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 : 000209 ( France/Analysis ); précédent : 000208; suivant : 000210Anti-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 [Hong Kong] ; Ming S. Yip [Hong Kong] ; Chung Y. Cheung [Hong Kong] ; Hiu L. Leung [Hong Kong] ; Ping H. Li [Hong Kong] ; Francois Kien [Hong Kong] ; Isabelle Dutry [Hong Kong] ; Benoit Callendret [France] ; Nicolas Escriou [France] ; Ralf Altmeyer [Hong Kong] ; Beatrice Nal [Hong Kong] ; Marc Daëron [France] ; Roberto Bruzzone [Hong Kong, France] ; J. S. Malik Peiris [Hong Kong]Source :
- Journal of virology [ 0022-538X ] ; 2011.
Descripteurs français
- Pascal (Inist)
- Wicri :
- topic : Homme.
English descriptors
- KwdEn :
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.
Affiliations:
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Pascal:12-0111133Le document en format XML
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Research Centre, 8 Sassoon Road</s1><s3>HKG</s3><sZ>1 aut.</sZ><sZ>2 aut.</sZ><sZ>4 aut.</sZ><sZ>5 aut.</sZ><sZ>6 aut.</sZ><sZ>7 aut.</sZ><sZ>10 aut.</sZ><sZ>11 aut.</sZ><sZ>13 aut.</sZ><sZ>14 aut.</sZ></inist:fA14><country>Hong Kong</country><wicri:noRegion>HKU-Pasteur Research Centre, 8 Sassoon Road</wicri:noRegion></affiliation><affiliation wicri:level="3"><inist:fA14 i1="08"><s1>Institut Pasteur, Department of Cell Biology and Infection, 25 Rue du Docteur Roux</s1><s2>75015 Paris</s2><s3>FRA</s3><sZ>13 aut.</sZ></inist:fA14><country>France</country><placeName><region type="region" nuts="2">Île-de-France</region><settlement type="city">Paris</settlement></placeName></affiliation></author><author><name sortKey="Malik Peiris, J S" sort="Malik Peiris, J S" uniqKey="Malik Peiris J" first="J. S." last="Malik Peiris">J. S. 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Yip</name><affiliation wicri:level="1"><inist:fA14 i1="01"><s1>HKU-Pasteur Research Centre, 8 Sassoon Road</s1><s3>HKG</s3><sZ>1 aut.</sZ><sZ>2 aut.</sZ><sZ>4 aut.</sZ><sZ>5 aut.</sZ><sZ>6 aut.</sZ><sZ>7 aut.</sZ><sZ>10 aut.</sZ><sZ>11 aut.</sZ><sZ>13 aut.</sZ><sZ>14 aut.</sZ></inist:fA14><country>Hong Kong</country><wicri:noRegion>HKU-Pasteur Research Centre, 8 Sassoon Road</wicri:noRegion></affiliation></author><author><name sortKey="Cheung, Chung Y" sort="Cheung, Chung Y" uniqKey="Cheung C" first="Chung Y." last="Cheung">Chung Y. Cheung</name><affiliation wicri:level="1"><inist:fA14 i1="02"><s1>Department of Microbiology, The University of Hong Kong, 21 Sassoon Road</s1><s3>HKG</s3><sZ>3 aut.</sZ><sZ>7 aut.</sZ></inist:fA14><country>Hong Kong</country><wicri:noRegion>Department of Microbiology, The University of Hong Kong, 21 Sassoon Road</wicri:noRegion></affiliation></author><author><name sortKey="Leung, Hiu L" sort="Leung, Hiu L" uniqKey="Leung H" first="Hiu L." last="Leung">Hiu L. Leung</name><affiliation wicri:level="1"><inist:fA14 i1="01"><s1>HKU-Pasteur Research Centre, 8 Sassoon Road</s1><s3>HKG</s3><sZ>1 aut.</sZ><sZ>2 aut.</sZ><sZ>4 aut.</sZ><sZ>5 aut.</sZ><sZ>6 aut.</sZ><sZ>7 aut.</sZ><sZ>10 aut.</sZ><sZ>11 aut.</sZ><sZ>13 aut.</sZ><sZ>14 aut.