8-oxodG accumulation within super-enhancers marks fragile CTCF-mediated chromatin loops.


Journal

Nucleic acids research
ISSN: 1362-4962
Titre abrégé: Nucleic Acids Res
Pays: England
ID NLM: 0411011

Informations de publication

Date de publication:
08 04 2022
Historique:
accepted: 15 02 2022
revised: 12 02 2022
received: 02 11 2021
pubmed: 3 3 2022
medline: 16 4 2022
entrez: 2 3 2022
Statut: ppublish

Résumé

8-Oxo-7,8-dihydro-2'-deoxyguanosine (8-oxodG), a major product of the DNA oxidization process, has been proposed to have an epigenetic function in gene regulation and has been associated with genome instability. NGS-based methodologies are contributing to the characterization of the 8-oxodG function in the genome. However, the 8-oxodG epigenetic role at a genomic level and the mechanisms controlling the genomic 8-oxodG accumulation/maintenance have not yet been fully characterized. In this study, we report the identification and characterization of a set of enhancer regions accumulating 8-oxodG in human epithelial cells. We found that these oxidized enhancers are mainly super-enhancers and are associated with bidirectional-transcribed enhancer RNAs and DNA Damage Response activation. Moreover, using ChIA-PET and HiC data, we identified specific CTCF-mediated chromatin loops in which the oxidized enhancer and promoter regions physically associate. Oxidized enhancers and their associated chromatin loops accumulate endogenous double-strand breaks which are in turn repaired by NHEJ pathway through a transcription-dependent mechanism. Our work suggests that 8-oxodG accumulation in enhancers-promoters pairs occurs in a transcription-dependent manner and provides novel mechanistic insights on the intrinsic fragility of chromatin loops containing oxidized enhancers-promoters interactions.

Identifiants

pubmed: 35234932
pii: 6541026
doi: 10.1093/nar/gkac143
pmc: PMC8989568
doi:

Substances chimiques

CCCTC-Binding Factor 0
CTCF protein, human 0
Chromatin 0
8-Hydroxy-2'-Deoxyguanosine 88847-89-6
DNA 9007-49-2

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

3292-3306

Informations de copyright

© The Author(s) 2022. Published by Oxford University Press on behalf of Nucleic Acids Research.

