Lytic Reactivation of the Kaposi's Sarcoma-Associated Herpesvirus (KSHV) Is Accompanied by Major Nucleolar Alterations.

2′-O-methylation FBL Fibrillarin KSHV Kaposi’s sarcoma-associated herpesvirus UBF nucleolus nucleophosmin (NPM1/B23) pseudouridylation ribosomal RNA (rRNA) upstream binding factor

Journal

Viruses
ISSN: 1999-4915
Titre abrégé: Viruses
Pays: Switzerland
ID NLM: 101509722

Informations de publication

Date de publication:
04 08 2022
Historique:
received: 14 06 2022
revised: 21 07 2022
accepted: 28 07 2022
entrez: 26 8 2022
pubmed: 27 8 2022
medline: 30 8 2022
Statut: epublish

Résumé

The nucleolus is a subnuclear compartment whose primary function is the biogenesis of ribosomal subunits. Certain viral infections affect the morphology and composition of the nucleolar compartment and influence ribosomal RNA (rRNA) transcription and maturation. However, no description of nucleolar morphology and function during infection with Kaposi's sarcoma-associated herpesvirus (KSHV) is available to date. Using immunofluorescence microscopy, we documented extensive destruction of the nuclear and nucleolar architecture during the lytic reactivation of KSHV. This was manifested by the redistribution of key nucleolar proteins, including the rRNA transcription factor UBF. Distinct delocalization patterns were evident; certain nucleolar proteins remained together whereas others dissociated, implying that nucleolar proteins undergo nonrandom programmed dispersion. Significantly, the redistribution of UBF was dependent on viral DNA replication or late viral gene expression. No significant changes in pre-rRNA levels and no accumulation of pre-rRNA intermediates were found by RT-qPCR and Northern blot analysis. Furthermore, fluorescent in situ hybridization (FISH), combined with immunofluorescence, revealed an overlap between Fibrillarin and internal transcribed spacer 1 (ITS1), which represents the primary product of the pre-rRNA, suggesting that the processing of rRNA proceeds during lytic reactivation. Finally, small changes in the levels of pseudouridylation (Ψ) and 2'-

Identifiants

pubmed: 36016343
pii: v14081720
doi: 10.3390/v14081720
pmc: PMC9412354
pii:
doi:

Substances chimiques

DNA, Viral 0
Nuclear Proteins 0
RNA Precursors 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Références

