Contribution of autophagy machinery factors to HCV and SARS-CoV-2 replication organelle formation.
Autophagosomes
/ metabolism
Autophagy
/ physiology
Carrier Proteins
/ metabolism
Class III Phosphatidylinositol 3-Kinases
/ antagonists & inhibitors
Hepacivirus
/ physiology
Humans
Phosphatidylinositol Phosphates
/ metabolism
RNA, Viral
/ biosynthesis
SARS-CoV-2
/ physiology
Viral Nonstructural Proteins
/ metabolism
Viral Replication Compartments
/ metabolism
Virus Replication
Beclin 1
DFCP1
DMV
PI3P
autophagy
class III PI3K
coronavirus
daclatasvir
hepatitis C virus
replication organelle
Journal
Cell reports
ISSN: 2211-1247
Titre abrégé: Cell Rep
Pays: United States
ID NLM: 101573691
Informations de publication
Date de publication:
23 11 2021
23 11 2021
Historique:
received:
30
04
2021
revised:
02
09
2021
accepted:
02
11
2021
pubmed:
18
11
2021
medline:
15
12
2021
entrez:
17
11
2021
Statut:
ppublish
Résumé
Positive-strand RNA viruses replicate in close association with rearranged intracellular membranes. For hepatitis C virus (HCV) and severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), these rearrangements comprise endoplasmic reticulum (ER)-derived double membrane vesicles (DMVs) serving as RNA replication sites. Cellular factors involved in DMV biogenesis are poorly defined. Here, we show that despite structural similarity of viral DMVs with autophagosomes, conventional macroautophagy is dispensable for HCV and SARS-CoV-2 replication. However, both viruses exploit factors involved in autophagosome formation, most notably class III phosphatidylinositol 3-kinase (PI3K). As revealed with a biosensor, PI3K is activated in cells infected with either virus to produce phosphatidylinositol 3-phosphate (PI3P) while kinase complex inhibition or depletion profoundly reduces replication and viral DMV formation. The PI3P-binding protein DFCP1, recruited to omegasomes in early steps of autophagosome formation, participates in replication and DMV formation of both viruses. These results indicate that phylogenetically unrelated HCV and SARS-CoV-2 exploit similar components of the autophagy machinery to create their replication organelles.
Identifiants
pubmed: 34788596
pii: S2211-1247(21)01535-7
doi: 10.1016/j.celrep.2021.110049
pmc: PMC8577994
pii:
doi:
Substances chimiques
Carrier Proteins
0
Phosphatidylinositol Phosphates
0
RNA, Viral
0
Viral Nonstructural Proteins
0
ZFYVE1 protein, human
0
phosphatidylinositol 3-phosphate
0
Class III Phosphatidylinositol 3-Kinases
EC 2.7.1.137
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
110049Informations de copyright
Copyright © 2021 The Author(s). Published by Elsevier Inc. All rights reserved.
Déclaration de conflit d'intérêts
Declaration of interests The authors declare no competing interests.
Références
Cell Rep. 2021 Aug 3;36(5):109479
pubmed: 34320401
Sci Rep. 2017 Jan 09;7:40351
pubmed: 28067309
PLoS Pathog. 2020 Dec 16;16(12):e1009127
pubmed: 33326472
Hepatology. 2008 Oct;48(4):1054-61
pubmed: 18688877
J Cell Sci. 2016 Dec 1;129(23):4424-4435
pubmed: 27793976
Prog Mol Biol Transl Sci. 2008;83:135-79
pubmed: 19186254
PLoS Pathog. 2016 Jan 04;12(1):e1005376
pubmed: 26727512
J Virol. 2007 May;81(9):4591-603
pubmed: 17301154
PLoS Pathog. 2019 Sep 16;15(9):e1008021
pubmed: 31525236
Cell Rep. 2019 Apr 9;27(2):343-358.e5
pubmed: 30970241
J Virol. 2011 Dec;85(24):13185-94
pubmed: 21994453
J Virol. 2017 Dec 14;92(1):
pubmed: 29046459
PLoS Pathog. 2015 Jan 08;11(1):e1004573
pubmed: 25569684
Cell Rep. 2019 Jun 18;27(12):3602-3617.e5
pubmed: 31216478
Autophagy. 2009 Oct;5(7):937-45
pubmed: 19625776
Biomed Res. 2015;36(2):121-33
