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Global and transcription-coupled repair of 8-oxoG is initiated by nucleotide excision repair proteins.

Kumar, N ; Theil, AF ; et al.
In: Nature communications, Jg. 13 (2022-02-21), Heft 1, S. 974
Online academicJournal

Titel:
Global and transcription-coupled repair of 8-oxoG is initiated by nucleotide excision repair proteins.
Autor/in / Beteiligte Person: Kumar, N ; Theil, AF ; Roginskaya, V ; Ali, Y ; Calderon, M ; Watkins, SC ; Barnes, RP ; Opresko, PL ; Pines, A ; Lans, H ; Vermeulen, W ; Van Houten, B
Link:
Zeitschrift: Nature communications, Jg. 13 (2022-02-21), Heft 1, S. 974
Veröffentlichung: [London] : Nature Pub. Group, 2022
Medientyp: academicJournal
ISSN: 2041-1723 (electronic)
DOI: 10.1038/s41467-022-28642-9
Schlagwort:
  • Cell Line, Tumor
  • Chromatin metabolism
  • Chromatin Assembly and Disassembly
  • DNA Damage radiation effects
  • DNA Glycosylases metabolism
  • DNA-Binding Proteins genetics
  • Gene Knockdown Techniques
  • Gene Knockout Techniques
  • Guanine metabolism
  • Guanine radiation effects
  • HEK293 Cells
  • Humans
  • Ultraviolet Rays adverse effects
  • Xeroderma Pigmentosum Group A Protein genetics
  • Xeroderma Pigmentosum Group A Protein metabolism
  • DNA Repair
  • DNA-Binding Proteins metabolism
  • Guanine analogs & derivatives
Sonstiges:
  • Nachgewiesen in: MEDLINE
  • Sprachen: English
  • Publication Type: Journal Article; Research Support, N.I.H., Extramural; Research Support, Non-U.S. Gov't
  • Language: English
  • [Nat Commun] 2022 Feb 21; Vol. 13 (1), pp. 974. <i>Date of Electronic Publication: </i>2022 Feb 21.
  • MeSH Terms: DNA Repair* ; DNA-Binding Proteins / *metabolism ; Guanine / *analogs & derivatives ; Cell Line, Tumor ; Chromatin / metabolism ; Chromatin Assembly and Disassembly ; DNA Damage / radiation effects ; DNA Glycosylases / metabolism ; DNA-Binding Proteins / genetics ; Gene Knockdown Techniques ; Gene Knockout Techniques ; Guanine / metabolism ; Guanine / radiation effects ; HEK293 Cells ; Humans ; Ultraviolet Rays / adverse effects ; Xeroderma Pigmentosum Group A Protein / genetics ; Xeroderma Pigmentosum Group A Protein / metabolism
  • References: Poetsch, A. R. The genomics of oxidative DNA damage, repair, and resulting mutagenesis. Comput Struct. Biotechnol. J. 18, 207–219 (2020). (PMID: 31993111697470010.1016/j.csbj.2019.12.013) ; Steenken, S. Electron transfer in DNA? Competition by ultra-fast proton transfer? Biol. Chem. 378, 1293–1297 (1997). (PMID: 9426189) ; Ohno, M. et al. A genome-wide distribution of 8-oxoguanine correlates with the preferred regions for recombination and single nucleotide polymorphism in the human genome. Genome Res. 16, 567–575 (2006). (PMID: 16651663145704110.1101/gr.4769606) ; Tubbs, A. & Nussenzweig, A. Endogenous DNA damage as a source of genomic instability in cancer. Cell 168, 644–656 (2017). (PMID: 28187286659173010.1016/j.cell.2017.01.002) ; Lindahl, T. & Barnes, D. E. Repair of endogenous DNA damage. Cold Spring Harb. Symp. Quant. Biol. 65, 127–133 (2000). (PMID: 1276002710.1101/sqb.2000.65.127) ; Kouchakdjian, M. et al. NMR structural studies of the ionizing radiation adduct 7-hydro-8-oxodeoxyguanosine (8-oxo-7H-dG) opposite deoxyadenosine in a DNA duplex. 