R-Loops and Its Chro-Mates: The Strange Case of Dr. Jekyll and Mr. Hyde.
DNA damage
R-T conflicts
R-loops
RNA:DNA hybrids
chromatin remodelers
genome stability
histone modifiers
Journal
International journal of molecular sciences
ISSN: 1422-0067
Titre abrégé: Int J Mol Sci
Pays: Switzerland
ID NLM: 101092791
Informations de publication
Date de publication:
17 Aug 2021
17 Aug 2021
Historique:
received:
14
07
2021
revised:
04
08
2021
accepted:
12
08
2021
entrez:
27
8
2021
pubmed:
28
8
2021
medline:
14
9
2021
Statut:
epublish
Résumé
Since their discovery, R-loops have been associated with both physiological and pathological functions that are conserved across species. R-loops are a source of replication stress and genome instability, as seen in neurodegenerative disorders and cancer. In response, cells have evolved pathways to prevent R-loop accumulation as well as to resolve them. A growing body of evidence correlates R-loop accumulation with changes in the epigenetic landscape. However, the role of chromatin modification and remodeling in R-loops homeostasis remains unclear. This review covers various mechanisms precluding R-loop accumulation and highlights the role of chromatin modifiers and remodelers in facilitating timely R-loop resolution. We also discuss the enigmatic role of RNA:DNA hybrids in facilitating DNA repair, epigenetic landscape and the potential role of replication fork preservation pathways, active fork stability and stalled fork protection pathways, in avoiding replication-transcription conflicts. Finally, we discuss the potential role of several Chro-Mates (chromatin modifiers and remodelers) in the likely differentiation between persistent/detrimental R-loops and transient/benign R-loops that assist in various physiological processes relevant for therapeutic interventions.
Identifiants
pubmed: 34445553
pii: ijms22168850
doi: 10.3390/ijms22168850
pmc: PMC8396322
pii:
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Références
Cell Rep. 2020 May 5;31(5):107603
pubmed: 32375052
Mol Cell. 2011 Dec 23;44(6):966-77
pubmed: 22195969
J Biochem. 2019 Jun 1;165(6):465-470
pubmed: 30821334
PLoS Genet. 2015 Feb 23;11(2):e1004990
pubmed: 25705897
Cell. 1995 May 19;81(4):533-40
pubmed: 7758107
Mol Cell. 2012 Mar 30;45(6):814-25
pubmed: 22387027
Nat Commun. 2017 Oct 16;8(1):859
pubmed: 29038466
J Immunol. 2014 Dec 1;193(11):5370-8
pubmed: 25411432
Cell Rep. 2018 Jan 23;22(4):1031-1039
pubmed: 29386125
Proc Natl Acad Sci U S A. 2013 Aug 20;110(34):13938-43
pubmed: 23918391
