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STAT2 signaling as double-edged sword restricting viral dissemination but driving severe pneumonia in SARS-CoV-2 infected hamsters

View ORCID ProfileRobbert Boudewijns, View ORCID ProfileHendrik Jan Thibaut, View ORCID ProfileSuzanne J. F. Kaptein, View ORCID ProfileRong Li, View ORCID ProfileValentijn Vergote, View ORCID ProfileLaura Seldeslachts, Carolien De Keyzer, Lindsey Bervoets, View ORCID ProfileSapna Sharma, View ORCID ProfileJohan Van Weyenbergh, Laurens Liesenborghs, View ORCID ProfileJi Ma, View ORCID ProfileSander Jansen, Dominique Van Looveren, Thomas Vercruysse, Dirk Jochmans, Xinyu Wang, View ORCID ProfileErik Martens, Kenny Roose, Dorien De Vlieger, Bert Schepens, Tina Van Buyten, View ORCID ProfileSofie Jacobs, Yanan Liu, View ORCID ProfileJoan Martí-Carreras, Bert Vanmechelen, View ORCID ProfileTony Wawina-Bokalanga, View ORCID ProfileLeen Delang, View ORCID ProfileJoana Rocha-Pereira, View ORCID ProfileLotte Coelmont, View ORCID ProfileWinston Chiu, View ORCID ProfilePieter Leyssen, View ORCID ProfileElisabeth Heylen, View ORCID ProfileDominique Schols, Lanjiao Wang, Lila Close, View ORCID ProfileJelle Matthijnssens, View ORCID ProfileMarc Van Ranst, Veerle Compernolle, View ORCID ProfileGeorg Schramm, View ORCID ProfileKoen Van Laere, Xavier Saelens, Nico Callewaert, View ORCID ProfileGhislain Opdenakker, View ORCID ProfilePiet Maes, View ORCID ProfileBirgit Weynand, View ORCID ProfileChristopher Cawthorne, View ORCID ProfileGreetje Vande Velde, View ORCID ProfileZhongde Wang, View ORCID ProfileJohan Neyts, View ORCID ProfileKai Dallmeier
doi: https://doi.org/10.1101/2020.04.23.056838
Robbert Boudewijns
1KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Virology and Chemotherapy, BE-3000 Leuven, Belgium
2Molecular Vaccinology and Vaccine Discovery Group
18GVN, Global Virus Network
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Hendrik Jan Thibaut
1KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Virology and Chemotherapy, BE-3000 Leuven, Belgium
3Translational Platform Virology and Chemotherapy
18GVN, Global Virus Network
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  • For correspondence: kai.dallmeier@kuleuven.be hendrikjan.thibaut@kuleuven.be johan.neyts@kuleuven.be
Suzanne J. F. Kaptein
1KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Virology and Chemotherapy, BE-3000 Leuven, Belgium
18GVN, Global Virus Network
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Rong Li
4Department of Animal, Dairy, and Veterinary Sciences, Utah State University, UT 84322-4815 Logan, Utah, United States of America
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Valentijn Vergote
1KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Virology and Chemotherapy, BE-3000 Leuven, Belgium
5KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Clinical and Epidemiological Virology, BE-3000 Leuven, Belgium
6Zoonotic Infectious Diseases Unit
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Laura Seldeslachts
9KU Leuven Department of Imaging and Pathology, Biomedical MRI and MoSAIC, BE-3000 Leuven, Belgium
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Carolien De Keyzer
1KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Virology and Chemotherapy, BE-3000 Leuven, Belgium
2Molecular Vaccinology and Vaccine Discovery Group
18GVN, Global Virus Network
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Lindsey Bervoets
1KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Virology and Chemotherapy, BE-3000 Leuven, Belgium
18GVN, Global Virus Network
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Sapna Sharma
1KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Virology and Chemotherapy, BE-3000 Leuven, Belgium
2Molecular Vaccinology and Vaccine Discovery Group
18GVN, Global Virus Network
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Johan Van Weyenbergh
5KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Clinical and Epidemiological Virology, BE-3000 Leuven, Belgium
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Laurens Liesenborghs
1KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Virology and Chemotherapy, BE-3000 Leuven, Belgium
2Molecular Vaccinology and Vaccine Discovery Group
18GVN, Global Virus Network
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Ji Ma
1KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Virology and Chemotherapy, BE-3000 Leuven, Belgium
2Molecular Vaccinology and Vaccine Discovery Group
18GVN, Global Virus Network
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Sander Jansen
1KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Virology and Chemotherapy, BE-3000 Leuven, Belgium
2Molecular Vaccinology and Vaccine Discovery Group
18GVN, Global Virus Network
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Dominique Van Looveren
1KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Virology and Chemotherapy, BE-3000 Leuven, Belgium
3Translational Platform Virology and Chemotherapy
18GVN, Global Virus Network
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Thomas Vercruysse
1KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Virology and Chemotherapy, BE-3000 Leuven, Belgium
3Translational Platform Virology and Chemotherapy
18GVN, Global Virus Network
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Dirk Jochmans
1KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Virology and Chemotherapy, BE-3000 Leuven, Belgium
2Molecular Vaccinology and Vaccine Discovery Group
18GVN, Global Virus Network
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Xinyu Wang
1KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Virology and Chemotherapy, BE-3000 Leuven, Belgium
2Molecular Vaccinology and Vaccine Discovery Group
18GVN, Global Virus Network
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Erik Martens
13KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute, Immunity and Inflammation Research Group, Immunobiology Unit, BE-3000 Leuven, Belgium
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Kenny Roose
19VIB-UGent Center for Medical Biotechnology, VIB, 9052 Ghent, Belgium
20Department of Biochemistry and Microbiology, Ghent University, 9052 Ghent, Belgium
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Dorien De Vlieger
19VIB-UGent Center for Medical Biotechnology, VIB, 9052 Ghent, Belgium
20Department of Biochemistry and Microbiology, Ghent University, 9052 Ghent, Belgium
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Bert Schepens
19VIB-UGent Center for Medical Biotechnology, VIB, 9052 Ghent, Belgium
20Department of Biochemistry and Microbiology, Ghent University, 9052 Ghent, Belgium
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Tina Van Buyten
1KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Virology and Chemotherapy, BE-3000 Leuven, Belgium
18GVN, Global Virus Network
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Sofie Jacobs
1KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Virology and Chemotherapy, BE-3000 Leuven, Belgium
18GVN, Global Virus Network
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Yanan Liu
4Department of Animal, Dairy, and Veterinary Sciences, Utah State University, UT 84322-4815 Logan, Utah, United States of America
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Joan Martí-Carreras
5KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Clinical and Epidemiological Virology, BE-3000 Leuven, Belgium
6Zoonotic Infectious Diseases Unit
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Bert Vanmechelen
5KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Clinical and Epidemiological Virology, BE-3000 Leuven, Belgium
6Zoonotic Infectious Diseases Unit
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Tony Wawina-Bokalanga
5KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Clinical and Epidemiological Virology, BE-3000 Leuven, Belgium
6Zoonotic Infectious Diseases Unit
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Leen Delang
1KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Virology and Chemotherapy, BE-3000 Leuven, Belgium
18GVN, Global Virus Network
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Joana Rocha-Pereira
1KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Virology and Chemotherapy, BE-3000 Leuven, Belgium
18GVN, Global Virus Network
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Lotte Coelmont
1KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Virology and Chemotherapy, BE-3000 Leuven, Belgium
2Molecular Vaccinology and Vaccine Discovery Group
18GVN, Global Virus Network
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Winston Chiu
1KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Virology and Chemotherapy, BE-3000 Leuven, Belgium
18GVN, Global Virus Network
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Pieter Leyssen
1KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Virology and Chemotherapy, BE-3000 Leuven, Belgium
18GVN, Global Virus Network
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Elisabeth Heylen
1KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Virology and Chemotherapy, BE-3000 Leuven, Belgium
18GVN, Global Virus Network
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Dominique Schols
1KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Virology and Chemotherapy, BE-3000 Leuven, Belgium
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  • ORCID record for Dominique Schols
Lanjiao Wang
1KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Virology and Chemotherapy, BE-3000 Leuven, Belgium
18GVN, Global Virus Network
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Lila Close
5KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Clinical and Epidemiological Virology, BE-3000 Leuven, Belgium
7Laboratory of Viral Metagenomics
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Jelle Matthijnssens
5KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Clinical and Epidemiological Virology, BE-3000 Leuven, Belgium
7Laboratory of Viral Metagenomics
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Marc Van Ranst
5KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Clinical and Epidemiological Virology, BE-3000 Leuven, Belgium
14KU Leuven Department of Laboratory Medicine, University Hospitals Leuven, BE-3000 Leuven, Belgium
15National Reference Center for Respiratory Pathogens and Enteroviruses, BE-3000 Leuven, Belgium
16Leuven University Vaccinology Center (LUVAC), 3000 Leuven, Belgium
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Veerle Compernolle
21Blood Service, Belgian Red Cross Flanders, Mechelen, Belgium
22Faculty of Medicine and Health Sciences, Ghent University, Ghent, Belgium
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Georg Schramm
10KU Leuven Department of Imaging and Pathology, Nuclear Medicine and Molecular Imaging and MoSAIC, BE-3000 Leuven, Belgium
11Division of Nuclear Medicine, University Hospitals Leuven, BE-3000 Leuven, Belgium
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Koen Van Laere
10KU Leuven Department of Imaging and Pathology, Nuclear Medicine and Molecular Imaging and MoSAIC, BE-3000 Leuven, Belgium
11Division of Nuclear Medicine, University Hospitals Leuven, BE-3000 Leuven, Belgium
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Xavier Saelens
19VIB-UGent Center for Medical Biotechnology, VIB, 9052 Ghent, Belgium
20Department of Biochemistry and Microbiology, Ghent University, 9052 Ghent, Belgium
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Nico Callewaert
19VIB-UGent Center for Medical Biotechnology, VIB, 9052 Ghent, Belgium
20Department of Biochemistry and Microbiology, Ghent University, 9052 Ghent, Belgium
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Ghislain Opdenakker
13KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute, Immunity and Inflammation Research Group, Immunobiology Unit, BE-3000 Leuven, Belgium
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Piet Maes
5KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Clinical and Epidemiological Virology, BE-3000 Leuven, Belgium
6Zoonotic Infectious Diseases Unit
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Birgit Weynand
8KU Leuven Department of Imaging and Pathology, Translational Cell and Tissue Research, BE-3000 Leuven, Belgium
12Division of Translational Cell and Tissue Research
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Christopher Cawthorne
10KU Leuven Department of Imaging and Pathology, Nuclear Medicine and Molecular Imaging and MoSAIC, BE-3000 Leuven, Belgium
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Greetje Vande Velde
9KU Leuven Department of Imaging and Pathology, Biomedical MRI and MoSAIC, BE-3000 Leuven, Belgium
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  • ORCID record for Greetje Vande Velde
Zhongde Wang
4Department of Animal, Dairy, and Veterinary Sciences, Utah State University, UT 84322-4815 Logan, Utah, United States of America
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Johan Neyts
1KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Virology and Chemotherapy, BE-3000 Leuven, Belgium
2Molecular Vaccinology and Vaccine Discovery Group
18GVN, Global Virus Network
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  • For correspondence: kai.dallmeier@kuleuven.be hendrikjan.thibaut@kuleuven.be johan.neyts@kuleuven.be
Kai Dallmeier
1KU Leuven Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory of Virology and Chemotherapy, BE-3000 Leuven, Belgium
2Molecular Vaccinology and Vaccine Discovery Group
18GVN, Global Virus Network
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  • ORCID record for Kai Dallmeier
  • For correspondence: kai.dallmeier@kuleuven.be hendrikjan.thibaut@kuleuven.be johan.neyts@kuleuven.be
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Introductory paragraph