8-Oxo-7H-dG(syn).dA(anti) alignment at lesion site. Biochemistry 30, 1403–1412 (1991). (PMID: 199112110.1021/bi00219a034) ; Neeley, W. L. & Essigmann, J. M. Mechanisms of formation, genotoxicity, and mutation of guanine oxidation products. Chem. Res Toxicol. 19, 491–505 (2006). (PMID: 1660816010.1021/tx0600043) ; Hsu, G. W. et al. Error-prone replication of oxidatively damaged DNA by a high-fidelity DNA polymerase. Nature 431, 217–221 (2004). (PMID: 1532255810.1038/nature02908) ; Sedelnikova, O. A. et al. Role of oxidatively induced DNA lesions in human pathogenesis. Mutat. Res 704, 152–159 (2010). (PMID: 20060490307495410.1016/j.mrrev.2009.12.005) ; Wallace, S. S. Base excision repair: a critical player in many games. DNA Repair 19, 14–26 (2014). (PMID: 24780558410024510.1016/j.dnarep.2014.03.030) ; Whitaker, A. M. et al. Base excision repair of oxidative DNA damage: from mechanism to disease. Front Biosci. (Landmark Ed.) 22, 1493–1522 (2017). (PMID: 10.2741/4555) ; Svilar, D. et al. Base excision repair and lesion-dependent subpathways for repair of oxidative DNA damage. Antioxid. Redox Signal 14, 2491–2507 (2011). (PMID: 20649466309649610.1089/ars.2010.3466) ; Bauer, N. C., Corbett, A. H. & Doetsch, P. W. The current state of eukaryotic DNA base damage and repair. Nucleic Acids Res. 43, 10083–10101 (2015). (PMID: 265194674666366) ; Lindahl, T., Karran, P. & Wood, R. D. DNA excision repair pathways. Curr. Opin. Genet Dev. 7, 158–169 (1997). (PMID: 911541910.1016/S0959-437X(97)80124-4) ; Dalhus, B. et al. Separation-of-function mutants unravel the dual-reaction mode of human 8-oxoguanine DNA glycosylase. Structure 19, 117–127 (2011). (PMID: 2122012210.1016/j.str.2010.09.023) ; Vidal, A. E. et al. Mechanism of stimulation of the DNA glycosylase activity of hOGG1 by the major human AP endonuclease: bypass of the AP lyase activity step. Nucleic Acids Res. 29, 1285–1292 (2001). (PMID: 112389942975510.1093/nar/29.6.1285) ; Hill, J. W. et al. Stimulation of human 8-oxoguanine-DNA glycosylase by AP-endonuclease: potential coordination of the initial steps in base excision repair. Nucleic Acids Res. 29, 430–438 (2001). (PMID: 111396132966210.1093/nar/29.2.430) ; Olmon, E. D. & Delaney, S. Differential ability of five DNA glycosylases to recognize and repair damage on nucleosomal DNA. ACS Chem. Biol. 12, 692–701 (2017). (PMID: 28085251655726410.1021/acschembio.6b00921) ; Bilotti, K. et al. Human OGG1 activity in nucleosomes is facilitated by transient unwrapping of DNA and is influenced by the local histone environment. DNA Repair 59, 1–8 (2017). (PMID: 28892740564325210.1016/j.dnarep.2017.08.010) ; Bilotti, K., Tarantino, M. E. & Delaney, S. Human oxoguanine glycosylase 1 removes solution accessible 8-Oxo-7,8-dihydroguanine lesions from globally substituted nucleosomes except in the dyad region. Biochemistry 57, 1436–1439 (2018). (PMID: 2934160610.1021/acs.biochem.7b01125) ; Luger, K. et al. