UAP56/DDX39B is a major cotranscriptional RNA-DNA helicase that unwinds harmful R loops genome-wide.


Journal

Genes & development
ISSN: 1549-5477
Titre abrégé: Genes Dev
Pays: United States
ID NLM: 8711660

Informations de publication

Date de publication:
01 07 2020
Historique:
received: 13 12 2019
accepted: 20 04 2020
pubmed: 23 5 2020
medline: 11 11 2020
entrez: 23 5 2020
Statut: ppublish

Résumé

Nonscheduled R loops represent a major source of DNA damage and replication stress. Cells have different ways to prevent R-loop accumulation. One mechanism relies on the conserved THO complex in association with cotranscriptional RNA processing factors including the RNA-dependent ATPase UAP56/DDX39B and histone modifiers such as the SIN3 deacetylase in humans. We investigated the function of UAP56/DDX39B in R-loop removal. We show that UAP56 depletion causes R-loop accumulation, R-loop-mediated genome instability, and replication fork stalling. We demonstrate an RNA-DNA helicase activity in UAP56 and show that its overexpression suppresses R loops and genome instability induced by depleting five different unrelated factors. UAP56/DDX39B localizes to active chromatin and prevents the accumulation of RNA-DNA hybrids over the entire genome. We propose that, in addition to its RNA processing role, UAP56/DDX39B is a key helicase required to eliminate harmful cotranscriptional RNA structures that otherwise would block transcription and replication.

Identifiants

pubmed: 32439635
pii: gad.336024.119
doi: 10.1101/gad.336024.119
pmc: PMC7328515
doi:

Substances chimiques

Chromatin 0
DDX39B protein, human EC 3.6.1.-
DEAD-box RNA Helicases EC 3.6.4.13

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

Pagination

898-912

Subventions

Organisme : NIEHS NIH HHS
ID : R21 ES028792
Pays : United States
Organisme : NCI NIH HHS
ID : R35 CA241801
Pays : United States

Commentaires et corrections

Type : ErratumIn

Informations de copyright

© 2020 Pérez-Calero et al.; Published by Cold Spring Harbor Laboratory Press.

