An RNA-Binding Protein Secreted by a Bacterial Pathogen Modulates RIG-I Signaling.
Animals
Bacterial Proteins
/ metabolism
DEAD Box Protein 58
/ immunology
HEK293 Cells
Host Microbial Interactions
Humans
Immunity, Innate
Interferon-beta
/ metabolism
Listeria monocytogenes
/ immunology
Mice
RNA, Bacterial
/ metabolism
RNA-Binding Proteins
/ metabolism
Signal Transduction
/ immunology
Virulence
/ immunology
bacteriophage A118
extracellular RNA
type I IFN
Journal
Cell host & microbe
ISSN: 1934-6069
Titre abrégé: Cell Host Microbe
Pays: United States
ID NLM: 101302316
Informations de publication
Date de publication:
11 12 2019
11 12 2019
Historique:
received:
24
05
2019
revised:
21
08
2019
accepted:
07
10
2019
pubmed:
26
11
2019
medline:
16
4
2020
entrez:
26
11
2019
Statut:
ppublish
Résumé
RNA-binding proteins (RBPs) perform key cellular activities by controlling the function of bound RNAs. The widely held assumption that RBPs are strictly intracellular has been challenged by the discovery of secreted RBPs. However, extracellular RBPs have been described in eukaryotes, while secreted bacterial RBPs have not been reported. Here, we show that the bacterial pathogen Listeria monocytogenes secretes a small RBP that we named Zea. We show that Zea binds a subset of L. monocytogenes RNAs, causing their accumulation in the extracellular medium. Furthermore, during L. monocytogenes infection, Zea binds RIG-I, the non-self-RNA innate immunity sensor, potentiating interferon-β production. Mouse infection studies reveal that Zea affects L. monocytogenes virulence. Together, our results unveil that bacterial RNAs can be present extracellularly in association with RBPs, acting as "social RNAs" to trigger a host response during infection.
Identifiants
pubmed: 31761719
pii: S1931-3128(19)30528-1
doi: 10.1016/j.chom.2019.10.004
pmc: PMC6907008
pii:
doi:
Substances chimiques
Bacterial Proteins
0
RNA, Bacterial
0
RNA-Binding Proteins
0
Interferon-beta
77238-31-4
Ddx58 protein, mouse
EC 3.6.1.-
DEAD Box Protein 58
EC 3.6.4.13
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
823-835.e11Subventions
Organisme : European Research Council
ID : 670823
Pays : International
Commentaires et corrections
Type : CommentIn
Informations de copyright
Copyright © 2019 The Authors. Published by Elsevier Inc. All rights reserved.
Références
Mol Microbiol. 2005 Apr;56(2):383-96
pubmed: 15813732
Genome Biol. 2014;15(12):550
pubmed: 25516281
Proc Natl Acad Sci U S A. 2013 Aug 6;110(32):13132-7
pubmed: 23878253
PLoS Pathog. 2013;9(10):e1003678
pubmed: 24098125
Int J Syst Evol Microbiol. 2010 Jun;60(Pt 6):1280-8
pubmed: 19667380
Bioinformatics. 2015 Jan 15;31(2):166-9
pubmed: 25260700
J Bacteriol. 2016 Sep 22;198(20):2784-93
pubmed: 27457717
Gene. 1991 Jun 15;102(1):99-104
pubmed: 1864514
Sci Rep. 2017 Aug 24;7(1):9328
pubmed: 28839189
PLoS Pathog. 2009 Mar;5(3):e1000355
pubmed: 19325882
Bioinformatics. 2014 Apr 1;30(7):923-30
pubmed: 24227677
Nucleic Acids Res. 2016 Jul 8;44(W1):W160-5
pubmed: 27079975
J Exp Med. 2004 Aug 16;200(4):527-33
pubmed: 15302899
PLoS One. 2016 Jun 09;11(6):e0157022
pubmed: 27280887
Science. 2001 Oct 26;294(5543):849-52
pubmed: 11679669
Nat Cell Biol. 2011 Apr;13(4):423-33
pubmed: 21423178
Appl Environ Microbiol. 2004 Nov;70(11):6887-91
pubmed: 15528558
Proc Natl Acad Sci U S A. 2011 Mar 22;108(12):5003-8
pubmed: 21383194
Annu Rev Immunol. 2018 Apr 26;36:667-694
pubmed: 29677479
Proteins. 2007 Nov 15;69(3):672-8
pubmed: 17879352
J Bacteriol. 2009 Dec;191(23):7206-15
pubmed: 19783628
Nat Rev Microbiol. 2018 Oct;16(10):601-615
pubmed: 29995832
Methods Mol Biol. 2009;540:215-32
pubmed: 19381563
Cell. 2009 Oct 30;139(3):523-34
pubmed: 19879839
Nat Rev Microbiol. 2011 Aug 15;9(8):578-89
pubmed: 21760622
PLoS One. 2013 Apr 30;8(4):e62872
pubmed: 23653683
Elife. 2016 Mar 24;5:e11275
pubmed: 27011352
J Biol Chem. 2018 Jun 15;293(24):9265-9276
pubmed: 29666193
Genomics. 2013 Nov-Dec;102(5-6):500-6
pubmed: 23912058
Nat Struct Mol Biol. 2006 Jan;13(1):22-9
pubmed: 16341228
Elife. 2016 Aug 25;5:
pubmed: 27559612
EMBO J. 2012 Nov 5;31(21):4153-64
pubmed: 23064150
J Exp Med. 2004 Aug 16;200(4):437-45
pubmed: 15302901
Cell Rep. 2018 Jul 10;24(2):320-328
pubmed: 29996094
Bioinformatics. 2016 Oct 1;32(19):3047-8
pubmed: 27312411
Bioinformatics. 2010 Jan 1;26(1):139-40
pubmed: 19910308
Nat Commun. 2018 Aug 10;9(1):3199
pubmed: 30097581
J Exp Med. 2004 Aug 16;200(4):535-40
pubmed: 15302900
Nat Methods. 2012 Mar 04;9(4):357-9
pubmed: 22388286
PLoS Genet. 2016 Sep 23;12(9):e1006318
pubmed: 27662573
RNA. 2006 Jul;12(7):1383-96
pubmed: 16682563
Nature. 1995 Apr 20;374(6524):693-700
pubmed: 7715723
Mol Microbiol. 1990 Jul;4(7):1091-9
pubmed: 2172692
Appl Environ Microbiol. 2010 Jun;76(11):3625-36
pubmed: 20363781
J Virol. 2017 Jan 3;91(2):
pubmed: 27807226
Nucleic Acids Res. 2010 Nov;38(20):7248-59
pubmed: 20615901
mSystems. 2017 Mar 14;2(2):
pubmed: 28317029
Mol Syst Biol. 2012 May 22;8:583
pubmed: 22617957
Methods Mol Biol. 2016;1418:283-334
pubmed: 27008021
mBio. 2017 Oct 31;8(5):
pubmed: 29089430
Bioinformatics. 2009 Aug 15;25(16):2078-9
pubmed: 19505943
Mol Cell. 2019 May 2;74(3):598-608.e6
pubmed: 31051140
Proc Natl Acad Sci U S A. 1995 Aug 15;92(17):7916-20
pubmed: 7544009
Front Cell Infect Microbiol. 2014 Apr 28;4:50
pubmed: 24809023
Cell Rep. 2018 Apr 24;23(4):1124-1137
pubmed: 29694890