ADAR1 RNA editing regulates endothelial cell functions via the MDA-5 RNA sensing signaling pathway.


Journal

Life science alliance
ISSN: 2575-1077
Titre abrégé: Life Sci Alliance
Pays: United States
ID NLM: 101728869

Informations de publication

Date de publication:
03 2022
Historique:
received: 12 08 2021
revised: 11 12 2021
accepted: 13 12 2021
entrez: 31 12 2021
pubmed: 1 1 2022
medline: 29 3 2022
Statut: epublish

Résumé

The RNA-sensing signaling pathway has been well studied as an essential antiviral mechanism of innate immunity. However, its role in non-infected cells is yet to be thoroughly characterized. Here, we demonstrated that the RNA sensing signaling pathway also reacts to the endogenous cellular RNAs in endothelial cells (ECs), and this reaction is regulated by the RNA-editing enzyme ADAR1. Cellular RNA sequencing analysis showed that EC RNAs endure extensive RNA editing, especially in the RNA transcripts of short interspersed nuclear elements. The EC-specific deletion of ADAR1 dramatically reduced the editing level on short interspersed nuclear element RNAs, resulting in newborn death in mice with damage evident in multiple organs. Genome-wide gene expression analysis revealed a prominent innate immune activation with a dramatically elevated expression of interferon-stimulated genes. However, blocking the RNA sensing signaling pathway by deletion of the cellular RNA receptor MDA-5 prevented interferon-stimulated gene expression and rescued the newborn mice from death. This evidence demonstrated that the RNA-editing/RNA-sensing signaling pathway dramatically modulates EC function, representing a novel molecular mechanism for the regulation of EC functions.

Identifiants

pubmed: 34969816
pii: 5/3/e202101191
doi: 10.26508/lsa.202101191
pmc: PMC8739526
pii:
doi:

Substances chimiques

Biomarkers 0
ADAR1 protein, mouse EC 3.5.4.4
Adenosine Deaminase EC 3.5.4.4
Ifih1 protein, mouse EC 3.6.1.-
Interferon-Induced Helicase, IFIH1 EC 3.6.4.13

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : RRD VA
ID : I01 RX001455
Pays : United States
Organisme : NIDDK NIH HHS
ID : P30 DK120531
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI139544
Pays : United States
Organisme : NIA NIH HHS
ID : R21 AG052912
Pays : United States

Informations de copyright

© 2021 Guo et al.

