HSV-1 exploits host heterochromatin for nuclear egress.
Journal
The Journal of cell biology
ISSN: 1540-8140
Titre abrégé: J Cell Biol
Pays: United States
ID NLM: 0375356
Informations de publication
Date de publication:
04 09 2023
04 09 2023
Historique:
received:
28
04
2023
revised:
13
06
2023
accepted:
14
06
2023
medline:
31
7
2023
pubmed:
30
7
2023
entrez:
30
7
2023
Statut:
ppublish
Résumé
Herpes simplex virus (HSV-1) progeny form in the nucleus and exit to successfully infect other cells. Newly formed capsids navigate complex chromatin architecture to reach the inner nuclear membrane (INM) and egress. Here, we demonstrate by transmission electron microscopy (TEM) that HSV-1 capsids traverse heterochromatin associated with trimethylation on histone H3 lysine 27 (H3K27me3) and the histone variant macroH2A1. Through chromatin profiling during infection, we revealed global redistribution of these marks whereby massive host genomic regions bound by macroH2A1 and H3K27me3 correlate with decreased host transcription in active compartments. We found that the loss of these markers resulted in significantly lower viral titers but did not impact viral genome or protein accumulation. Strikingly, we discovered that loss of macroH2A1 or H3K27me3 resulted in nuclear trapping of capsids. Finally, by live-capsid tracking, we quantified this decreased capsid movement. Thus, our work demonstrates that HSV-1 takes advantage of the dynamic nature of host heterochromatin formation during infection for efficient nuclear egress.
Identifiants
pubmed: 37516914
pii: 276130
doi: 10.1083/jcb.202304106
pmc: PMC10373338
pii:
doi:
Substances chimiques
Chromatin
0
Heterochromatin
0
Histones
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Wellcome Trust
ID : 209250/Z/17/Z
Pays : United Kingdom
Organisme : NIGMS NIH HHS
ID : R35 GM133434
Pays : United States
Organisme : NIAID NIH HHS
ID : T32 AI083203
Pays : United States
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : NIGMS NIH HHS
ID : R35 GM133441
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA015704
Pays : United States
Informations de copyright
© 2023 Lewis et al.
Références
J Biol Chem. 2011 Jul 8;286(27):23852-64
pubmed: 21532035
PLoS Pathog. 2014 Nov 06;10(11):e1004503
pubmed: 25375629
Proc Natl Acad Sci U S A. 2015 Oct 20;112(42):E5725-33
pubmed: 26438852
Curr Issues Mol Biol. 2021;41:125-170
pubmed: 32764158
Curr Hematol Malig Rep. 2018 Oct;13(5):369-382
pubmed: 30112706
PLoS Pathog. 2021 Jan 26;17(1):e1009088
pubmed: 33497413
Antiviral Res. 2020 Apr;176:104730
pubmed: 32014498
Viruses. 2021 Nov 24;13(12):
pubmed: 34960625
Viruses. 2021 Apr 25;13(5):
pubmed: 33923040
J Gen Virol. 1973 Mar;18(3):329-46
pubmed: 4348796
Nat Commun. 2019 Apr 29;10(1):1930
pubmed: 31036827
Proc Natl Acad Sci U S A. 2005 Apr 19;102(16):5844-9
