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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Masutani, C., Kusumoto, R., Yamada, A., Dohmae, N., Yokoi, M., Yuasa, M., Araki, M., Iwai, S., Takio, K., & Hanaoka, F. (1999) · Nature · doi:10.1038/21447 · Cited by 1,292
Control of spontaneous and damage-induced mutagenesis by SUMO and ubiquitin conjugation
Stelter, P., & Ulrich, H. D. (2003) · Nature · doi:10.1038/nature01965 · Cited by 850
Interaction of Human DNA Polymerase η with Monoubiquitinated PCNA
Kannouche, P. L., Wing, J., & Lehmann, A. R. (2004) · Molecular Cell · doi:10.1016/s1097-2765(04)00259-x · Cited by 845
Identification of multiple distinct Snf2 subfamilies with conserved structural motifs
Flaus, A. (2006) · Nucleic Acids Research · doi:10.1093/nar/gkl295 · Cited by 750
SUMO-modified PCNA recruits Srs2 to prevent recombination during S phase
Pfander, B., Moldovan, G., Sacher, M., Hoege, C., & Jentsch, S. (2005) · Nature · doi:10.1038/nature03665 · Cited by 626
Regulation of monoubiquitinated PCNA by DUB autocleavage
Huang, T. T., Nijman, S. M. B., Mirchandani, K. D., Galardy, P. J., Cohn, M. A., Haas, W., Gygi, S. P., Ploegh, H. L., Bernards, R., & D’Andrea, A. D. (2006) · Nature Cell Biology · doi:10.1038/ncb1378 · Cited by 597
The novel functions of ubiquitination in signaling
Sun, L., & Chen, Z. J. (2004) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2004.02.005 · Cited by 465
Translesion synthesis: Y-family polymerases and the polymerase switch
LEHMANN, A., NIIMI, A., OGI, T., BROWN, S., SABBIONEDA, S., WING, J., KANNOUCHE, P., & GREEN, C. (2007) · DNA Repair · doi:10.1016/j.dnarep.2007.02.003 · Cited by 389
Human Fanconi anemia monoubiquitination pathway promotes homologous DNA repair
Nakanishi, K., Yang, Y.-G., Pierce, A. J., Taniguchi, T., Digweed, M., D'Andrea, A. D., Wang, Z.-Q., & Jasin, M. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0407796102 · Cited by 384 · cited 1×
“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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Elvers, I. (2011) · KTH Publication Database DiVA (KTH Royal Institute of Technology)
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Guler, G. D. (2012)
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Additional file 11 of Genomic analysis of field pennycress (Thlaspi arvense) provides insights into mechanisms of adaptation to high elevation
Geng, Y., Guan, Y., Qiong, L., Lu, S., An, M., Crabbe, M. J. C., Qi, J., Zhao, F., Qiao, Q., & Zhang, T. (2021) · Figshare · doi:10.6084/m9.figshare.15041196
Additional file 13 of Genomic analysis of field pennycress (Thlaspi arvense) provides insights into mechanisms of adaptation to high elevation
Geng, Y., Guan, Y., Qiong, L., Lu, S., An, M., Crabbe, M. J. C., Qi, J., Zhao, F., Qiao, Q., & Zhang, T. (2021) · Figshare · doi:10.6084/m9.figshare.15041202
Additional file 6 of Genomic analysis of field pennycress (Thlaspi arvense) provides insights into mechanisms of adaptation to high elevation
Geng, Y., Guan, Y., Qiong, L., Lu, S., An, M., Crabbe, M. J. C., Qi, J., Zhao, F., Qiao, Q., & Zhang, T. (2021) · Figshare · doi:10.6084/m9.figshare.15041241