Mol Cell. 2012 Mar 30;45(6):710-8
pubmed: 22464441
Trends Biochem Sci. 2011 Jan;36(1):19-29
pubmed: 20813532
Mol Cell. 2016 Sep 1;63(5):898-911
pubmed: 27477910
Science. 2001 Jun 8;292(5523):1876-82
pubmed: 11313499
Genes (Basel). 2016 Dec 21;7(12):
pubmed: 28009828
DNA Repair (Amst). 2011 Jun 10;10(6):654-65
pubmed: 21561811
Genes Dev. 2014 Apr 1;28(7):735-48
pubmed: 24636987
Cold Spring Harb Perspect Biol. 2014 Sep 16;6(12):a016576
pubmed: 25228584
Proc Natl Acad Sci U S A. 2013 Dec 24;110(52):20982-7
pubmed: 24324146
Sci Adv. 2021 May 5;7(19):
pubmed: 33952518
Nucleic Acids Res. 2013 Mar 1;41(5):2881-93
pubmed: 23325844
Nat Plants. 2017 Sep;3(9):704-714
pubmed: 28848233
EMBO J. 2021 Apr 1;40(7):e106018
pubmed: 33634895
Nat Commun. 2018 Dec 18;9(1):5376
pubmed: 30560944
EMBO Rep. 2019 Sep;20(9):e47250
pubmed: 31338941
Genome Res. 2015 Feb;25(2):189-200
pubmed: 25373142
Sci China Life Sci. 2012 Jan;55(1):89-96
pubmed: 22314495
Biochim Biophys Acta. 2013 Jan;1829(1):2-8
pubmed: 23000482
Proc Natl Acad Sci U S A. 2013 Jan 2;110(1):258-63
pubmed: 23251031
Genes Dev. 2017 Jul 1;31(13):1370-1381
pubmed: 28790157
Nat Cell Biol. 2020 Apr;22(4):372-379
pubmed: 32231306
J Biol Chem. 2017 Mar 31;292(13):5271-5281
pubmed: 28202543
EMBO J. 2010 Aug 4;29(15):2538-52
pubmed: 20588255
Cell Res. 2019 Dec;29(12):1035-1038
pubmed: 31606733
Cell Rep. 2018 May 8;23(6):1891-1905
pubmed: 29742442
PLoS One. 2014 Aug 01;9(8):e103819
pubmed: 25084169
Genes (Basel). 2018 Nov 27;9(12):
pubmed: 30486458
Nature. 2014 Jul 17;511(7509):362-5
pubmed: 24896180
Cell. 2017 Jun 29;170(1):86-101.e16
pubmed: 28666128
PLoS Genet. 2011 Mar;7(3):e1002008
pubmed: 21408204
Cell. 2010 Oct 29;143(3):367-78
pubmed: 21029860
Cell. 1997 Sep 19;90(6):1107-12
pubmed: 9323138
Nature. 2014 Dec 18;516(7531):436-9
pubmed: 25296254
Cell Rep. 2019 Jun 4;27(10):2978-2989.e5
pubmed: 31167142
Cell Rep. 2020 Feb 18;30(7):2094-2105.e9
pubmed: 32075754
Cell Rep. 2020 Dec 22;33(12):108546
pubmed: 33357438
Nat Commun. 2019 Jul 23;10(1):3287
pubmed: 31337767
Mol Cell. 2013 Nov 21;52(4):583-90
pubmed: 24211264
Nat Struct Mol Biol. 2005 Sep;12(9):737-8
pubmed: 16142225
PLoS Genet. 2012;8(7):e1002772
pubmed: 22829774
Genes Dev. 2014 Jul 1;28(13):1384-96
pubmed: 24990962
Cell. 2018 Oct 4;175(2):558-570.e11
pubmed: 30245011
Biochemistry. 1995 Sep 5;34(35):11211-6
pubmed: 7545436
Nature. 2005 Dec 22;438(7071):1116-22
pubmed: 16222246
Proc Natl Acad Sci U S A. 2019 Jan 15;116(3):816-825
pubmed: 30591567
Mol Cell. 2017 Jul 6;67(1):19-29.e3
