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Global analysis of protein-RNA interactions in SARS-CoV-2 infected cells reveals key regulators of infection

View ORCID ProfileWael Kamel, View ORCID ProfileMarko Noerenberg, Berati Cerikan, Honglin Chen, Aino I. Järvelin, Mohamed Kammoun, Jeff Lee, Ni Shuai, Manuel Garcia-Moreno, Anja Andrejeva, Michael J. Deery, Christopher J. Neufeldt, Mirko Cortese, View ORCID ProfileMichael L. Knight, View ORCID ProfileKathryn S. Lilley, View ORCID ProfileJavier Martinez, View ORCID ProfileIlan Davis, View ORCID ProfileRalf Bartenschlager, View ORCID ProfileShabaz Mohammed, View ORCID ProfileAlfredo Castello
doi: https://doi.org/10.1101/2020.11.25.398008
Wael Kamel
1MRC-University of Glasgow Centre for Virus Research, 464 Bearsden Road, Glasgow G61 1QH, Scotland (UK)
2Department of Biochemistry, University of Oxford, South Parks road, OX1 3QU, Oxford, UK
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  • ORCID record for Wael Kamel
Marko Noerenberg
1MRC-University of Glasgow Centre for Virus Research, 464 Bearsden Road, Glasgow G61 1QH, Scotland (UK)
2Department of Biochemistry, University of Oxford, South Parks road, OX1 3QU, Oxford, UK
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Berati Cerikan
3Department of Infectious Diseases, Molecular Virology, Heidelberg University, 69120 Heidelberg, Germany
4German Center for Infection Research, Heidelberg Partner Site, 69120 Heidelberg, Germany
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Honglin Chen
2Department of Biochemistry, University of Oxford, South Parks road, OX1 3QU, Oxford, UK
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Aino I. Järvelin
2Department of Biochemistry, University of Oxford, South Parks road, OX1 3QU, Oxford, UK
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Mohamed Kammoun
5German Cancer Research Center (DKFZ), 69120 Heidelberg, Germany
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Jeff Lee
2Department of Biochemistry, University of Oxford, South Parks road, OX1 3QU, Oxford, UK
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Ni Shuai
5German Cancer Research Center (DKFZ), 69120 Heidelberg, Germany
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Manuel Garcia-Moreno
2Department of Biochemistry, University of Oxford, South Parks road, OX1 3QU, Oxford, UK
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Anja Andrejeva
7Department of Biochemistry, University of Cambridge, 80 Tennis Court Road, Cambridge CB2 1GA
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Michael J. Deery
7Department of Biochemistry, University of Cambridge, 80 Tennis Court Road, Cambridge CB2 1GA
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Christopher J. Neufeldt
3Department of Infectious Diseases, Molecular Virology, Heidelberg University, 69120 Heidelberg, Germany
4German Center for Infection Research, Heidelberg Partner Site, 69120 Heidelberg, Germany
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Mirko Cortese
3Department of Infectious Diseases, Molecular Virology, Heidelberg University, 69120 Heidelberg, Germany
4German Center for Infection Research, Heidelberg Partner Site, 69120 Heidelberg, Germany
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Michael L. Knight
6Sir William Dunn School of Pathology, University of Oxford, South Parks road, OX1 3RE, Oxford, UK
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Kathryn S. Lilley
7Department of Biochemistry, University of Cambridge, 80 Tennis Court Road, Cambridge CB2 1GA
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Javier Martinez
8Center of Medical Biochemistry, Max Perutz Labs, Medical University of Vienna, Dr. Bohr-Gasse 9/2, 1030, Vienna, Austria
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Ilan Davis
2Department of Biochemistry, University of Oxford, South Parks road, OX1 3QU, Oxford, UK
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Ralf Bartenschlager
3Department of Infectious Diseases, Molecular Virology, Heidelberg University, 69120 Heidelberg, Germany
4German Center for Infection Research, Heidelberg Partner Site, 69120 Heidelberg, Germany
10Division Virus-Associated Carcinogenesis, Germany Cancer Research Center (DKFZ), 69120 Heidelberg, Germany
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  • For correspondence: alfredo.castello@glasgow.ac.uk shabaz.mohammed@chem.ox.ac.uk Ralf.Bartenschlager@med.uni-heidelberg.de
Shabaz Mohammed
2Department of Biochemistry, University of Oxford, South Parks road, OX1 3QU, Oxford, UK
9Department of Chemistry, Chemistry Research Laboratory, Mansfield Road, Oxford, OX1 3TA, UK
11The Rosalind Franklin Institute, Oxfordshire, OX11 0FA, UK
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  • For correspondence: alfredo.castello@glasgow.ac.uk shabaz.mohammed@chem.ox.ac.uk Ralf.Bartenschlager@med.uni-heidelberg.de
Alfredo Castello
1MRC-University of Glasgow Centre for Virus Research, 464 Bearsden Road, Glasgow G61 1QH, Scotland (UK)
2Department of Biochemistry, University of Oxford, South Parks road, OX1 3QU, Oxford, UK
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  • ORCID record for Alfredo Castello
  • For correspondence: alfredo.castello@glasgow.ac.uk shabaz.mohammed@chem.ox.ac.uk Ralf.Bartenschlager@med.uni-heidelberg.de
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ABSTRACT

Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) causes COVID-19. SARS-CoV-2 relies on cellular RNA-binding proteins (RBPs) to replicate and spread, although which RBPs control SARS-CoV-2 infection remains largely unknown. Here, we employ a multi-omic approach to identify systematically and comprehensively which cellular and viral RBPs are involved in SARS-CoV-2 infection. We reveal that the cellular RNA-bound proteome is remodelled upon SARS-CoV-2 infection, having widespread effects on RNA metabolic pathways, non-canonical RBPs and antiviral factors. Moreover, we apply a new method to identify the proteins that directly interact with viral RNA, uncovering dozens of cellular RBPs and seven viral proteins. Amongst them, several components of the tRNA ligase complex, which we show regulate SARS-CoV-2 infection. Furthermore, we discover that available drugs targeting host RBPs that interact with SARS-CoV-2 RNA inhibit infection. Collectively, our results uncover a new universe of host-virus interactions with potential for new antiviral therapies against COVID-19.

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 November 25, 2020.
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Global analysis of protein-RNA interactions in SARS-CoV-2 infected cells reveals key regulators of infection
Wael Kamel, Marko Noerenberg, Berati Cerikan, Honglin Chen, Aino I. Järvelin, Mohamed Kammoun, Jeff Lee, Ni Shuai, Manuel Garcia-Moreno, Anja Andrejeva, Michael J. Deery, Christopher J. Neufeldt, Mirko Cortese, Michael L. Knight, Kathryn S. Lilley, Javier Martinez, Ilan Davis, Ralf Bartenschlager, Shabaz Mohammed, Alfredo Castello
bioRxiv 2020.11.25.398008; doi: https://doi.org/10.1101/2020.11.25.398008
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Global analysis of protein-RNA interactions in SARS-CoV-2 infected cells reveals key regulators of infection
Wael Kamel, Marko Noerenberg, Berati Cerikan, Honglin Chen, Aino I. Järvelin, Mohamed Kammoun, Jeff Lee, Ni Shuai, Manuel Garcia-Moreno, Anja Andrejeva, Michael J. Deery, Christopher J. Neufeldt, Mirko Cortese, Michael L. Knight, Kathryn S. Lilley, Javier Martinez, Ilan Davis, Ralf Bartenschlager, Shabaz Mohammed, Alfredo Castello
bioRxiv 2020.11.25.398008; doi: https://doi.org/10.1101/2020.11.25.398008

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