Host-specific sensing of coronaviruses and picornaviruses by the CARD8 inflammasome.
Journal
PLoS biology
ISSN: 1545-7885
Titre abrégé: PLoS Biol
Pays: United States
ID NLM: 101183755
Informations de publication
Date de publication:
Jun 2023
Jun 2023
Historique:
received:
22
09
2022
accepted:
02
05
2023
medline:
12
6
2023
pubmed:
8
6
2023
entrez:
8
6
2023
Statut:
epublish
Résumé
Hosts have evolved diverse strategies to respond to microbial infections, including the detection of pathogen-encoded proteases by inflammasome-forming sensors such as NLRP1 and CARD8. Here, we find that the 3CL protease (3CLpro) encoded by diverse coronaviruses, including Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2), cleaves a rapidly evolving region of human CARD8 and activates a robust inflammasome response. CARD8 is required for cell death and the release of pro-inflammatory cytokines during SARS-CoV-2 infection. We further find that natural variation alters CARD8 sensing of 3CLpro, including 3CLpro-mediated antagonism rather than activation of megabat CARD8. Likewise, we find that a single nucleotide polymorphism (SNP) in humans reduces CARD8's ability to sense coronavirus 3CLpros and, instead, enables sensing of 3C proteases (3Cpro) from select picornaviruses. Our findings demonstrate that CARD8 is a broad sensor of viral protease activities and suggests that CARD8 diversity contributes to inter- and intraspecies variation in inflammasome-mediated viral sensing and immunopathology.
Identifiants
pubmed: 37289745
doi: 10.1371/journal.pbio.3002144
pii: PBIOLOGY-D-22-02080
pmc: PMC10249858
doi:
Substances chimiques
Inflammasomes
0
Protease Inhibitors
0
Apoptosis Regulatory Proteins
0
CARD8 protein, human
0
Neoplasm Proteins
0
CARD Signaling Adaptor Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e3002144Subventions
Organisme : NIGMS NIH HHS
ID : R35 GM133633
Pays : United States
Organisme : NIAID NIH HHS
ID : R37 AI075039
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM133351
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM007240
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM136534
Pays : United States
Commentaires et corrections
Type : UpdateOf
Informations de copyright
Copyright: © 2023 Tsu et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Déclaration de conflit d'intérêts
The authors have declared that no competing interests exist.
Références
Genome Res. 2014 Oct;24(10):1719-23
pubmed: 25186908
Nat Rev Genet. 2015 Apr;16(4):224-36
pubmed: 25783448
Cell. 2016 May 5;165(4):792-800
pubmed: 27153493
PLoS One. 2011;6(11):e27228
pubmed: 22073294
Lancet Respir Med. 2020 Jul;8(7):687-695
pubmed: 32386571
Nat Med. 2018 Aug;24(8):1151-1156
pubmed: 29967349
Annu Rev Plant Biol. 2015;66:487-511
pubmed: 25494461
PLoS One. 2011;6(11):e27396
pubmed: 22087307
Nature. 2022 Jun;606(7914):576-584
pubmed: 35385861
Mol Biol Evol. 2013 Apr;30(4):772-80
pubmed: 23329690
Life Sci Alliance. 2020 Feb 12;3(3):
pubmed: 32051255
Cell Death Dis. 2020 Aug 14;11(8):628