Références

Mol Cell. 2012 Mar 30;45(6):814-25
pubmed: 22387027
Mol Microbiol. 2006 Feb;59(3):723-30
pubmed: 16420346
Mol Cell. 2003 Sep;12(3):711-21
pubmed: 14527416
Nat Cell Biol. 2009 Nov;11(11):1315-24
pubmed: 19838172
Nucleic Acids Res. 2014 Aug;42(14):9047-62
pubmed: 25030905
Proc Natl Acad Sci U S A. 2018 Oct 23;115(43):11024-11029
pubmed: 30301808
Nucleic Acids Res. 2018 Jan 4;46(D1):D754-D761
pubmed: 29155950
Nat Rev Mol Cell Biol. 2011 Jul 22;12(8):505-16
pubmed: 21779027
J Biol Chem. 2007 Aug 3;282(31):22544-50
pubmed: 17562711
Science. 2007 Jun 8;316(5830):1497-502
pubmed: 17540862
PLoS Genet. 2015 Nov 19;11(11):e1005674
pubmed: 26584049
Bioinformatics. 2009 Jul 15;25(14):1754-60
pubmed: 19451168
DNA Repair (Amst). 2011 Jun 10;10(6):654-65
pubmed: 21561811
Genes Dev. 2014 Apr 1;28(7):735-48
pubmed: 24636987
Genes Dev. 2017 Jul 1;31(13):1370-1381
pubmed: 28790157
EMBO Rep. 2019 Sep;20(9):e47250
pubmed: 31338941
Cell Rep. 2018 May 8;23(6):1891-1905
pubmed: 29742442
Mol Cell. 2018 Apr 19;70(2):312-326.e7
pubmed: 29656924
Nucleic Acids Res. 2016 Jul 8;44(W1):W160-5
pubmed: 27079975
Mol Cell. 2007 Oct 26;28(2):253-63
pubmed: 17964264
Nature. 2014 Jul 17;511(7509):362-5
pubmed: 24896180
Mol Cell. 2011 Jun 24;42(6):794-805
pubmed: 21700224
Cell. 2019 Oct 17;179(3):604-618
pubmed: 31607512
Nat Biotechnol. 2019 Aug;37(8):907-915
pubmed: 31375807
Mol Cell. 2009 Jul 31;35(2):228-39
pubmed: 19647519
Nat Rev Genet. 2015 Oct;16(10):583-97
pubmed: 26370899
Cell. 2016 Nov 3;167(4):1001-1013.e7
pubmed: 27881299
EMBO J. 2019 Aug 1;38(15):e100986
pubmed: 31267554
EMBO J. 2002 Jul 1;21(13):3526-35
pubmed: 12093753
Cell Rep. 2017 Jan 10;18(2):334-343
pubmed: 28076779
Mol Cell. 2016 Jul 7;63(1):167-78
pubmed: 27373332
RNA. 2013 Oct;19(10):1363-71
pubmed: 23962665
Mol Cell. 2014 Dec 18;56(6):777-85
pubmed: 25435140
Nat Protoc. 2019 Jun;14(6):1734-1755
pubmed: 31053798
PLoS Genet. 2014 Apr 17;10(4):e1004288
pubmed: 24743342
Methods Mol Biol. 2018;1672:347-361
pubmed: 29043635
Genes Dev. 2018 Jul 1;32(13-14):965-977
pubmed: 29954833
Mol Cell Biol. 2016 Oct 28;36(22):2794-2810
pubmed: 27550810
Mol Cell. 2015 Feb 19;57(4):636-647
pubmed: 25699710
PLoS Genet. 2011 Dec;7(12):e1002386
pubmed: 22144908
Mol Cell Biol. 2006 Apr;26(8):3327-34
pubmed: 16581804
EMBO J. 2011 Jun 24;30(15):3106-19
pubmed: 21701562
Mol Cell. 2015 Nov 5;60(3):351-61
pubmed: 26593718
Genome Biol. 2008;9(9):R137
pubmed: 18798982
Nature. 2002 May 16;417(6886):304-8
pubmed: 11979277
Genes Dev. 2010 Jul 15;24(14):1546-58
pubmed: 20634320
Nat Methods. 2012 Mar 04;9(4):357-9
pubmed: 22388286
Bioinformatics. 2015 Jul 15;31(14):2382-3
pubmed: 25765347
Genes Dev. 2019 Aug 1;33(15-16):1008-1026
pubmed: 31123061
EMBO J. 2002 Feb 1;21(3):195-201
pubmed: 11823412
Mol Cell. 2017 Jun 1;66(5):597-609.e5
pubmed: 28575656
Genes Dev. 2016 Jun 1;30(11):1327-38
pubmed: 27298336
Nat Struct Mol Biol. 2017 May 4;24(5):439-443
pubmed: 28471430
EMBO J. 2017 Dec 1;36(23):3532-3547
pubmed: 29074626
EMBO J. 2000 Nov 1;19(21):5824-34
pubmed: 11060033
Cell. 2005 Aug 12;122(3):365-78
pubmed: 16096057
Genes Dev. 2019 Dec 1;33(23-24):1751-1774
pubmed: 31753913
Bioinformatics. 2009 Aug 15;25(16):2078-9
pubmed: 19505943
Nucleic Acids Res. 2016 Jan 4;44(D1):D726-32
pubmed: 26527727
J Mol Biol. 2018 Feb 2;430(3):272-284
pubmed: 29289567
Bioinformatics. 2010 Mar 15;26(6):841-2
pubmed: 20110278
Aging Cell. 2011 Aug;10(4):557-71
pubmed: 21388492
EMBO J. 2012 Mar 21;31(6):1605-16
pubmed: 22314234
Cell. 2017 Aug 10;170(4):774-786.e19
pubmed: 28802045
Mol Cell Biol. 2008 Oct;28(20):6413-25
pubmed: 18710941
Nat Commun. 2018 Feb 7;9(1):533
pubmed: 29416069
EMBO J. 2017 May 2;36(9):1182-1198
pubmed: 28314779

Auteurs

Carmen Pérez-Calero (C)

Centro Andaluz de Biología Molecular y Medicina Regenerativa (CABIMER) Universidad de Sevilla-CSIC-Universidad Pablo de Olavide, Sevilla 41092, Spain.

Aleix Bayona-Feliu (A)

Centro Andaluz de Biología Molecular y Medicina Regenerativa (CABIMER) Universidad de Sevilla-CSIC-Universidad Pablo de Olavide, Sevilla 41092, Spain.

Xiaoyu Xue (X)

Molecular Biophysics and Biochemistry, School of Medicine, University of Yale, New Haven, Connecticut 06510, USA.
Department of Chemistry and Biochemistry, Texas State University, San Marcos, Texas 78666, USA.

Sonia I Barroso (SI)

Centro Andaluz de Biología Molecular y Medicina Regenerativa (CABIMER) Universidad de Sevilla-CSIC-Universidad Pablo de Olavide, Sevilla 41092, Spain.

Sergio Muñoz (S)

Centro Andaluz de Biología Molecular y Medicina Regenerativa (CABIMER) Universidad de Sevilla-CSIC-Universidad Pablo de Olavide, Sevilla 41092, Spain.

Víctor M González-Basallote (VM)

Centro Andaluz de Biología Molecular y Medicina Regenerativa (CABIMER) Universidad de Sevilla-CSIC-Universidad Pablo de Olavide, Sevilla 41092, Spain.

Patrick Sung (P)

Molecular Biophysics and Biochemistry, School of Medicine, University of Yale, New Haven, Connecticut 06510, USA.
Department of Biochemistry and Structural Biology, University of Texas Health Science Center at San Antonio, San Antonio, Texas 78229, USA.

Andrés Aguilera (A)

Centro Andaluz de Biología Molecular y Medicina Regenerativa (CABIMER) Universidad de Sevilla-CSIC-Universidad Pablo de Olavide, Sevilla 41092, Spain.

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