The C-terminal domain of the MERS coronavirus M protein contains a trans-Golgi network localization signal
Identifieur interne : 000D84 ( Pmc/Curation ); précédent : 000D83; suivant : 000D85The C-terminal domain of the MERS coronavirus M protein contains a trans-Golgi network localization signal
Auteurs : Anabelle Perrier [France] ; Ariane Bonnin [France] ; Lowiese Desmarets [France] ; Adeline Danneels [France] ; Anne Goffard [France] ; Yves Rouillé [France] ; Jean Dubuisson [France] ; Sandrine Belouzard [France]Source :
- The Journal of Biological Chemistry [ 0021-9258 ] ; 2019.
Abstract
Coronavirus M proteins represent the major protein component of the viral
envelope. They play an essential role during viral assembly by interacting with
all of the other structural proteins. Coronaviruses bud into the endoplasmic
reticulum (ER)–Golgi intermediate compartment (ERGIC), but the mechanisms
by which M proteins are transported from their site of synthesis, the ER, to the
budding site remain poorly understood. Here, we investigated the intracellular
trafficking of the Middle East respiratory syndrome coronavirus (MERS-CoV) M
protein. Subcellular localization analyses revealed that the MERS-CoV M protein
is retained intracellularly in the
Url:
DOI: 10.1074/jbc.RA119.008964
PubMed: 31399512
PubMed Central: 6768645
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-Golgi network localization signal</title>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">The C-terminal domain of the MERS coronavirus M protein contains a
<italic>trans</italic>
-Golgi network localization signal</title>
<author><name sortKey="Perrier, Anabelle" sort="Perrier, Anabelle" uniqKey="Perrier A" first="Anabelle" last="Perrier">Anabelle Perrier</name>
<affiliation wicri:level="1"><nlm:aff id="aff1">Université Lille, CNRS, INSERM, CHU Lille, Institut Pasteur de Lille, U1019-UMR 8204-CIIL-Center for Infection and Immunity of Lille, F-59000 Lille, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Université Lille, CNRS, INSERM, CHU Lille, Institut Pasteur de Lille, U1019-UMR 8204-CIIL-Center for Infection and Immunity of Lille, F-59000 Lille</wicri:regionArea>
</affiliation>
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<author><name sortKey="Bonnin, Ariane" sort="Bonnin, Ariane" uniqKey="Bonnin A" first="Ariane" last="Bonnin">Ariane Bonnin</name>
<affiliation wicri:level="1"><nlm:aff id="aff1">Université Lille, CNRS, INSERM, CHU Lille, Institut Pasteur de Lille, U1019-UMR 8204-CIIL-Center for Infection and Immunity of Lille, F-59000 Lille, France</nlm:aff>
<country xml:lang="fr">France</country>
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</affiliation>
</author>
<author><name sortKey="Desmarets, Lowiese" sort="Desmarets, Lowiese" uniqKey="Desmarets L" first="Lowiese" last="Desmarets">Lowiese Desmarets</name>
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</affiliation>
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<author><name sortKey="Danneels, Adeline" sort="Danneels, Adeline" uniqKey="Danneels A" first="Adeline" last="Danneels">Adeline Danneels</name>
<affiliation wicri:level="1"><nlm:aff id="aff1">Université Lille, CNRS, INSERM, CHU Lille, Institut Pasteur de Lille, U1019-UMR 8204-CIIL-Center for Infection and Immunity of Lille, F-59000 Lille, France</nlm:aff>
<country xml:lang="fr">France</country>
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</affiliation>
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<author><name sortKey="Goffard, Anne" sort="Goffard, Anne" uniqKey="Goffard A" first="Anne" last="Goffard">Anne Goffard</name>
<affiliation wicri:level="1"><nlm:aff id="aff1">Université Lille, CNRS, INSERM, CHU Lille, Institut Pasteur de Lille, U1019-UMR 8204-CIIL-Center for Infection and Immunity of Lille, F-59000 Lille, France</nlm:aff>
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</affiliation>
