The Salmonella Effector SteD Mediates MARCH8-Dependent Ubiquitination of MHC II Molecules and Inhibits T Cell Activation.
Identifieur interne : 001648 ( PubMed/Corpus ); précédent : 001647; suivant : 001649The Salmonella Effector SteD Mediates MARCH8-Dependent Ubiquitination of MHC II Molecules and Inhibits T Cell Activation.
Auteurs : Ethel Bayer-Santos ; Charlotte H. Durkin ; Luciano A. Rigano ; Andreas Kupz ; Eric Alix ; Ondrej Cerny ; Elliott Jennings ; Mei Liu ; Aindrias S. Ryan ; Nicolas Lapaque ; Stefan H E. Kaufmann ; David W. HoldenSource :
- Cell host & microbe [ 1934-6069 ] ; 2016.
English descriptors
- KwdEn :
- Animals, Bacterial Proteins (metabolism), Cell Line, Dendritic Cells (immunology), Dendritic Cells (microbiology), Histocompatibility Antigens Class II (metabolism), Host-Pathogen Interactions, Humans, Immune Evasion, Lymphocyte Activation, Mice, Protein Binding, Salmonella Infections, Animal (immunology), Salmonella Infections, Animal (microbiology), Salmonella typhimurium (pathogenicity), T-Lymphocytes (immunology), Ubiquitin-Protein Ligases (metabolism), Ubiquitination.
- MESH :
- chemical , metabolism : Bacterial Proteins, Histocompatibility Antigens Class II, Ubiquitin-Protein Ligases.
- immunology : Dendritic Cells, Salmonella Infections, Animal, T-Lymphocytes.
- microbiology : Dendritic Cells, Salmonella Infections, Animal.
- pathogenicity : Salmonella typhimurium.
- Animals, Cell Line, Host-Pathogen Interactions, Humans, Immune Evasion, Lymphocyte Activation, Mice, Protein Binding, Ubiquitination.
Abstract
The SPI-2 type III secretion system (T3SS) of intracellular Salmonella enterica translocates effector proteins into mammalian cells. Infection of antigen-presenting cells results in SPI-2 T3SS-dependent ubiquitination and reduction of surface-localized mature MHC class II (mMHCII). We identify the effector SteD as required and sufficient for this process. In Mel Juso cells, SteD localized to the Golgi network and vesicles containing the E3 ubiquitin ligase MARCH8 and mMHCII. SteD caused MARCH8-dependent ubiquitination and depletion of surface mMHCII. One of two transmembrane domains and the C-terminal cytoplasmic region of SteD mediated binding to MARCH8 and mMHCII, respectively. Infection of dendritic cells resulted in SteD-dependent depletion of surface MHCII, the co-stimulatory molecule B7.2, and suppression of T cell activation. SteD also accounted for suppression of T cell activation during Salmonella infection of mice. We propose that SteD is an adaptor, forcing inappropriate ubiquitination of mMHCII by MARCH8 and thereby suppressing T cell activation.