</sZ></inist:fA14><country>Hong Kong</country><wicri:noRegion>HKU-Pasteur Research Centre, 8 Sassoon Road</wicri:noRegion></affiliation></author><author><name sortKey="Li, Ping H" sort="Li, Ping H" uniqKey="Li P" first="Ping H." last="Li">Ping H. Li</name><affiliation wicri:level="1"><inist:fA14 i1="01"><s1>HKU-Pasteur Research Centre, 8 Sassoon Road</s1><s3>HKG</s3><sZ>1 aut.</sZ><sZ>2 aut.</sZ><sZ>4 aut.</sZ><sZ>5 aut.</sZ><sZ>6 aut.</sZ><sZ>7 aut.</sZ><sZ>10 aut.</sZ><sZ>11 aut.</sZ><sZ>13 aut.</sZ><sZ>14 aut.</sZ></inist:fA14><country>Hong Kong</country><wicri:noRegion>HKU-Pasteur Research Centre, 8 Sassoon Road</wicri:noRegion></affiliation></author><author><name sortKey="Kien, Francois" sort="Kien, Francois" uniqKey="Kien F" first="Francois" last="Kien">Francois Kien</name><affiliation wicri:level="1"><inist:fA14 i1="01"><s1>HKU-Pasteur Research Centre, 8 Sassoon Road</s1><s3>HKG</s3><sZ>1 aut.</sZ><sZ>2 aut.</sZ><sZ>4 aut.</sZ><sZ>5 aut.</sZ><sZ>6 aut.</sZ><sZ>7 aut.</sZ><sZ>10 aut.</sZ><sZ>11 aut.</sZ><sZ>13 aut.</sZ><sZ>14 aut.</sZ></inist:fA14><country>Hong Kong</country><wicri:noRegion>HKU-Pasteur Research Centre, 8 Sassoon Road</wicri:noRegion></affiliation></author><author><name sortKey="Dutry, Isabelle" 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Docteur Roux</s1><s2>75015 Paris</s2><s3>FRA</s3><sZ>8 aut.</sZ><sZ>9 aut.</sZ></inist:fA14><country>France</country><placeName><region type="region" nuts="2">Île-de-France</region><settlement type="city">Paris</settlement></placeName></affiliation><affiliation wicri:level="3"><inist:fA14 i1="04"><s1>CNRS, UPA3015</s1><s2>75015 Paris</s2><s3>FRA</s3><sZ>8 aut.</sZ><sZ>9 aut.</sZ></inist:fA14><country>France</country><placeName><region type="region" nuts="2">Île-de-France</region><settlement type="city">Paris</settlement></placeName></affiliation></author><author><name sortKey="Altmeyer, Ralf" sort="Altmeyer, Ralf" uniqKey="Altmeyer R" first="Ralf" last="Altmeyer">Ralf Altmeyer</name><affiliation wicri:level="1"><inist:fA14 i1="01"><s1>HKU-Pasteur Research Centre, 8 Sassoon Road</s1><s3>HKG</s3><sZ>1 aut.</sZ><sZ>2 aut.</sZ><sZ>4 aut.</sZ><sZ>5 aut.</sZ><sZ>6 aut.</sZ><sZ>7 aut.</sZ><sZ>10 aut.</sZ><sZ>11 aut.</sZ><sZ>13 aut.</sZ><sZ>14 aut.</sZ></inist:fA14><country>Hong Kong</country><wicri:noRegion>HKU-Pasteur Research Centre, 8 Sassoon Road</wicri:noRegion></affiliation></author><author><name sortKey="Nal, Beatrice" sort="Nal, Beatrice" uniqKey="Nal B" first="Beatrice" last="Nal">Beatrice Nal</name><affiliation wicri:level="1"><inist:fA14 i1="01"><s1>HKU-Pasteur Research Centre, 8 Sassoon Road</s1><s3>HKG</s3><sZ>1 aut.</sZ><sZ>2 aut.</sZ><sZ>4 aut.</sZ><sZ>5 aut.</sZ><sZ>6 aut.</sZ><sZ>7 aut.</sZ><sZ>10 aut.</sZ><sZ>11 aut.</sZ><sZ>13 aut.</sZ><sZ>14 aut.</sZ></inist:fA14><country>Hong Kong</country><wicri:noRegion>HKU-Pasteur Research Centre, 8 Sassoon Road</wicri:noRegion></affiliation><affiliation wicri:level="1"><inist:fA14 i1="05"><s1>Department of Anatomy, The University of Hong Kong, 21 Sassoon Road</s1><s3>HKG</s3><sZ>11 aut.