Anti-severe acute respiratory syndrome coronavirus spike antibodies trigger infection of human immune cells via a pH- and cysteine protease-independent FcγR pathway.
Identifieur interne : 001492 ( PubMed/Corpus ); précédent : 001491; suivant : 001493Anti-severe acute respiratory syndrome coronavirus spike antibodies trigger infection of human immune cells via a pH- and cysteine protease-independent FcγR pathway.
Auteurs : Martial Jaume ; Ming S. Yip ; Chung Y. Cheung ; Hiu L. Leung ; Ping H. Li ; Francois Kien ; Isabelle Dutry ; Benoît Callendret ; Nicolas Escriou ; Ralf Altmeyer ; Beatrice Nal ; Marc Daëron ; Roberto Bruzzone ; J S Malik PeirisSource :
- Journal of virology [ 1098-5514 ] ; 2011.
English descriptors
- KwdEn :
- Animals, Antibodies, Neutralizing (metabolism), Antibodies, Viral (metabolism), Antibody-Dependent Enhancement, Cells, Cultured, Chlorocebus aethiops, Cysteine Proteases, Humans, Hydrogen-Ion Concentration, Lymphocytes (virology), Membrane Glycoproteins (metabolism), Mice, Mice, Inbred BALB C, Receptors, IgG (metabolism), SARS Virus (immunology), SARS Virus (pathogenicity), Spike Glycoprotein, Coronavirus, Viral Envelope Proteins (metabolism), Virus Internalization.
- MESH :
- chemical , metabolism : Antibodies, Neutralizing, Antibodies, Viral, Membrane Glycoproteins, Receptors, IgG, Viral Envelope Proteins.
- immunology : SARS Virus.
- pathogenicity : SARS Virus.
- virology : Lymphocytes.
- Animals, Antibody-Dependent Enhancement, Cells, Cultured, Chlorocebus aethiops, Cysteine Proteases, Humans, Hydrogen-Ion Concentration, Mice, Mice, Inbred BALB C, Spike Glycoprotein, Coronavirus, Virus Internalization.
Abstract
Public health measures successfully contained outbreaks of the severe acute respiratory syndrome coronavirus (SARS-CoV) infection. However, the precursor of the SARS-CoV remains in its natural bat reservoir, and reemergence of a human-adapted SARS-like coronavirus remains a plausible public health concern. Vaccination is a major strategy for containing resurgence of SARS in humans, and a number of vaccine candidates have been tested in experimental animal models. We previously reported that antibody elicited by a SARS-CoV vaccine candidate based on recombinant full-length Spike-protein trimers potentiated infection of human B cell lines despite eliciting in vivo a neutralizing and protective immune response in rodents. These observations prompted us to investigate the mechanisms underlying antibody-dependent enhancement (ADE) of SARS-CoV infection in vitro. We demonstrate here that anti-Spike immune serum, while inhibiting viral entry in a permissive cell line, potentiated infection of immune cells by SARS-CoV Spike-pseudotyped lentiviral particles, as well as replication-competent SARS coronavirus. Antibody-mediated infection was dependent on Fcγ receptor II but did not use the endosomal/lysosomal pathway utilized by angiotensin I converting enzyme 2 (ACE2), the accepted receptor for SARS-CoV. This suggests that ADE of SARS-CoV utilizes a novel cell entry mechanism into immune cells. Different SARS vaccine candidates elicit sera that differ in their capacity to induce ADE in immune cells despite their comparable potency to neutralize infection in ACE2-bearing cells. Our results suggest a novel mechanism by which SARS-CoV can enter target cells and illustrate the potential pitfalls associated with immunization against it. These findings should prompt further investigations into SARS pathogenesis.
DOI: 10.1128/JVI.00671-11
PubMed: 21775467
Links to Exploration step
pubmed:21775467Le document en format XML
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However, the precursor of the SARS-CoV remains in its natural bat reservoir, and reemergence of a human-adapted SARS-like coronavirus remains a plausible public health concern. Vaccination is a major strategy for containing resurgence of SARS in humans, and a number of vaccine candidates have been tested in experimental animal models. We previously reported that antibody elicited by a SARS-CoV vaccine candidate based on recombinant full-length Spike-protein trimers potentiated infection of human B cell lines despite eliciting in vivo a neutralizing and protective immune response in rodents. These observations prompted us to investigate the mechanisms underlying antibody-dependent enhancement (ADE) of SARS-CoV infection in vitro. We demonstrate here that anti-Spike immune serum, while inhibiting viral entry in a permissive cell line, potentiated infection of immune cells by SARS-CoV Spike-pseudotyped lentiviral particles, as well as replication-competent SARS coronavirus. Antibody-mediated infection was dependent on Fcγ receptor II but did not use the endosomal/lysosomal pathway utilized by angiotensin I converting enzyme 2 (ACE2), the accepted receptor for SARS-CoV. This suggests that ADE of SARS-CoV utilizes a novel cell entry mechanism into immune cells. Different SARS vaccine candidates elicit sera that differ in their capacity to induce ADE in immune cells despite their comparable potency to neutralize infection in ACE2-bearing cells. Our results suggest a novel mechanism by which SARS-CoV can enter target cells and illustrate the potential pitfalls associated with immunization against it. These findings should prompt further investigations into SARS pathogenesis.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">21775467</PMID><DateCompleted><Year>2011</Year><Month>11</Month><Day>07</Day></DateCompleted><DateRevised><Year>2020</Year><Month>04</Month><Day>15</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1098-5514</ISSN><JournalIssue CitedMedium="Internet"><Volume>85</Volume><Issue>20</Issue><PubDate><Year>2011</Year><Month>Oct</Month></PubDate></JournalIssue><Title>Journal of virology</Title><ISOAbbreviation>J. Virol.</ISOAbbreviation></Journal><ArticleTitle>Anti-severe acute respiratory syndrome coronavirus spike antibodies trigger infection of human immune cells via a pH- and cysteine protease-independent FcγR pathway.