubiquitin proteasome system (UPS). This subarray of the human proteome represents a range of essential cellular functions and promiscuous targets for many viruses. The screening pipeline was applied to the influenza A virus (IAV) PB2 polymer-ase proteins of five strains representing different levels of virulence in humans. An extensive PB2-UPS interplay has been detected that recapitulates the evolution of IAVs in humans. Functional validation with several IAV strains, including the seasonal H1N1 pdm09 and H3N2 viruses, confirmed the biological relevance of most identified UPS factors and revealed strain-independent and strain-specific effects of UPS factor invalidation on IAV infection. This strategy is applicable to proteins from any other virus or pathogen, providing a valuable resource with which to explore the UPS-pathogen interplay and its relationship with pathogenicity. IMPORTANCE Influenza A viruses (IAVs) are responsible for mild-to-severe seasonal respiratory illness of public health concern worldwide, and the risk of avian strain outbreaks in humans is a constant threat. Elucidating the requisites of IAV adaptation to humans is thus of prime importance. In this study, we explored how PB2 replication proteins of IAV strains with different levels of virulence in humans hijack a major protein modification pathway of the human host cell, the ubiquitin protea-some system (UPS). We found that the PB2 protein engages in an extended interplay with the UPS that evolved along with the virus's adaptation to humans. This suggests that UPS hijacking underlies the efficient infection of humans and can be used as an indicator for evaluation of the potential of avian IAVs to infect humans. Several UPS factors were found to be necessary for infection with circulating IAV strains, pointing to potential targets for therapeutic approaches.</p>
</div>
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<hal api="V3">
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<title xml:lang="en">Comparative Profiling of Ubiquitin Proteasome System Interplay with Influenza A Virus PB2 Polymerase Protein Recapitulating Virus Evolution in Humans</title>
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<persName>
<forename type="first">Elise</forename>
<surname>Biquand</surname>
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<forename type="first">Juline</forename>
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<forename type="first">Marwah</forename>
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<forename type="first">Marion</forename>
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<forename type="first">Nicolas</forename>
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<forename type="first">Patricia</forename>
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<forename type="first">Cyril</forename>
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</author>
<author role="aut">
<persName>
<forename type="first">Marie-Laure</forename>
<surname>Straub</surname>
</persName>
<idno type="halauthorid">135738</idno>
<affiliation ref="#struct-207563"></affiliation>
</author>
<author role="aut">
<persName>
<forename type="first">Louis</forename>
<surname>Jones</surname>
</persName>
<idno type="halauthorid">1003776</idno>
<affiliation ref="#struct-417138"></affiliation>
</author>
<author role="aut">
<persName>
<forename type="first">Sandie</forename>
<surname>Munier</surname>
</persName>
<email type="md5">b440763ac4aca24e6b1221e25cf98265</email>
<email type="domain">pasteur.fr</email>
<idno type="halauthorid">295536</idno>
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</author>
<author role="aut">
<persName>
<forename type="first">Nadia</forename>
<surname>Naffakh</surname>
</persName>
<email type="md5">aa37e6eec8574e8aadab07bfd4ecce2e</email>
<email type="domain">pasteur.fr</email>
<idno type="idhal" notation="string">nadia-naffakh</idno>