</sZ></inist:fA14><country>Hong Kong</country><wicri:noRegion>Department of Anatomy, The University of Hong Kong, 21 Sassoon Road</wicri:noRegion></affiliation></author><author><name sortKey="Daeron, Marc" sort="Daeron, Marc" uniqKey="Daeron M" first="Marc" last="Daëron">Marc Daëron</name><affiliation wicri:level="3"><inist:fA14 i1="06"><s1>Institut Pasteur, Département d'lmmunologie, Unité d'Allergologie Moléculaire et Cellulaire, 25 Rue du Docteur Roux</s1><s2>75015 Paris</s2><s3>FRA</s3><sZ>12 aut.</sZ></inist:fA14><country>France</country><placeName><region type="region" nuts="2">Île-de-France</region><settlement type="city">Paris</settlement></placeName></affiliation><affiliation wicri:level="3"><inist:fA14 i1="07"><s1>INSERM, Unité 760, 25 Rue du Docteur Roux</s1><s2>75015 Paris</s2><s3>FRA</s3><sZ>12 aut.</sZ></inist:fA14><country>France</country><placeName><region type="region" nuts="2">Île-de-France</region><settlement type="city">Paris</settlement></placeName></affiliation></author><author><name sortKey="Bruzzone, Roberto" sort="Bruzzone, Roberto" uniqKey="Bruzzone R" first="Roberto" last="Bruzzone">Roberto Bruzzone</name><affiliation wicri:level="1"><inist:fA14 i1="01"><s1>HKU-Pasteur Research Centre, 8 Sassoon Road</s1><s3>HKG</s3><sZ>1 aut.</sZ><sZ>2 aut.</sZ><sZ>4 aut.</sZ><sZ>5 aut.</sZ><sZ>6 aut.</sZ><sZ>7 aut.</sZ><sZ>10 aut.</sZ><sZ>11 aut.</sZ><sZ>13 aut.</sZ><sZ>14 aut.</sZ></inist:fA14><country>Hong Kong</country><wicri:noRegion>HKU-Pasteur Research Centre, 8 Sassoon Road</wicri:noRegion></affiliation><affiliation wicri:level="3"><inist:fA14 i1="08"><s1>Institut Pasteur, Department of Cell Biology and Infection, 25 Rue du Docteur Roux</s1><s2>75015 Paris</s2><s3>FRA</s3><sZ>13 aut.</sZ></inist:fA14><country>France</country><placeName><region type="region" nuts="2">Île-de-France</region><settlement type="city">Paris</settlement></placeName></affiliation></author><author><name sortKey="Malik Peiris, J S" sort="Malik Peiris, J S" uniqKey="Malik Peiris J" first="J. S." last="Malik Peiris">J. S. Malik Peiris</name><affiliation wicri:level="1"><inist:fA14 i1="01"><s1>HKU-Pasteur Research Centre, 8 Sassoon Road</s1><s3>HKG</s3><sZ>1 aut.</sZ><sZ>2 aut.</sZ><sZ>4 aut.</sZ><sZ>5 aut.</sZ><sZ>6 aut.</sZ><sZ>7 aut.</sZ><sZ>10 aut.</sZ><sZ>11 aut.</sZ><sZ>13 aut.</sZ><sZ>14 aut.</sZ></inist:fA14><country>Hong Kong</country><wicri:noRegion>HKU-Pasteur Research Centre, 8 Sassoon Road</wicri:noRegion></affiliation></author></analytic><series><title level="j" type="main">Journal of virology</title><title level="j" type="abbreviated">J. virol.</title><idno type="ISSN">0022-538X</idno><imprint><date when="2011">2011</date></imprint></series></biblStruct></sourceDesc><seriesStmt><title level="j" type="main">Journal of virology</title><title level="j" type="abbreviated">J. virol.</title><idno type="ISSN">0022-538X</idno></seriesStmt></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Antibody</term><term>Coronavirus</term><term>Cysteine endopeptidases</term><term>FcγR receptor</term><term>Human</term><term>Severe acute respiratory syndrome</term></keywords><keywords scheme="Pascal" xml:lang="fr"><term>Coronavirus</term><term>Homme</term><term>Anticorps</term><term>Cysteine endopeptidases</term><term>Récepteur FcγR</term><term>Syndrome respiratoire aigu sévère</term></keywords><keywords scheme="Wicri" type="topic" xml:lang="fr"><term>Homme</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">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.