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Global BioID-based SARS-CoV-2 proteins proximal interactome unveils novel ties between viral polypeptides and host factors involved in multiple COVID19-associated mechanisms

Estelle M.N. Laurent, Yorgos Sofianatos, Anastassia Komarova, Jean-Pascal Gimeno, Payman Samavarchi Tehrani, Dae-Kyum Kim, Hala Abdouni, Marie Duhamel, Patricia Cassonnet, Jennifer J. Knapp, Da Kuang, Aditya Chawla, Dayag Sheykhkarimli, Ashyad Rayhan, Roujia Li, Oxana Pogoutse, David E. Hill, Michael A. Calderwood, Pascal Falter-Braun, Patrick Aloy, Ulrich Stelzl, Marc Vidal, Anne-Claude Gingras, Georgios A. Pavlopoulos, Sylvie Van Der Werf, Isabelle Fournier, Frederick P. Roth, View ORCID ProfileMichel Salzet, Caroline Demeret, Yves Jacob, Etienne Coyaud
doi: https://doi.org/10.1101/2020.08.28.272955
Estelle M.N. Laurent
1Univ. Lille, Inserm, CHU Lille, U1192 - Protéomique Réponse Inflammatoire Spectrométrie de Masse - PRISM, F-59000 Lille, France
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Yorgos Sofianatos
2Institute for Fundamental Biomedical Research, BSRC “Alexander Fleming”, 34 Fleming Street, 16672, Vari, Greece
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  • For correspondence: yorgos@fleming.gr michel.salzet@univ-lille.fr caroline.demeret@pasteur.fr yves.jacob@pasteur.fr etienne.coyaud@inserm.fr
Anastassia Komarova
3Département de Virologie, Unité de Génétique Moléculaire des Virus à ARN (GMVR), Institut Pasteur, UMR3569, Centre National de la Recherche Scientifique (CNRS), Université Paris Diderot, Sorbonne Paris Cité, 28 rue du Docteur Roux, 75015, Paris, France
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Jean-Pascal Gimeno
1Univ. Lille, Inserm, CHU Lille, U1192 - Protéomique Réponse Inflammatoire Spectrométrie de Masse - PRISM, F-59000 Lille, France
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Payman Samavarchi Tehrani
4Lunenfeld-Tanenbaum Research Institute, Sinai Health System, Toronto, ON, Canada
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Dae-Kyum Kim
4Lunenfeld-Tanenbaum Research Institute, Sinai Health System, Toronto, ON, Canada
5Donnelly Centre and Departments of Molecular Genetics and Computer Science, University of Toronto and Lunenfeld-Tanenbaum Research Institute, Sinai Health System, Toronto, ON M5G 1X5, Canada
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Hala Abdouni
4Lunenfeld-Tanenbaum Research Institute, Sinai Health System, Toronto, ON, Canada
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Marie Duhamel
1Univ. Lille, Inserm, CHU Lille, U1192 - Protéomique Réponse Inflammatoire Spectrométrie de Masse - PRISM, F-59000 Lille, France
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Patricia Cassonnet
3Département de Virologie, Unité de Génétique Moléculaire des Virus à ARN (GMVR), Institut Pasteur, UMR3569, Centre National de la Recherche Scientifique (CNRS), Université Paris Diderot, Sorbonne Paris Cité, 28 rue du Docteur Roux, 75015, Paris, France
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Jennifer J. Knapp
4Lunenfeld-Tanenbaum Research Institute, Sinai Health System, Toronto, ON, Canada
5Donnelly Centre and Departments of Molecular Genetics and Computer Science, University of Toronto and Lunenfeld-Tanenbaum Research Institute, Sinai Health System, Toronto, ON M5G 1X5, Canada
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Da Kuang
4Lunenfeld-Tanenbaum Research Institute, Sinai Health System, Toronto, ON, Canada
5Donnelly Centre and Departments of Molecular Genetics and Computer Science, University of Toronto and Lunenfeld-Tanenbaum Research Institute, Sinai Health System, Toronto, ON M5G 1X5, Canada
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Aditya Chawla
4Lunenfeld-Tanenbaum Research Institute, Sinai Health System, Toronto, ON, Canada
5Donnelly Centre and Departments of Molecular Genetics and Computer Science, University of Toronto and Lunenfeld-Tanenbaum Research Institute, Sinai Health System, Toronto, ON M5G 1X5, Canada
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Dayag Sheykhkarimli
4Lunenfeld-Tanenbaum Research Institute, Sinai Health System, Toronto, ON, Canada
5Donnelly Centre and Departments of Molecular Genetics and Computer Science, University of Toronto and Lunenfeld-Tanenbaum Research Institute, Sinai Health System, Toronto, ON M5G 1X5, Canada
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Ashyad Rayhan
4Lunenfeld-Tanenbaum Research Institute, Sinai Health System, Toronto, ON, Canada
5Donnelly Centre and Departments of Molecular Genetics and Computer Science, University of Toronto and Lunenfeld-Tanenbaum Research Institute, Sinai Health System, Toronto, ON M5G 1X5, Canada