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<author><name sortKey="Rouille, Yves" sort="Rouille, Yves" uniqKey="Rouille Y" first="Yves" last="Rouillé">Yves Rouillé</name>
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<country xml:lang="fr">France</country>
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</affiliation>
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<author><name sortKey="Dubuisson, Jean" sort="Dubuisson, Jean" uniqKey="Dubuisson J" first="Jean" last="Dubuisson">Jean Dubuisson</name>
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</affiliation>
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<author><name sortKey="Belouzard, Sandrine" sort="Belouzard, Sandrine" uniqKey="Belouzard S" first="Sandrine" last="Belouzard">Sandrine Belouzard</name>
<affiliation wicri:level="1"><nlm:aff id="aff1">Université Lille, CNRS, INSERM, CHU Lille, Institut Pasteur de Lille, U1019-UMR 8204-CIIL-Center for Infection and Immunity of Lille, F-59000 Lille, France</nlm:aff>
<country xml:lang="fr">France</country>
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</affiliation>
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</analytic>
<series><title level="j">The Journal of Biological Chemistry</title>
<idno type="ISSN">0021-9258</idno>
<idno type="eISSN">1083-351X</idno>
<imprint><date when="2019">2019</date>
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<front><div type="abstract" xml:lang="en"><p>Coronavirus M proteins represent the major protein component of the viral
envelope. They play an essential role during viral assembly by interacting with
all of the other structural proteins. Coronaviruses bud into the endoplasmic
reticulum (ER)–Golgi intermediate compartment (ERGIC), but the mechanisms
by which M proteins are transported from their site of synthesis, the ER, to the
budding site remain poorly understood. Here, we investigated the intracellular
trafficking of the Middle East respiratory syndrome coronavirus (MERS-CoV) M
protein. Subcellular localization analyses revealed that the MERS-CoV M protein
is retained intracellularly in the <italic>trans</italic>
-Golgi network (TGN),
and we identified two motifs in the distal part of the C-terminal domain as
being important for this specific localization. We identified the first motif as
a functional diacidic DxE ER export signal, because substituting Asp-211 and
Glu-213 with alanine induced retention of the MERS-CoV M in the ER. The second
motif, <sup>199</sup>
KxGxYR<sup>204</sup>
, was responsible for retaining the M
protein in the TGN. Substitution of this motif resulted in MERS-CoV M leakage
toward the plasma membrane. We further confirmed the role of
<sup>199</sup>
KxGxYR<sup>204</sup>
as a TGN retention signal by using
chimeras between MERS-CoV M and the M protein of infectious bronchitis virus
(IBV). Our results indicated that the C-terminal domains of both proteins
determine their specific localization, namely TGN and
ERGIC/<italic>cis</italic>
-Golgi for MERS-M and IBV-M, respectively. Our
findings indicate that MERS-CoV M protein localizes to the TGN because of the
combined presence of an ER export signal and a TGN retention motif.</p>
</div>
</front>
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</TEI>
<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">J Biol Chem</journal-id>
<journal-id journal-id-type="iso-abbrev">J. Biol. Chem</journal-id>
<journal-id journal-id-type="hwp">jbc</journal-id>
<journal-id journal-id-type="pmc">jbc</journal-id>
<journal-id journal-id-type="publisher-id">JBC</journal-id>
<journal-title-group><journal-title>The Journal of Biological Chemistry</journal-title>
</journal-title-group>
<issn pub-type="ppub">0021-9258</issn>
<issn pub-type="epub">1083-351X</issn>
<publisher><publisher-name>American Society for Biochemistry and Molecular
Biology</publisher-name>