</div></front></TEI><affiliations><list><country><li>France</li><li>Hong Kong</li></country><region><li>Île-de-France</li></region><settlement><li>Paris</li></settlement></list><tree><country name="Hong Kong"><noRegion><name sortKey="Jaume, Martial" sort="Jaume, Martial" uniqKey="Jaume M" first="Martial" last="Jaume">Martial Jaume</name></noRegion><name sortKey="Altmeyer, Ralf" sort="Altmeyer, Ralf" uniqKey="Altmeyer R" first="Ralf" last="Altmeyer">Ralf Altmeyer</name><name sortKey="Bruzzone, Roberto" sort="Bruzzone, Roberto" uniqKey="Bruzzone R" first="Roberto" last="Bruzzone">Roberto Bruzzone</name><name sortKey="Cheung, Chung Y" sort="Cheung, Chung Y" uniqKey="Cheung C" first="Chung Y." last="Cheung">Chung Y. Cheung</name><name sortKey="Dutry, Isabelle" sort="Dutry, Isabelle" uniqKey="Dutry I" first="Isabelle" last="Dutry">Isabelle Dutry</name><name sortKey="Dutry, Isabelle" sort="Dutry, Isabelle" uniqKey="Dutry I" first="Isabelle" last="Dutry">Isabelle Dutry</name><name sortKey="Kien, Francois" sort="Kien, Francois" uniqKey="Kien F" first="Francois" last="Kien">Francois Kien</name><name sortKey="Leung, Hiu L" sort="Leung, Hiu L" uniqKey="Leung H" first="Hiu L." last="Leung">Hiu L. Leung</name><name sortKey="Li, Ping H" sort="Li, Ping H" uniqKey="Li P" first="Ping H." last="Li">Ping H. Li</name><name sortKey="Malik Peiris, J S" sort="Malik Peiris, J S" uniqKey="Malik Peiris J" first="J. S." last="Malik Peiris">J. S. Malik Peiris</name><name sortKey="Nal, Beatrice" sort="Nal, Beatrice" uniqKey="Nal B" first="Beatrice" last="Nal">Beatrice Nal</name><name sortKey="Nal, Beatrice" sort="Nal, Beatrice" uniqKey="Nal B" first="Beatrice" last="Nal">Beatrice Nal</name><name sortKey="Yip, Ming S" sort="Yip, Ming S" uniqKey="Yip M" first="Ming S." last="Yip">Ming S. Yip</name></country><country name="France"><region name="Île-de-France"><name sortKey="Callendret, Benoit" sort="Callendret, Benoit" uniqKey="Callendret B" first="Benoit" last="Callendret">Benoit Callendret</name></region><name sortKey="Bruzzone, Roberto" sort="Bruzzone, Roberto" uniqKey="Bruzzone R" first="Roberto" last="Bruzzone">Roberto Bruzzone</name><name sortKey="Callendret, Benoit" sort="Callendret, Benoit" uniqKey="Callendret B" first="Benoit" last="Callendret">Benoit Callendret</name><name sortKey="Daeron, Marc" sort="Daeron, Marc" uniqKey="Daeron M" first="Marc" last="Daëron">Marc Daëron</name><name sortKey="Daeron, Marc" sort="Daeron, Marc" uniqKey="Daeron M" first="Marc" last="Daëron">Marc Daëron</name><name sortKey="Escriou, Nicolas" sort="Escriou, Nicolas" uniqKey="Escriou N" first="Nicolas" last="Escriou">Nicolas Escriou</name><name sortKey="Escriou, Nicolas" sort="Escriou, Nicolas" uniqKey="Escriou N" first="Nicolas" last="Escriou">Nicolas Escriou</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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