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389, 251–60. (1997). (PMID: 930583710.1038/38444) ; Cutter, A. R. & Hayes, J. J. A brief review of nucleosome structure. FEBS Lett. 589, 2914–2922 (2015). (PMID: 25980611459826310.1016/j.febslet.2015.05.016) ; Menoni, H. et al. Base excision repair of 8-oxoG in dinucleosomes. Nucleic Acids Res. 40, 692–700 (2012). (PMID: 2193050810.1093/nar/gkr761) ; Hinz, J. M. & Czaja, W. Facilitation of base excision repair by chromatin remodeling. DNA Repair 36, 91–97 (2015). (PMID: 26422134468810410.1016/j.dnarep.2015.09.011) ; Rodriguez, Y., Hinz, J. M. & Smerdon, M. J. Accessing DNA damage in chromatin: Preparing the chromatin landscape for base excision repair. DNA Repair (Amst.) 32, 113–119 (2015). (PMID: 452233810.1016/j.dnarep.2015.04.021) ; Aydin, O. Z., Vermeulen, W. & Lans, H. ISWI chromatin remodeling complexes in the DNA damage response. Cell Cycle 13, 3016–3025 (2014). (PMID: 25486562461505110.4161/15384101.2014.956551) ; Kumar, N., Raja, S. & Van Houten, B. The involvement of nucleotide excision repair proteins in the removal of oxidative DNA damage. Nucleic Acids Res 48, 11227–11243 (2020). (PMID: 33010169767247710.1093/nar/gkaa777) ; Kumar, N. et al. Cooperation and interplay between base and nucleotide excision repair pathways: From DNA lesions to proteins. Genet Mol. Biol. 43, e20190104 (2020). (PMID: 32141475719802710.1590/1678-4685-gmb-2019-0104) ; Limpose, K. L., Corbett, A. H. & Doetsch, P. W. BERing the burden of damage: Pathway crosstalk and posttranslational modification of base excision repair proteins regulate DNA damage management. DNA Repair 56, 51–64 (2017). (PMID: 28629773557698910.1016/j.dnarep.2017.06.007) ; Melis, J. P., van Steeg, H. & Luijten, M. Oxidative DNA damage and nucleotide excision repair. Antioxid. Redox Signal 18, 2409–2419 (2013). (PMID: 23216312367163010.1089/ars.2012.5036) ; Shafirovich, V. & Geacintov, N. E. Removal of oxidatively generated DNA damage by overlapping repair pathways. Free Radic. Biol. Med 107, 53–61 (2017). (PMID: 2781821910.1016/j.freeradbiomed.2016.10.507) ; Scharer, O. D. Nucleotide excision repair in eukaryotes. Cold Spring Harb. Perspect. Biol. 5, a012609 (2013). (PMID: 24086042378304410.1101/cshperspect.a012609) ; Marteijn, J. A. et al. Understanding nucleotide excision repair and its roles in cancer and ageing. Nat. Rev. Mol. Cell Biol. 15, 465–481 (2014). (PMID: 2495420910.1038/nrm3822) ; Sugasawa, K. Molecular mechanisms of DNA damage recognition for mammalian nucleotide excision repair. DNA Repair 44, 110–117 (2016). (PMID: 2726455610.1016/j.dnarep.2016.05.015) ; Beecher, M. et al. Expanding molecular roles of UV-DDB: Shining light on genome stability and cancer. DNA Repair 94, 102860 (2020). (PMID: 32739133787365910.1016/j.dnarep.2020.102860) ; Lan, L. et al. Monoubiquitinated histone H2A destabilizes photolesion-containing nucleosomes with concomitant release of UV-damaged DNA-binding protein E3 ligase. J. Biol. Chem. 287, 12036–12049 (2012). (PMID: 22334663332095010.1074/jbc.M111.307058) ; El-Mahdy, M. A. et al. Cullin 4A-mediated proteolysis of DDB2 protein at DNA damage sites regulates in vivo lesion recognition by XPC. J. Biol. Chem. 281, 13404–11. (2006). (PMID: 1652780710.1074/jbc.M511834200) ; van den Heuvel, D., et al. Transcription-coupled DNA repair: from mechanism to human disorder. Trends Cell Biol. 31, 359–371 (2021). ; D’Errico, M. et al. New functions of XPC in the protection of human skin cells from oxidative damage. EMBO J. 25, 4305–4315 (2006). (PMID: 16957781157044510.1038/sj.emboj.7601277) ; Parlanti, E. et al. The cross talk between pathways in the repair of 8-oxo-7,8-dihydroguanine