J Cell Sci. 2006 Jun 15;119(Pt 12):2621-31
pubmed: 16763197
Trends Biochem Sci. 2002 Jul;27(7):344-51
pubmed: 12114023
Nat Struct Mol Biol. 2021 Nov;28(11):889-899
pubmed: 34759377
Mol Cell Proteomics. 2017 Dec;16(12):2079-2097
pubmed: 28972080
PLoS Pathog. 2018 Mar 2;14(3):e1006937
pubmed: 29499066
Curr Opin Cell Biol. 2018 Jun;52:105-111
pubmed: 29529563
Cells. 2021 Jun 25;10(7):
pubmed: 34202380
Front Microbiol. 2012 Feb 20;3:59
pubmed: 22363332
Mol Cell. 2011 Nov 18;44(4):660-6
pubmed: 22099312
Biochem Biophys Res Commun. 2010 Jul 2;397(3):520-5
pubmed: 20515658
J Virol. 2005 Oct;79(20):12840-51
pubmed: 16188986
PLoS Pathog. 2015 May 12;11(5):e1004899
pubmed: 25965334
Methods Enzymol. 2007;425:21-53
pubmed: 17673078
Angew Chem Int Ed Engl. 2015 Jan 7;54(2):451-5
pubmed: 25417815
Nucleic Acids Res. 2020 Nov 4;48(19):e110
pubmed: 32976574
J Virol. 2010 Mar;84(6):2935-45
pubmed: 20042497
J Mol Biol. 2001 Aug 3;311(1):41-55
pubmed: 11469856
Cell. 2014 Sep 25;159(1):148-162
pubmed: 25219674
J Cell Sci. 1996 Jan;109 ( Pt 1):119-29
pubmed: 8834797
FEBS Lett. 2007 Jul 10;581(17):3283-8
pubmed: 17602943
Virology. 2012 Oct 25;432(2):283-95
pubmed: 22717133
Virology. 2011 Apr 10;412(2):341-8
pubmed: 21316727
J Virol. 1998 Aug;72(8):6699-709
pubmed: 9658117
Cell Microbiol. 2011 Jun;13(6):806-13
pubmed: 21501365
Nat Rev Mol Cell Biol. 2007 Jul;8(7):574-85
pubmed: 17519961
J Virol. 2010 May;84(9):4810-5
pubmed: 20147409
FEBS J. 2020 Jan;287(1):205-217
pubmed: 31365788
Virology. 2004 Oct 10;328(1):7-18
pubmed: 15380353
J Gen Virol. 2005 Aug;86(Pt 8):2315-2322
pubmed: 16033979
Proc Natl Acad Sci U S A. 2006 Oct 10;103(41):15190-5
pubmed: 17005724
J Gen Virol. 1997 Feb;78 ( Pt 2):435-43
pubmed: 9018067
PLoS Pathog. 2010 Mar 19;6(3):e1000818
pubmed: 20333249
Virology. 2007 Jul 5;363(2):397-409
pubmed: 17346762
RNA Biol. 2017 Sep 2;14(9):1138-1152
pubmed: 27911188
Cell Microbiol. 2015 Aug;17(8):1108-20
pubmed: 26041433
Microbes Infect. 2019 Jan - Feb;21(1):20-32
pubmed: 29953921
Genes Dev. 2002 Oct 1;16(19):2465-78
pubmed: 12368257
J Virol. 2008 Mar;82(6):2867-82
pubmed: 18199640
Biochim Biophys Acta Gene Regul Mech. 2019 Mar;1862(3):253-269
pubmed: 30572123
mBio. 2012 Feb 07;3(1):
pubmed: 22318319
Biomolecules. 2018 Jun 05;8(2):
pubmed: 29874862
J Virol. 1990 Feb;64(2):881-5
pubmed: 2404140
Cell Rep. 2013 Oct 17;5(1):237-47
pubmed: 24120868
Virology. 2019 Mar;529:205-215
pubmed: 30735904
J Gen Virol. 2009 Jan;90(Pt 1):69-73
pubmed: 19088274
J Virol Methods. 2011 Jun;174(1-2):12-21
pubmed: 21419799
J Virol. 2006 Oct;80(20):10073-82
pubmed: 17005685
J Gen Virol. 2020 Aug;101(8):873-883
pubmed: 32501196
RNA. 2010 Jan;16(1):131-40
pubmed: 19934231
Mol Cell. 2003 Feb;11(2):425-35
pubmed: 12620230
Proc Natl Acad Sci U S A. 2010 Jun 1;107(22):10220-5
pubmed: 20479244
J Virol. 2014 Nov;88(21):12839-52
pubmed: 25165104
PLoS Pathog. 2011 May;7(5):e1002054
pubmed: 21625536
Viruses. 2018 Apr 20;10(4):
pubmed: 29677136
Arch Virol. 2002 Jun;147(6):1077-89
pubmed: 12111420
J Virol. 2000 Dec;74(23):10920-9
pubmed: 11069986
Nature. 2017 Nov 23;551(7681):472-477
pubmed: 29143818
J Clin Med. 2019 Sep 07;8(9):
pubmed: 31500286
Biochim Biophys Acta. 2014 Jun;1842(6):840-7
pubmed: 24378568
J Biol Chem. 2019 Dec 13;294(50):19365-19380
pubmed: 31662437
Curr Opin HIV AIDS. 2017 Jan;12(1):47-56
pubmed: 27662501
RNA Biol. 2020 Jul;17(7):1018-1039
pubmed: 32250712
Nat Cell Biol. 2000 Sep;2(9):661-5
pubmed: 10980708
Biochemistry. 1993 Sep 21;32(37):9754-62
pubmed: 8373778
Virol Sin. 2019 Apr;34(2):135-161
pubmed: 31025296
Histochem Cell Biol. 2018 Dec;150(6):607-629
pubmed: 30105457
Proteomics. 2010 Nov;10(22):4077-86
pubmed: 20661956
Sci Rep. 2016 May 04;6:25296
pubmed: 27142987
J Virol. 2010 Feb;84(4):1771-84
pubmed: 20007282
Nucleic Acids Res. 2009 Dec;37(22):7665-77
pubmed: 19820108
J Virol. 1998 Sep;72(9):7697-702
pubmed: 9696879
Bioinformatics. 2013 Jan 1;29(1):15-21
pubmed: 23104886
PLoS Pathog. 2014 Jan;10(1):e1003863
pubmed: 24453968
J Virol. 2003 Apr;77(7):4205-20
pubmed: 12634378
Trends Cell Biol. 2019 Aug;29(8):647-659
pubmed: 31176528
Proc Natl Acad Sci U S A. 2017 Dec 5;114(49):12934-12939
pubmed: 29158377
Virology. 1998 Jan 5;240(1):118-26
pubmed: 9448696
Virology. 2003 May 10;309(2):232-47
pubmed: 12758171
J Gen Virol. 2008 May;89(Pt 5):1142-1151
pubmed: 18420791
Int J Mol Sci. 2017 Jul 01;18(7):
pubmed: 28671574
Curr Opin Cell Biol. 2018 Jun;52:154-161
pubmed: 29723661
J Virol. 2008 May;82(10):4762-73
pubmed: 18321972
Cells. 2019 Aug 10;8(8):
pubmed: 31405125
Biochem Biophys Res Commun. 1989 Aug 15;162(3):963-70
pubmed: 2788417
Rev Med Virol. 2009 Jul;19(4):201-14
pubmed: 19399920
J Virol. 2001 Jan;75(2):1031-8
pubmed: 11134316
J Pathol. 2015 Jan;235(2):368-80
pubmed: 25212381
World J Clin Oncol. 2018 Jun 10;9(3):42-55
pubmed: 29900123
J Biol Chem. 2003 Dec 19;278(51):51469-78
pubmed: 14532264
J Virol. 2009 Apr;83(7):3342-64
pubmed: 19158252
Genes (Basel). 2019 Feb 05;10(2):
pubmed: 30764532
J Virol. 2017 May 12;91(11):
pubmed: 28331082
Curr Opin Virol. 2013 Jun;3(3):238-44
pubmed: 23769237
Bioinformatics. 2009 Aug 15;25(16):2078-9
pubmed: 19505943
Biomolecules. 2018 Oct 03;8(4):
pubmed: 30282949
Nat Med. 1997 Mar;3(3):293-8
pubmed: 9055856
J Virol. 2012 Sep;86(18):9708-20
pubmed: 22740391
NAR Cancer. 2020 Dec 22;2(4):zcaa035
pubmed: 34316692
RNA Biol. 2021 Oct 15;18(sup1):88-97
pubmed: 34503375
J Virol. 2005 Feb;79(4):2626-30
pubmed: 15681463
Cold Spring Harb Perspect Biol. 2011 Mar 01;3(3):
pubmed: 21106648
Mol Cell. 2018 Aug 2;71(3):364-374
pubmed: 30075139
Wiley Interdiscip Rev RNA. 2015 Mar-Apr;6(2):173-89
pubmed: 25363811
Nat Rev Cancer. 2010 Oct;10(10):707-19
pubmed: 20865011
Bioinformatics. 2010 Mar 15;26(6):841-2
pubmed: 20110278
J Virol. 2018 Jun 13;92(13):
pubmed: 29643239
J Virol. 2016 Dec 16;91(1):
pubmed: 27795408
Proc Natl Acad Sci U S A. 1997 Jan 21;94(2):690-4
pubmed: 9012846
Science. 1994 Dec 16;266(5192):1865-9
pubmed: 7997879

