Ubiquitin-dependent DNA damage bypass is separable from genome replication

Daigaku, Yasukazu; Davies, Adelina A.; Ulrich, Helle D.

doi:10.1038/nature09097

Cited by 259DNA Repair MechanismsUbiquitin and proteasome pathwaysGenomics and Chromatin Dynamics

Ubiquitin-dependent DNA damage bypass is separable from genome replication

Open access

Daigaku, Yasukazu, Davies, Adelina A., Ulrich, Helle D.·2010·Nature

DOI 10.1038/nature09097PMC PMC2888004

Open this paper in CoChat — free account

Abstract

Post-replication repair (PRR) is a pathway that allows cells to bypass or overcome lesions during DNA replication. In eukaryotes, damage bypass is activated by ubiquitylation of the replication clamp PCNA through components of the RAD6 pathway. Whereas monoubiquitylation of PCNA allows mutagenic translesion synthesis by damage-tolerant DNA polymerases, polyubiquitylation is required for an error-free pathway that probably involves a template switch to the undamaged sister chromatid. Both the timing of PRR events during the cell cycle and their location relative to replication forks, as well as the factors required downstream of PCNA ubiquitylation, have remained poorly characterized. Here we demonstrate that the RAD6 pathway normally operates during S phase. However, using an inducible system of DNA damage bypass in budding yeast (Saccharomyces cerevisiae), we show that the process is separable in time and space from genome replication, thus allowing direct visualization and quantification of productive PRR tracts. We found that both during and after S phase ultraviolet-radiation-induced lesions are bypassed predominantly via translesion synthesis, whereas the error-free pathway functions as a backup system. Our approach has revealed the distribution of PRR tracts in a synchronized cell population. It will allow an in-depth mechanistic analysis of how cells manage the processing of lesions to their genomes during and after replication.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1038/nature09097

Cites

30 of 30 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

In these conditions, repair may not be completed and ssDNA extension may both activate the checkpoint and channel the problematic lesion to another repair pathway such as recombination.
“In these conditions, repair may not be completed and the extension of the ssDNA region may meet two purposes: activating the checkpoint response and channeling the problematic lesion to a different repair pathway (e.g., recombination) [66–68].”
From Mind the gap: keeping UV lesions in check (2011) · cites this paper as [67]
S phase can be completed without PRR, but gapped replicated DNA must be refilled by PRR in G2 for cell survival.
“In fact, S phase can be completed in the absence of PRR, but the gapped replicated DNA needs to be refilled by PRR in G2 in order to warrant cell survival [66,67].”
From Mind the gap: keeping UV lesions in check (2011) · cites this paper as [67]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