Since the emergence of SARS-CoV-2 causing COVID-19, the world is being shaken to its core with numerous hospitalizations and hundreds of thousands of deaths. In search for key targets of effective therapeutics, robust animal models mimicking COVID-19 in humans are urgently needed. Here, we show that productive SARS-CoV-2 infection in the lungs of mice is limited and restricted by early type I interferon responses. In contrast, we show that Syrian hamsters are highly permissive to SARS- CoV-2 and develop bronchopneumonia and a strong inflammatory response in the lungs with neutrophil infiltration and edema. Moreover, we identify an exuberant innate immune response as a key player in pathogenesis, in which STAT2 signaling plays a dual role, driving severe lung injury on the one hand, yet restricting systemic virus dissemination on the other. Finally, we assess SARS-CoV- 2-induced lung pathology in hamsters by micro-CT alike used in clinical practice. Our results reveal the importance of STAT2-dependent interferon responses in the pathogenesis and virus control during SARS-CoV-2 infection and may help rationalizing new strategies for the treatment of COVID-19 patients.

Competing Interest Statement

D.D.V., B.S., and X.S. are named as inventors on US patent application no. 62/988,610, entitled 'Coronavirus Binders'. D.D.V., B.S., X.S., and N.C. are named as inventors on US patent application no. 62/991,408, entitled 'SARS-CoV-2 Virus Binders'.

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  • ↵& Co-senior authors

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STAT2 signaling as double-edged sword restricting viral dissemination but driving severe pneumonia in SARS-CoV-2 infected hamsters
Robbert Boudewijns, Hendrik Jan Thibaut, Suzanne J. F. Kaptein, Rong Li, Valentijn Vergote, Laura Seldeslachts, Carolien De Keyzer, Lindsey Bervoets, Sapna Sharma, Johan Van Weyenbergh, Laurens Liesenborghs, Ji Ma, Sander Jansen, Dominique Van Looveren, Thomas Vercruysse, Dirk Jochmans, Xinyu Wang, Erik Martens, Kenny Roose, Dorien De Vlieger, Bert Schepens, Tina Van Buyten, Sofie Jacobs, Yanan Liu, Joan Martí-Carreras, Bert Vanmechelen, Tony Wawina-Bokalanga, Leen Delang, Joana Rocha-Pereira, Lotte Coelmont, Winston Chiu, Pieter Leyssen, Elisabeth Heylen, Dominique Schols, Lanjiao Wang, Lila Close, Jelle Matthijnssens, Marc Van Ranst, Veerle Compernolle, Georg Schramm, Koen Van Laere, Xavier Saelens, Nico Callewaert, Ghislain Opdenakker, Piet Maes, Birgit Weynand, Christopher Cawthorne, Greetje Vande Velde, Zhongde Wang, Johan Neyts, Kai Dallmeier
bioRxiv 2020.04.23.056838; doi: https://doi.org/10.1101/2020.04.23.056838
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STAT2 signaling as double-edged sword restricting viral dissemination but driving severe pneumonia in SARS-CoV-2 infected hamsters
Robbert Boudewijns, Hendrik Jan Thibaut, Suzanne J. F. Kaptein, Rong Li, Valentijn Vergote, Laura Seldeslachts, Carolien De Keyzer, Lindsey Bervoets, Sapna Sharma, Johan Van Weyenbergh, Laurens Liesenborghs, Ji Ma, Sander Jansen, Dominique Van Looveren, Thomas Vercruysse, Dirk Jochmans, Xinyu Wang, Erik Martens, Kenny Roose, Dorien De Vlieger, Bert Schepens, Tina Van Buyten, Sofie Jacobs, Yanan Liu, Joan Martí-Carreras, Bert Vanmechelen, Tony Wawina-Bokalanga, Leen Delang, Joana Rocha-Pereira, Lotte Coelmont, Winston Chiu, Pieter Leyssen, Elisabeth Heylen, Dominique Schols, Lanjiao Wang, Lila Close, Jelle Matthijnssens, Marc Van Ranst, Veerle Compernolle, Georg Schramm, Koen Van Laere, Xavier Saelens, Nico Callewaert, Ghislain Opdenakker, Piet Maes, Birgit Weynand, Christopher Cawthorne, Greetje Vande Velde, Zhongde Wang, Johan Neyts, Kai Dallmeier
bioRxiv 2020.04.23.056838; doi: https://doi.org/10.1101/2020.04.23.056838

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