Systematic functional analysis of SARS-CoV-2 proteins uncovers viral innate immune antagonists and remaining vulnerabilities.


Journal

Cell reports
ISSN: 2211-1247
Titre abrégé: Cell Rep
Pays: United States
ID NLM: 101573691

Informations de publication

Date de publication:
18 05 2021
Historique:
received: 10 11 2020
revised: 03 03 2021
accepted: 22 04 2021
pubmed: 12 5 2021
medline: 29 5 2021
entrez: 11 5 2021
Statut: ppublish

Résumé

Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) evades most innate immune responses but may still be vulnerable to some. Here, we systematically analyze the impact of SARS-CoV-2 proteins on interferon (IFN) responses and autophagy. We show that SARS-CoV-2 proteins synergize to counteract anti-viral immune responses. For example, Nsp14 targets the type I IFN receptor for lysosomal degradation, ORF3a prevents fusion of autophagosomes and lysosomes, and ORF7a interferes with autophagosome acidification. Most activities are evolutionarily conserved. However, SARS-CoV-2 Nsp15 antagonizes IFN signaling less efficiently than the orthologs of closely related RaTG13-CoV and SARS-CoV-1. Overall, SARS-CoV-2 proteins counteract autophagy and type I IFN more efficiently than type II or III IFN signaling, and infection experiments confirm potent inhibition by IFN-γ and -λ1. Our results define the repertoire and selected mechanisms of SARS-CoV-2 innate immune antagonists but also reveal vulnerability to type II and III IFN that may help to develop safe and effective anti-viral approaches.

Identifiants

pubmed: 33974846
pii: S2211-1247(21)00465-4
doi: 10.1016/j.celrep.2021.109126
pmc: PMC8078906
pii:
doi:

Substances chimiques

Antiviral Agents 0
Interferon Type I 0
Viral Nonstructural Proteins 0
Viral Proteins 0
Receptor, Interferon alpha-beta 156986-95-7
Interferons 9008-11-1
nsp14 protein, SARS coronavirus EC 2.1.1.56
Exoribonucleases EC 3.1.-

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

109126

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2021 The Author(s). Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests F.I.S. is a co-founder of DiosCURE Therapeutics SE and a consultant to IFM Therapeutics.