Références

Bioinformatics. 2015 Jan 15;31(2):166-9
pubmed: 25260700
J Interferon Cytokine Res. 2014 Jun;34(6):437-46
pubmed: 24905200
Circulation. 2003 Oct 21;108(16):1917-23
pubmed: 14568885
Am J Pathol. 2015 Dec;185(12):3224-37
pubmed: 26453800
Proc Natl Acad Sci U S A. 2011 Jun 14;108(24):E199; author reply E200
pubmed: 21593418
Nature. 2017 Oct 11;550(7675):249-254
pubmed: 29022589
Front Immunol. 2019 Jul 25;10:1763
pubmed: 31404141
Circ Res. 2020 Jul 31;127(4):550-552
pubmed: 32362246
Trends Genet. 2019 Dec;35(12):903-913
pubmed: 31648814
Circ Res. 2016 Jul 22;119(3):463-9
pubmed: 27199464
Viruses. 2019 Mar 12;11(3):
pubmed: 30871003
Cells. 2020 Jul 16;9(7):
pubmed: 32708595
J Biol Chem. 2004 Feb 6;279(6):4894-902
pubmed: 14615479
Intensive Care Med. 2011 Oct;37(10):1664-71
pubmed: 21720910
Nat Med. 2016 Oct;22(10):1140-1150
pubmed: 27595325
J Dermatol Sci. 2011 Oct;64(1):70-2
pubmed: 21788117
J Virol. 2012 Mar;86(6):2900-10
pubmed: 22258243
Nat Protoc. 2010 Apr;5(4):628-35
pubmed: 20224563
Methods Mol Biol. 2021;2181:149-162
pubmed: 32729079
J Biol Chem. 2004 Feb 6;279(6):4952-61
pubmed: 14613934
Nat Immunol. 2009 Jan;10(1):109-15
pubmed: 19060901
Proc Natl Acad Sci U S A. 2006 May 30;103(22):8459-64
pubmed: 16714379
J Immunol. 2014 Oct 1;193(7):3436-45
pubmed: 25172485
Science. 2000 Dec 1;290(5497):1765-8
pubmed: 11099415
RNA Biol. 2018;15(7):877-885
pubmed: 30064337
Bioinformatics. 2014 Aug 1;30(15):2114-20
pubmed: 24695404
Genome Biol. 2014;15(12):550
pubmed: 25516281
Circ Res. 2018 Feb 2;122(3):444-456
pubmed: 29284691
Cell Rep. 2014 Nov 20;9(4):1482-94
pubmed: 25456137
Proc Natl Acad Sci U S A. 2009 Oct 20;106(42):17763-8
pubmed: 19805087
Front Immunol. 2021 Jan 28;11:625833
pubmed: 33633744
Genome Res. 2004 Sep;14(9):1719-25
pubmed: 15342557
Dev Dyn. 2006 Mar;235(3):759-67
pubmed: 16450386
RNA. 1997 Sep;3(9):947-9
pubmed: 9292492
Nat Rev Genet. 2018 Aug;19(8):473-490
pubmed: 29692414
EMBO J. 2018 Oct 1;37(19):
pubmed: 30087110
Am J Physiol Lung Cell Mol Physiol. 2021 May 1;320(5):L726-L738
pubmed: 33565360
Immunity. 2015 Nov 17;43(5):933-44
pubmed: 26588779
RNA. 2006 Oct;12(10):1802-9
pubmed: 16940548
Nat Rev Immunol. 2007 Oct;7(10):803-15
pubmed: 17893694
Gene. 2013 Jan 15;513(1):101-10
pubmed: 23123729
Bioinformatics. 2011 Nov 1;27(21):2987-93
pubmed: 21903627
Nat Rev Mol Cell Biol. 2016 Feb;17(2):83-96
pubmed: 26648264
Front Cardiovasc Med. 2020 Mar 18;7:30
pubmed: 32258062
Genome Biol. 2011 Dec 28;12(12):236
pubmed: 22204421
Genome Res. 2014 Mar;24(3):365-76
pubmed: 24347612
Bioinformatics. 2013 Jan 1;29(1):15-21
pubmed: 23104886
RNA Biol. 2013 Oct;10(10):1611-7
pubmed: 24025532
Science. 2015 Sep 4;349(6252):1115-20
pubmed: 26275108
Int J Cancer. 2013 Apr 15;132(8):1741-50
pubmed: 22987615
Cell. 2018 Feb 8;172(4):811-824.e14
pubmed: 29395325
Circ Res. 2020 Aug 14;127(5):677-692
pubmed: 32493166
Nucleic Acids Res. 2014 Jun;42(11):6876-84
pubmed: 24829451
Cell Death Dis. 2013 Apr 18;4:e599
pubmed: 23598411
Nat Rev Immunol. 2020 Sep;20(9):537-551
pubmed: 32203325
Am J Physiol Heart Circ Physiol. 2014 Feb;306(3):H317-25
pubmed: 24285111

Auteurs

Xinfeng Guo (X)

Department of Surgery, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA.

Silvia Liu (S)

Department of Pathology, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA.
Pittsburgh Liver Research Center, University of Pittsburgh Medical Center (UPMC) and University of Pittsburgh School of Medicine, Pittsburgh, PA, USA.

Rose Yan (R)

Department of Surgery, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA.

Vy Nguyen (V)

Department of Surgery, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA.

Mazen Zenati (M)

Department of Surgery, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA.

Timothy R Billiar (TR)

Department of Surgery, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA billiartr@upmc.edu.

Qingde Wang (Q)

Department of Surgery, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA wangqd@pitt.edu.
Pittsburgh Liver Research Center, University of Pittsburgh Medical Center (UPMC) and University of Pittsburgh School of Medicine, Pittsburgh, PA, USA.
VA Pittsburgh Health System, Pittsburgh, PA, USA.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
C-Reactive Protein Humans Biomarkers Inflammation
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice

Classifications MeSH