Additional file 10 of Genomic analysis of field pennycress (Thlaspi arvense) provides insights into mechanisms of adaptation to high elevation
Geng, Y., Guan, Y., Qiong, L., Lu, S., An, M., Crabbe, M. J. C., Qi, J., Zhao, F., Qiao, Q., & Zhang, T. (2021) · Figshare · doi:10.6084/m9.figshare.15041193
Additional file 8 of Genomic analysis of field pennycress (Thlaspi arvense) provides insights into mechanisms of adaptation to high elevation
Geng, Y., Guan, Y., Qiong, L., Lu, S., An, M., Crabbe, M. J. C., Qi, J., Zhao, F., Qiao, Q., & Zhang, T. (2021) · Figshare · doi:10.6084/m9.figshare.15041250
Additional file 4 of Genomic analysis of field pennycress (Thlaspi arvense) provides insights into mechanisms of adaptation to high elevation
Geng, Y., Guan, Y., Qiong, L., Lu, S., An, M., Crabbe, M. J. C., Qi, J., Zhao, F., Qiao, Q., & Zhang, T. (2021) · Figshare · doi:10.6084/m9.figshare.15041235
Additional file 16 of Genomic analysis of field pennycress (Thlaspi arvense) provides insights into mechanisms of adaptation to high elevation
Geng, Y., Guan, Y., Qiong, L., Lu, S., An, M., Crabbe, M. J. C., Qi, J., Zhao, F., Qiao, Q., & Zhang, T. (2021) · Figshare · doi:10.6084/m9.figshare.15041211
Additional file 9 of Genomic analysis of field pennycress (Thlaspi arvense) provides insights into mechanisms of adaptation to high elevation
Geng, Y., Guan, Y., Qiong, L., Lu, S., An, M., Crabbe, M. J. C., Qi, J., Zhao, F., Qiao, Q., & Zhang, T. (2021) · Figshare · doi:10.6084/m9.figshare.15041253
Additional file 20 of Genomic analysis of field pennycress (Thlaspi arvense) provides insights into mechanisms of adaptation to high elevation
Geng, Y., Guan, Y., Qiong, L., Lu, S., An, M., Crabbe, M. J. C., Qi, J., Zhao, F., Qiao, Q., & Zhang, T. (2021) · Figshare · doi:10.6084/m9.figshare.15041226
Additional file 17 of Genomic analysis of field pennycress (Thlaspi arvense) provides insights into mechanisms of adaptation to high elevation
Geng, Y., Guan, Y., Qiong, L., Lu, S., An, M., Crabbe, M. J. C., Qi, J., Zhao, F., Qiao, Q., & Zhang, T. (2021) · Figshare · doi:10.6084/m9.figshare.15041214
Additional file 18 of Genomic analysis of field pennycress (Thlaspi arvense) provides insights into mechanisms of adaptation to high elevation
Geng, Y., Guan, Y., Qiong, L., Lu, S., An, M., Crabbe, M. J. C., Qi, J., Zhao, F., Qiao, Q., & Zhang, T. (2021) · Figshare · doi:10.6084/m9.figshare.15041217
Additional file 12 of Genomic analysis of field pennycress (Thlaspi arvense) provides insights into mechanisms of adaptation to high elevation
Geng, Y., Guan, Y., Qiong, L., Lu, S., An, M., Crabbe, M. J. C., Qi, J., Zhao, F., Qiao, Q., & Zhang, T. (2021) · Figshare · doi:10.6084/m9.figshare.15041199
Additional file 19 of Genomic analysis of field pennycress (Thlaspi arvense) provides insights into mechanisms of adaptation to high elevation
Geng, Y., Guan, Y., Qiong, L., Lu, S., An, M., Crabbe, M. J. C., Qi, J., Zhao, F., Qiao, Q., & Zhang, T. (2021) · Figshare · doi:10.6084/m9.figshare.15041220
Additional file 7 of Genomic analysis of field pennycress (Thlaspi arvense) provides insights into mechanisms of adaptation to high elevation
Geng, Y., Guan, Y., Qiong, L., Lu, S., An, M., Crabbe, M. J. C., Qi, J., Zhao, F., Qiao, Q., & Zhang, T. (2021) · Figshare · doi:10.6084/m9.figshare.15041247