DOI: 10.1016/j.chom.2016.10.007
PubMed: 27832589
Links to Exploration step
pubmed:27832589Le document en format XML
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Rigano</name><affiliation><nlm:affiliation>MRC Centre for Molecular Bacteriology and Infection, Imperial College London, Armstrong Road, London SW7 2AZ, UK.</nlm:affiliation></affiliation></author><author><name sortKey="Kupz, Andreas" sort="Kupz, Andreas" uniqKey="Kupz A" first="Andreas" last="Kupz">Andreas Kupz</name><affiliation><nlm:affiliation>Department of Immunology, Max Planck Institute for Infection Biology, 10117 Berlin, Germany; Centre for Biosecurity and Tropical Infectious Diseases, Australian Institute of Tropical Health and Medicine, James Cook University, McGregor Road, Cairns, QLD 4878, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Alix, Eric" sort="Alix, Eric" uniqKey="Alix E" first="Eric" last="Alix">Eric Alix</name><affiliation><nlm:affiliation>MRC Centre for Molecular Bacteriology and Infection, Imperial College London, Armstrong Road, London SW7 2AZ, UK.</nlm:affiliation></affiliation></author><author><name sortKey="Cerny, Ondrej" sort="Cerny, Ondrej" uniqKey="Cerny O" first="Ondrej" last="Cerny">Ondrej Cerny</name><affiliation><nlm:affiliation>MRC Centre for Molecular Bacteriology and Infection, Imperial College London, Armstrong Road, London SW7 2AZ, UK.</nlm:affiliation></affiliation></author><author><name sortKey="Jennings, Elliott" sort="Jennings, Elliott" uniqKey="Jennings E" first="Elliott" last="Jennings">Elliott Jennings</name><affiliation><nlm:affiliation>MRC Centre for Molecular Bacteriology and Infection, Imperial College London, Armstrong Road, London SW7 2AZ, UK.</nlm:affiliation></affiliation></author><author><name sortKey="Liu, Mei" sort="Liu, Mei" uniqKey="Liu M" first="Mei" last="Liu">Mei Liu</name><affiliation><nlm:affiliation>MRC Centre for Molecular Bacteriology and Infection, Imperial College London, Armstrong Road, London SW7 2AZ, UK.</nlm:affiliation></affiliation></author><author><name sortKey="Ryan, Aindrias S" sort="Ryan, Aindrias S" uniqKey="Ryan A" first="Aindrias S" last="Ryan">Aindrias S. 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Holden</name><affiliation><nlm:affiliation>MRC Centre for Molecular Bacteriology and Infection, Imperial College London, Armstrong Road, London SW7 2AZ, UK. Electronic address: d.holden@imperial.ac.uk.</nlm:affiliation></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2016">2016</date><idno type="RBID">pubmed:27832589</idno><idno type="pmid">27832589</idno><idno type="doi">10.1016/j.chom.2016.10.007</idno><idno type="wicri:Area/PubMed/Corpus">001648</idno><idno type="wicri:explorRef" wicri:stream="PubMed" wicri:step="Corpus" wicri:corpus="PubMed">001648</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">The Salmonella Effector SteD Mediates MARCH8-Dependent Ubiquitination of MHC II Molecules and Inhibits T Cell Activation.</title><author><name sortKey="Bayer Santos, Ethel" sort="Bayer Santos, Ethel" uniqKey="Bayer Santos E" first="Ethel" last="Bayer-Santos">Ethel Bayer-Santos</name><affiliation><nlm:affiliation>MRC Centre for Molecular Bacteriology and Infection, Imperial College London, Armstrong Road, London SW7 2AZ, UK.</nlm:affiliation></affiliation></author><author><name sortKey="Durkin, Charlotte H" sort="Durkin, Charlotte H" uniqKey="Durkin C" first="Charlotte H" last="Durkin">Charlotte H. Durkin</name><affiliation><nlm:affiliation>MRC Centre for Molecular Bacteriology and Infection, Imperial College London, Armstrong Road, London SW7 2AZ, UK.</nlm:affiliation></affiliation></author><author><name sortKey="Rigano, Luciano A" sort="Rigano, Luciano A" uniqKey="Rigano L" first="Luciano A" last="Rigano">Luciano A. Rigano</name><affiliation><nlm:affiliation>MRC Centre for Molecular Bacteriology and Infection, Imperial College London, Armstrong Road, London SW7 2AZ, UK.</nlm:affiliation></affiliation></author><author><name sortKey="Kupz, Andreas" sort="Kupz, Andreas" uniqKey="Kupz A" first="Andreas" last="Kupz">Andreas Kupz</name><affiliation><nlm:affiliation>Department of Immunology, Max Planck Institute for Infection Biology, 10117 Berlin, Germany; Centre for Biosecurity and Tropical Infectious Diseases, Australian Institute of Tropical Health and Medicine, James Cook University, McGregor Road, Cairns, QLD 4878, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Alix, Eric" sort="Alix, Eric" uniqKey="Alix E" first="Eric" last="Alix">Eric Alix</name><affiliation><nlm:affiliation>MRC Centre for Molecular Bacteriology and Infection, Imperial College London, Armstrong Road, London SW7 2AZ, UK.