pubmed: 15824307
Mol Cell Proteomics. 2017 Apr;16(4 suppl 1):S92-S107
pubmed: 28179408
PLoS Pathog. 2021 Dec 15;17(12):e1010132
pubmed: 34910768
J Virol. 2005 Oct;79(20):12840-51
pubmed: 16188986
Bioinformatics. 2012 Aug 15;28(16):2184-5
pubmed: 22743226
Science. 2009 Oct 9;326(5950):289-93
pubmed: 19815776
PLoS Comput Biol. 2013;9(8):e1003118
pubmed: 23950696
Bioinformatics. 2014 Apr 1;30(7):923-30
pubmed: 24227677
Sci Rep. 2016 Jun 28;6:28844
pubmed: 27349677
Curr Biol. 2021 Dec 6;31(23):5227-5237.e7
pubmed: 34666003
Mol Cell. 2016 Jul 21;63(2):318-328
pubmed: 27447986
Cell Microbiol. 2013 Feb;15(2):248-69
pubmed: 23186167
Cell. 2014 Dec 18;159(7):1665-80
pubmed: 25497547
J Cell Biol. 2010 Nov 15;191(4):721-9
pubmed: 21059850
PLoS Pathog. 2018 Mar 26;14(3):e1006954
pubmed: 29579120
Nat Commun. 2014 Jun 11;5:4131
pubmed: 24916797
Cold Spring Harb Perspect Biol. 2012 Sep 01;4(9):a013011
pubmed: 22952399
Nucleic Acids Res. 2019 Jul 2;47(W1):W199-W205
pubmed: 31114916
J Virol. 1990 Feb;64(2):563-73
pubmed: 2153224
Nature. 2010 Dec 23;468(7327):1105-9
pubmed: 21179167
Nature. 2011 Jan 20;469(7330):343-9
pubmed: 21248841
Mol Ther Nucleic Acids. 2014 Feb 04;3:e146
pubmed: 24496438
J Virol. 2004 Jun;78(11):5591-600
pubmed: 15140956
Nat Methods. 2012 Jun 28;9(7):676-82
pubmed: 22743772
Mol Cancer Ther. 2014 Apr;13(4):842-54
pubmed: 24563539
J Virol. 2003 Dec;77(24):13182-93
pubmed: 14645575
Cell Cycle. 2010 Jul 1;9(13):2568-74
pubmed: 20543561
Sci Rep. 2017 Jun 16;7(1):3692
pubmed: 28623258
Bioinformatics. 2010 Jan 1;26(1):139-40
pubmed: 19910308
Nat Cell Biol. 2000 Sep;2(9):661-5
pubmed: 10980708
J Virol. 1972 Nov;10(5):1044-52
pubmed: 4344252
mBio. 2017 Aug 15;8(4):
pubmed: 28811345
Nat Rev Microbiol. 2008 Mar;6(3):211-21
pubmed: 18264117
Bioinformatics. 2013 Jan 1;29(1):15-21
pubmed: 23104886
J Virol. 2006 Mar;80(5):2582-4
pubmed: 16474165
Virology. 2006 Apr 10;347(2):261-76
pubmed: 16427676
Sci Rep. 2015 Nov 25;5:17186
pubmed: 26603343
mBio. 2014 Oct 07;5(5):e01909-14
pubmed: 25293761
Nat Rev Cancer. 2021 Apr;21(4):257-275
pubmed: 33568791
J Virol. 2021 Mar 3;95(10):
pubmed: 33658339
Virology. 2010 Oct 10;406(1):127-37
pubmed: 20674954
Mol Cancer Ther. 2017 Nov;16(11):2586-2597
pubmed: 28835384
Intervirology. 2001;44(4):232-42
pubmed: 11509886
Proc Natl Acad Sci U S A. 2015 Apr 7;112(14):4471-6
pubmed: 25831500
J Cell Sci. 2017 May 1;130(9):1570-1582
pubmed: 28283545
Bioinformatics. 2010 Mar 15;26(6):841-2
pubmed: 20110278
Nat Rev Cancer. 2010 Jul;10(7):457-69
pubmed: 20574448
Viruses. 2019 Oct 11;11(10):
pubmed: 31614678
EMBO Rep. 2018 Oct;19(10):
pubmed: 30177554
Nat Methods. 2022 Jul;19(7):829-832
pubmed: 35654950
J Virol. 1992 May;66(5):2904-15
pubmed: 1313909
Immunoinformatics (Amst). 2021 Oct;1-2:
pubmed: 37034276