DICER- and MMSET-catalyzed H4K20me2 recruits the nucleotide excision repair factor XPA to DNA damage sites

Ultraviolet (UV) irradiation triggers the recruitment of DNA repair factors to the lesion sites and the deposition of histone marks as part of the DNA damage response. The major DNA repair pathway removing DNA lesions caused by exposure to UV light is nucleotide excision repair (NER). We have previously demonstrated that the endoribonuclease DICER facilitates chromatin decondensation during lesion recognition in the global-genomic branch of NER. Here, we report that DICER mediates the recruitment of the methyltransferase MMSET to the DNA damage site. We show that MMSET is required for efficient NER and that it catalyzes the dimethylation of histone H4 at lysine 20 (H4K20me2). H4K20me2 at DNA damage sites facilitates the recruitment of the NER factor XPA. Our work thus provides evidence for an H4K20me2-dependent mechanism of XPA recruitment during lesion recognition in the global-genomic branch of NER.

• Publication year

  2018

• Venue

  Journal of Cell Biology

• Publication date

  2018-02-05

• Fields of study

  Biology, Medicine

• Identifiers
  DOI 10.1083/jcb.201704028PMID 29233865PMCID 5800799
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Nuclear organization of nucleotide excision repair is mediated by RING1B dependent H2A-ubiquitylation

  2017cited by this paper
• Shaping chromatin with DICER

  2017influential reference
• DICER and ZRF1 contribute to chromatin decondensation during nucleotide excision repair

  2017influential reference
• ZRF1 mediates remodeling of E3 ligases at DNA lesion sites during nucleotide excision repair

  2016cited by this paper
• The emerging role of lysine methyltransferase SETD8 in human diseases

  2016cited by this paper
• Small RNAs Recruit Chromatin-Modifying Enzymes MMSET and Tip60 to Reconfigure Damaged DNA upon Double-Strand Break and Facilitate Repair.

  2016cited by this paper
• On‐site remodeling at chromatin: How multiprotein complexes are rebuilt during DNA repair and transcriptional activation

  2016cited by this paper
• Overview of xeroderma pigmentosum proteins architecture, mutations and post-translational modifications.

  2015cited by this paper
• Small-RNA loading licenses Argonaute for assembly into a transcriptional silencing complex

  2015cited by this paper
• SET8 methyltransferase activity during the DNA double-strand break response is required for recruitment of 53BP1

  2014cited by this paper
• A rapid, comprehensive system for assaying DNA repair activity and cytotoxic effects of DNA-damaging reagents

  2014cited by this paper
• Concerted activities of distinct H4K20 methyltransferases at DNA double-strand breaks regulate 53BP1 nucleation and NHEJ-directed repair.

  2014cited by this paper
• Understanding nucleotide excision repair and its roles in cancer and ageing

  2014cited by this paper
• 53BP1: pro choice in DNA repair.

  2014cited by this paper
• NSD2 is recruited through its PHD domain to oncogenic gene loci to drive multiple myeloma.

  2013cited by this paper
• Double-strand break repair: 53BP1 comes into focus

  2013cited by this paper
• 53BP1 is a reader of the DNA damage-induced H2A Lys15 ubiquitin mark

  2013cited by this paper
• Molecular mechanisms of RNA interference.

  2013cited by this paper
• Poly(ADP-ribose) Contributes to an Association between Poly(ADP-ribose) Polymerase-1 and Xeroderma Pigmentosum Complementation Group A in Nucleotide Excision Repair*

  2012cited by this paper
• Implication of Posttranslational Histone Modifications in Nucleotide Excision Repair

  2012cited by this paper
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  2010cited by this paper
• Transcriptional activation of polycomb-repressed genes by ZRF1

  2010cited by this paper
• Nucleotide excision repair–induced H2A ubiquitination is dependent on MDC1 and RNF8 and reveals a universal DNA damage response

  2009cited by this paper
• The cullin 4B-based UV-damaged DNA-binding protein ligase binds to UV-damaged chromatin and ubiquitinates histone H2A.

  2008cited by this paper
• The effect of H3K79 dimethylation and H4K20 trimethylation on nucleosome and chromatin structure

  2008cited by this paper
• A chromatin-wide transition to H4K20 monomethylation impairs genome integrity and programmed DNA rearrangements in the mouse.

  2008cited by this paper
• Transcription-coupled nucleotide excision repair in mammalian cells: molecular mechanisms and biological effects

  2008cited by this paper
• Identifying novel proteins recognizing histone modifications using peptide pull-down assay.

  2006cited by this paper
• Specific and efficient binding of xeroderma pigmentosum complementation group A to double-strand/single-strand DNA junctions with 3'- and/or 5'-ssDNA branches.

  2006cited by this paper
• Phosphorylation of nucleotide excision repair factor xeroderma pigmentosum group A by ataxia telangiectasia mutated and Rad3-related-dependent checkpoint pathway promotes cell survival in response to UV irradiation.

  2006cited by this paper
• The DDB1-CUL4ADDB2 ubiquitin ligase is deficient in xeroderma pigmentosum group E and targets histone H2A at UV-damaged DNA sites.

  2006cited by this paper
• Structural basis for the methylation state-specific recognition of histone H4-K20 by 53BP1 and Crb2 in DNA repair.

  2006cited by this paper
• DNA damage triggers nucleotide excision repair-dependent monoubiquitylation of histone H2A.

  2006cited by this paper
• From silencing to gene expression: real-time analysis in single cells.

  2004cited by this paper
• A silencing pathway to induce H 3K 9 and H 4K 20 trimethylation at constitutive heterochromatin

  2004cited by this paper
• A silencing pathway to induce H3-K9 and H4-K20 trimethylation at constitutive heterochromatin.

  2004cited by this paper
• Restoration of UV sensitivity in UV‐resistant HeLa cells by antisense‐mediated depletion of damaged DNA‐binding protein 2 (DDB2)

  2002cited by this paper
• In situ visualization of ultraviolet-light-induced DNA damage repair in locally irradiated human fibroblasts.

  2001cited by this paper
• DNA Repair—Deficient Xpa and Xpa/p53+/- Knock-Out Mice: Nature of the Models

  2001cited by this paper
• Molecular mechanism of nucleotide excision repair.

  1999cited by this paper
• Cerebellar neurodegeneration in human hereditary DNA repair disorders.

  1998cited by this paper
• Loss of the Xeroderma Pigmentosum Group A Gene (XPA) Enhances Apoptosis of Cultured Cerebellar Neurons Induced by UV but Not by Low‐K+ Medium

  1997cited by this paper
• Xpa knockout mice.

  1996cited by this paper
• CONTRASTING STRUCTURAL IMPACTS INDUCED BY cis‐syn CYCLOBUTANE DIMER AND (6–4) ADDUCT IN DNA DUPLEX DECAMERS: IMPLICATION IN MUTAGENESIS AND REPAIR ACTIVITY

  1995cited by this paper
• Nucleotide excision repair genes involved in xeroderma pigmentosum.

  1994cited by this paper

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  2022cites this paper
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  2022cites this paper
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  2021cites this paper
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  2020cites this paper
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  2020cites this paper
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  2020cites this paper
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  2020cites this paper
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  2020cites this paper
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  2020cites this paper
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  2020cites this paper
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