Références

J Virol. 2020 Nov 9;94(23):
pubmed: 32938761
J Clin Gastroenterol. 2010 Oct;44(9):e210-7
pubmed: 20838237
Proc Natl Acad Sci U S A. 2017 Apr 25;114(17):E3462-E3471
pubmed: 28389568
Science. 2020 Oct 23;370(6515):
pubmed: 32972996
J Clin Invest. 2002 Jun;109(12):1541-50
pubmed: 12070301
mBio. 2020 Sep 10;11(5):
pubmed: 32913009
Lancet. 2020 Feb 15;395(10223):497-506
pubmed: 31986264
Lancet. 2015 Sep 5;386(9997):995-1007
pubmed: 26049252
Hepatology. 2002 Nov;36(5 Suppl 1):S237-44
pubmed: 12407599
Respirology. 2003 Nov;8 Suppl:S9-14
pubmed: 15018127
J Clin Invest. 2020 May 1;130(5):2620-2629
pubmed: 32217835
Nature. 2020 Mar;579(7798):270-273
pubmed: 32015507
Curr Opin Microbiol. 2015 Aug;26:1-9
pubmed: 25795286
Nature. 2020 Aug;584(7821):457-462
pubmed: 32668444
Cell Rep. 2020 Jul 7;32(1):107863
pubmed: 32610043
J Virol. 2008 Dec;82(24):12365-73
pubmed: 18922877
Cell. 2012 Dec 7;151(6):1168-78
pubmed: 23217704
Lancet. 2020 May 30;395(10238):1695-1704
pubmed: 32401715
Nat Microbiol. 2021 Apr;6(4):467-478
pubmed: 33727702
Nat Microbiol. 2017 Nov;2(11):1543-1557
pubmed: 28871090
Emerg Microbes Infect. 2020 Dec;9(1):1418-1428
pubmed: 32529952
Science. 2010 Jan 15;327(5963):291-5
pubmed: 20075244
Clin Microbiol Infect. 2020 Aug;26(8):988-998
pubmed: 32454187
Lancet Digit Health. 2020 Jun;2(6):e286-e287
pubmed: 32363333
Aliment Pharmacol Ther. 2005 May 1;21(9):1163-71
pubmed: 15854180
J Virol. 2015 Dec 16;90(5):2403-17
pubmed: 26676772
Nat Med. 2020 Apr;26(4):450-452
pubmed: 32284615
J Virol. 2004 Jul;78(14):7833-8
pubmed: 15220459
Lancet. 2020 May 30;395(10238):1670-1671
pubmed: 32401712
Curr Opin Virol. 2012 Jun;2(3):264-75
pubmed: 22572391
Science. 2020 May 8;368(6491):
pubmed: 32234805
Nat Immunol. 2020 Oct;21(10):1293-1301
pubmed: 32807944
mBio. 2020 Oct 16;11(5):
pubmed: 33067384
Front Immunol. 2020 May 15;11:1061
pubmed: 32574262
Virology. 2018 Apr;517:157-163
pubmed: 29307596
Science. 2020 Oct 23;370(6515):
pubmed: 32972995
Adv Virus Res. 2018;100:163-188
pubmed: 29551135
Nat Immunol. 2015 Apr;16(4):343-53
pubmed: 25789684
Virus Res. 2008 Apr;133(1):101-12
pubmed: 17451827
J Cell Sci. 2016 Nov 1;129(21):3971-3982
pubmed: 27802132
Trends Cell Biol. 2020 Jun;30(6):467-477
pubmed: 32413316
Virology. 2015 May;479-480:110-21
pubmed: 25749629
PLoS Pathog. 2018 Feb 1;14(2):e1006787
pubmed: 29389992
Sci Rep. 2020 Jul 22;10(1):12241
pubmed: 32699244
Nature. 2020 Nov;587(7835):657-662
pubmed: 32726803
Nat Rev Immunol. 2013 Oct;13(10):722-37
pubmed: 24064518
Autophagy. 2016;12(1):1-222
pubmed: 26799652
J Virol. 2014 Nov;88(21):12511-27
pubmed: 25142582
J Virol. 2005 Jun;79(12):7673-81
pubmed: 15919920
Proc Natl Acad Sci U S A. 2016 Nov 15;113(46):12997-13002
pubmed: 27799534
Nat Rev Microbiol. 2018 Jun;16(6):341-354
pubmed: 29556036
Nature. 2021 Jun;594(7862):246-252
pubmed: 33845483
Immunol Rev. 2009 Jan;227(1):75-86
pubmed: 19120477
Cell Rep. 2020 Sep 22;32(12):108185
pubmed: 32941788
Nat Struct Mol Biol. 2020 Oct;27(10):959-966
pubmed: 32908316
Cell Rep. 2020 Oct 6;33(1):108234
pubmed: 32979938
Cell Host Microbe. 2020 Sep 9;28(3):455-464.e2
pubmed: 32707096
Nat Immunol. 2018 Jan;19(1):53-62
pubmed: 29180807
Nat Commun. 2018 Feb 15;9(1):689
pubmed: 29449567
Curr Opin Microbiol. 2021 Feb;59:50-57
pubmed: 32829025
Nat Rev Immunol. 2020 Aug;20(8):457-458
pubmed: 32636479
Annu Rev Immunol. 2018 Apr 26;36:73-101
pubmed: 29144836
Virol Sin. 2020 Jun;35(3):321-329
pubmed: 32500504
Nature. 2011 Jan 20;469(7330):323-35
pubmed: 21248839
J Virol. 2013 Dec;87(23):12611-8
pubmed: 24027335
Cell. 2020 May 28;181(5):1036-1045.e9
pubmed: 32416070
Nat Commun. 2020 Jul 30;11(1):3810
pubmed: 32733001
Lancet Infect Dis. 2020 Sep;20(9):e238-e244
pubmed: 32628905
Dev Cell. 2021 Feb 22;56(4):427-442.e5
pubmed: 33422265
Antiviral Res. 2020 Jun;178:104791
pubmed: 32275914
Annu Rev Virol. 2018 Sep 29;5(1):385-405
pubmed: 29949725
Nat Rev Mol Cell Biol. 2013 Jun;14(6):382-92
pubmed: 23698585
Cell Rep. 2021 Mar 30;34(13):108916
pubmed: 33765414
Nat Rev Immunol. 2020 Jun;20(6):363-374
pubmed: 32346093
J Virol. 2012 Jan;86(2):796-805
pubmed: 22072748
Nature. 2020 Jul;583(7816):459-468
pubmed: 32353859
Science. 2020 Aug 7;369(6504):718-724
pubmed: 32661059
Antiviral Res. 2018 Jan;149:58-74
pubmed: 29128390
Science. 2020 Sep 4;369(6508):1249-1255
pubmed: 32680882
Pharm World Sci. 2005 Dec;27(6):423-31
pubmed: 16341948
Nature. 2020 Mar;579(7798):265-269
pubmed: 32015508

Auteurs

Manuel Hayn (M)

Institute of Molecular Virology, Ulm University Medical Center, 89081 Ulm, Germany.