pubmed: 28602639
Mol Cell. 2011 Jun 24;42(6):794-805
pubmed: 21700224
Genome Res. 2018 Jan;28(1):37-51
pubmed: 29229671
Nucleic Acids Res. 2013 Mar 1;41(5):3130-43
pubmed: 23355612
DNA Repair (Amst). 2014 Jul;19:84-94
pubmed: 24746923
Cell. 2019 Oct 17;179(3):604-618
pubmed: 31607512
PLoS Genet. 2014 Sep 18;10(9):e1004630
pubmed: 25233079
J Cell Biol. 2017 Dec 4;216(12):3991-4005
pubmed: 29042409
Cancer Lett. 2003 May 15;194(2):155-62
pubmed: 12757973
Am J Hum Genet. 2004 Jun;74(6):1128-35
pubmed: 15106121
Nat Rev Genet. 2015 Oct;16(10):583-97
pubmed: 26370899
Int J Mol Sci. 2020 Feb 22;21(4):
pubmed: 32098397
Proc Natl Acad Sci U S A. 1995 Apr 11;92(8):3526-30
pubmed: 7536935
Cell. 2016 Nov 3;167(4):1001-1013.e7
pubmed: 27881299
Nucleic Acids Res. 2018 Feb 16;46(3):1227-1239
pubmed: 29059325
PLoS Genet. 2014 May 01;10(5):e1004318
pubmed: 24787137
J Cell Biol. 2013 Apr 1;201(1):33-48
pubmed: 23530069
EMBO J. 2019 Aug 1;38(15):e100986
pubmed: 31267554
Int J Mol Sci. 2018 Nov 12;19(11):
pubmed: 30424570
EMBO Rep. 2017 Jun;18(6):914-928
pubmed: 28487353
Nat Genet. 2020 Jan;52(1):48-55
pubmed: 31844323
Mol Cell. 2013 May 9;50(3):437-43
pubmed: 23603118
Int J Mol Sci. 2018 Feb 18;19(2):
pubmed: 29463031
Nucleic Acids Res. 1978 May;5(5):1627-37
pubmed: 208059
Mol Cell. 2016 Jul 7;63(1):167-78
pubmed: 27373332
PLoS One. 2009 Dec 01;4(12):e8111
pubmed: 19956593
Mol Cell. 2020 Aug 6;79(3):425-442.e7
pubmed: 32615088
Nat Genet. 2004 Mar;36(3):225-7
pubmed: 14770181
Science. 2004 Feb 13;303(5660):983-8
pubmed: 14963322
Biochem Biophys Res Commun. 2000 Jul 5;273(2):793-8
pubmed: 10873683
Crit Rev Biochem Mol Biol. 2019 Aug;54(4):333-351
pubmed: 31509023
Nat Commun. 2021 May 21;12(1):3016
pubmed: 34021146
Mol Cell. 2003 Sep;12(3):711-21
pubmed: 14527416
Trends Genet. 2016 Dec;32(12):828-838
pubmed: 27793359
Mol Cell. 2017 Apr 6;66(1):50-62.e6
pubmed: 28318821
Mol Cell. 2011 May 6;42(3):267-9
pubmed: 21549303
Cell. 2017 Jun 29;170(1):72-85.e14
pubmed: 28666126
Semin Cell Dev Biol. 2011 Oct;22(8):906-12
pubmed: 21782962
Cell. 2009 Apr 17;137(2):247-58
pubmed: 19361851
Mol Cell. 2014 Dec 18;56(6):777-85
pubmed: 25435140
Mol Cell Biol. 2010 Jan;30(1):146-59
pubmed: 19841062
Proc Natl Acad Sci U S A. 1972 Mar;69(3):737-41
pubmed: 4501588
Oncogene. 2002 Jan 21;21(4):598-610
pubmed: 11850785
Nat Cell Biol. 2009 Nov;11(11):1315-24
pubmed: 19838172
Mol Cell. 2001 Aug;8(2):251-62
pubmed: 11545728
Mutat Res Rev Mutat Res. 2020 Apr - Jun;784:108300
pubmed: 32430097
Nat Commun. 2019 May 28;10(1):2253
pubmed: 31138795