A versatile toolbox for PCR‐based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes
Janke, C., Magiera, M., Rathfelder, N., Taxis, C., Reber, S., Maekawa, H., Moreno-Borchart, A. C., Doenges, G., Schwob, E., Schiebel, E., et al. (2004) · Yeast · doi:10.1002/yea.1142 · Cited by 2,251 · see citing works
RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO
Hoege, C., Pfander, B., Moldovan, G., Pyrowolakis, G., & Jentsch, S. (2002) · Nature · doi:10.1038/nature00991 · Cited by 2,202 · see citing works
EUKARYOTIC TRANSLESION SYNTHESIS DNA POLYMERASES: Specificity of Structure and Function
Prakash, S., Johnson, R. E., & Prakash, L. (2005) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.74.082803.133250 · Cited by 999 · see citing works
Replicon Clusters Are Stable Units of Chromosome Structure: Evidence That Nuclear Organization Contributes to the Efficient Activation and Propagation of S Phase in Human Cells
Jackson, D., & Pombo, A. (1998) · Journal of Cell Biology · doi:10.1083/jcb.140.6.1285 · Cited by 881 · see citing works
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 849 · see citing works
Self-citation
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 · see citing works
Eukaryotic polymerases ι and ζ act sequentially to bypass DNA lesions
Johnson, R. E., Washington, M. T., Haracska, L., Prakash, S., & Prakash, L. (2000) · Nature · doi:10.1038/35023030 · Cited by 632 · see citing works
Multiple mechanisms control chromosome integrity after replication fork uncoupling and restart at irreparable UV lesions
Lopes, M., Foiani, M., & Sogo, J. M. (2006) · Molecular Cell · doi:10.1016/j.molcel.2005.11.015 · Cited by 563 · see citing works
Rad18 guides polη to replication stalling sites through physical interaction and PCNA monoubiquitination
Watanabe, K., Tateishi, S., Kawasuji, M., Tsurimoto, T., Inoue, H., & Yamaizumi, M. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600383 · Cited by 538 · see citing works
Crosstalk between SUMO and Ubiquitin on PCNA Is Mediated by Recruitment of the Helicase Srs2p
Papouli, E., Chen, S., Davies, A. A., Huttner, D., Krejčí, L., Sung, P., & Ulrich, H. D. (2005) · Molecular Cell · doi:10.1016/j.molcel.2005.06.001 · Cited by 522 · see citing works
Self-citation
Postreplication repair of DNA in ultraviolet-irradiated mammalian cells
Lehmann, A. R. (1972) · Journal of Molecular Biology · doi:10.1016/0022-2836(72)90418-4 · Cited by 437 · see citing works
Persistent initiation of DNA replication and chromatin-bound MCM proteins during the cell cycle in cdc6 mutantsPreprint
Liang, C., & Stillman, B. (1997) · Genes & Development · doi:10.1101/gad.11.24.3375 · Cited by 358 · see citing works
Characterization of postreplication repair in Saccharomyces cerevisiae and effects of rad6, rad18, rev3 and rad52 mutations
Prakash, L. (1981) · Molecular and General Genetics MGG · doi:10.1007/bf00352525 · Cited by 291 · see citing works
An activator/repressor dual system allows tight tetracycline-regulated gene expression in budding yeast [published erratum appears in Nucleic Acids Res 1998 Apr 1;26(7):following 1855]
Bellı́, G. (1998) · Nucleic Acids Research · doi:10.1093/nar/26.4.942 · Cited by 285 · see citing works
Two-polymerase mechanisms dictate error-free and error-prone translesion DNA synthesis in mammals
Shachar, S., Ziv, O., Avkin, S., Adar, S., Wittschieben, J., Reißner, T., Chaney, S., Friedberg, E. C., Wang, Z., Carell, T., et al. (2009) · The EMBO Journal · doi:10.1038/emboj.2008.281 · Cited by 284 · see citing works