</ArticleTitle><Pagination><MedlinePgn>10582-97</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1128/JVI.00671-11</ELocationID><Abstract><AbstractText>Public health measures successfully contained outbreaks of the severe acute respiratory syndrome coronavirus (SARS-CoV) infection. However, the precursor of the SARS-CoV remains in its natural bat reservoir, and reemergence of a human-adapted SARS-like coronavirus remains a plausible public health concern. Vaccination is a major strategy for containing resurgence of SARS in humans, and a number of vaccine candidates have been tested in experimental animal models. We previously reported that antibody elicited by a SARS-CoV vaccine candidate based on recombinant full-length Spike-protein trimers potentiated infection of human B cell lines despite eliciting in vivo a neutralizing and protective immune response in rodents. These observations prompted us to investigate the mechanisms underlying antibody-dependent enhancement (ADE) of SARS-CoV infection in vitro. We demonstrate here that anti-Spike immune serum, while inhibiting viral entry in a permissive cell line, potentiated infection of immune cells by SARS-CoV Spike-pseudotyped lentiviral particles, as well as replication-competent SARS coronavirus. Antibody-mediated infection was dependent on Fcγ receptor II but did not use the endosomal/lysosomal pathway utilized by angiotensin I converting enzyme 2 (ACE2), the accepted receptor for SARS-CoV. This suggests that ADE of SARS-CoV utilizes a novel cell entry mechanism into immune cells. Different SARS vaccine candidates elicit sera that differ in their capacity to induce ADE in immune cells despite their comparable potency to neutralize infection in ACE2-bearing cells. Our results suggest a novel mechanism by which SARS-CoV can enter target cells and illustrate the potential pitfalls associated with immunization against it. These findings should prompt further investigations into SARS pathogenesis.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Jaume</LastName><ForeName>Martial</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>HKU-Pasteur Research Centre, Dexter H. C. Man Building, 8 Sassoon Road, Pokfulam, Hong Kong SAR, China. breizh@hku.hk</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Yip</LastName><ForeName>Ming S</ForeName><Initials>MS</Initials></Author><Author ValidYN="Y"><LastName>Cheung</LastName><ForeName>Chung Y</ForeName><Initials>CY</Initials></Author><Author ValidYN="Y"><LastName>Leung</LastName><ForeName>Hiu L</ForeName><Initials>HL</Initials></Author><Author ValidYN="Y"><LastName>Li</LastName><ForeName>Ping H</ForeName><Initials>PH</Initials></Author><Author ValidYN="Y"><LastName>Kien</LastName><ForeName>Francois</ForeName><Initials>F</Initials></Author><Author ValidYN="Y"><LastName>Dutry</LastName><ForeName>Isabelle</ForeName><Initials>I</Initials></Author><Author ValidYN="Y"><LastName>Callendret</LastName><ForeName>Benoît</ForeName><Initials>B</Initials></Author><Author ValidYN="Y"><LastName>Escriou</LastName><ForeName>Nicolas</ForeName><Initials>N</Initials></Author><Author ValidYN="Y"><LastName>Altmeyer</LastName><ForeName>Ralf</ForeName><Initials>R</Initials></Author><Author ValidYN="Y"><LastName>Nal</LastName><ForeName>Beatrice</ForeName><Initials>B</Initials></Author><Author ValidYN="Y"><LastName>Daëron</LastName><ForeName>Marc</ForeName><Initials>M</Initials></Author><Author ValidYN="Y"><LastName>Bruzzone</LastName><ForeName>Roberto</ForeName><Initials>R</Initials></Author><Author ValidYN="Y"><LastName>Peiris</LastName><ForeName>J S Malik</ForeName><Initials>JS</Initials></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2011</Year><Month>07</Month><Day>20</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>J Virol</MedlineTA><NlmUniqueID>0113724</NlmUniqueID><ISSNLinking>0022-538X</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D057134">Antibodies, Neutralizing</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D000914">Antibodies, Viral</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D008562">Membrane Glycoproteins</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D017452">Receptors, IgG</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D064370">Spike Glycoprotein, Coronavirus</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D014759">Viral Envelope Proteins</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="C578557">spike glycoprotein, SARS-CoV</NameOfSubstance></Chemical><Chemical><RegistryNumber>EC 3.4.-</RegistryNumber><NameOfSubstance UI="D057056">Cysteine Proteases</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D000818" MajorTopicYN="N">Animals</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D057134" MajorTopicYN="N">Antibodies, Neutralizing</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D000914" MajorTopicYN="N">Antibodies, Viral</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D019067" MajorTopicYN="Y">Antibody-Dependent Enhancement</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D002478" MajorTopicYN="N">Cells, Cultured</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D002522" MajorTopicYN="N">Chlorocebus aethiops</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D057056" MajorTopicYN="N">Cysteine Proteases</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D006801" MajorTopicYN="N">Humans</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D006863" MajorTopicYN="N">Hydrogen-Ion Concentration</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D008214" MajorTopicYN="N">Lymphocytes</DescriptorName><QualifierName UI="Q000821" MajorTopicYN="Y">virology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D008562" MajorTopicYN="N">Membrane Glycoproteins</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D051379" MajorTopicYN="N">Mice</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D008807" MajorTopicYN="N">Mice, Inbred BALB C</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D017452" MajorTopicYN="N">Receptors, 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