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<idno type="halauthorid">467936</idno>
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</author>
<author role="aut">
<persName>
<forename type="first">Sylvie</forename>
<surname>Van Der Werf</surname>
</persName>
<idno type="halauthorid">202082</idno>
<affiliation ref="#struct-417138"></affiliation>
</author>
<author role="aut">
<persName>
<forename type="first">Yves</forename>
<surname>Jacob</surname>
</persName>
<idno type="halauthorid">203034</idno>
<affiliation ref="#struct-417138"></affiliation>
</author>
<author role="aut">
<persName>
<forename type="first">Murielle</forename>
<surname>Masson</surname>
</persName>
<idno type="halauthorid">184662</idno>
<affiliation ref="#struct-207563"></affiliation>
</author>
<author role="crp">
<persName>
<forename type="first">Caroline</forename>
<surname>Demeret</surname>
</persName>
<email type="md5">74d7c2dcb47382e0eb80a945f7afddd3</email>
<email type="domain">pasteur.fr</email>
<idno type="idhal" notation="string">caroline-demeret</idno>
<idno type="idhal" notation="numeric">172913</idno>
<idno type="halauthorid">640063</idno>
<idno type="ORCID">https://orcid.org/0000-0002-1103-6805</idno>
<affiliation ref="#struct-417138"></affiliation>
</author>
<editor role="depositor">
<persName>
<forename>caroline</forename>
<surname>demeret</surname>
</persName>
<email type="md5">74d7c2dcb47382e0eb80a945f7afddd3</email>
<email type="domain">pasteur.fr</email>
</editor>
<funder ref="#projeurop-89460"></funder>
<funder ref="#projeurop-140826"></funder>
<funder>This work was supported by the Institut Pasteur in the framework of PTR call 2015 (PTR no. 546), EU FP7 PREDEMICS (grant agreement 278433), and Labex IBEID. E.B. and M.D. were recipients of a MENRT Ph.D. fellowship, J.P. was a recipient of a Ph.D. fellowship from the Ligue Nationale Contre le Cancer and Alsace Contre le Cancer. M.K. received funding from the European Union Horizon 2020 research and innovation program under Marie Skłodowska-Curie grant agreement 665850.</funder>
</titleStmt>
<editionStmt>
<edition n="v1" type="current">
<date type="whenSubmitted">2019-01-07 10:21:10</date>
<date type="whenModified">2020-03-27 03:47:14</date>
<date type="whenReleased">2019-01-17 15:13:25</date>
<date type="whenProduced">2017-11-22</date>
<date type="whenEndEmbargoed">2019-01-17</date>
<ref type="file" target="https://hal-pasteur.archives-ouvertes.fr/pasteur-01971491/document">
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<date notBefore="2019-01-17"></date>
</ref>
<ref type="externalLink" target="https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5700371/pdf"></ref>
</edition>
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<name key="680851">
<persName>
<forename>caroline</forename>
<surname>demeret</surname>
</persName>
<email type="md5">74d7c2dcb47382e0eb80a945f7afddd3</email>
<email type="domain">pasteur.fr</email>
</name>
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<idno type="halId">pasteur-01971491</idno>
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<idno type="halBibtex">biquand:pasteur-01971491</idno>
<idno type="halRefHtml">MSphere, American Society for Microbiology., 2017, 2 (6), pp.e00330-17. ⟨10.1128/mSphere.00330-17⟩</idno>
<idno type="halRef">MSphere, American Society for Microbiology., 2017, 2 (6), pp.e00330-17. ⟨10.1128/mSphere.00330-17⟩</idno>
<availability status="restricted">
<licence target="http://creativecommons.org/licenses/by/">Attribution</licence>
</availability>
</publicationStmt>
<seriesStmt>
<idno type="stamp" n="PASTEUR">Institut Pasteur</idno>
<idno type="stamp" n="CNRS">CNRS - Centre national de la recherche scientifique</idno>
<idno type="stamp" n="UNIV-PARIS7" corresp="UNIV-PARIS">Université Denis Diderot - Paris VII</idno>
<idno type="stamp" n="UNIV-STRASBG">Université de Strasbourg</idno>
<idno type="stamp" n="OPENAIRE">OpenAIRE</idno>
