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SARS-CoV-2 transmission via apical syncytia release from primary bronchial epithelia and infectivity restriction in children epithelia

Guillaume Beucher, Marie-Lise Blondot, Alexis Celle, Noémie Pied, Patricia Recordon-Pinson, Pauline Esteves, Muriel Faure, Mathieu Métifiot, Sabrina Lacomme, Denis Dacheaux, View ORCID ProfileDerrick Robinson, Gernot Längst, Fabien Beaufils, Marie-Edith Lafon, Patrick Berger, Marc Landry, Denis Malvy, Thomas Trian, Marie-Line Andreola, View ORCID ProfileHarald Wodrich
doi: https://doi.org/10.1101/2021.05.28.446159
Guillaume Beucher
aUniv. Bordeaux, CNRS, Microbiologie Fondamentale et Pathogénicité, UMR 5234, F-33000 Bordeaux, France
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Marie-Lise Blondot
aUniv. Bordeaux, CNRS, Microbiologie Fondamentale et Pathogénicité, UMR 5234, F-33000 Bordeaux, France
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Alexis Celle
bINSERM, Centre de Recherche Cardio-thoracique de Bordeaux, U1045, CIC 1401, Bordeaux, 33000, France
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Noémie Pied
aUniv. Bordeaux, CNRS, Microbiologie Fondamentale et Pathogénicité, UMR 5234, F-33000 Bordeaux, France
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Patricia Recordon-Pinson
aUniv. Bordeaux, CNRS, Microbiologie Fondamentale et Pathogénicité, UMR 5234, F-33000 Bordeaux, France
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Pauline Esteves
bINSERM, Centre de Recherche Cardio-thoracique de Bordeaux, U1045, CIC 1401, Bordeaux, 33000, France
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Muriel Faure
aUniv. Bordeaux, CNRS, Microbiologie Fondamentale et Pathogénicité, UMR 5234, F-33000 Bordeaux, France
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Mathieu Métifiot
aUniv. Bordeaux, CNRS, Microbiologie Fondamentale et Pathogénicité, UMR 5234, F-33000 Bordeaux, France
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Sabrina Lacomme
cUniversity of Bordeaux, CNRS, Institute of Neurodegenerative Diseases, IINS, UMR 5293, Bordeaux, France, University of Bordeaux, CNRS, INSERM, Bordeaux Imaging Center, BIC, UMS 3420, US 4, Bordeaux, France
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Denis Dacheaux
aUniv. Bordeaux, CNRS, Microbiologie Fondamentale et Pathogénicité, UMR 5234, F-33000 Bordeaux, France
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Derrick Robinson
aUniv. Bordeaux, CNRS, Microbiologie Fondamentale et Pathogénicité, UMR 5234, F-33000 Bordeaux, France
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  • ORCID record for Derrick Robinson
Gernot Längst
dBiochemistry Center Regensburg, Universität Regensburg, Regensburg, Germany
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Fabien Beaufils
bINSERM, Centre de Recherche Cardio-thoracique de Bordeaux, U1045, CIC 1401, Bordeaux, 33000, France
eCHU de Bordeaux, Service d’exploration fonctionnelle respiratoire, service de pédiatrie médicale, CIC 1401, 33000, Bordeaux, France
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Marie-Edith Lafon
aUniv. Bordeaux, CNRS, Microbiologie Fondamentale et Pathogénicité, UMR 5234, F-33000 Bordeaux, France
fCHU de Bordeaux, Laboratoire de Virologie, 33000 Bordeaux, France
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Patrick Berger
bINSERM, Centre de Recherche Cardio-thoracique de Bordeaux, U1045, CIC 1401, Bordeaux, 33000, France
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Marc Landry
cUniversity of Bordeaux, CNRS, Institute of Neurodegenerative Diseases, IINS, UMR 5293, Bordeaux, France, University of Bordeaux, CNRS, INSERM, Bordeaux Imaging Center, BIC, UMS 3420, US 4, Bordeaux, France
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Denis Malvy
gDepartment for infectious and tropical d’idéales, University Hospital center Pellegrin, Bordeaux, & Inserm 1219, University of Bordeaux, Bordeaux, France
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Thomas Trian
bINSERM, Centre de Recherche Cardio-thoracique de Bordeaux, U1045, CIC 1401, Bordeaux, 33000, France
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Marie-Line Andreola
aUniv. Bordeaux, CNRS, Microbiologie Fondamentale et Pathogénicité, UMR 5234, F-33000 Bordeaux, France
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Harald Wodrich
aUniv. Bordeaux, CNRS, Microbiologie Fondamentale et Pathogénicité, UMR 5234, F-33000 Bordeaux, France
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  • ORCID record for Harald Wodrich
  • For correspondence: harald.wodrich@u-bordeaux.fr
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Abstract