Maximilian Hirschenberger (M)

Institute of Molecular Virology, Ulm University Medical Center, 89081 Ulm, Germany.

Lennart Koepke (L)

Institute of Molecular Virology, Ulm University Medical Center, 89081 Ulm, Germany.

Rayhane Nchioua (R)

Institute of Molecular Virology, Ulm University Medical Center, 89081 Ulm, Germany.

Jan Hendrik Straub (JH)

Institute of Molecular Virology, Ulm University Medical Center, 89081 Ulm, Germany.

Susanne Klute (S)

Institute of Molecular Virology, Ulm University Medical Center, 89081 Ulm, Germany.

Victoria Hunszinger (V)

Institute of Molecular Virology, Ulm University Medical Center, 89081 Ulm, Germany.

Fabian Zech (F)

Institute of Molecular Virology, Ulm University Medical Center, 89081 Ulm, Germany.

Caterina Prelli Bozzo (C)

Institute of Molecular Virology, Ulm University Medical Center, 89081 Ulm, Germany.

Wasim Aftab (W)

Biomedical Center, Zentrallabor für Proteinanalytik (Protein Analysis Unit), Medical Faculty, Ludwig-Maximilians-Universität München, 82152 Planegg-Martinsried, Germany; Graduate School for Quantitative Biosciences (QBM), Ludwig-Maximilians-University of Munich, 81377 Munich, Germany.

Maria Hønholt Christensen (MH)

Institute of Innate Immunity, Medical Faculty, University of Bonn, 53127 Bonn, Germany.

Carina Conzelmann (C)

Institute of Molecular Virology, Ulm University Medical Center, 89081 Ulm, Germany.

Janis Alexander Müller (JA)

Institute of Molecular Virology, Ulm University Medical Center, 89081 Ulm, Germany.

Smitha Srinivasachar Badarinarayan (S)

Institute of Molecular Virology, Ulm University Medical Center, 89081 Ulm, Germany; Institute of Medical Virology and Epidemiology of Viral Diseases, University Hospital Tübingen, 72076 Tübingen, Germany.

Christina Martina Stürzel (CM)

Institute of Molecular Virology, Ulm University Medical Center, 89081 Ulm, Germany.

Ignasi Forne (I)

Biomedical Center, Zentrallabor für Proteinanalytik (Protein Analysis Unit), Medical Faculty, Ludwig-Maximilians-Universität München, 82152 Planegg-Martinsried, Germany.

Steffen Stenger (S)

Institute for Medical Microbiology and Hygiene, Ulm University Medical Center, 89081 Ulm, Germany.

Karl-Klaus Conzelmann (KK)

Max von Pettenkofer-Institute of Virology, Medical Faculty, and Gene Center, Ludwig-Maximilians-Universität München, 81377 Munich, Germany.

Jan Münch (J)

Institute of Molecular Virology, Ulm University Medical Center, 89081 Ulm, Germany.

Florian Ingo Schmidt (FI)

Institute of Innate Immunity, Medical Faculty, University of Bonn, 53127 Bonn, Germany.

Daniel Sauter (D)

Institute of Molecular Virology, Ulm University Medical Center, 89081 Ulm, Germany; Institute of Medical Virology and Epidemiology of Viral Diseases, University Hospital Tübingen, 72076 Tübingen, Germany.

Axel Imhof (A)

Biomedical Center, Zentrallabor für Proteinanalytik (Protein Analysis Unit), Medical Faculty, Ludwig-Maximilians-Universität München, 82152 Planegg-Martinsried, Germany.

Frank Kirchhoff (F)

Institute of Molecular Virology, Ulm University Medical Center, 89081 Ulm, Germany.

Konstantin Maria Johannes Sparrer (KMJ)

Institute of Molecular Virology, Ulm University Medical Center, 89081 Ulm, Germany. Electronic address: konstantin.sparrer@uni-ulm.de.

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