in mouse and human cells. Free Radic. Biol. Med 53, 2171–2177 (2012). (PMID: 2301047010.1016/j.freeradbiomed.2012.08.593) ; Will, O. et al. Oxidative DNA damage and mutations induced by a polar photosensitizer, Ro19-8022. Mutat. Res. 435, 89–101 (1999). (PMID: 1052622010.1016/S0921-8777(99)00039-7) ; Menoni, H., Hoeijmakers, J. H. & Vermeulen, W. Nucleotide excision repair-initiating proteins bind to oxidative DNA lesions in vivo. J. Cell Biol. 199, 1037–1046 (2012). (PMID: 23253478352952110.1083/jcb.201205149) ; Menoni, H. et al. The transcription-coupled DNA repair-initiating protein CSB promotes XRCC1 recruitment to oxidative DNA damage. Nucleic Acids Res. 46, 7747–7756 (2018). (PMID: 29955842612563410.1093/nar/gky579) ; Guo, J., Hanawalt, P. C. & Spivak, G. Comet-FISH with strand-specific probes reveals transcription-coupled repair of 8-oxoGuanine in human cells. Nucleic Acids Res. 41, 7700–7712 (2013). (PMID: 23775797376353110.1093/nar/gkt524) ; Jang, S. et al. Damage sensor role of UV-DDB during base excision repair. Nat. Struct. Mol. Biol. 26, 695–703 (2019). (PMID: 31332353668437210.1038/s41594-019-0261-7) ; He, J. et al. A genetically targetable near-infrared photosensitizer. Nat. Methods 13, 263–268 (2016). (PMID: 26808669491615910.1038/nmeth.3735) ; Fouquerel, E. et al. Targeted and persistent 8-oxoguanine base damage at telomeres promotes telomere loss and crisis. Mol. Cell 75, 117–130 (2019). (PMID: 31101499662585410.1016/j.molcel.2019.04.024) ; Kruk, P. A., Rampino, N. J. & Bohr, V. A. DNA damage and repair in telomeres: relation to aging. Proc. Natl Acad. Sci. 92, 258–262 (1995). (PMID: 78168284285710.1073/pnas.92.1.258) ; Lu, J. & Liu, Y. Deletion of Ogg1 DNA glycosylase results in telomere base damage and length alteration in yeast. EMBO J. 29, 398–409 (2010). (PMID: 1994285810.1038/emboj.2009.355) ; Agnez-Lima, L. F. et al. DNA damage by singlet oxygen and cellular protective mechanisms. Mutat. Res Rev. Mutat. Res 751, 15–28 (2012). (PMID: 2226656810.1016/j.mrrev.2011.12.005) ; Ravanat, J. L. et al. Singlet oxygen induces oxidation of cellular DNA. J. Biol. Chem. 275, 40601–40604 (2000). (PMID: 1100778310.1074/jbc.M006681200) ; Nichols, A. F., Ong, P. & Linn, S. Mutations specific to the xeroderma pigmentosum group E Ddb- phenotype. J. Biol. Chem. 271, 24317–24320. (1996). (PMID: 879868010.1074/jbc.271.40.24317) ; Ghodke, H. et al. Single-molecule analysis reveals human UV-damaged DNA-binding protein (UV-DDB) dimerizes on DNA via multiple kinetic intermediates. Proc. Natl Acad. Sci. 111, E1862–E1871 (2014). (PMID: 24760829402004810.1073/pnas.1323856111) ; Rapic-Otrin, V. et al. True XP group E patients have a defective UV-damaged DNA binding protein complex and mutations in DDB2 which reveal the functional domains of its p48 product. Hum. Mol. Genet 12, 1507–1522 (2003). (PMID: 1281297910.1093/hmg/ddg174) ; Sugasawa, K. et al. UV-induced ubiquitylation of XPC protein mediated by UV-DDB-ubiquitin ligase complex. Cell 121, 387–400 (2005). (PMID: 1588262110.1016/j.cell.2005.02.035) ; Kitsera, N. et al. 8-Oxo-7,8-dihydroguanine in DNA does not constitute a barrier to transcription, but is converted into transcription-blocking damage by OGG1. Nucleic Acids Res 39, 5926–5934 (2011). (PMID: 21441539315232610.1093/nar/gkr163) ; Tornaletti, S., Maeda, L. S. & Hanawalt, P. C. Transcription arrest at an abasic site in the transcribed strand of template DNA. Chem. Res Toxicol. 