<publisher-loc>11200 Rockville Pike, Suite 302, Rockville, MD 20852-3110,
U.S.A.</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">31399512</article-id>
<article-id pub-id-type="pmc">6768645</article-id>
<article-id pub-id-type="publisher-id">RA119.008964</article-id>
<article-id pub-id-type="doi">10.1074/jbc.RA119.008964</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Cell Biology</subject>
</subj-group>
</article-categories>
<title-group><article-title>The C-terminal domain of the MERS coronavirus M protein contains a
<italic>trans</italic>
-Golgi network localization signal</article-title>
<alt-title alt-title-type="short">MERS-CoV M protein TGN localization</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Perrier</surname>
<given-names>Anabelle</given-names>
</name>
<xref ref-type="aff" rid="aff1"></xref>
<xref ref-type="author-notes" rid="FN1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Bonnin</surname>
<given-names>Ariane</given-names>
</name>
<xref ref-type="aff" rid="aff1"></xref>
</contrib>
<contrib contrib-type="author"><name><surname>Desmarets</surname>
<given-names>Lowiese</given-names>
</name>
<xref ref-type="aff" rid="aff1"></xref>
<xref ref-type="author-notes" rid="FN2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Danneels</surname>
<given-names>Adeline</given-names>
</name>
<xref ref-type="aff" rid="aff1"></xref>
</contrib>
<contrib contrib-type="author"><name><surname>Goffard</surname>
<given-names>Anne</given-names>
</name>
<xref ref-type="aff" rid="aff1"></xref>
</contrib>
<contrib contrib-type="author"><name><surname>Rouillé</surname>
<given-names>Yves</given-names>
</name>
<xref ref-type="aff" rid="aff1"></xref>
</contrib>
<contrib contrib-type="author"><name><surname>Dubuisson</surname>
<given-names>Jean</given-names>
</name>
<xref ref-type="aff" rid="aff1"></xref>
</contrib>
<contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0002-9972-4054</contrib-id>
<name><surname>Belouzard</surname>
<given-names>Sandrine</given-names>
</name>
<xref ref-type="aff" rid="aff1"></xref>
<xref ref-type="corresp" rid="cor1"><sup>3</sup>
</xref>
</contrib>
<aff id="aff1">Université Lille, CNRS, INSERM, CHU Lille, Institut Pasteur de Lille, U1019-UMR 8204-CIIL-Center for Infection and Immunity of Lille, F-59000 Lille, France</aff>
</contrib-group>
<author-notes><corresp id="cor1"><label>3</label>
To whom correspondence should be addressed.
E-mail: <email>sandrine.belouzard@ibl.cnrs.fr</email>
.</corresp>
<fn fn-type="supported-by" id="FN1"><label>1</label>
<p>Supported by a fellowship from the University of Lille and the Region
Hauts-de-France.</p>
</fn>
<fn fn-type="supported-by" id="FN2"><label>2</label>
<p>Supported by a fellowship from the Region Hauts-de-France.</p>
</fn>
<fn fn-type="edited-by"><p>Edited by Phyllis I. Hanson</p>
</fn>
</author-notes>
<pub-date pub-type="ppub"><day>27</day>
<month>9</month>
<year>2019</year>
</pub-date>
<pub-date pub-type="epub"><day>9</day>
<month>8</month>
<year>2019</year>
</pub-date>
<pub-date pub-type="pmc-release"><day>9</day>
<month>8</month>
<year>2019</year>
</pub-date>
<pmc-comment> PMC Release delay is 0 months and 0 days and was based on the . </pmc-comment>
<volume>294</volume>
<issue>39</issue>
<fpage>14406</fpage>
<lpage>14421</lpage>
<history><date date-type="received"><day>18</day>
<month>4</month>
<year>2019</year>
</date>
<date date-type="rev-recd"><day>6</day>
<month>8</month>
<year>2019</year>
</date>
</history>
<permissions><copyright-statement>© 2019 Perrier et al.</copyright-statement>
<copyright-year>2019</copyright-year>
<copyright-holder>Perrier et al.</copyright-holder>
<license><license-p>Published under exclusive license by The American Society for
Biochemistry and Molecular Biology, Inc.</license-p>
<license-p>This article is made available via the PMC Open Access Subset for
unrestricted re-use and analyses in any form or by any means with