Activation of Ubiquitin-Dependent DNA Damage Bypass Is Mediated by Replication Protein A
Davies, A. A., Huttner, D., Daigaku, Y., Chen, S., & Ulrich, H. D. (2008) · Molecular Cell · doi:10.1016/j.molcel.2007.12.016 · Cited by 281 · see citing works
Self-citation
PCNA ubiquitination and REV1 define temporally distinct mechanisms for controlling translesion synthesis in the avian cell line DT40
Edmunds, C. E., Simpson, L. J., & Sale, J. E. (2008) · Molecular Cell · doi:10.1016/j.molcel.2008.03.024 · Cited by 239 · see citing works
Ubiquitinated proliferating cell nuclear antigen activates translesion DNA polymerases η and REV1
Garg, P., & Burgers, P. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0505949102 · Cited by 236 · see citing works
The RAD6 DNA repair pathway in Saccharomyces cerevisiae: What does it do, and how does it do it?
Lawrence, C. W. (1994) · BioEssays · doi:10.1002/bies.950160408 · Cited by 188 · see citing works
The error-free component of the RAD6/RAD18 DNA damage tolerance pathway of budding yeast employs sister-strand recombination
Zhang, H., & Lawrence, C. W. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504586102 · Cited by 185 · see citing works
The critical mutagenic translesion DNA polymerase Rev1 is highly expressed during G 2 /M phase rather than S phase
Waters, L. S., & Walker, G. C. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0510167103 · Cited by 171 · see citing works
Ubiquitylation of yeast proliferating cell nuclear antigen and its implications for translesion DNA synthesis
Haracska, L., Unk, I., Prakash, L., & Prakash, S. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0510924103 · Cited by 136 · see citing works
Repair of Pyrimidine Dimer Damage Induced in Yeast by Ultraviolet Light
Resnick, M. A., & Setlow, J. K. (1972) · Journal of Bacteriology · doi:10.1128/jb.109.3.979-986.1972 · Cited by 122 · see citing works
A genomic view of eukaryotic DNA replication
MacAlpine, D. M., & Bell, S. P. (2005) · Chromosome Research · doi:10.1007/s10577-005-1508-1 · Cited by 118 · see citing works
Lesion bypass in yeast cells: Pol η participates in a multi‐DNA polymerase process
Bresson, A., & Fuchs, R. P. P. (2002) · The EMBO Journal · doi:10.1093/emboj/cdf363 · Cited by 112 · see citing works
Contributions of ubiquitin- and PCNA-binding domains to the activity of Polymerase in Saccharomyces cerevisiae
Parker, J. L., Bielen, A. B., Đikić, I., & Ulrich, H. D. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkl1102 · Cited by 104 · see citing works
Self-citation
The formation of pyrimidine dimers in the DNA of fungi and bacteria
Unrau, P., Wheatcroft, R., Cox, B. S., & Olive, T. (1973) · Biochimica et Biophysica Acta (BBA) - Nucleic Acids and Protein Synthesis · doi:10.1016/0005-2787(73)90065-8 · Cited by 86 · see citing works
New vectors for simplified construction of BrdU‐Incorporating strains of Saccharomyces cerevisiae
Viggiani, C. J., & Aparicio, O. M. (2006) · Yeast · doi:10.1002/yea.1406 · Cited by 82 · see citing works
RAD6-RAD18-RAD5-pathway-dependent tolerance to chronic low-dose ultraviolet light
Hishida, T., Kubota, Y., Carr, A. M., & Iwasaki, H. (2009) · Nature · doi:10.1038/nature07580 · Cited by 77 · see citing works
DNA synthesis in UV-irradiated yeast
di Caprio, L., & Cox, B. S. (1981) · Mutation Research · doi:10.1016/0027-5107(81)90139-1 · Cited by 71 · see citing works

Flagged first, then by citations

Sorted by citations

The DNA Damage Response: Making It Safe to Play with Knives
Ciccia, A., & Elledge, S. J. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.09.019 · Cited by 4,368 · see citing works
The control of DNA repair by the cell cycle
Hustedt, N., & Durocher, D. (2017) · Nature Cell Biology · doi:10.1038/ncb3452 · Cited by 738 · see citing works
Y-family DNA polymerases and their role in tolerance of cellular DNA damage
Sale, J. E., Lehmann, A. R., & Woodgate, R. (2012) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3289 · Cited by 665 · see citing works
DNA polymerases and cancer
Lange, S. S., Takata, K.-I., & Wood, R. D. (2011) · Nature Reviews Cancer · doi:10.1038/nrc2998 · Cited by 615 · see citing works
Chromatin replication and epigenome maintenance
Alabert, C., & Groth, A. (2012) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3288 · Cited by 586 · see citing works
The Mechanisms of UV Mutagenesis
Ikehata, H., & Ono, T. (2011) · Journal of Radiation Research · doi:10.1269/jrr.10175 · Cited by 515 · see citing works
The Ubiquitin–Proteasome System of Saccharomyces cerevisiae
Finley, D. J., Ulrich, H. D., Sommer, T., & Kaiser, P. (2012) · Genetics · doi:10.1534/genetics.112.140467 · Cited by 427 · see citing works
Self-citation
Regulation of PCNA–protein interactions for genome stability
Mailand, N., Gibbs‐Seymour, I., & Bekker‐Jensen, S. (2013) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3562 · Cited by 375 · see citing works
Chromosome Duplication in Saccharomyces cerevisiae
Bell, S. P., & Labib, K. P. M. (2016) · Genetics · doi:10.1534/genetics.115.186452 · Cited by 352 · see citing works
Forging Ahead through Darkness: PCNA, Still the Principal Conductor at the Replication Fork
Choe, K. N., & Moldovan, G.-L. (2017) · Molecular Cell · doi:10.1016/j.molcel.2016.12.020 · Cited by 325 · see citing works
Repriming of DNA synthesis at stalled replication forks by human PrimPol
Mouron, S. A., Rodríguez‐Acebes, S., Martínez-Jiménez, M. I., García-Gómez, S., Chocrón, S., Blanco, L., & Méndez, J. (2013) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2719 · Cited by 322 · see citing works
Epigenetic Instability due to Defective Replication of Structured DNA
Sarkies, P., Reams, C., Simpson, L. J., & Sale, J. E. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.11.009 · Cited by 302 · see citing works
Ubiquitin signalling in DNA replication and repair
Ulrich, H. D., & Walden, H. (2010) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2921 · Cited by 272 · see citing works
Self-citation
Emerging critical roles of Fe–S clusters in DNA replication and repair
Fuss, J. O., Tsai, C.-L., Ishida, J. P., & Tainer, J. A. (2015) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2015.01.018 · Cited by 253 · see citing works
Rescuing Stalled or Damaged Replication ForksPreprint
Yeeles, J. T. P., Poli, J., Marians, K. J., & Pasero, P. (2013) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a012815 · Cited by 253 · see citing works
Replication stress: getting back on track
Berti, M., & Vindigni, A. (2016) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.3163 · Cited by 249 · see citing works
DNA Fiber Analysis: Mind the Gap!
Quinet, A., Carvajal-Maldonado, D., Lemacon, D. S., & Vindigni, A. (2017) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/bs.mie.2017.03.019 · Cited by 240 · see citing works
DNA Repair Mechanisms and the Bypass of DNA Damage in Saccharomyces cerevisiae
Boiteux, S., & Jinks-Robertson, S. (2013) · Genetics · doi:10.1534/genetics.112.145219 · Cited by 227 · see citing works
The ubiquitous role of ubiquitin in the DNA damage response
Al-Hakim, A., Escribano‐Diaz, C., Landry, M.-C., O’Donnell, L., Panier, S., Szilard, R. K., & Durocher, D. (2010) · DNA repair · doi:10.1016/j.dnarep.2010.09.011 · Cited by 224 · see citing works
DNA damage tolerance: a double-edged sword guarding the genome.
Ghosal, G., & Chen, J. (2013) · PubMed · doi:10.3978/j.issn.2218-676x.2013.04.01 · Cited by 204 · see citing works
Temporally distinct post-replicative repair mechanisms fill PRIMPOL-dependent ssDNA gaps in human cells
Tirman, S., Quinet, A., Wood, M. D., Meroni, A., Cybulla, E., Jackson, J., Pegoraro, S., Simoneau, A., Zou, L., & Vindigni, A. (2021) · Molecular Cell · doi:10.1016/j.molcel.2021.09.013 · Cited by 193 · see citing works