19, 1215–1220. (2006). (PMID: 1697802610.1021/tx060103g) ; Cusanelli, E. & Chartrand, P. Telomeric repeat-containing RNA TERRA: a noncoding RNA connecting telomere biology to genome integrity. Front Genet 6, 143 (2015). (PMID: 25926849439641410.3389/fgene.2015.00143) ; Schoeftner, S. & Blasco, M. A. Developmentally regulated transcription of mammalian telomeres by DNA-dependent RNA polymerase II. Nat. Cell Biol. 10, 228–236 (2008). (PMID: 1815712010.1038/ncb1685) ; Roy, D. et al. Competition between the RNA transcript and the nontemplate DNA strand during R-loop formation in vitro: a nick can serve as a strong R-loop initiation site. Mol. Cell Biol. 30, 146–159 (2010). (PMID: 1984106210.1128/MCB.00897-09) ; Sollier, J. et al. Transcription-coupled nucleotide excision repair factors promote R-loop-induced genome instability. Mol. Cell 56, 777–785 (2014). (PMID: 25435140427263810.1016/j.molcel.2014.10.020) ; Cleaver, J. E. Transcription coupled repair deficiency protects against human mutagenesis and carcinogenesis: Personal Reflections on the 50th anniversary of the discovery of xeroderma pigmentosum. DNA Repair 58, 21–28 (2017). (PMID: 2884686810.1016/j.dnarep.2017.08.004) ; Conomos, D. et al. Variant repeats are interspersed throughout the telomeres and recruit nuclear receptors in ALT cells. J. Cell Biol. 199, 893–906 (2012). (PMID: 23229897351822310.1083/jcb.201207189) ; Ribeiro-Silva, C. et al. Ubiquitin and TFIIH-stimulated DDB2 dissociation drives DNA damage handover in nucleotide excision repair. Nat. Commun. 11, 4868 (2020). (PMID: 32985517752223110.1038/s41467-020-18705-0) ; Adam, S. et al. Real-time tracking of parental histones reveals their contribution to chromatin integrity following DNA damage. Mol. Cell 64, 65–78 (2016). (PMID: 27642047506552610.1016/j.molcel.2016.08.019) ; Luijsterburg, M. S. et al. DDB2 promotes chromatin decondensation at UV-induced DNA damage. J. Cell Biol. 197, 267–281 (2012). (PMID: 22492724332839310.1083/jcb.201106074) ; Pines, A. et al. PARP1 promotes nucleotide excision repair through DDB2 stabilization and recruitment of ALC1. J. Cell Biol. 199, 235–249 (2012). (PMID: 23045548347122310.1083/jcb.201112132) ; Groisman, R. et al. CSA-dependent degradation of CSB by the ubiquitin-proteasome pathway establishes a link between complementation factors of the Cockayne syndrome. Genes Dev. 20, 1429–1434 (2006). (PMID: 16751180147575510.1101/gad.378206) ; Groisman, R. et al. The ubiquitin ligase activity in the DDB2 and CSA complexes is differentially regulated by the COP9 signalosome in response to DNA damage. Cell 113, 357–367 (2003). (PMID: 1273214310.1016/S0092-8674(03)00316-7) ; Scrima, A. et al. Detecting UV-lesions in the genome: The modular CRL4 ubiquitin ligase does it best! FEBS Lett. 585, 2818–2825 (2011). (PMID: 2155034110.1016/j.febslet.2011.04.064) ; Cho, N. W. et al. Interchromosomal homology searches drive directional ALT telomere movement and synapsis. Cell 159, 108–121 (2014). (PMID: 25259924417703910.1016/j.cell.2014.08.030) ; Fayyad, N. et al. Xeroderma pigmentosum C (XPC) mutations in primary fibroblasts impair base excision repair pathway