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Roujia Li
4Lunenfeld-Tanenbaum Research Institute, Sinai Health System, Toronto, ON, Canada
5Donnelly Centre and Departments of Molecular Genetics and Computer Science, University of Toronto and Lunenfeld-Tanenbaum Research Institute, Sinai Health System, Toronto, ON M5G 1X5, Canada
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Oxana Pogoutse
4Lunenfeld-Tanenbaum Research Institute, Sinai Health System, Toronto, ON, Canada
5Donnelly Centre and Departments of Molecular Genetics and Computer Science, University of Toronto and Lunenfeld-Tanenbaum Research Institute, Sinai Health System, Toronto, ON M5G 1X5, Canada
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David E. Hill
6Center for Cancer Systems Biology (CCSB) and Department of Cancer Biology, Dana-Farber Cancer Institute, Boston, MA 02215, USA; Department of Genetics, Blavatnik Institute, Harvard Medical School, Boston, MA 02115, USA
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Michael A. Calderwood
6Center for Cancer Systems Biology (CCSB) and Department of Cancer Biology, Dana-Farber Cancer Institute, Boston, MA 02215, USA; Department of Genetics, Blavatnik Institute, Harvard Medical School, Boston, MA 02115, USA
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Pascal Falter-Braun
7Institute of Network Biology (INET), Helmholtz Center Munich, German Research Center for Environmental Health, Munich-Neuherberg, Germany and Microbe-Host Interactions, Faculty of Biology, Ludwig-Maximilians-Universität (LMU) München, Planegg-Martinsried, Germany
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Patrick Aloy
8Institute for Research in Biomedicine (IRB Barcelona), The Barcelona Institute of Science and Technology, Baldiri Reixac 10-12, 08020 Barcelona, Catalonia, Spain
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Ulrich Stelzl
9Department of Pharmaceutical Chemistry, Institute of Pharmaceutical Sciences, University of Graz and BioTechMed-Graz, Graz, Austria
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Marc Vidal
6Center for Cancer Systems Biology (CCSB) and Department of Cancer Biology, Dana-Farber Cancer Institute, Boston, MA 02215, USA; Department of Genetics, Blavatnik Institute, Harvard Medical School, Boston, MA 02115, USA
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Anne-Claude Gingras
4Lunenfeld-Tanenbaum Research Institute, Sinai Health System, Toronto, ON, Canada
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Georgios A. Pavlopoulos
2Institute for Fundamental Biomedical Research, BSRC “Alexander Fleming”, 34 Fleming Street, 16672, Vari, Greece
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Sylvie Van Der Werf
3Département de Virologie, Unité de Génétique Moléculaire des Virus à ARN (GMVR), Institut Pasteur, UMR3569, Centre National de la Recherche Scientifique (CNRS), Université Paris Diderot, Sorbonne Paris Cité, 28 rue du Docteur Roux, 75015, Paris, France
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Isabelle Fournier
1Univ. Lille, Inserm, CHU Lille, U1192 - Protéomique Réponse Inflammatoire Spectrométrie de Masse - PRISM, F-59000 Lille, France
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Frederick P. Roth
4Lunenfeld-Tanenbaum Research Institute, Sinai Health System, Toronto, ON, Canada
5Donnelly Centre and Departments of Molecular Genetics and Computer Science, University of Toronto and Lunenfeld-Tanenbaum Research Institute, Sinai Health System, Toronto, ON M5G 1X5, Canada
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Michel Salzet
1Univ. Lille, Inserm, CHU Lille, U1192 - Protéomique Réponse Inflammatoire Spectrométrie de Masse - PRISM, F-59000 Lille, France
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  • ORCID record for Michel Salzet
  • For correspondence: yorgos@fleming.gr michel.salzet@univ-lille.fr caroline.demeret@pasteur.fr yves.jacob@pasteur.fr etienne.coyaud@inserm.fr
Caroline Demeret
3Département de Virologie, Unité de Génétique Moléculaire des Virus à ARN (GMVR), Institut Pasteur, UMR3569, Centre National de la Recherche Scientifique (CNRS), Université Paris Diderot, Sorbonne Paris Cité, 28 rue du Docteur Roux, 75015, Paris, France
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  • For correspondence: yorgos@fleming.gr michel.salzet@univ-lille.fr caroline.demeret@pasteur.fr yves.jacob@pasteur.fr etienne.coyaud@inserm.fr
Yves Jacob
3Département de Virologie, Unité de Génétique Moléculaire des Virus à ARN (GMVR), Institut Pasteur, UMR3569, Centre National de la Recherche Scientifique (CNRS), Université Paris Diderot, Sorbonne Paris Cité, 28 rue du Docteur Roux, 75015, Paris, France