</nlm:affiliation></affiliation></author><author><name sortKey="Cerny, Ondrej" sort="Cerny, Ondrej" uniqKey="Cerny O" first="Ondrej" last="Cerny">Ondrej Cerny</name><affiliation><nlm:affiliation>MRC Centre for Molecular Bacteriology and Infection, Imperial College London, Armstrong Road, London SW7 2AZ, UK.</nlm:affiliation></affiliation></author><author><name sortKey="Jennings, Elliott" sort="Jennings, Elliott" uniqKey="Jennings E" first="Elliott" last="Jennings">Elliott Jennings</name><affiliation><nlm:affiliation>MRC Centre for Molecular Bacteriology and Infection, Imperial College London, Armstrong Road, London SW7 2AZ, UK.</nlm:affiliation></affiliation></author><author><name sortKey="Liu, Mei" sort="Liu, Mei" uniqKey="Liu M" first="Mei" last="Liu">Mei Liu</name><affiliation><nlm:affiliation>MRC Centre for Molecular Bacteriology and Infection, Imperial College London, Armstrong Road, London SW7 2AZ, UK.</nlm:affiliation></affiliation></author><author><name sortKey="Ryan, Aindrias S" sort="Ryan, Aindrias S" uniqKey="Ryan A" first="Aindrias S" last="Ryan">Aindrias S. Ryan</name><affiliation><nlm:affiliation>MRC Centre for Molecular Bacteriology and Infection, Imperial College London, Armstrong Road, London SW7 2AZ, UK.</nlm:affiliation></affiliation></author><author><name sortKey="Lapaque, Nicolas" sort="Lapaque, Nicolas" uniqKey="Lapaque N" first="Nicolas" last="Lapaque">Nicolas Lapaque</name><affiliation><nlm:affiliation>INRA, UMR 1319 Micalis, Domaine de Vilvert, Jouy-en-Josas 78352, France; AgroParisTech, UMR Micalis, Jouy-en-Josas 78350, France.</nlm:affiliation></affiliation></author><author><name sortKey="Kaufmann, Stefan H E" sort="Kaufmann, Stefan H E" uniqKey="Kaufmann S" first="Stefan H E" last="Kaufmann">Stefan H E. Kaufmann</name><affiliation><nlm:affiliation>Department of Immunology, Max Planck Institute for Infection Biology, 10117 Berlin, Germany.</nlm:affiliation></affiliation></author><author><name sortKey="Holden, David W" sort="Holden, David W" uniqKey="Holden D" first="David W" last="Holden">David W. Holden</name><affiliation><nlm:affiliation>MRC Centre for Molecular Bacteriology and Infection, Imperial College London, Armstrong Road, London SW7 2AZ, UK. Electronic address: d.holden@imperial.ac.uk.</nlm:affiliation></affiliation></author></analytic><series><title level="j">Cell host & microbe</title><idno type="eISSN">1934-6069</idno><imprint><date when="2016" type="published">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Animals</term><term>Bacterial Proteins (metabolism)</term><term>Cell Line</term><term>Dendritic Cells (immunology)</term><term>Dendritic Cells (microbiology)</term><term>Histocompatibility Antigens Class II (metabolism)</term><term>Host-Pathogen Interactions</term><term>Humans</term><term>Immune Evasion</term><term>Lymphocyte Activation</term><term>Mice</term><term>Protein Binding</term><term>Salmonella Infections, Animal (immunology)</term><term>Salmonella Infections, Animal (microbiology)</term><term>Salmonella typhimurium (pathogenicity)</term><term>T-Lymphocytes (immunology)</term><term>Ubiquitin-Protein Ligases (metabolism)</term><term>Ubiquitination</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Bacterial Proteins</term><term>Histocompatibility Antigens Class II</term><term>Ubiquitin-Protein Ligases</term></keywords><keywords scheme="MESH" qualifier="immunology" xml:lang="en"><term>Dendritic Cells</term><term>Salmonella Infections, Animal</term><term>T-Lymphocytes</term></keywords><keywords scheme="MESH" qualifier="microbiology" xml:lang="en"><term>Dendritic Cells</term><term>Salmonella Infections, Animal</term></keywords><keywords scheme="MESH" qualifier="pathogenicity" xml:lang="en"><term>Salmonella typhimurium</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Animals</term><term>Cell Line</term><term>Host-Pathogen Interactions</term><term>Humans</term><term>Immune Evasion</term><term>Lymphocyte Activation</term><term>Mice</term><term>Protein Binding</term><term>Ubiquitination</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">The SPI-2 type III secretion system (T3SS) of intracellular Salmonella enterica translocates effector proteins into mammalian cells. Infection