PreprintCited by 314DNA Repair MechanismsUbiquitin and proteasome pathwaysEffects of Radiation Exposure

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RNF4, a SUMO-targeted ubiquitin E3 ligase, promotes DNA double-strand break repair

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Galanty, Yaron, Belotserkovskaya, Rimma, Coates, Julia, Jackson, Stephen P.·2012·Genes & Development

DOI 10.1101/gad.188284.112PMC PMC3371407

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Abstract

Protein ubiquitylation and sumoylation play key roles in regulating cellular responses to DNA double-strand breaks (DSBs). Here, we show that human RNF4, a small ubiquitin-like modifier (SUMO)-targeted ubiquitin E3 ligase, is recruited to DSBs in a manner requiring its SUMO interaction motifs, the SUMO E3 ligases PIAS1 and PIAS4, and various DSB-responsive proteins. Furthermore, we reveal that RNF4 depletion impairs ubiquitin adduct formation at DSB sites and causes persistent histone H2AX phosphorylation (γH2AX) associated with defective DSB repair, hypersensitivity toward DSB-inducing agents, and delayed recovery from radiation-induced cell cycle arrest. We establish that RNF4 regulates turnover of the DSB-responsive factors MDC1 and replication protein A (RPA) at DNA damage sites and that RNF4-depleted cells fail to effectively replace RPA by the homologous recombination factors BRCA2 and RAD51 on resected DNA. Consistent with previous data showing that RNF4 targets proteins to the proteasome, we show that the proteasome component PSMD4 is recruited to DNA damage sites in a manner requiring its ubiquitin-interacting domains, RNF4 and RNF8. Finally, we establish that PSMD4 binds MDC1 and RPA1 in a DNA damage-induced, RNF4-dependent manner and that PSMD4 depletion cause MDC1 and γH2AX persistence in irradiated cells. RNF4 thus operates as a DSB response factor at the crossroads between the SUMO and ubiquitin systems.

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Authors: Galanty, Y., Belotserkovskaya, R., Coates, J., & Jackson, S. P.
Affiliations: University of Cambridge (GB)
ORCID: Galanty, Yaron
Belotserkovskaya, Rimma
Jackson, Stephen P.
Venue: Genes & Development
Publisher: Cold Spring Harbor Laboratory
Published: 2012-06-01
Volume: 26
Issue: 11
Pages: 1179-1195
ISSN: 0890-9369 (ISSN-L)
1549-5477
DOI: 10.1101/gad.188284.112
PMC: PMC3371407
OpenAlex: W2113354406
Cited by: 314
References: 68
Citations by year: 2026: 12 · 2025: 12 · 2024: 15 · 2023: 14 · 2022: 20 · 2021: 19 · 2020: 19 · 2019: 16 · 2018: 14 · 2017: 30 · 2016: 37 · 2015: 27 · 2014: 26 · 2013: 37 · 2012: 15
Type: posted content
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Genes & Development (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Wellcome Trust (092096)
Cancer Research UK (C6/A11226, 11224, A11224)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ubiquitin and proteasome pathways
Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Effects of Radiation Exposure
Keywords: RNF4, DNA double-strand break repair, SUMO interaction motif, PIAS1, PIAS4, H2AX phosphorylation, MDC1, replication protein A, BRCA2, RAD51, homologous recombination, proteasome, PSMD4, RNF8, radiation-induced cell cycle arrest, DNA damage response
MeSH terms: DNA Repair, DNA, Single-Stranded, Histones, Humans, Nuclear Proteins, Transcription Factors, Trans-Activators, Cell Cycle Proteins, Ubiquitin-Protein Ligases, Cell Line, Tumor, Proteasome Endopeptidase Complex, Adaptor Proteins, Signal Transducing, Rad51 Recombinase, Replication Protein A, DNA Breaks, Double-Stranded

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RNF4, a SUMO-targeted ubiquitin E3 ligase, promotes DNA double-strand break repair

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