Auteurs

Nofar Atari (N)

The Mina and Everard Goodman Faculty of Life Sciences, Advanced Materials and Nanotechnology Institute, Bar-Ilan University, Ramat-Gan 5290002, Israel.

K Shanmugha Rajan (KS)

The Mina and Everard Goodman Faculty of Life Sciences, Advanced Materials and Nanotechnology Institute, Bar-Ilan University, Ramat-Gan 5290002, Israel.

Vaibhav Chikne (V)

The Mina and Everard Goodman Faculty of Life Sciences, Advanced Materials and Nanotechnology Institute, Bar-Ilan University, Ramat-Gan 5290002, Israel.

Smadar Cohen-Chalamish (S)

The Mina and Everard Goodman Faculty of Life Sciences, Advanced Materials and Nanotechnology Institute, Bar-Ilan University, Ramat-Gan 5290002, Israel.

Tirza Doniger (T)

The Mina and Everard Goodman Faculty of Life Sciences, Advanced Materials and Nanotechnology Institute, Bar-Ilan University, Ramat-Gan 5290002, Israel.

Odelia Orbaum (O)

The Mina and Everard Goodman Faculty of Life Sciences, Advanced Materials and Nanotechnology Institute, Bar-Ilan University, Ramat-Gan 5290002, Israel.

Avi Jacob (A)

The Mina and Everard Goodman Faculty of Life Sciences, Advanced Materials and Nanotechnology Institute, Bar-Ilan University, Ramat-Gan 5290002, Israel.

Inna Kalt (I)

The Mina and Everard Goodman Faculty of Life Sciences, Advanced Materials and Nanotechnology Institute, Bar-Ilan University, Ramat-Gan 5290002, Israel.

Shulamit Michaeli (S)

The Mina and Everard Goodman Faculty of Life Sciences, Advanced Materials and Nanotechnology Institute, Bar-Ilan University, Ramat-Gan 5290002, Israel.

Ronit Sarid (R)

The Mina and Everard Goodman Faculty of Life Sciences, Advanced Materials and Nanotechnology Institute, Bar-Ilan University, Ramat-Gan 5290002, Israel.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH