Interaction with single-stranded DNA-binding protein localizes ribonuclease HI to DNA replication forks and facilitates R-loop removal.
DNA replication
genome maintenance
transcription
Journal
Molecular microbiology
ISSN: 1365-2958
Titre abrégé: Mol Microbiol
Pays: England
ID NLM: 8712028
Informations de publication
Date de publication:
09 2020
09 2020
Historique:
received:
03
01
2020
revised:
30
04
2020
accepted:
09
05
2020
pubmed:
20
5
2020
medline:
10
6
2021
entrez:
20
5
2020
Statut:
ppublish
Résumé
DNA replication complexes (replisomes) routinely encounter proteins and unusual nucleic acid structures that can impede their progress. Barriers can include transcription complexes and R-loops that form when RNA hybridizes with complementary DNA templates behind RNA polymerases. Cells encode several RNA polymerase and R-loop clearance mechanisms to limit replisome exposure to these potential obstructions. One such mechanism is hydrolysis of R-loops by ribonuclease HI (RNase HI). Here, we examine the cellular role of the interaction between Escherichia coli RNase HI and the single-stranded DNA-binding protein (SSB) in this process. Interaction with SSB localizes RNase HI foci to DNA replication sites. Mutation of rnhA to encode an RNase HI variant that cannot interact with SSB but that maintains enzymatic activity (rnhAK60E) eliminates RNase HI foci. The mutation also produces a media-dependent slow-growth phenotype and an activated DNA damage response in cells lacking Rep helicase, which is an enzyme that disrupts stalled transcription complexes. RNA polymerase variants that are thought to increase or decrease R-loop accumulation enhance or suppress, respectively, the growth phenotype of rnhAK60E rep::kan strains. These results identify a cellular role for the RNase HI/SSB interaction in helping to clear R-loops that block DNA replication.
Identifiants
pubmed: 32426857
doi: 10.1111/mmi.14529
pmc: PMC7934204
mid: NIHMS1669278
doi:
Substances chimiques
DNA, Bacterial
0
DNA-Binding Proteins
0
Escherichia coli Proteins
0
Ribonuclease H
EC 3.1.26.4
ribonuclease HI
EC 3.1.26.4
DNA Helicases
EC 3.6.4.-
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
495-509Subventions
Organisme : NIGMS NIH HHS
ID : R01 GM098885
Pays : United States
Informations de copyright
© 2020 John Wiley & Sons Ltd.
Références
Nucleic Acids Res. 1987 Jul 10;15(13):5041-9
pubmed: 3037486
Proc Natl Acad Sci U S A. 2019 Jun 11;116(24):11747-11753
pubmed: 31127046
Methods. 2015 Oct 15;88:81-8
pubmed: 25637032
Mol Gen Genet. 1996 Sep 25;252(4):398-403
pubmed: 8879240
Annu Rev Genet. 2012;46:121-43
pubmed: 22934648
Nat Commun. 2017 Dec 18;8(1):2170
pubmed: 29255195
Nat Commun. 2014 Dec 18;5:5820
pubmed: 25520215
Mol Cell. 2011 Dec 23;44(6):966-77
pubmed: 22195969
Nucleic Acids Res. 2019 Jul 9;47(12):6287-6298
pubmed: 31028385
Science. 2016 May 20;352(6288):993-6
pubmed: 27199428
Biochimie. 1993;75(1-2):89-99
pubmed: 8389213
J Bacteriol. 1994 Mar;176(5):1521-3
pubmed: 8113195
Int J Biol Sci. 2008 Sep 23;4(6):338-44
pubmed: 18825275
J Biol Chem. 2015 Jun 5;290(23):14626-36
pubmed: 25903123
Mol Microbiol. 2001 Aug;41(3):697-704
pubmed: 11532137
PLoS Biol. 2005 Jul;3(7):e255
pubmed: 16000023
J Bacteriol. 1985 Nov;164(2):653-8
pubmed: 2997124
Science. 2004 Feb 13;303(5660):1014-6
pubmed: 14963331
J Biol Chem. 2017 Sep 15;292(37):15216-15224
pubmed: 28717002
Nucleic Acids Res. 2011 Feb;39(3):949-57
pubmed: 20923786
Nat Methods. 2008 Feb;5(2):159-61
pubmed: 18176568
Nature. 2014 Jan 16;505(7483):372-7
pubmed: 24402227
Microbiol Mol Biol Rev. 1997 Jun;61(2):212-38
pubmed: 9184011
Genetics. 2005 Apr;169(4):1799-806
pubmed: 15716497
J Biol Chem. 1976 Jul 10;251(13):4078-84
pubmed: 6470
Science. 2010 Apr 23;328(5977):498-501
pubmed: 20413500
Mol Cell. 2017 Mar 2;65(5):832-847.e4
pubmed: 28257700
Proc Natl Acad Sci U S A. 1980 May;77(5):2450-4
pubmed: 6156450
J Biol Chem. 2000 Apr 14;275(15):11257-63
pubmed: 10753935
Proc Natl Acad Sci U S A. 1995 Apr 11;92(8):3526-30
pubmed: 7536935
PLoS Genet. 2010 Jan 15;6(1):e1000810
pubmed: 20090829
Mol Gen Genet. 1994 Sep 1;244(5):557-62
pubmed: 8078483
Mol Microbiol. 2015 Mar;95(5):754-68
pubmed: 25425430
BMC Microbiol. 2004 Dec 08;4:47
pubmed: 15588282
EMBO J. 2007 Oct 3;26(19):4239-51
pubmed: 17853894
Nucleic Acids Res. 2017 Apr 20;45(7):3875-3887
pubmed: 28160601
EMBO J. 2005 Mar 23;24(6):1267-76
pubmed: 15775982
New Biol. 1990 Sep;2(9):771-7
pubmed: 2177653
Mol Cell. 2003 Sep;12(3):711-21
pubmed: 14527416
Methods Mol Biol. 2012;922:245-53
pubmed: 22976192
Cell Cycle. 2011 Jan 1;10(1):108-17
pubmed: 21191184
J Biol Chem. 2013 Jun 14;288(24):17569-78
pubmed: 23629733
Cell. 2011 Aug 19;146(4):533-43
pubmed: 21854980
Proc Natl Acad Sci U S A. 1992 Feb 15;89(4):1453-7
pubmed: 1741399
Science. 1996 May 17;272(5264):1030-3
pubmed: 8638128
Proc Natl Acad Sci U S A. 2001 Jul 17;98(15):8241-6
pubmed: 11459959
Mol Gen Genet. 1981;182(2):364-6
pubmed: 7026978
Nat Cell Biol. 2009 Nov;11(11):1315-24
pubmed: 19838172
Genetics. 1996 May;143(1):5-13
pubmed: 8722757
EMBO J. 2010 Jan 6;29(1):145-57
pubmed: 19851282
EMBO J. 1995 May 15;14(10):2385-92
pubmed: 7774596
Proc Natl Acad Sci U S A. 2011 Jan 11;108(2):792-7
pubmed: 21183718
Proc Natl Acad Sci U S A. 2013 May 14;110(20):8063-8
pubmed: 23630273
Proc Natl Acad Sci U S A. 2013 Jul 30;110(31):12577-82
pubmed: 23858453
PLoS Genet. 2010 Dec 09;6(12):e1001238
pubmed: 21170359
Proc Natl Acad Sci U S A. 2014 Jan 28;111(4):1373-8
pubmed: 24379377
PLoS One. 2015 Aug 05;10(8):e0134892
pubmed: 26244508
Mol Microbiol. 2011 May;80(3):612-27
pubmed: 21414037
Cold Spring Harb Perspect Biol. 2013 Jul 01;5(7):
pubmed: 23818497
Proc Natl Acad Sci U S A. 2000 Jun 6;97(12):6640-5
pubmed: 10829079
Mol Cell. 2012 Apr 27;46(2):115-24
pubmed: 22541554
DNA Repair (Amst). 2003 Nov 21;2(11):1280-7
pubmed: 15272456
J Bacteriol. 1996 Dec;178(23):6701-5