A four-subunit DNA polymerase ζ complex containing Pol δ accessory subunits is essential for PCNA-mediated mutagenesis
Makarova, А. V., Stodola, J. L., & Burgers, P. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks948 · Cited by 186 · see citing works
RAD51- and MRE11-dependent reassembly of uncoupled CMG helicase complex at collapsed replication forks
Hashimoto, Y., Puddu, F., & Costanzo, V. (2011) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2177 · Cited by 161 · see citing works
Visualization of recombination-mediated damage bypass by template switching
Giannattasio, M., Zwicky, K., Follonier, C., Foiani, M., Lopes, M., & Branzei, D. (2014) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2888 · Cited by 147 · see citing works
Signaling Pathways of Replication Stress in Yeast
Pardo, B., Crabbé, L., & Pasero, P. (2016) · FEMS Yeast Research · doi:10.1093/femsyr/fow101 · Cited by 146 · see citing works
DNA damage tolerance by recombination: Molecular pathways and DNA structures
Branzei, D., & Szakál, B. (2016) · DNA repair · doi:10.1016/j.dnarep.2016.05.008 · Cited by 145 · see citing works
Targeting DNA repair pathway in cancer: Mechanisms and clinical application
Wang, M., Chen, S., & Ao, D. (2021) · MedComm · doi:10.1002/mco2.103 · Cited by 134 · see citing works
Translesion DNA Synthesis and Mutagenesis in ProkaryotesPreprint
Fuchs, R. P., & Fujii, S. (2013) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a012682 · Cited by 128 · see citing works
The trans cell cycle effects of PARP inhibitors underlie their selectivity toward BRCA1/2-deficient cellsPreprint
Simoneau, A., Xiong, R., & Zou, L. (2021) · Genes & Development · doi:10.1101/gad.348479.121 · Cited by 125 · see citing works
Premature Cdk1/Cdc5/Mus81 pathway activation induces aberrant replication and deleterious crossover
Szakál, B., & Branzei, D. (2013) · The EMBO Journal · doi:10.1038/emboj.2013.67 · Cited by 122 · see citing works
The Initial Response of a Eukaryotic Replisome to DNA Damage
Taylor, M. R. G., & Yeeles, J. T. P. (2018) · Molecular Cell · doi:10.1016/j.molcel.2018.04.022 · Cited by 121 · see citing works
Nucleases Acting at Stalled Forks: How to Reboot the Replication Program with a Few Shortcuts
Pasero, P., & Vindigni, A. (2017) · Annual Review of Genetics · doi:10.1146/annurev-genet-120116-024745 · Cited by 120 · see citing works
UV stalled replication forks restart by re-priming in human fibroblasts
Elvers, I., Johansson, F., Groth, P., Erixon, K., & Helleday, T. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr420 · Cited by 120 · see citing works
DNA damage bypass operates in the S and G2 phases of the cell cycle and exhibits differential mutagenicity
Diamant, N., Hendel, A., Vered, I., Carell, T., Reißner, T., de Wind, N., Geacinov, N., & Livneh, Z. (2012) · Nucleic Acids Research · doi:10.1093/nar/gkr596 · Cited by 109 · see citing works
To skip or not to skip: choosing repriming to tolerate DNA damage
Quinet, A., Tirman, S., Cybulla, E., Meroni, A., & Vindigni, A. (2021) · Molecular Cell · doi:10.1016/j.molcel.2021.01.012 · Cited by 109 · see citing works
Regulation of Rad6/Rad18 Activity During DNA Damage Tolerance
Hedglin, M., & Benkovic, S. J. (2015) · Annual Review of Biophysics · doi:10.1146/annurev-biophys-060414-033841 · Cited by 106 · see citing works
The ADP-ribosyltransferase PARP10/ARTD10 Interacts with Proliferating Cell Nuclear Antigen (PCNA) and Is Required for DNA Damage Tolerance
Nicolae, C. M., Aho, E. R., Vlahos, A. H. S., Choe, K. N., De, S., Karras, G. I., & Moldovan, G. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.556340 · Cited by 104 · see citing works
Mechanisms of DNA Damage Tolerance: Post-Translational Regulation of PCNA
Leung, W., Baxley, R. M., Moldovan, G., & Bielinsky, A. (2018) · Genes · doi:10.3390/genes10010010 · Cited by 96 · see citing works
Mutator phenotypes due to DNA replication infidelity
Arana, M. E., & Kunkel, T. A. (2010) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2010.10.003 · Cited by 96 · see citing works
High-Resolution Genome-Wide Analysis of Irradiated (UV and γ-Rays) Diploid Yeast Cells Reveals a High Frequency of Genomic Loss of Heterozygosity (LOH) Events