of antigen-presenting cells results in SPI-2 T3SS-dependent ubiquitination and reduction of surface-localized mature MHC class II (mMHCII). We identify the effector SteD as required and sufficient for this process. In Mel Juso cells, SteD localized to the Golgi network and vesicles containing the E3 ubiquitin ligase MARCH8 and mMHCII. SteD caused MARCH8-dependent ubiquitination and depletion of surface mMHCII. One of two transmembrane domains and the C-terminal cytoplasmic region of SteD mediated binding to MARCH8 and mMHCII, respectively. Infection of dendritic cells resulted in SteD-dependent depletion of surface MHCII, the co-stimulatory molecule B7.2, and suppression of T cell activation. SteD also accounted for suppression of T cell activation during Salmonella infection of mice. We propose that SteD is an adaptor, forcing inappropriate ubiquitination of mMHCII by MARCH8 and thereby suppressing T cell activation.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">27832589</PMID><DateCreated><Year>2016</Year><Month>11</Month><Day>10</Day></DateCreated><DateCompleted><Year>2017</Year><Month>09</Month><Day>06</Day></DateCompleted><DateRevised><Year>2017</Year><Month>09</Month><Day>22</Day></DateRevised><Article PubModel="Print"><Journal><ISSN IssnType="Electronic">1934-6069</ISSN><JournalIssue CitedMedium="Internet"><Volume>20</Volume><Issue>5</Issue><PubDate><Year>2016</Year><Month>Nov</Month><Day>09</Day></PubDate></JournalIssue><Title>Cell host & microbe</Title><ISOAbbreviation>Cell Host Microbe</ISOAbbreviation></Journal><ArticleTitle>The Salmonella Effector SteD Mediates MARCH8-Dependent Ubiquitination of MHC II Molecules and Inhibits T Cell Activation.</ArticleTitle><Pagination><MedlinePgn>584-595</MedlinePgn></Pagination><ELocationID EIdType="pii" ValidYN="Y">S1931-3128(16)30433-4</ELocationID><ELocationID EIdType="doi" ValidYN="Y">10.1016/j.chom.2016.10.007</ELocationID><Abstract><AbstractText>The SPI-2 type III secretion system (T3SS) of intracellular Salmonella enterica translocates effector proteins into mammalian cells. Infection of antigen-presenting cells results in SPI-2 T3SS-dependent ubiquitination and reduction of surface-localized mature MHC class II (mMHCII). We identify the effector SteD as required and sufficient for this process. In Mel Juso cells, SteD localized to the Golgi network and vesicles containing the E3 ubiquitin ligase MARCH8 and mMHCII. SteD caused MARCH8-dependent ubiquitination and depletion of surface mMHCII. One of two transmembrane domains and the C-terminal cytoplasmic region of SteD mediated binding to MARCH8 and mMHCII, respectively. Infection of dendritic cells resulted in SteD-dependent depletion of surface MHCII, the co-stimulatory molecule B7.2, and suppression of T cell activation. SteD also accounted for suppression of T cell activation during Salmonella infection of mice. We propose that SteD is an adaptor, forcing inappropriate ubiquitination of mMHCII by MARCH8 and thereby suppressing T cell activation.</AbstractText><CopyrightInformation>Copyright © 2016 The Authors. Published by Elsevier Inc. All rights reserved.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Bayer-Santos</LastName><ForeName>Ethel</ForeName><Initials>E</Initials><AffiliationInfo><Affiliation>MRC Centre for Molecular Bacteriology and Infection, Imperial College London, Armstrong Road, London SW7 2AZ, UK.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Durkin</LastName><ForeName>Charlotte H</ForeName><Initials>CH</Initials><AffiliationInfo><Affiliation>MRC Centre for Molecular Bacteriology and Infection, Imperial College London, Armstrong Road, London SW7 2AZ, UK.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Rigano</LastName><ForeName>Luciano A</ForeName><Initials>LA</Initials><AffiliationInfo><Affiliation>MRC Centre for Molecular Bacteriology and Infection, Imperial College London, Armstrong Road, London SW7 2AZ, UK.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kupz</LastName><ForeName>Andreas</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Department of Immunology, Max Planck Institute for Infection Biology, 10117 Berlin, Germany; Centre for Biosecurity and Tropical Infectious Diseases, Australian Institute of Tropical Health and Medicine, James Cook University, McGregor Road, Cairns, QLD 4878, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Alix</LastName><ForeName>Eric</ForeName><Initials>E</Initials><AffiliationInfo><Affiliation>MRC Centre for Molecular Bacteriology and Infection, Imperial College London, Armstrong Road, London SW7 2AZ, UK.