The beta-coronavirus SARS-CoV-2 is at the origin of a persistent worldwide pandemic. SARS-CoV-2 infections initiate in the bronchi of the upper respiratory tract and are able to disseminate to the lower respiratory tract eventually causing acute severe respiratory syndrome with a high degree of mortality in the elderly. Here we use reconstituted primary bronchial epithelia from adult and children donors to follow the infection dynamic following infection with SARS-CoV-2. We show that in bronchial epithelia derived from adult donors, infections initiate in multi-ciliated cells. Then, infection rapidly spread within 24-48h throughout the whole epithelia. Within 3-4 days, large apical syncytia form between multi-ciliated cells and basal cells, which dissipate into the apical lumen. We show that these syncytia are a significant source of the released infectious dose. In stark contrast to these findings, bronchial epithelia reconstituted from children donors are intrinsically more resistant to virus infection and show active restriction of virus spread. This restriction is paired with accelerated release of IFN compared to adult donors. Taken together our findings reveal apical syncytia formation as an underappreciated source of infectious virus for either local dissemination or release into the environment. Furthermore, we provide direct evidence that children bronchial epithelia are more resistant to infection with SARS-CoV-2 providing experimental support for epidemiological observations that SARS-CoV-2 cases’ fatality is linked to age.

Significance Statement Bronchial epithelia are the primary target for SARS-CoV-2 infections. Our work uses reconstituted bronchial epithelia from adults and children. We show that infection of adult epithelia with SARS-CoV-2 is rapid and results in the synchronized release of large clusters of infected cells and syncytia into the apical lumen contributing to the released infectious virus dose. Infection of children derived bronchial epithelia revealed an intrinsic resistance to infection and virus spread, probably as a result of a faster onset of interferon secretion. Thus, our data provide direct evidence for the epidemiological observation that children are less susceptible to SARS-CoV-2.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted May 28, 2021.
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SARS-CoV-2 transmission via apical syncytia release from primary bronchial epithelia and infectivity restriction in children epithelia
Guillaume Beucher, Marie-Lise Blondot, Alexis Celle, Noémie Pied, Patricia Recordon-Pinson, Pauline Esteves, Muriel Faure, Mathieu Métifiot, Sabrina Lacomme, Denis Dacheaux, Derrick Robinson, Gernot Längst, Fabien Beaufils, Marie-Edith Lafon, Patrick Berger, Marc Landry, Denis Malvy, Thomas Trian, Marie-Line Andreola, Harald Wodrich
bioRxiv 2021.05.28.446159; doi: https://doi.org/10.1101/2021.05.28.446159
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SARS-CoV-2 transmission via apical syncytia release from primary bronchial epithelia and infectivity restriction in children epithelia
Guillaume Beucher, Marie-Lise Blondot, Alexis Celle, Noémie Pied, Patricia Recordon-Pinson, Pauline Esteves, Muriel Faure, Mathieu Métifiot, Sabrina Lacomme, Denis Dacheaux, Derrick Robinson, Gernot Längst, Fabien Beaufils, Marie-Edith Lafon, Patrick Berger, Marc Landry, Denis Malvy, Thomas Trian, Marie-Line Andreola, Harald Wodrich
bioRxiv 2021.05.28.446159; doi: https://doi.org/10.1101/2021.05.28.446159

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