Nat Commun. 2020 Sep 10;11(1):4534
pubmed: 32913330
Nat Genet. 1998 Jul;19(3):254-6
pubmed: 9662397
EMBO J. 2001 Jul 2;20(13):3506-17
pubmed: 11432837
Nat Rev Genet. 2010 May;11(5):319-30
pubmed: 20351727
Genome Res. 2013 Oct;23(10):1590-600
pubmed: 23868195
Mol Biol Cell. 2008 Oct;19(10):4310-8
pubmed: 18667528
Cell. 2012 Sep 14;150(6):1182-95
pubmed: 22980979
Mol Cell. 2014 Feb 6;53(3):484-97
pubmed: 24507716
Clin Epigenetics. 2020 Oct 14;12(1):147
pubmed: 33054831
Science. 1991 Jun 21;252(5013):1711-4
pubmed: 1675488
Mol Cell. 2015 Dec 3;60(5):784-796
pubmed: 26656161
J Cell Biol. 2007 Jun 18;177(6):969-79
pubmed: 17562789
Mol Cell. 1999 Feb;3(2):247-53
pubmed: 10078207
Cell. 2004 Nov 12;119(4):481-9
pubmed: 15537538
Front Cell Dev Biol. 2021 Jan 11;8:618157
pubmed: 33505970
Cell. 2017 Aug 10;170(4):787-799.e18
pubmed: 28802046
Cell. 2012 Dec 7;151(6):1185-99
pubmed: 23217706
Genes Dev. 2011 Apr 15;25(8):781-8
pubmed: 21498567
Mol Cell. 2016 Jan 7;61(1):68-83
pubmed: 26748827
Mol Cell. 2012 Apr 27;46(2):115-24
pubmed: 22541554
Nucleic Acids Res. 2021 Jan 11;49(1):269-284
pubmed: 33313823
Annu Rev Microbiol. 2018 Sep 08;72:71-88
pubmed: 29856930
J Biol Chem. 2011 May 27;286(21):18369-74
pubmed: 21454601
Genes Dev. 1996 Nov 1;10(21):2657-83
pubmed: 8946909
DNA Repair (Amst). 2019 Sep;81:102660
pubmed: 31302006
Genome Biol. 2010;11(11):R114
pubmed: 21108794
Mol Cell Biol. 2005 Feb;25(3):888-95
pubmed: 15657418
Genome Biol. 2018 Jul 30;19(1):100
pubmed: 30060749
Annu Rev Genet. 2007;41:169-92
pubmed: 17608616
Mol Cell. 2015 Feb 19;57(4):636-647
pubmed: 25699710
PLoS Genet. 2011 Dec;7(12):e1002386
pubmed: 22144908
Mol Cell. 1999 Jul;4(1):129-35
pubmed: 10445035
Nat Rev Mol Cell Biol. 2012 Feb 23;13(3):153-67
pubmed: 22358331
Cell. 1986 Apr 11;45(1):95-104
pubmed: 3955658
PLoS One. 2014 Mar 17;9(3):e90219
pubmed: 24637776
Mol Cell. 2015 Nov 5;60(3):351-61
pubmed: 26593718
Cancer Cell. 2012 Jul 10;22(1):106-16
pubmed: 22789542
Nature. 2002 May 16;417(6886):304-8
pubmed: 11979277
Genes Dev. 2010 Jul 15;24(14):1546-58
pubmed: 20634320
Can J Ophthalmol. 2018 Oct;53(5):e203-e205
pubmed: 30340744
Trends Cancer. 2019 Oct;5(10):619-631
pubmed: 31706509
FEBS J. 2009 Mar;276(6):1494-505
pubmed: 19228196
Nucleic Acids Res. 2020 Sep 18;48(16):9195-9203
pubmed: 32810236
Microbiol Mol Biol Rev. 2007 Mar;71(1):13-35
pubmed: 17347517
Science. 1992 Nov 20;258(5086):1362-5
pubmed: 1455232
Nat Immunol. 2003 May;4(5):442-51
pubmed: 12679812
DNA Repair (Amst). 2018 Nov;71:69-81
pubmed: 30190235
Proc Natl Acad Sci U S A. 1976 Jul;73(7):2294-8
pubmed: 781674
Genes Dev. 2019 Aug 1;33(15-16):1008-1026
pubmed: 31123061
Cell. 2011 Apr 29;145(3):435-46
pubmed: 21529715
EMBO J. 2002 Feb 1;21(3):195-201
pubmed: 11823412
Mol Cell. 2011 May 6;42(3):285-96
pubmed: 21549307
Genes Dev. 2016 Jun 1;30(11):1327-38
pubmed: 27298336
Cell. 2017 Aug 10;170(4):603-604
pubmed: 28802036
Mol Cell Biol. 2010 Nov;30(21):5123-34
pubmed: 20823270
Mol Cell. 2011 Dec 23;44(6):978-88
pubmed: 22195970
Cell. 2013 Jan 31;152(3):620-32
pubmed: 23352430
Nat Struct Mol Biol. 2020 May;27(5):424-437
pubmed: 32398827
Nat Commun. 2019 Jul 22;10(1):3274
pubmed: 31332171
Proc Natl Acad Sci U S A. 2018 Nov 27;115(48):E11311-E11320
pubmed: 30413623
DNA Repair (Amst). 2017 Aug;56:26-32
pubmed: 28629774
Mol Cell. 2020 Feb 6;77(3):528-541.e8
pubmed: 31759821
Genes Cells. 2012 Mar;17(3):218-33
pubmed: 22280061
Mol Cell. 2019 Feb 7;73(3):398-411
pubmed: 30735654
Cell. 1997 Oct 31;91(3):325-34
pubmed: 9363941
Mol Cell. 2010 Aug 27;39(4):595-605
pubmed: 20797631
Elife. 2017 Mar 21;6:
pubmed: 28322723
Genes Dev. 2016 Feb 1;30(3):337-54
pubmed: 26798134
J Clin Invest. 2021 Feb 1;131(3):
pubmed: 33529165
J Biol Chem. 2020 Apr 3;295(14):4684-4695
pubmed: 32107311
Science. 2018 Sep 14;361(6407):1126-1129
pubmed: 30213916
Mol Cell. 2006 May 5;22(3):363-74
pubmed: 16678108
Cell. 2012 Nov 9;151(4):835-846
pubmed: 23141540
Mol Cell Biol. 1997 Jul;17(7):4178-90
pubmed: 9199353
Nature. 2011 Feb 3;470(7332):120-3
pubmed: 21258320
Plant Cell. 2020 Apr;32(4):888-903
pubmed: 32075864
Nat Rev Mol Cell Biol. 2011 Jul 22;12(8):505-16
pubmed: 21779027
Cold Spring Harb Perspect Biol. 2013 Aug 01;5(8):a010207
pubmed: 23751185
Nat Commun. 2016 Jul 20;7:12235
pubmed: 27436229
Nucleic Acids Res. 2020 Dec 2;48(21):11942-11957
pubmed: 33137181
J Biol Chem. 2018 Apr 20;293(16):6121-6133
pubmed: 29514976
Mol Cell. 2003 Mar;11(3):807-15
pubmed: 12667461
Nat Genet. 2021 Jul;53(7):1050-1063
pubmed: 33986538
Cell. 2011 May 13;145(4):529-42
pubmed: 21565612
Mol Cell Biol. 2013 Jan;33(2):406-17
pubmed: 23149945
Curr Biol. 2006 Jul 11;16(13):1280-9
pubmed: 16815704
Mutat Res. 2007 May 1;618(1-2):18-29
pubmed: 17316710
Nat Genet. 2020 Jan;52(1):27-28
pubmed: 31873295
Cell Rep. 2019 Nov 26;29(9):2890-2900.e5
pubmed: 31775053
EMBO J. 2016 Jul 15;35(14):1488-503
pubmed: 27225932
Am J Hum Genet. 2015 Jul 2;97(1):186-93
pubmed: 26094573
EMBO J. 2017 Dec 1;36(23):3532-3547
pubmed: 29074626
Nat Commun. 2018 Feb 7;9(1):532
pubmed: 29416038
Cell. 2005 Aug 12;122(3):365-78