<idno type="stamp" n="USPC">Université Sorbonne Paris Cité</idno>
<idno type="stamp" n="SITE-ALSACE">Archive ouverte du site Alsace</idno>
<idno type="stamp" n="UNIV-PARIS">Université de Paris</idno>
</seriesStmt>
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<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">Comparative Profiling of Ubiquitin Proteasome System Interplay with Influenza A Virus PB2 Polymerase Protein Recapitulating Virus Evolution in Humans</title>
<author role="aut">
<persName>
<forename type="first">Elise</forename>
<surname>Biquand</surname>
</persName>
<idno type="halauthorid">664162</idno>
<affiliation ref="#struct-417138"></affiliation>
</author>
<author role="aut">
<persName>
<forename type="first">Juline</forename>
<surname>Poirson</surname>
</persName>
<idno type="halauthorid">1458149</idno>
<affiliation ref="#struct-207563"></affiliation>
</author>
<author role="aut">
<persName>
<forename type="first">Marwah</forename>
<surname>Karim</surname>
</persName>
<idno type="halauthorid">11366259</idno>
<affiliation ref="#struct-417138"></affiliation>
</author>
<author role="aut">
<persName>
<forename type="first">Marion</forename>
<surname>Declercq</surname>
</persName>
<idno type="halauthorid">11366260</idno>
<affiliation ref="#struct-417138"></affiliation>
</author>
<author role="aut">
<persName>
<forename type="first">Nicolas</forename>
<surname>Malausse</surname>
</persName>
<idno type="halauthorid">11366261</idno>
<affiliation ref="#struct-417138"></affiliation>
</author>
<author role="aut">
<persName>
<forename type="first">Patricia</forename>
<surname>Cassonnet</surname>
</persName>
<idno type="halauthorid">212109</idno>
<affiliation ref="#struct-417138"></affiliation>
</author>
<author role="aut">
<persName>
<forename type="first">Cyril</forename>
<surname>Barbezange</surname>
</persName>
<idno type="halauthorid">400597</idno>
<affiliation ref="#struct-417138"></affiliation>
</author>
<author role="aut">
<persName>
<forename type="first">Marie-Laure</forename>
<surname>Straub</surname>
</persName>
<idno type="halauthorid">135738</idno>
<affiliation ref="#struct-207563"></affiliation>
</author>
<author role="aut">
<persName>
<forename type="first">Louis</forename>
<surname>Jones</surname>
</persName>
<idno type="halauthorid">1003776</idno>
<affiliation ref="#struct-417138"></affiliation>
</author>
<author role="aut">
<persName>
<forename type="first">Sandie</forename>
<surname>Munier</surname>
</persName>
<email type="md5">b440763ac4aca24e6b1221e25cf98265</email>
<email type="domain">pasteur.fr</email>
<idno type="halauthorid">295536</idno>
<affiliation ref="#struct-417138"></affiliation>
</author>
<author role="aut">
<persName>
<forename type="first">Nadia</forename>
<surname>Naffakh</surname>
</persName>
<email type="md5">aa37e6eec8574e8aadab07bfd4ecce2e</email>
<email type="domain">pasteur.fr</email>
<idno type="idhal" notation="string">nadia-naffakh</idno>
<idno type="idhal" notation="numeric">179330</idno>
<idno type="halauthorid">467936</idno>
<idno type="ORCID">https://orcid.org/0000-0002-0424-0277</idno>
<affiliation ref="#struct-417138"></affiliation>
</author>
<author role="aut">
<persName>
<forename type="first">Sylvie</forename>
<surname>Van Der Werf</surname>
</persName>
<idno type="halauthorid">202082</idno>
<affiliation ref="#struct-417138"></affiliation>
</author>
<author role="aut">
<persName>
<forename type="first">Yves</forename>
<surname>Jacob</surname>
</persName>
<idno type="halauthorid">203034</idno>
<affiliation ref="#struct-417138"></affiliation>
</author>
<author role="aut">
<persName>
<forename type="first">Murielle</forename>
<surname>Masson</surname>
</persName>
<idno type="halauthorid">184662</idno>
<affiliation ref="#struct-207563"></affiliation>
</author>
<author role="crp">
<persName>
<forename type="first">Caroline</forename>
<surname>Demeret</surname>
</persName>