pubmed: 25876663
Biomed Res Int. 2014;2014:265353
pubmed: 25162004
J Med Virol. 2021 Apr;93(4):2076-2083
pubmed: 33026649
J Virol. 2003 Mar;77(5):3007-19
pubmed: 12584326
Virology. 2021 Apr;556:9-22
pubmed: 33524849
J Virol. 2010 Jun;84(11):5775-89
pubmed: 20335258
Nat Commun. 2020 Nov 18;11(1):5885
pubmed: 33208793
Annu Rev Cell Dev Biol. 2011;27:107-32
pubmed: 21801009
PLoS Pathog. 2019 Jan 9;15(1):e1007530
pubmed: 30625229
mBio. 2011 Oct 04;2(5):
pubmed: 21972238
Gastroenterology. 2014 Nov;147(5):1094-105.e25
pubmed: 25046163
Autophagy. 2007 Nov-Dec;3(6):581-5
pubmed: 17700057
mBio. 2015 Jul 07;6(4):e00759
pubmed: 26152585
J Virol. 2013 Oct;87(19):10612-27
pubmed: 23885072
J Virol. 2008 Mar;82(5):2241-9
pubmed: 18077704
J Cell Biol. 2008 Aug 25;182(4):685-701
pubmed: 18725538
Cell Host Microbe. 2020 Dec 9;28(6):853-866.e5
pubmed: 33245857
PLoS Biol. 2008 Sep 16;6(9):e226
pubmed: 18798692
J Virol. 2011 Jul;85(14):6963-76
pubmed: 21543474
Autophagy. 2011 Dec;7(12):1500-13
pubmed: 22082872
Nature. 2010 May 6;465(7294):96-100
pubmed: 20410884
Cell Host Microbe. 2011 Jan 20;9(1):32-45
pubmed: 21238945
Nat Cell Biol. 2014 Nov;16(11):1069-79
pubmed: 25327288
Cell Biol Int. 2019 Dec;43(12):1492-1504
pubmed: 31293035
Trends Microbiol. 2020 Dec;28(12):1022-1033
pubmed: 32536523
Trends Cell Biol. 2006 Jul;16(7):351-61
pubmed: 16793271
Mol Ther. 2000 Aug;2(2):170-6
pubmed: 10947945
PLoS One. 2018 Oct 4;13(10):e0205189
pubmed: 30286180
J Virol. 2021 Jan 28;95(4):
pubmed: 33257477
J Virol. 2004 Sep;78(18):9977-86
pubmed: 15331731
Chem Biol. 2005 Jan;12(1):99-107
pubmed: 15664519
Cell Host Microbe. 2010 Jun 25;7(6):500-8
pubmed: 20542253
J Virol. 2002 Dec;76(24):13001-14
pubmed: 12438626
Annu Rev Virol. 2015 Nov;2(1):289-310
pubmed: 26958917
Proc Natl Acad Sci U S A. 2006 May 9;103(19):7408-13
pubmed: 16651538
Nat Commun. 2021 Dec 14;12(1):7276
pubmed: 34907161
J Biol Chem. 2014 Feb 28;289(9):6120-32
pubmed: 24415756
J Virol. 2012 Jan;86(1):302-12
pubmed: 22072780
J Biol Chem. 2012 May 25;287(22):18036-43
pubmed: 22496373
World J Virol. 2013 May 12;2(2):32-48
pubmed: 24175228
J Gen Virol. 2016 Mar;97(3):680-693
pubmed: 26727924
Virology. 2010 Sep 15;405(1):1-7
pubmed: 20580051
Biochem Biophys Res Commun. 2008 Jul 4;371(3):405-10
pubmed: 18452703
Nature. 2013 Mar 21;495(7441):389-93
pubmed: 23455425
Autophagy. 2020 Dec;16(12):2131-2139
pubmed: 32964796
Cell Microbiol. 2015 Jan;17(1):45-50
pubmed: 25287059
Autophagy. 2011 Nov;7(11):1335-47
pubmed: 21799305
Proc Natl Acad Sci U S A. 2009 Aug 18;106(33):14046-51
pubmed: 19666601
J Gen Virol. 1977 Jul;36(1):59-74
pubmed: 886304
Cytokine Growth Factor Rev. 2017 Oct;37:17-27
pubmed: 28709747
J Virol. 2012 Sep;86(18):10112-22
pubmed: 22787216
Nucleic Acids Res. 1992 Jun 11;20(11):2902
pubmed: 1614888
Crit Care Res Pract. 2010;2010:
pubmed: 20948883
Nat Med. 2005 Jul;11(7):791-6
pubmed: 15951748
J Biol Chem. 2004 Mar 12;279(11):10136-41
pubmed: 14699140
mBio. 2017 Nov 21;8(6):
pubmed: 29162711
Nat Commun. 2021 Jun 21;12(1):3818
pubmed: 34155207
STAR Protoc. 2020 Nov 25;1(3):100173
pubmed: 33377067
Sci Rep. 2016 Mar 31;6:23864
pubmed: 27029407
Nat Cell Biol. 2009 Apr;11(4):385-96
pubmed: 19270696
ACS Infect Dis. 2021 Jun 11;7(6):1457-1468
pubmed: 33570381
J Biol Chem. 1997 Jul 18;272(29):18358-66
pubmed: 9218477
J Cell Biol. 2008 May 19;181(4):655-66
pubmed: 18474623
J Virol. 2011 Oct;85(20):10561-71
pubmed: 21835792
Nat Rev Mol Cell Biol. 2013 Dec;14(12):759-74
pubmed: 24201109
PLoS Biol. 2020 Jun 8;18(6):e3000715
pubmed: 32511245
J Virol. 2006 Jun;80(11):5308-20
pubmed: 16699011
PLoS Pathog. 2012;8(12):e1003056
pubmed: 23236278