Cited by 304DNA Repair MechanismsUbiquitin and proteasome pathwaysGenetic factors in colorectal cancer

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Polyubiquitination of proliferating cell nuclear antigen by HLTF and SHPRH prevents genomic instability from stalled replication forks.

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Motegi, Akira, Liaw, Hung-Jiun, Lee, Kyoo-Young, Roest, Henk P., Maas, Alex, Wu, Xiaoli, Moinova, Helen, Markowitz, Sanford D., Ding, Hao, Hoeijmakers, Jan H. J., Myung, Kyungjae·2008·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.0805685105PMC PMC2518831

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Abstract

Chronic stalling of DNA replication forks caused by DNA damage can lead to genomic instability. Cells have evolved lesion bypass pathways such as postreplication repair (PRR) to resolve these arrested forks. In yeast, one branch of PRR involves proliferating cell nuclear antigen (PCNA) polyubiquitination mediated by the Rad5-Ubc13-Mms2 complex that allows bypass of DNA lesion by a template-switching mechanism. Previously, we identified human SHPRH as a functional homologue of yeast Rad5 and revealed the existence of RAD5-like pathway in human cells. Here we report the identification of HLTF as a second RAD5 homologue in human cells. HLTF, like SHPRH, shares a unique domain architecture with Rad5 and promotes lysine 63-linked polyubiquitination of PCNA. Similar to yeast Rad5, HLTF is able to interact with UBC13 and PCNA, as well as SHPRH; and the reduction of either SHPRH or HLTF expression enhances spontaneous mutagenesis. Moreover, Hltf-deficient mouse embryonic fibroblasts show elevated chromosome breaks and fusions after methyl methane sulfonate treatment. Our results suggest that HLTF and SHPRH are functional homologues of yeast Rad5 that cooperatively mediate PCNA polyubiquitination and maintain genomic stability.

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“To determine whether SHPRH and HLTF are involved in HR, we used a recombination reporter assay (DR-GFP reporter assay), which can measure the frequency of HR between tandem GFP repeats with inactivating mutations (25).”
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Authors: Motegi, A., Liaw, H.-J., Lee, K.-Y., Roest, H. P., Maas, A., Wu, X., Moinova, H., Markowitz, S. D., Ding, H., Hoeijmakers, J. H. J., & Myung, K.
Affiliations: National Institutes of Health (US)
*Genome Instability Section, Genetics and Molecular Biology Branch, National Human Genome Research Institute, National Institutes of Health, Bethesda, MD 20892;
Erasmus MC (NL)
University of Manitoba (CA)
Case Western Reserve University (US)
Howard Hughes Medical Institute (US)
ORCID: Motegi, Akira
Roest, Henk P.
Maas, Alex
Wu, Xiaoli
Moinova, Helen
Markowitz, Sanford D.
Ding, Hao
Hoeijmakers, Jan H. J.
Myung, Kyungjae
Venue: Proceedings of the National Academy of Sciences
Publisher: National Academy of Sciences
Published: 2008-08-26
Volume: 105
Issue: 34
Pages: 12411-12416
ISSN: 0027-8424 (ISSN-L)
1091-6490
DOI: 10.1073/pnas.0805685105
PMC: PMC2518831
OpenAlex: W2113224775
Cited by: 304
References: 36
Citations by year: 2026: 10 · 2025: 13 · 2024: 10 · 2023: 14 · 2022: 16 · 2021: 32 · 2020: 24 · 2019: 19 · 2018: 19 · 2017: 14 · 2016: 20 · 2015: 12 · 2014: 13 · 2013: 15 · 2012: 19
FWCI: 7.41
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Proceedings of the National Academy of Sciences (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
EUR Research Repository (Erasmus University Rotterdam) (publishedVersion)
EUR Research Repository (Erasmus University Rotterdam) (submittedVersion)
RePub (Erasmus University Rotterdam) (submittedVersion, other-oa)
RePub (Erasmus University Rotterdam) (submittedVersion)
Scholarworks@UNIST (Ulsan National Institute of Science and Technology) (submittedVersion)
Funders: Howard Hughes Medical Institute
National Institutes of Health
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 › Pathology and Forensic Medicine › Genetic factors in colorectal cancer
Keywords: HLTF, proliferating cell nuclear antigen, replication fork stalling, postreplication repair, Ubc13, genomic instability, spontaneous mutagenesis, methyl methanesulfonate, DNA damage response
MeSH terms: Adenosine Triphosphatases, DNA Damage, DNA Replication, DNA Helicases, DNA-Binding Proteins, Humans, Transcription Factors, Proliferating Cell Nuclear Antigen, Polyubiquitin, Saccharomyces cerevisiae Proteins, Structural Homology, Protein, Genomic Instability, Ubiquitin-Conjugating Enzymes, Ubiquitin-Protein Ligases, Ubiquitination

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Polyubiquitination of proliferating cell nuclear antigen by HLTF and SHPRH prevents genomic instability from stalled replication forks.

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