Kaposi's sarcoma-associated herpesvirus induces specialised ribosomes to efficiently translate viral lytic mRNAs.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
18 01 2023
18 01 2023
Historique:
received:
25
03
2022
accepted:
06
01
2023
entrez:
18
1
2023
pubmed:
19
1
2023
medline:
21
1
2023
Statut:
epublish
Résumé
Historically, ribosomes were viewed as unchanged homogeneous macromolecular machines with no regulatory capacity for mRNA translation. An emerging concept is that heterogeneity of ribosomal composition exists, exerting a regulatory function or specificity in translational control. This is supported by recent discoveries identifying compositionally distinct specialised ribosomes that actively regulate mRNA translation. Viruses lack their own translational machinery and impose high translational demands on the host during replication. We explore the possibility that KSHV manipulates ribosome biogenesis producing specialised ribosomes which preferentially translate viral transcripts. Quantitative proteomic analysis identified changes in the stoichiometry and composition of precursor ribosomal complexes during the switch from latent to lytic replication. We demonstrate the enhanced association of ribosomal biogenesis factors BUD23 and NOC4L, and the KSHV ORF11 protein, with small ribosomal subunit precursor complexes during lytic replication. BUD23 depletion resulted in significantly reduced viral gene expression, culminating in dramatic reduction of infectious virion production. Ribosome profiling demonstrated BUD23 is essential for reduced association of ribosomes with KSHV uORFs in late lytic genes, required for the efficient translation of the downstream coding sequence. Results provide mechanistic insights into KSHV-mediated manipulation of cellular ribosome composition inducing a population of specialised ribosomes facilitating efficient translation of viral mRNAs.
Identifiants
pubmed: 36653366
doi: 10.1038/s41467-023-35914-5
pii: 10.1038/s41467-023-35914-5
pmc: PMC9849454
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
300Subventions
Organisme : Wellcome Trust
Pays : United Kingdom
Informations de copyright
© 2023. The Author(s).
Références
J Biol Chem. 2001 Jun 8;276(23):19905-12
pubmed: 11278515
Hum Mol Genet. 2016 Dec 15;25(24):5353-5364
pubmed: 27798105
Wiley Interdiscip Rev RNA. 2021 Jul;12(4):e1644
pubmed: 33565275
Nat Methods. 2012 Mar 04;9(4):357-9
pubmed: 22388286
Nat Rev Mol Cell Biol. 2021 Feb;22(2):96-118
pubmed: 33353982
Nat Struct Mol Biol. 2017 Mar;24(3):214-220
pubmed: 28112732
Nat Commun. 2016 Jun 06;7:11390
pubmed: 27265389
Genes Dev. 2016 Mar 15;30(6):718-32
pubmed: 26980190
Nat Microbiol. 2016 Oct 31;2:16201
pubmed: 27798559
Nat Struct Mol Biol. 2012 Aug;19(8):744-53
pubmed: 22751017
Biochemistry. 2018 Jul 3;57(26):3537-3539
pubmed: 29894169
EMBO J. 2019 Jul 1;38(13):e100278
pubmed: 31268599
Bioinformatics. 2014 Apr 1;30(7):923-30
pubmed: 24227677