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  • For correspondence: yorgos@fleming.gr michel.salzet@univ-lille.fr caroline.demeret@pasteur.fr yves.jacob@pasteur.fr etienne.coyaud@inserm.fr
Etienne Coyaud
1Univ. Lille, Inserm, CHU Lille, U1192 - Protéomique Réponse Inflammatoire Spectrométrie de Masse - PRISM, F-59000 Lille, France
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  • For correspondence: yorgos@fleming.gr michel.salzet@univ-lille.fr caroline.demeret@pasteur.fr yves.jacob@pasteur.fr etienne.coyaud@inserm.fr
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Abstract

The worldwide SARS-CoV-2 outbreak poses a serious challenge to human societies and economies. SARS-CoV-2 proteins orchestrate complex pathogenic mechanisms that underlie COVID-19 disease. Thus, understanding how viral polypeptides rewire host protein networks enables better-founded therapeutic research. In complement to existing proteomic studies, in this study we define the first proximal interaction network of SARS-CoV-2 proteins, at the whole proteome level in human cells. Applying a proximity-dependent biotinylation (BioID)-based approach greatly expanded the current knowledge by detecting interactions within poorly soluble compartments, transient, and/or of weak affinity in living cells. Our BioID study was complemented by a stringent filtering and uncovered 2,128 unique cellular targets (1,717 not previously associated with SARS-CoV-1 or 2 proteins) connected to the N- and C-ter BioID-tagged 28 SARS-CoV-2 proteins by a total of 5,415 (5,236 new) proximal interactions. In order to facilitate data exploitation, an innovative interactive 3D web interface was developed to allow customized analysis and exploration of the landscape of interactions (accessible at http://www.sars-cov-2-interactome.org/). Interestingly, 342 membrane proteins including interferon and interleukin pathways factors, were associated with specific viral proteins. We uncovered ORF7a and ORF7b protein proximal partners that could be related to anosmia and ageusia symptoms. Moreover, comparing proximal interactomes in basal and infection-mimicking conditions (poly(I:C) treatment) allowed us to detect novel links with major antiviral response pathway components, such as ORF9b with MAVS and ISG20; N with PKR and TARB2; NSP2 with RIG-I and STAT1; NSP16 with PARP9-DTX3L. Altogether, our study provides an unprecedented comprehensive resource for understanding how SARS-CoV-2 proteins orchestrate host proteome remodeling and innate immune response evasion, which can inform development of targeted therapeutic strategies.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • http://www.sars-cov-2-interactome.org/

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC 4.0 International license.
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Global BioID-based SARS-CoV-2 proteins proximal interactome unveils novel ties between viral polypeptides and host factors involved in multiple COVID19-associated mechanisms
Estelle M.N. Laurent, Yorgos Sofianatos, Anastassia Komarova, Jean-Pascal Gimeno, Payman Samavarchi Tehrani, Dae-Kyum Kim, Hala Abdouni, Marie Duhamel, Patricia Cassonnet, Jennifer J. Knapp, Da Kuang, Aditya Chawla, Dayag Sheykhkarimli, Ashyad Rayhan, Roujia Li, Oxana Pogoutse, David E. Hill, Michael A. Calderwood, Pascal Falter-Braun, Patrick Aloy, Ulrich Stelzl, Marc Vidal, Anne-Claude Gingras, Georgios A. Pavlopoulos, Sylvie Van Der Werf, Isabelle Fournier, Frederick P. Roth, Michel Salzet, Caroline Demeret, Yves Jacob, Etienne Coyaud
bioRxiv 2020.08.28.272955; doi: https://doi.org/10.1101/2020.08.28.272955
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Global BioID-based SARS-CoV-2 proteins proximal interactome unveils novel ties between viral polypeptides and host factors involved in multiple COVID19-associated mechanisms
Estelle M.N. Laurent, Yorgos Sofianatos, Anastassia Komarova, Jean-Pascal Gimeno, Payman Samavarchi Tehrani, Dae-Kyum Kim, Hala Abdouni, Marie Duhamel, Patricia Cassonnet, Jennifer J. Knapp, Da Kuang, Aditya Chawla, Dayag Sheykhkarimli, Ashyad Rayhan, Roujia Li, Oxana Pogoutse, David E. Hill, Michael A. Calderwood, Pascal Falter-Braun, Patrick Aloy, Ulrich Stelzl, Marc Vidal, Anne-Claude Gingras, Georgios A. Pavlopoulos, Sylvie Van Der Werf, Isabelle Fournier, Frederick P. Roth, Michel Salzet, Caroline Demeret, Yves Jacob, Etienne Coyaud
bioRxiv 2020.08.28.272955; doi: https://doi.org/10.1101/2020.08.28.272955

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