acknowledgement of the original source. These permissions are granted for
the duration of the COVID-19 pandemic or until permissions are revoked in
writing. Upon expiration of these permissions, PMC is granted a perpetual
license to make this article available via PMC and Europe PMC, consistent
with existing copyright protections.</license-p>
</license>
</permissions>
<self-uri content-type="pdf" xlink:href="zbc03919014406.pdf"></self-uri>
<abstract><p>Coronavirus M proteins represent the major protein component of the viral
envelope. They play an essential role during viral assembly by interacting with
all of the other structural proteins. Coronaviruses bud into the endoplasmic
reticulum (ER)–Golgi intermediate compartment (ERGIC), but the mechanisms
by which M proteins are transported from their site of synthesis, the ER, to the
budding site remain poorly understood. Here, we investigated the intracellular
trafficking of the Middle East respiratory syndrome coronavirus (MERS-CoV) M
protein. Subcellular localization analyses revealed that the MERS-CoV M protein
is retained intracellularly in the <italic>trans</italic>
-Golgi network (TGN),
and we identified two motifs in the distal part of the C-terminal domain as
being important for this specific localization. We identified the first motif as
a functional diacidic DxE ER export signal, because substituting Asp-211 and
Glu-213 with alanine induced retention of the MERS-CoV M in the ER. The second
motif, <sup>199</sup>
KxGxYR<sup>204</sup>
, was responsible for retaining the M
protein in the TGN. Substitution of this motif resulted in MERS-CoV M leakage
toward the plasma membrane. We further confirmed the role of
<sup>199</sup>
KxGxYR<sup>204</sup>
as a TGN retention signal by using
chimeras between MERS-CoV M and the M protein of infectious bronchitis virus
(IBV). Our results indicated that the C-terminal domains of both proteins
determine their specific localization, namely TGN and
ERGIC/<italic>cis</italic>
-Golgi for MERS-M and IBV-M, respectively. Our
findings indicate that MERS-CoV M protein localizes to the TGN because of the
combined presence of an ER export signal and a TGN retention motif.</p>
</abstract>
<kwd-group><kwd>viral protein</kwd>
<kwd>protein motif</kwd>
<kwd>protein sorting</kwd>
<kwd>intracellular trafficking</kwd>
<kwd>endoplasmic reticulum (ER)</kwd>
<kwd>coronavirus</kwd>
<kwd>MERS-CoV</kwd>
<kwd>Middle East respiratory syndrome</kwd>
<kwd>trans-Golgi network localization</kwd>
<kwd>plasma membrane</kwd>
</kwd-group>
<funding-group><award-group id="award1"><funding-source>Région Hauts de France</funding-source>
<award-id>Visionn-AIRR</award-id>
<principal-award-recipient><name><surname>Perrier</surname>
<given-names>Anabelle</given-names>
</name>
</principal-award-recipient>
<principal-award-recipient><name><surname>Belouzard</surname>
<given-names>Sandrine</given-names>
</name>
</principal-award-recipient>
</award-group>
<award-group id="award2"><funding-source>Région Hauts-de-France/ Lille university</funding-source>
<award-id>Graduate Student Fellowship</award-id>
<principal-award-recipient><name><surname>Perrier</surname>
<given-names>Anabelle</given-names>
</name>
</principal-award-recipient>
<principal-award-recipient><name><surname>Belouzard</surname>
<given-names>Sandrine</given-names>
</name>
</principal-award-recipient>
</award-group>
<award-group id="award3"><funding-source><institution-wrap><institution>Région Hauts-de-France </institution>
<institution-id institution-id-type="open-funder-registry">10.13039/501100010095</institution-id>
</institution-wrap>
</funding-source>
<award-id>Postdoctoral Fellowship</award-id>
<principal-award-recipient><name><surname>Desmarets</surname>
<given-names>Lowiese</given-names>
</name>
</principal-award-recipient>
</award-group>
</funding-group>
</article-meta>
</front>
</pmc>
</record>
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