pubmed: 16096057
Front Genet. 2015 Apr 28;6:166
pubmed: 25972894
Genes (Basel). 2017 Jan 14;8(1):
pubmed: 28098815
Mol Cell Biol. 2009 Jun;29(11):3124-33
pubmed: 19307304
Nat Genet. 2016 Nov;48(11):1385-1395
pubmed: 27668659
iScience. 2018 Apr 27;2:123-135
pubmed: 29888761
Nat Genet. 2006 Aug;38(8):910-6
pubmed: 16845400
Nat Commun. 2018 Oct 8;9(1):4115
pubmed: 30297739
Cell Stress. 2019 Jan 21;3(2):38-46
pubmed: 31225499
J Biol Chem. 2013 Aug 9;288(32):23182-93
pubmed: 23779104
Nature. 1997 Sep 18;389(6648):251-60
pubmed: 9305837
Annu Rev Pathol. 2015;10:425-48
pubmed: 25621662
Cell. 2016 Dec 1;167(6):1455-1467
pubmed: 27912056
Nat Cell Biol. 2021 Apr;23(4):305-313
pubmed: 33837288
Front Genet. 2020 Feb 06;11:43
pubmed: 32117455
Mol Cell Proteomics. 2012 May;11(5):60-76
pubmed: 22586326
Mol Cell. 2018 Feb 1;69(3):426-437.e7
pubmed: 29395064
Mol Cell. 2011 Jan 7;41(1):21-32
pubmed: 21211720
Nat Genet. 2013 Jun;45(6):592-601
pubmed: 23644491
Nat Commun. 2018 Apr 18;9(1):1548
pubmed: 29670078
Genes Dev. 2007 Aug 1;21(15):1921-36
pubmed: 17671091
Mol Cell Biol. 2018 Mar 29;38(8):
pubmed: 29378830
Nucleic Acids Res. 2021 May 21;49(9):4848-4863
pubmed: 33755171
Mol Cell. 2008 Jul 11;31(1):57-66
pubmed: 18614047
Am J Hum Genet. 1998 Mar;62(3):676-89
pubmed: 9497246
Cell. 2017 Aug 10;170(4):774-786.e19
pubmed: 28802045
Curr Biol. 2007 Jul 17;17(14):1219-24
pubmed: 17614284
Nat Cell Biol. 2014 Jan;16(1):2-9
pubmed: 24366029
Philos Trans R Soc Lond B Biol Sci. 2017 Oct 5;372(1731):
pubmed: 28847827
J Biol Chem. 2020 Jan 24;295(4):905-913
pubmed: 31843970
Cell Mol Life Sci. 2014 Dec;71(23):4489-94
pubmed: 25248392
Genes Dev. 2004 Jul 1;18(13):1618-29
pubmed: 15231739
Cell. 1991 May 31;65(5):905-14
pubmed: 1710175
Nat Genet. 2000 Apr;24(4):368-71
pubmed: 10742099
Genes Dev. 2010 Oct 1;24(19):2133-45
pubmed: 20889714
Hum Mol Genet. 2014 Sep 15;23(18):4758-69
pubmed: 24760770
J Biol Chem. 2010 Mar 26;285(13):9477-9484
pubmed: 20075079
Nat Rev Mol Cell Biol. 2020 Mar;21(3):167-178
pubmed: 32005969
Cell Cycle. 2009 Aug 15;8(16):2664-6
pubmed: 19625767
Nucleic Acids Res. 2010 Sep;38(17):5797-806
pubmed: 20460456
PLoS Genet. 2015 Nov 19;11(11):e1005674
pubmed: 26584049
Cytogenet Genome Res. 2003;100(1-4):77-84
pubmed: 14526166
Nucleic Acids Res. 2012 Jan;40(2):e16
pubmed: 22121227
Nat Struct Mol Biol. 2016 Jul;23(7):647-55
pubmed: 27239795
Nat Commun. 2018 Feb 7;9(1):533
pubmed: 29416069
Development. 2006 Jan;133(2):229-35
pubmed: 16339185
Front Immunol. 2019 Apr 26;10:922
pubmed: 31080453