Nucleic Acids Res. 2014 Dec 16;42(22):e168
pubmed: 25300484
Nat Struct Mol Biol. 2017 Sep;24(9):700-707
pubmed: 28759050
Cell Rep. 2020 May 5;31(5):107611
pubmed: 32375039
Nucleic Acids Res. 2010 Apr;38(7):2387-98
pubmed: 20047967
Genome Biol. 2018 Dec 27;19(1):229
pubmed: 30591072
Bioinformatics. 2017 Jun 01;33(11):1735-1737
pubmed: 28158331
J Virol. 2013 Dec;87(24):13853-67
pubmed: 24109239
RNA. 2015 Feb;21(2):180-7
pubmed: 25525153
Front Physiol. 2018 Jul 24;9:910
pubmed: 30087616
Mol Cell Biol. 2012 Jun;32(12):2254-67
pubmed: 22493060
Genome Biol. 2014;15(12):550
pubmed: 25516281
EMBO J. 2017 Apr 3;36(7):854-868
pubmed: 28179369
PLoS Pathog. 2015 Nov 20;11(11):e1005274
pubmed: 26587836
Annu Rev Pathol. 2006;1:273-96
pubmed: 18039116
J Biol Chem. 1966 Dec 25;241(24):5936-40
pubmed: 5954370
Proc Natl Acad Sci U S A. 2013 Jan 2;110(1):324-9
pubmed: 23169626
J Biol Chem. 2016 Mar 18;291(12):6546-58
pubmed: 26817837
Trends Biochem Sci. 2019 Sep;44(9):782-794
pubmed: 31003826
J Cell Biol. 2010 Sep 6;190(5):853-66
pubmed: 20819938
Am J Hum Genet. 2009 Jun;84(6):728-39
pubmed: 19463982
Biophys J. 2008 Apr 1;94(7):2884-90
pubmed: 18096629
Elife. 2020 Jan 15;9:
pubmed: 31939735
RNA Biol. 2020 Jan;17(1):150-164
pubmed: 31566069
J Virol. 1988 Aug;62(8):2636-43
pubmed: 2839690
Anal Bioanal Chem. 2012 Sep;404(4):939-65
pubmed: 22772140
J Cell Sci. 2013 Nov 1;126(Pt 21):4815-21
pubmed: 24172536
Mol Med Rep. 2015 Jan;11(1):295-302
pubmed: 25352209
J Virol. 2012 Jan;86(1):594-8
pubmed: 22013050
Elife. 2021 Apr 28;10:
pubmed: 33908345
Curr Opin Virol. 2018 Oct;32:60-70
pubmed: 30268927
Bioinformatics. 2010 Jan 1;26(1):139-40
pubmed: 19910308
J Virol. 2015 Oct 14;90(1):356-67
pubmed: 26468525
EMBO Rep. 2022 May 4;23(5):e54117
pubmed: 35239998
Sci Rep. 2017 Mar 23;7(1):329
pubmed: 28336944
Elife. 2019 Oct 24;8:
pubmed: 31647415
Bioinformatics. 2013 Jan 1;29(1):15-21
pubmed: 23104886
PLoS One. 2017 May 10;12(5):e0175963
pubmed: 28489911
J Virol. 2003 Apr;77(7):4205-20
pubmed: 12634378
Cell. 2011 Apr 29;145(3):383-397
pubmed: 21529712
Cell. 2016 Jul 14;166(2):380-393
pubmed: 27419870
Paediatr Anaesth. 2019 May;29(5):483-490
pubmed: 30811742
PLoS Pathog. 2018 Sep 6;14(9):e1007276
pubmed: 30188954
Annu Rev Biochem. 2015;84:93-129
pubmed: 25706898
Nucleic Acids Res. 2016 Sep 19;44(16):7884-95
pubmed: 27257078
Nature. 2018 Jun;558(7709):249-253
pubmed: 29875412
Front Mol Biosci. 2022 Jan 25;8:791455
pubmed: 35145996
Nature. 1988 Jul 28;334(6180):320-5
pubmed: 2839775
Bioinformatics. 2009 Aug 15;25(16):2078-9
pubmed: 19505943
PLoS Pathog. 2014 Jan;10(1):e1003847
pubmed: 24453964
Nucleic Acids Res. 2016 Oct 14;44(18):8951-8961
pubmed: 27325748
EMBO J. 2018 Apr 3;37(7):
pubmed: 29459436
Trends Biochem Sci. 2015 Oct;40(10):560-575
pubmed: 26410597
Nature. 2018 Jul;559(7712):130-134
pubmed: 29950728
RNA. 2021 Sep;27(9):1082-1101
pubmed: 34193551
Nature. 2017 Jun 29;546(7660):651-655
pubmed: 28636603
J Gen Virol. 2004 Jan;85(Pt 1):147-153
pubmed: 14718629