pubmed: 32796818
Proc Natl Acad Sci U S A. 2014 Dec 2;111(48):17254-9
pubmed: 25404286
Annu Rev Immunol. 2023 Apr 26;41:453-481
pubmed: 36750319
J Exp Med. 2021 Mar 1;218(3):
pubmed: 33231615
Elife. 2021 Jan 07;10:
pubmed: 33410748
Nature. 2020 May;581(7809):434-443
pubmed: 32461654
Methods Mol Biol. 2016;1338:261-72
pubmed: 26443227
Front Immunol. 2021 Nov 01;12:769543
pubmed: 34790204
Nat Rev Microbiol. 2020 Aug;18(8):461-471
pubmed: 32528128
EMBO J. 2020 Oct 1;39(19):e105071
pubmed: 32840892
Mol Biol Evol. 2007 Aug;24(8):1586-91
pubmed: 17483113
FEBS Lett. 2010 Feb 5;584(3):469-76
pubmed: 20026333
Mol Biol Evol. 2005 May;22(5):1208-22
pubmed: 15703242
PLoS Pathog. 2016 Dec 7;12(12):e1006052
pubmed: 27926929
Science. 2016 Dec 2;354(6316):
pubmed: 27934708
Nature. 2022 Jun;606(7914):585-593
pubmed: 35483404
Immunity. 2019 Oct 15;51(4):609-624
pubmed: 31473100
Mol Cell. 2022 Jul 7;82(13):2385-2400.e9
pubmed: 35594856
Mol Biol Evol. 2015 May;32(5):1365-71
pubmed: 25701167
Nat Microbiol. 2019 May;4(5):789-799
pubmed: 30804542
Biochemistry. 2007 Jul 31;46(30):8744-52
pubmed: 17605471
J Virol. 2010 Jul;84(14):7325-36
pubmed: 20444893
Bioinformatics. 2012 Jun 15;28(12):1647-9
pubmed: 22543367
Eur J Hum Genet. 2008 May;16(5):619-25
pubmed: 18212821
Virology. 2017 Feb;502:33-38
pubmed: 27984784
Cell Host Microbe. 2009 Jul 23;6(1):10-21
pubmed: 19616762
Annu Rev Genet. 2012;46:677-700
pubmed: 23145935
Sci Rep. 2015 Oct 08;5:14987
pubmed: 26446710
Mol Biol Evol. 2013 May;30(5):1196-205
pubmed: 23420840
J Virol. 2017 Apr 28;91(10):
pubmed: 28250121
Nat Microbiol. 2020 Mar;5(3):528
pubmed: 32042131
Curr Opin Immunol. 2019 Oct;60:37-45
pubmed: 31121538
Mol Biol Evol. 2018 Mar 1;35(3):773-777
pubmed: 29301006
Trends Immunol. 2022 Dec;43(12):1006-1017
pubmed: 36369102
Nat Methods. 2014 Aug;11(8):783-784
pubmed: 25075903
Nature. 2021 Dec;600(7887):138-142
pubmed: 34759314
Cell Host Microbe. 2010 Dec 16;8(6):471-83
pubmed: 21147462
Science. 2020 Dec 4;370(6521):
pubmed: 33093214
PLoS One. 2010 Oct 06;5(10):e13197
pubmed: 20949131
J Immunol. 2020 Jul 15;205(2):307-312
pubmed: 32493814
Emerg Microbes Infect. 2021 Dec;10(1):178-195
pubmed: 33372854
Science. 2019 Apr 5;364(6435):
pubmed: 30872533
Nat Med. 2015 Dec;21(12):1508-13
pubmed: 26552008
Science. 2019 Apr 5;364(6435):82-85
pubmed: 30872531
Viruses. 2019 Dec 30;12(1):
pubmed: 31905881
Cancer Res. 2005 Oct 1;65(19):8706-14
pubmed: 16204039
J Exp Med. 2022 Oct 3;219(10):
pubmed: 36129453
J Biol Chem. 2001 Nov 23;276(47):44069-77
pubmed: 11551959
Cell. 2020 Apr 16;181(2):271-280.e8
pubmed: 32142651
Trends Microbiol. 2020 Jan;28(1):46-56
pubmed: 31597598
Nucleic Acids Res. 2019 Jul 2;47(W1):W171-W174
pubmed: 31106371
Science. 2021 Mar 19;371(6535):
pubmed: 33542150
Nat Rev Immunol. 2021 Nov;21(11):694-703
pubmed: 34373622
Nat Rev Immunol. 2016 Jul;16(7):407-20
pubmed: 27291964
BMC Bioinformatics. 2009 Dec 15;10:421
pubmed: 20003500
J Gen Virol. 2021 Mar;102(3):
pubmed: 33507143
Viruses. 2012 Nov 19;4(11):3209-26
pubmed: 23202522