and increase oxidative DNA damage. Front Genet 11, 561687 (2020). (PMID: 33329698772872210.3389/fgene.2020.561687) ; Yoshihara, M. et al. Genome-wide profiling of 8-oxoguanine reveals its association with spatial positioning in nucleus. DNA Res. 21, 603–612 (2014). (PMID: 25008760426329410.1093/dnares/dsu023) ; Amouroux, R. et al. Oxidative stress triggers the preferential assembly of base excision repair complexes on open chromatin regions. Nucleic Acids Res 38, 2878–2890 (2010). (PMID: 20071746287500510.1093/nar/gkp1247) ; Matsumoto, S. et al. DNA damage detection in nucleosomes involves DNA register shifting. Nature 571, 79–84 (2019). (PMID: 31142837661172610.1038/s41586-019-1259-3) ; Menoni, H. et al. Chromatin associated mechanisms in base excision repair - nucleosome remodeling and DNA transcription, two key players. Free Radic. Biol. Med 107, 159–169 (2017). (PMID: 2801114910.1016/j.freeradbiomed.2016.12.026) ; Hewitt, G. et al. Defective ALC1 nucleosome remodeling confers PARPi sensitization and synthetic lethality with HRD. Mol. Cell 81, 767–783 e11 (2021). (PMID: 33333017789590710.1016/j.molcel.2020.12.006) ; Tsuda, M. et al. ALC1/CHD1L, a chromatin-remodeling enzyme, is required for efficient base excision repair. PLoS One 12, e0188320 (2017). (PMID: 29149203569346710.1371/journal.pone.0188320) ; Ouellette, M. M. et al. The establishment of telomerase-immortalized cell lines representing human chromosome instability syndromes. Hum. Mol. Genet 9, 403–411 (2000). (PMID: 1065555010.1093/hmg/9.3.403) ; Ribeiro-Silva, C. et al. DNA damage sensitivity of SWI/SNF-deficient cells depends on TFIIH subunit p62/GTF2H1. Nat. Commun. 9, 4067 (2018). (PMID: 30287812617227810.1038/s41467-018-06402-y) ; Luijsterburg, M. S. et al. Dynamic in vivo interaction of DDB2 E3 ubiquitin ligase with UV-damaged DNA is independent of damage-recognition protein XPC. J. Cell Sci. 120, 2706–2716. (2007). (PMID: 1763599110.1242/jcs.008367) ; Campalans, A. et al. UVA irradiation induces relocalisation of the DNA repair protein hOGG1 to nuclear speckles. J. Cell Sci. 120, 23–32 (2007). (PMID: 1714857310.1242/jcs.03312) ; Furda, A. M. et al. Analysis of DNA damage and repair in nuclear and mitochondrial DNA of animal cells using quantitative PCR. Methods Mol. Biol. 920, 111–132 (2012). (PMID: 22941600442239210.1007/978-1-61779-998-3_9) ; Schlierf, A. et al. Targeted inhibition of the COP9 signalosome for treatment of cancer. Nat. Commun. 7, 13166 (2016). (PMID: 27774986507898910.1038/ncomms13166)
  • Grant Information: R01 ES019566 United States ES NIEHS NIH HHS; R35 ES030396 United States ES NIEHS NIH HHS; R01 ES028686 United States ES NIEHS NIH HHS; F32 AG067710 United States AG NIA NIH HHS; R35 ES031638 United States ES NIEHS NIH HHS
  • Substance Nomenclature: 0 (Chromatin) ; 0 (DDB2 protein, human) ; 0 (DNA-Binding Proteins) ; 0 (XPA protein, human) ; 0 (Xeroderma Pigmentosum Group A Protein) ; 156533-34-5 (XPC protein, human) ; 5614-64-2 (8-hydroxyguanine) ; 5Z93L87A1R (Guanine) ; EC 3.2.2.- (DNA Glycosylases) ; EC 3.2.2.- (oxoguanine glycosylase 1, human)
  • Entry Date(s): Date Created: 20220222 Date Completed: 20220304 Latest Revision: 20221023
  • Update Code: 20240513
  • PubMed Central ID: PMC8861037

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