<email type="md5">74d7c2dcb47382e0eb80a945f7afddd3</email>
<email type="domain">pasteur.fr</email>
<idno type="idhal" notation="string">caroline-demeret</idno>
<idno type="idhal" notation="numeric">172913</idno>
<idno type="halauthorid">640063</idno>
<idno type="ORCID">https://orcid.org/0000-0002-1103-6805</idno>
<affiliation ref="#struct-417138"></affiliation>
</author>
</analytic>
<monogr>
<idno type="halJournalId" status="VALID">110107</idno>
<idno type="eissn">2379-5042</idno>
<title level="j">MSphere</title>
<imprint>
<publisher>American Society for Microbiology.</publisher>
<biblScope unit="volume">2</biblScope>
<biblScope unit="issue">6</biblScope>
<biblScope unit="pp">e00330-17</biblScope>
<date type="datePub">2017-11-22</date>
</imprint>
</monogr>
<idno type="doi">10.1128/mSphere.00330-17</idno>
<idno type="pubmed">29202037</idno>
<idno type="pubmedcentral">PMC5700371</idno>
</biblStruct>
</sourceDesc>
<profileDesc>
<langUsage>
<language ident="en">English</language>
</langUsage>
<textClass>
<keywords scheme="author">
<term xml:lang="en">influenza viruses</term>
<term xml:lang="en">ubiquitination</term>
<term xml:lang="en">virus-host interactions</term>
<term xml:lang="en">comparative interactomics</term>
</keywords>
<classCode scheme="halDomain" n="sdv.mp.vir">Life Sciences [q-bio]/Microbiology and Parasitology/Virology</classCode>
<classCode scheme="halTypology" n="ART">Journal articles</classCode>
</textClass>
<abstract xml:lang="en">
<p>The optimized exploitation of cell resources is one cornerstone of a successful infection. Differential mapping of host-pathogen protein-protein interactions (PPIs) on the basis of comparative interactomics of multiple strains is an effective strategy to highlight correlations between host proteome hijacking and biological or pathogenic traits. Here, we developed an interactomic pipeline to deliver high-confidence comparative maps of PPIs between a given pathogen and the human ubiquitin proteasome system (UPS). This subarray of the human proteome represents a range of essential cellular functions and promiscuous targets for many viruses. The screening pipeline was applied to the influenza A virus (IAV) PB2 polymer-ase proteins of five strains representing different levels of virulence in humans. An extensive PB2-UPS interplay has been detected that recapitulates the evolution of IAVs in humans. Functional validation with several IAV strains, including the seasonal H1N1 pdm09 and H3N2 viruses, confirmed the biological relevance of most identified UPS factors and revealed strain-independent and strain-specific effects of UPS factor invalidation on IAV infection. This strategy is applicable to proteins from any other virus or pathogen, providing a valuable resource with which to explore the UPS-pathogen interplay and its relationship with pathogenicity. IMPORTANCE Influenza A viruses (IAVs) are responsible for mild-to-severe seasonal respiratory illness of public health concern worldwide, and the risk of avian strain outbreaks in humans is a constant threat. Elucidating the requisites of IAV adaptation to humans is thus of prime importance. In this study, we explored how PB2 replication proteins of IAV strains with different levels of virulence in humans hijack a major protein modification pathway of the human host cell, the ubiquitin protea-some system (UPS). We found that the PB2 protein engages in an extended interplay with the UPS that evolved along with the virus's adaptation to humans. This suggests that UPS hijacking underlies the efficient infection of humans and can be used as an indicator for evaluation of the potential of avian IAVs to infect humans. Several UPS factors were found to be necessary for infection with circulating IAV strains, pointing to potential targets for therapeutic approaches.</p>
</abstract>
</profileDesc>
</hal>
</record>

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