SARS-CoV-2 Mac1 is required for IFN antagonism and efficient virus replication in cell culture and in mice

This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas. 2302083120/-/DCSupplemental.

Detalles Bibliográficos
Autores: Alhammad, Yousef M., Parthasarathy, Srivatsan, Ghimire, Roshan, Kerr, Catherine M., O'Connor, Joseph J., Pfannenstiel, Jessica J., Chanda, Debarati, Miller, Caden A., Baumlin, Nathalie, Salathe, Matthias, Unckless, Robert L., Zúñiga Lucas, Sonia, Enjuanes Sánchez, Luis, More, Sunil, Channappanavar, Rudragouda, Fehr, Anthony R.
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2023
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/363879
Acceso en línea:http://hdl.handle.net/10261/363879
https://api.elsevier.com/content/abstract/scopus_id/85168781208
Access Level:acceso abierto
Palabra clave:ADP-ribosylation
SARS-CoV-2
coronavirus
interferon
macrodomain
id ES_205fe641f39df48c4eb17dafc74e9cd2
oai_identifier_str oai:digital.csic.es:10261/363879
network_acronym_str ES
network_name_str España
repository_id_str
dc.title.none.fl_str_mv SARS-CoV-2 Mac1 is required for IFN antagonism and efficient virus replication in cell culture and in mice
title SARS-CoV-2 Mac1 is required for IFN antagonism and efficient virus replication in cell culture and in mice
spellingShingle SARS-CoV-2 Mac1 is required for IFN antagonism and efficient virus replication in cell culture and in mice
Alhammad, Yousef M.
ADP-ribosylation
SARS-CoV-2
coronavirus
interferon
macrodomain
title_short SARS-CoV-2 Mac1 is required for IFN antagonism and efficient virus replication in cell culture and in mice
title_full SARS-CoV-2 Mac1 is required for IFN antagonism and efficient virus replication in cell culture and in mice
title_fullStr SARS-CoV-2 Mac1 is required for IFN antagonism and efficient virus replication in cell culture and in mice
title_full_unstemmed SARS-CoV-2 Mac1 is required for IFN antagonism and efficient virus replication in cell culture and in mice
title_sort SARS-CoV-2 Mac1 is required for IFN antagonism and efficient virus replication in cell culture and in mice
dc.creator.none.fl_str_mv Alhammad, Yousef M.
Parthasarathy, Srivatsan
Ghimire, Roshan
Kerr, Catherine M.
O'Connor, Joseph J.
Pfannenstiel, Jessica J.
Chanda, Debarati
Miller, Caden A.
Baumlin, Nathalie
Salathe, Matthias
Unckless, Robert L.
Zúñiga Lucas, Sonia
Enjuanes Sánchez, Luis
More, Sunil
Channappanavar, Rudragouda
Fehr, Anthony R.
author Alhammad, Yousef M.
author_facet Alhammad, Yousef M.
Parthasarathy, Srivatsan
Ghimire, Roshan
Kerr, Catherine M.
O'Connor, Joseph J.
Pfannenstiel, Jessica J.
Chanda, Debarati
Miller, Caden A.
Baumlin, Nathalie
Salathe, Matthias
Unckless, Robert L.
Zúñiga Lucas, Sonia
Enjuanes Sánchez, Luis
More, Sunil
Channappanavar, Rudragouda
Fehr, Anthony R.
author_role author
author2 Parthasarathy, Srivatsan
Ghimire, Roshan
Kerr, Catherine M.
O'Connor, Joseph J.
Pfannenstiel, Jessica J.
Chanda, Debarati
Miller, Caden A.
Baumlin, Nathalie
Salathe, Matthias
Unckless, Robert L.
Zúñiga Lucas, Sonia
Enjuanes Sánchez, Luis
More, Sunil
Channappanavar, Rudragouda
Fehr, Anthony R.
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Ministerio de Ciencia e Innovación (España)
European Commission
Zuñiga, Sonia [0000-0003-2549-6826]
Enjuanes, Luis [0000-0002-0854-0226]
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv ADP-ribosylation
SARS-CoV-2
coronavirus
interferon
macrodomain
topic ADP-ribosylation
SARS-CoV-2
coronavirus
interferon
macrodomain
description This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas. 2302083120/-/DCSupplemental.
publishDate 2023
dc.date.none.fl_str_mv 2023
2024
2024
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/363879
https://api.elsevier.com/content/abstract/scopus_id/85168781208
url http://hdl.handle.net/10261/363879
https://api.elsevier.com/content/abstract/scopus_id/85168781208
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-107001RB-I00
Proceedings of the National Academy of Sciences of the United States of America
application/pdf
https://www.pnas.org/doi/10.1073/pnas.2302083120

dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv National Academy of Sciences (U.S.)
publisher.none.fl_str_mv National Academy of Sciences (U.S.)
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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spelling SARS-CoV-2 Mac1 is required for IFN antagonism and efficient virus replication in cell culture and in miceAlhammad, Yousef M.Parthasarathy, SrivatsanGhimire, RoshanKerr, Catherine M.O'Connor, Joseph J.Pfannenstiel, Jessica J.Chanda, DebaratiMiller, Caden A.Baumlin, NathalieSalathe, MatthiasUnckless, Robert L.Zúñiga Lucas, SoniaEnjuanes Sánchez, LuisMore, SunilChannappanavar, RudragoudaFehr, Anthony R.ADP-ribosylationSARS-CoV-2coronavirusinterferonmacrodomainThis article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas. 2302083120/-/DCSupplemental.Several coronavirus (CoV) encoded proteins are being evaluated as targets for antiviral therapies for COVID-19. Included in these drug targets is the conserved macrodomain, or Mac1, an ADP-ribosylhydrolase and ADP-ribose binding protein encoded as a small domain at the N terminus of nonstructural protein 3. Utilizing point mutant recombinant viruses, Mac1 was shown to be critical for both murine hepatitis virus (MHV) and severe acute respiratory syndrome (SARS)-CoV virulence. However, as a potential drug target, it is imperative to understand how a complete Mac1 deletion impacts the replication and pathogenesis of different CoVs. To this end, we created recombinant bacterial artificial chromosomes (BACs) containing complete Mac1 deletions (ΔMac1) in MHV, MERS-CoV, and SARS-CoV-2. While we were unable to recover infectious virus from MHV or MERS-CoV ΔMac1 BACs, SARS-CoV-2 ΔMac1 was readily recovered from BAC transfection, indicating a stark difference in the requirement for Mac1 between different CoVs. Furthermore, SARS-CoV-2 ΔMac1 replicated at or near wild-type levels in multiple cell lines susceptible to infection. However, in a mouse model of severe infection, ΔMac1 was quickly cleared causing minimal pathology without any morbidity. ΔMac1 SARS-CoV-2 induced increased levels of interferon (IFN) and IFN-stimulated gene expression in cell culture and mice, indicating that Mac1 blocks IFN responses which may contribute to its attenuation. ΔMac1 infection also led to a stark reduction in inflammatory monocytes and neutrophils. These results demonstrate that Mac1 only minimally impacts SARS-CoV-2 replication, unlike MHV and MERS-CoV, but is required for SARS-CoV-2 pathogenesis and is a unique antiviral drug target.Research reported in this publication was made possible in part by the services of the KU Genome Sequencing Core which is supported by the NIH under award number P30GM145499. We thank the Life Alliance Organ Recovery Agency from the University of Miami, Miami, FL, LifeCenter Northwest from Bellevue, Washington, Nevada Donor Network from Las Vegas, NV, and Midwest Transplant Network from Kansas City, KS, for provid- ing the lungs. NIH grant P20GM103648 (R.C.) NIH grant 2P01AI060699 (L.E.) NIH grant P20GM113117 (A.R.F.) NIH grant K22AI134993 (A.R.F.) NIH grant R35GM138029 (A.R.F.) NIH grant R01HL139365 (M.S.) NIH grant R01HL133240 (M.S.) NIH grant R01HL157942 (M.S.) Cystic Fibrosis Foundation grant SALATH18I0 (M.S.) NSF grant 2135167 (R.L.U.) University of Kansas General Research Fund and Start-up funds (A.R.F.) NIH Graduate Training at the Biology- Chemistry Interface grant T32GM132061 (C.M.K.) University of Kansas College of Liberal Arts and Sciences Graduate Research Fellowship (C.M.K.) Government of Spain (PID2019-107001RB-I00 AEI/FEDER, UE) (L.E.) European Commission (H2020-SC1-2019, ISOLDA Project no. 848166-2) (L.E.).Peer reviewedNational Academy of Sciences (U.S.)Ministerio de Ciencia e Innovación (España)European CommissionZuñiga, Sonia [0000-0003-2549-6826]Enjuanes, Luis [0000-0002-0854-0226]Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202420242023info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/363879https://api.elsevier.com/content/abstract/scopus_id/85168781208reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-107001RB-I00Proceedings of the National Academy of Sciences of the United States of Americaapplication/pdfhttps://www.pnas.org/doi/10.1073/pnas.2302083120Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3638792026-05-22T06:33:51Z
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