The C-terminal domain of the MERS coronavirus M protein contains a trans-Golgi network localization signal.
Identifieur interne : 000456 ( PubMed/Corpus ); précédent : 000455; suivant : 000457The C-terminal domain of the MERS coronavirus M protein contains a trans-Golgi network localization signal.
Auteurs : Anabelle Perrier ; Ariane Bonnin ; Lowiese Desmarets ; Adeline Danneels ; Anne Goffard ; Yves Rouillé ; Jean Dubuisson ; Sandrine BelouzardSource :
- The Journal of biological chemistry [ 1083-351X ] ; 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 trans-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, 199KxGxYR204, 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 199KxGxYR204 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/cis-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.
DOI: 10.1074/jbc.RA119.008964
PubMed: 31399512
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France.</nlm:affiliation></affiliation></author><author><name sortKey="Rouille, Yves" sort="Rouille, Yves" uniqKey="Rouille Y" first="Yves" last="Rouillé">Yves Rouillé</name><affiliation><nlm:affiliation>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:affiliation></affiliation></author><author><name sortKey="Dubuisson, Jean" sort="Dubuisson, Jean" uniqKey="Dubuisson J" first="Jean" last="Dubuisson">Jean Dubuisson</name><affiliation><nlm:affiliation>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:affiliation></affiliation></author><author><name sortKey="Belouzard, Sandrine" sort="Belouzard, Sandrine" uniqKey="Belouzard S" first="Sandrine" last="Belouzard">Sandrine Belouzard</name><affiliation><nlm:affiliation>Université Lille, CNRS, INSERM, CHU Lille, Institut 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8204-CIIL-Center for Infection and Immunity of Lille, F-59000 Lille, France.</nlm:affiliation></affiliation></author><author><name sortKey="Bonnin, Ariane" sort="Bonnin, Ariane" uniqKey="Bonnin A" first="Ariane" last="Bonnin">Ariane Bonnin</name><affiliation><nlm:affiliation>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:affiliation></affiliation></author><author><name sortKey="Desmarets, Lowiese" sort="Desmarets, Lowiese" uniqKey="Desmarets L" first="Lowiese" last="Desmarets">Lowiese Desmarets</name><affiliation><nlm:affiliation>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:affiliation></affiliation></author><author><name sortKey="Danneels, Adeline" sort="Danneels, Adeline" uniqKey="Danneels A" first="Adeline" last="Danneels">Adeline Danneels</name><affiliation><nlm:affiliation>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:affiliation></affiliation></author><author><name sortKey="Goffard, Anne" sort="Goffard, Anne" uniqKey="Goffard A" first="Anne" last="Goffard">Anne Goffard</name><affiliation><nlm:affiliation>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:affiliation></affiliation></author><author><name sortKey="Rouille, Yves" sort="Rouille, Yves" uniqKey="Rouille Y" first="Yves" last="Rouillé">Yves Rouillé</name><affiliation><nlm:affiliation>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:affiliation></affiliation></author><author><name sortKey="Dubuisson, Jean" sort="Dubuisson, Jean" uniqKey="Dubuisson J" first="Jean" last="Dubuisson">Jean Dubuisson</name><affiliation><nlm:affiliation>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:affiliation></affiliation></author><author><name sortKey="Belouzard, Sandrine" sort="Belouzard, Sandrine" uniqKey="Belouzard S" first="Sandrine" last="Belouzard">Sandrine Belouzard</name><affiliation><nlm:affiliation>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 sandrine.belouzard@ibl.cnrs.fr.</nlm:affiliation></affiliation></author></analytic><series><title level="j">The Journal of biological chemistry</title><idno type="eISSN">1083-351X</idno><imprint><date when="2019" type="published">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">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 <i>trans</i>-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/<i>cis</i>-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.</div></front></TEI><pubmed><MedlineCitation Status="In-Data-Review" Owner="NLM"><PMID Version="1">31399512</PMID><DateRevised><Year>2020</Year><Month>03</Month><Day>26</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1083-351X</ISSN><JournalIssue CitedMedium="Internet"><Volume>294</Volume><Issue>39</Issue><PubDate><Year>2019</Year><Month>Sep</Month><Day>27</Day></PubDate></JournalIssue><Title>The Journal of biological chemistry</Title><ISOAbbreviation>J. Biol. Chem.</ISOAbbreviation></Journal><ArticleTitle>The C-terminal domain of the MERS coronavirus M protein contains a <i>trans</i>-Golgi network localization signal.</ArticleTitle><Pagination><MedlinePgn>14406-14421</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1074/jbc.RA119.008964</ELocationID><Abstract><AbstractText>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 <i>trans</i>-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/<i>cis</i>-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.</AbstractText><CopyrightInformation>© 2019 Perrier et al.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Perrier</LastName><ForeName>Anabelle</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>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.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Bonnin</LastName><ForeName>Ariane</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>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.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Desmarets</LastName><ForeName>Lowiese</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>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.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Danneels</LastName><ForeName>Adeline</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>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.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Goffard</LastName><ForeName>Anne</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>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.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Rouillé</LastName><ForeName>Yves</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>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.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Dubuisson</LastName><ForeName>Jean</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>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.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Belouzard</LastName><ForeName>Sandrine</ForeName><Initials>S</Initials><Identifier Source="ORCID">https://orcid.org/0000-0002-9972-4054</Identifier><AffiliationInfo><Affiliation>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 sandrine.belouzard@ibl.cnrs.fr.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2019</Year><Month>08</Month><Day>09</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>J Biol Chem</MedlineTA><NlmUniqueID>2985121R</NlmUniqueID><ISSNLinking>0021-9258</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">MERS-CoV</Keyword><Keyword MajorTopicYN="N">Middle East respiratory syndrome</Keyword><Keyword MajorTopicYN="N">coronavirus</Keyword><Keyword MajorTopicYN="N">endoplasmic reticulum (ER)</Keyword><Keyword MajorTopicYN="N">intracellular trafficking</Keyword><Keyword MajorTopicYN="N">plasma membrane</Keyword><Keyword MajorTopicYN="N">protein motif</Keyword><Keyword MajorTopicYN="N">protein sorting</Keyword><Keyword MajorTopicYN="N">trans-Golgi network localization</Keyword><Keyword MajorTopicYN="N">viral protein</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2019</Year><Month>04</Month><Day>18</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2019</Year><Month>08</Month><Day>06</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2019</Year><Month>8</Month><Day>11</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2019</Year><Month>8</Month><Day>11</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2019</Year><Month>8</Month><Day>11</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">31399512</ArticleId><ArticleId IdType="pii">RA119.008964</ArticleId><ArticleId 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