Références

Nucleic Acids Res. 2020 May 7;48(8):4309-4324
pubmed: 32198884
J Am Chem Soc. 2017 Feb 22;139(7):2569-2572
pubmed: 28150947
DNA Repair (Amst). 2021 Jan;97:103027
pubmed: 33285475
Chem Res Toxicol. 2019 May 20;32(5):899-909
pubmed: 30821442
Bioinformatics. 2014 Aug 1;30(15):2114-20
pubmed: 24695404
Cell. 2014 Dec 18;159(7):1538-48
pubmed: 25483776
Nat Struct Mol Biol. 2010 Jul;17(7):889-90
pubmed: 20526335
Biochemistry. 2020 Jan 14;59(1):85-89
pubmed: 31618020
Trends Cell Biol. 2016 Jan;26(1):52-64
pubmed: 26437586
Mol Cell. 2010 May 28;38(4):576-89
pubmed: 20513432
Nucleic Acids Res. 2016 Jul 8;44(W1):W90-7
pubmed: 27141961
Genome Biol. 2009;10(3):R25
pubmed: 19261174
BMC Bioinformatics. 2013 Apr 15;14:128
pubmed: 23586463
Chem Soc Rev. 2020 Sep 21;49(18):6524-6528
pubmed: 32785348
Inflamm Regen. 2020 Aug 3;40:16
pubmed: 32922569
PLoS One. 2012;7(2):e30619
pubmed: 22312429
Redox Biol. 2020 Jan;29:101398
pubmed: 31926624
Bioinformatics. 2010 Mar 1;26(5):589-95
pubmed: 20080505
Nat Genet. 2021 Jul;53(7):1064-1074
pubmed: 34002095
Nucleic Acids Res. 2019 Jan 10;47(1):221-236
pubmed: 30462294
Nature. 2021 May;593(7859):440-444
pubmed: 33767446
Proc Natl Acad Sci U S A. 2020 May 26;117(21):11409-11420
pubmed: 32404420
Nucleic Acids Res. 2019 Dec 16;47(22):11481-11496
pubmed: 31724731
DNA Res. 2014 Dec;21(6):603-12
pubmed: 25008760
Science. 2008 Jan 11;319(5860):202-6
pubmed: 18187655
Oncogene. 2010 Jun 24;29(25):3691-702
pubmed: 20418916
Nucleic Acids Res. 2020 Sep 18;48(16):8943-8958
pubmed: 32697292
Proc Soc Exp Biol Med. 1999 Dec;222(3):246-52
pubmed: 10601883
ACS Chem Biol. 2017 Sep 15;12(9):2417-2426
pubmed: 28829124
Nat Biotechnol. 2015 Aug;33(8):877-81
pubmed: 26192317
Nat Chem. 2019 Jul;11(7):629-637
pubmed: 31209299
Curr Opin Genet Dev. 2020 Apr;61:9-16
pubmed: 32294612
Nat Genet. 2016 Oct;48(10):1267-72
pubmed: 27618450
Stat Appl Genet Mol Biol. 2012 Mar 31;11(3):Article 9
pubmed: 22499706
Cell. 2013 Apr 11;153(2):307-19
pubmed: 23582322
Science. 2018 Nov 16;362(6416):834-839
pubmed: 30442810
J Am Chem Soc. 2020 Jan 22;142(3):1115-1136
pubmed: 31880930
Cell Stem Cell. 2019 Nov 7;25(5):682-696.e8
pubmed: 31495782
J Exp Clin Cancer Res. 2021 May 19;40(1):174
pubmed: 34011395
Nucleic Acids Res. 2021 Dec 2;49(21):12252-12267
pubmed: 34788860
Nucleic Acids Res. 2014 Jul;42(Web Server issue):W187-91
pubmed: 24799436
J Immunol. 2014 Mar 1;192(5):2384-94
pubmed: 24489103
Cell Mol Life Sci. 2021 Nov;78(21-22):6745-6762
pubmed: 34463773
J Biol Chem. 2016 Dec 2;291(49):25553-25566
pubmed: 27756845
Bioinformatics. 2018 Feb 15;34(4):672-674
pubmed: 29028898
Proc Natl Acad Sci U S A. 2017 Mar 7;114(10):2604-2609
pubmed: 28143930
Genome Biol. 2015 Sep 28;16:214
pubmed: 26415882
Nucleic Acids Res. 2020 Jul 9;48(12):6715-6725
pubmed: 32484547
Cell. 2015 Dec 17;163(7):1611-27
pubmed: 26686651
Bioinformatics. 2009 Aug 15;25(16):2078-9
pubmed: 19505943
DNA Repair (Amst). 2017 Nov;59:82-105
pubmed: 28963982
Nucleic Acids Res. 2014;42(17):11040-55
pubmed: 25217584
Genome Biol. 2018 Dec 7;19(1):215
pubmed: 30526646
Genome Res. 2006 May;16(5):567-75
pubmed: 16651663
Bioinformatics. 2010 Mar 15;26(6):841-2
pubmed: 20110278
Nat Genet. 2019 Jun;51(6):1011-1023
pubmed: 31110352
J Cell Biol. 1999 Sep 6;146(5):905-16
pubmed: 10477747
NAR Cancer. 2021 Sep 16;3(3):zcab038
pubmed: 34541539
Biochim Biophys Acta Rev Cancer. 2020 Apr;1873(2):188353
pubmed: 32112817
J Am Chem Soc. 2018 Aug 8;140(31):9783-9787
pubmed: 29944356
Nat Struct Mol Biol. 2018 Jun;25(6):496-504
pubmed: 29867216
Oncogene. 2015 Sep 10;34(37):4845-54
pubmed: 25500544

Auteurs

Giovanni Scala (G)

Department of Biology, University of Naples 'Federico II', Naples, Italy.

Francesca Gorini (F)

Department of Molecular Medicine and Medical Biotechnologies, University of Naples 'Federico II', Naples, Italy.

Susanna Ambrosio (S)

Department of Biology, University of Naples 'Federico II', Naples, Italy.

Andrea M Chiariello (AM)

Department of Physics, University of Naples Federico II, and INFN, Naples, Italy.

Mario Nicodemi (M)

Department of Physics, University of Naples Federico II, and INFN, Naples, Italy.

Luigi Lania (L)

Department of Molecular Medicine and Medical Biotechnologies, University of Naples 'Federico II', Naples, Italy.

Barbara Majello (B)

Department of Biology, University of Naples 'Federico II', Naples, Italy.

Stefano Amente (S)

Department of Molecular Medicine and Medical Biotechnologies, University of Naples 'Federico II', Naples, Italy.

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