pubmed: 8955285
Mol Cell. 2009 Jun 26;34(6):722-34
pubmed: 19560424
Mol Gen Genet. 1991 Jul;227(3):424-32
pubmed: 1650908
J Mol Biol. 1984 Sep 15;178(2):227-36
pubmed: 6387151
J Mol Biol. 1985 Nov 20;186(2):283-93
pubmed: 3910840
Proc Natl Acad Sci U S A. 2007 Mar 27;104(13):5608-13
pubmed: 17372224
J Mol Biol. 1985 Jul 5;184(1):45-52
pubmed: 2411935
J Biol Chem. 1998 Sep 4;273(36):23476-84
pubmed: 9722585
Mol Gen Genet. 1984;193(2):231-7
pubmed: 6319961
Genes Dev. 2010 Jul 15;24(14):1546-58
pubmed: 20634320
Curr Protoc Mol Biol. 2002 Aug;Chapter 1:Unit 1.1
pubmed: 18265292
Microbiol Mol Biol Rev. 2007 Mar;71(1):13-35
pubmed: 17347517
Mol Cell. 2011 Dec 23;44(6):978-88
pubmed: 22195970
Genes Dev. 2011 Oct 1;25(19):2041-56
pubmed: 21979917
Annu Rev Biochem. 1980;49:421-57
pubmed: 6250445
Science. 1992 Nov 20;258(5086):1362-5
pubmed: 1455232
Mol Microbiol. 1996 Jun;20(6):1307-18
pubmed: 8809781
mBio. 2015 Nov 03;6(6):e01294-15
pubmed: 26530381
J Bacteriol. 1972 Mar;109(3):971-8
pubmed: 4551758
Nat Rev Microbiol. 2012 Jun 06;10(7):449-58
pubmed: 22669220
J Bacteriol. 1969 Jan;97(1):244-9
pubmed: 4884815
J Mol Biol. 1978 May 5;121(1):55-69
pubmed: 351189
Microbiol Rev. 1990 Dec;54(4):342-80
pubmed: 2087220
Methods Mol Biol. 2012;922:1-21
pubmed: 22976174
Cell Rep. 2015 Dec 22;13(11):2587-2596
pubmed: 26686641
Crit Rev Biochem Mol Biol. 2008 Sep-Oct;43(5):289-318
pubmed: 18937104
Philos Trans R Soc Lond B Biol Sci. 1987 Dec 15;317(1187):395-420
pubmed: 2894677
Cell. 2008 Apr 4;133(1):90-102
pubmed: 18394992
Mol Cell. 2005 Jul 22;19(2):247-58
pubmed: 16039593
Cell. 2005 Aug 12;122(3):365-78
pubmed: 16096057
Science. 2010 Apr 23;328(5977):504-8
pubmed: 20413502
J Mol Biol. 1975 May 5;94(1):127-32
pubmed: 1095767
Cell. 2010 May 14;141(4):595-605
pubmed: 20478253
EMBO J. 1983;2(3):463-8
pubmed: 11894964
Mol Microbiol. 2010 Jul;77(2):324-36
pubmed: 20497334
FEBS Lett. 2012 Nov 2;586(21):3825-30
pubmed: 23036643
Nucleic Acids Res. 2011 Mar;39(4):1351-9
pubmed: 20959294
Mol Microbiol. 2012 Jul;85(1):12-20
pubmed: 22607628
Mol Gen Genet. 1991 Jul;227(3):433-7
pubmed: 1650909
EMBO J. 2011 Aug 19;30(20):4236-47
pubmed: 21857649
PLoS Genet. 2016 Jan 14;12(1):e1005797
pubmed: 26765929
Proc Natl Acad Sci U S A. 1984 Feb;81(4):1040-4
pubmed: 6322184
Mol Gen Genet. 1984;196(2):283-9
pubmed: 6208456
J Mol Biol. 1988 Nov 20;204(2):247-61
pubmed: 2464690
Nucleic Acids Res. 2019 Jun 4;47(10):5100-5113
pubmed: 30869136
Nat Struct Mol Biol. 2013 Apr;20(4):412-8
pubmed: 23552296
Mol Microbiol. 2016 Nov;102(4):690-700
pubmed: 27569113
Cell Cycle. 2010 Jul 1;9(13):2537-43
pubmed: 20581460
Mol Cell. 2009 Nov 25;36(4):654-66
pubmed: 19941825
J Mol Biol. 2003 Sep 5;332(1):31-46
pubmed: 12946345
J Bacteriol. 2010 May;192(10):2575-82
pubmed: 20304994
J Bacteriol. 1987 Jun;169(6):2650-8
pubmed: 3034862
Mol Microbiol. 2010 Mar;75(5):1090-7
pubmed: 20487299
Nat Methods. 2013 May;10(5):407-9
pubmed: 23524392