Additional file 15 of Genomic analysis of field pennycress (Thlaspi arvense) provides insights into mechanisms of adaptation to high elevation
Geng, Y., Guan, Y., Qiong, L., Lu, S., An, M., Crabbe, M. J. C., Qi, J., Zhao, F., Qiao, Q., & Zhang, T. (2021) · Figshare · doi:10.6084/m9.figshare.15041208
Additional file 1 of Genomic analysis of field pennycress (Thlaspi arvense) provides insights into mechanisms of adaptation to high elevation
Geng, Y., Guan, Y., Qiong, L., Lu, S., An, M., Crabbe, M. J. C., Qi, J., Zhao, F., Qiao, Q., & Zhang, T. (2021) · Figshare · doi:10.6084/m9.figshare.15041223
Additional file 14 of Genomic analysis of field pennycress (Thlaspi arvense) provides insights into mechanisms of adaptation to high elevation
Geng, Y., Guan, Y., Qiong, L., Lu, S., An, M., Crabbe, M. J. C., Qi, J., Zhao, F., Qiao, Q., & Zhang, T. (2021) · Figshare · doi:10.6084/m9.figshare.15041205
Additional file 5 of Genomic analysis of field pennycress (Thlaspi arvense) provides insights into mechanisms of adaptation to high elevation
Geng, Y., Guan, Y., Qiong, L., Lu, S., An, M., Crabbe, M. J. C., Qi, J., Zhao, F., Qiao, Q., & Zhang, T. (2021) · Figshare · doi:10.6084/m9.figshare.15041238
Additional file 2 of Genomic analysis of field pennycress (Thlaspi arvense) provides insights into mechanisms of adaptation to high elevation
Geng, Y., Guan, Y., Qiong, L., Lu, S., An, M., Crabbe, M. J. C., Qi, J., Zhao, F., Qiao, Q., & Zhang, T. (2021) · Figshare · doi:10.6084/m9.figshare.15041229
Additional file 3 of Genomic analysis of field pennycress (Thlaspi arvense) provides insights into mechanisms of adaptation to high elevation
Geng, Y., Guan, Y., Qiong, L., Lu, S., An, M., Crabbe, M. J. C., Qi, J., Zhao, F., Qiao, Q., & Zhang, T. (2021) · Figshare · doi:10.6084/m9.figshare.15041232
USP1 inhibition promotes RAD18-dependent PCNA degradation and BRCA1 synthetic lethalityPreprint
Ashton, N. W., Ravindranathan, R., Korchak, E. J., Somuncu, O., Zambrano, G. A., Mukkavalli, S., Asada, S., Korzhnev, D. M., Bezsonova, I., & D’Andrea, A. D. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.02.25.708068
Importance of E3 Ligases for Preserving Genome Integrity: Progress and Challenges
Mahata, R., & Santra, M. K. (2026) · Molecular and Cellular Biology · doi:10.1080/10985549.2026.2638203
La voie de dégradation CRL4Cdt2 régule le recrutement des ADN polymérases translésionnelles eta et kappa en foyers nucléaires après endommagements aux UV-C en ciblant pour dégradation les protéines qui contiennent des PIP box spécialisées
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Furno, E. L. (2019) · theses.fr (ABES) · doi:10.70675/cf32bcd5z3031z4693z8b1bz62fe76673ccc
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Goulas, J. (2025) · theses.fr (ABES) · doi:10.70675/7894ebf5zbdf7z4147z940ezc553e0ed0e18
SHPRH together with the Ube2D family of enzymes directly ubiquitinates PCNA at Lys164 in vitro
Wang, X., Hu, Y., Wen, Y., Shen, M., Chen, P., & Xiang, S. (2026) · PLoS ONE · doi:10.1371/journal.pone.0347227

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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