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Cerny</LastName><ForeName>Ondrej</ForeName><Initials>O</Initials><AffiliationInfo><Affiliation>MRC Centre for Molecular Bacteriology and Infection, Imperial College London, Armstrong Road, London SW7 2AZ, UK.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Jennings</LastName><ForeName>Elliott</ForeName><Initials>E</Initials><AffiliationInfo><Affiliation>MRC Centre for Molecular Bacteriology and Infection, Imperial College London, Armstrong Road, London SW7 2AZ, UK.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Liu</LastName><ForeName>Mei</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>MRC Centre for Molecular Bacteriology and Infection, Imperial College London, Armstrong Road, London SW7 2AZ, UK.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ryan</LastName><ForeName>Aindrias S</ForeName><Initials>AS</Initials><AffiliationInfo><Affiliation>MRC Centre for Molecular Bacteriology and Infection, Imperial College London, Armstrong Road, London SW7 2AZ, UK.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lapaque</LastName><ForeName>Nicolas</ForeName><Initials>N</Initials><AffiliationInfo><Affiliation>INRA, UMR 1319 Micalis, Domaine de Vilvert, Jouy-en-Josas 78352, France; AgroParisTech, UMR Micalis, Jouy-en-Josas 78350, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kaufmann</LastName><ForeName>Stefan H E</ForeName><Initials>SHE</Initials><AffiliationInfo><Affiliation>Department of Immunology, Max Planck Institute for Infection Biology, 10117 Berlin, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Holden</LastName><ForeName>David W</ForeName><Initials>DW</Initials><AffiliationInfo><Affiliation>MRC Centre for Molecular Bacteriology and Infection, Imperial College London, Armstrong Road, London SW7 2AZ, UK. Electronic address: d.holden@imperial.ac.uk.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>MR/K027077/1</GrantID><Agency>Medical Research Council</Agency><Country>United Kingdom</Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>Cell Host Microbe</MedlineTA><NlmUniqueID>101302316</NlmUniqueID><ISSNLinking>1931-3128</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D001426">Bacterial Proteins</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D000949">Histocompatibility Antigens Class II</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="C000622320">SteD protein, Salmonella 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MajorTopicYN="N">microbiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D012486" MajorTopicYN="N">Salmonella typhimurium</DescriptorName><QualifierName UI="Q000472" MajorTopicYN="Y">pathogenicity</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D013601" MajorTopicYN="N">T-Lymphocytes</DescriptorName><QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D044767" MajorTopicYN="N">Ubiquitin-Protein Ligases</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D054875" MajorTopicYN="Y">Ubiquitination</DescriptorName></MeshHeading></MeshHeadingList><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Salmonella</Keyword><Keyword MajorTopicYN="N">dendritic cells</Keyword><Keyword MajorTopicYN="N">effector</Keyword><Keyword MajorTopicYN="N">ligase</Keyword><Keyword MajorTopicYN="N">major histocompatibility complex</Keyword><Keyword MajorTopicYN="N">ubiquitin</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2016</Year><Month>07</Month><Day>05</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2016</Year><Month>09</Month><Day>09</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2016</Year><Month>10</Month><Day>11</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2016</Year><Month>11</Month><Day>11</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2016</Year><Month>11</Month><Day>11</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2017</Year><Month>9</Month><Day>7</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">27832589</ArticleId><ArticleId IdType="pii">S1931-3128(16)30433-4</ArticleId><ArticleId IdType="doi">10.1016/j.chom.2016.10.007</ArticleId><ArticleId IdType="pmc">PMC5104694</ArticleId></ArticleIdList></PubmedData></pubmed></record>Pour manipuler ce document sous Unix (Dilib)
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