Charles, J. S., Hazkani‐Covo, E., Yin, Y. A., Andersen, S. L., Dietrich, F. S., Greenwell, P. W., Malc, E. P., Mieczkowski, P. A., & Petes, T. D. (2012) · Genetics · doi:10.1534/genetics.111.137927 · Cited by 90 · see citing works
Noncanonical Role of the 9-1-1 Clamp in the Error-Free DNA Damage Tolerance Pathway
Karras, G. I., Fumasoni, M., Sienski, G., Vanoli, F., Branzei, D., & Jentsch, S. (2012) · Molecular Cell · doi:10.1016/j.molcel.2012.11.016 · Cited by 89 · see citing works
Rad51 replication fork recruitment is required for DNA damage tolerance
González‐Prieto, R., Muñoz-Cabello, A. M., Cabello-Lobato, M. J., & Prado, F. (2013) · The EMBO Journal · doi:10.1038/emboj.2013.73 · Cited by 89 · see citing works
Ubiquitin family modifications and template switching
Branzei, D. (2011) · FEBS Letters · doi:10.1016/j.febslet.2011.04.053 · Cited by 83 · see citing works
Functions of Ubiquitin and SUMO in DNA Replication and Replication Stress
García‐Rodríguez, N., Wong, R. P. C., & Ulrich, H. D. (2016) · Frontiers in Genetics · doi:10.3389/fgene.2016.00087 · Cited by 82 · see citing works
Self-citation
Reconstitution of translesion synthesis reveals a mechanism of eukaryotic DNA replication restart
Guilliam, T. A., & Yeeles, J. T. P. (2020) · Nature Structural & Molecular Biology · doi:10.1038/s41594-020-0418-4 · Cited by 81 · see citing works
Building up and breaking down: mechanisms controlling recombination during replication
Branzei, D., & Szakál, B. (2017) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.1080/10409238.2017.1304355 · Cited by 81 · see citing works
Mismatch Repair–Independent Increase in Spontaneous Mutagenesis in Yeast Lacking Non-Essential Subunits of DNA Polymerase ε
Aksenova, A. Y., Volkov, K. V., Maceluch, J., Pursell, Z. F., Rogozin, I. B., Kunkel, T. A., Pavlov, Y. I., & Johansson, E. (2010) · PLoS Genetics · doi:10.1371/journal.pgen.1001209 · Cited by 78 · see citing works
Roles of sequential ubiquitination of PCNA in DNA‐damage tolerance
Zhang, W., Qin, Z., Zhang, X., & Xiao, W. (2011) · FEBS Letters · doi:10.1016/j.febslet.2011.04.044 · Cited by 78 · see citing works
NMR Structure and Dynamics of the C-Terminal Domain from Human Rev1 and Its Complex with Rev1 Interacting Region of DNA Polymerase η
Pozhidaeva, A., Pustovalova, Y., D’Souza, S., Bezsonova, I., Walker, G. C., & Korzhnev, D. M. (2012) · Biochemistry · doi:10.1021/bi300566z · Cited by 77 · see citing works
Translesion synthesis mechanisms depend on the nature of DNA damage in UV-irradiated human cells
Quinet, A., Martins, D. J., Vessoni, A. T., Biard, D., Sarasin, A., Stary, A., & Menck, C. F. M. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw280 · Cited by 76 · see citing works
The ubiquitin ligase RFWD3 is required for translesion DNA synthesis
Gallina, I., Hendriks, I. A., Hoffmann, S., Larsen, N. B., Johansen, J., Colding-Christensen, C. S., Schubert, L. A., Sellés‐Baiget, S., Fábián, Z., Kühbacher, U., et al. (2020) · Molecular Cell · doi:10.1016/j.molcel.2020.11.029 · Cited by 76 · see citing works
DNA damage tolerance
Branzei, D., & Psakhye, I. (2016) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2016.03.015 · Cited by 75 · see citing works
The Emerging Role of Cohesin in the DNA Damage Response
Litwin, I., Pilarczyk, E., & Wysocki, R. (2018) · Genes · doi:10.3390/genes9120581 · Cited by 74 · see citing works
Roles of trans-lesion synthesis (TLS) DNA polymerases in tumorigenesis and cancer therapy
Anand, J. R., Chiou, L. F., Sciandra, C. A., Zhang, X., Hong, J., Wu, D., Zhou, P., & Vaziri, C. (2023) · NAR Cancer · doi:10.1093/narcan/zcad005 · Cited by 73 · see citing works
Timing and spacing of ubiquitin‐dependent DNA damage bypass
Ulrich, H. D. (2011) · FEBS Letters · doi:10.1016/j.febslet.2011.05.028 · Cited by 73 · see citing works
Self-citation
Processing of DNA Polymerase-Blocking Lesions during Genome Replication Is Spatially and Temporally Segregated from Replication Forks
Wong, R. P. C., García‐Rodríguez, N., Zilio, N., Hanulová, M., & Ulrich, H. D. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.09.015 · Cited by 72 · see citing works
Self-citation
Srs2 mediates PCNA‐SUMO‐dependent inhibition of DNA repair synthesis
Burkovics, P., Šebesta, M., Sisáková, A., Plault, N., Szukacsov, V., Robert, T., Pintér, L., Marini, V., Kolesár, P., Haracska, L., et al. (2013) · The EMBO Journal · doi:10.1038/emboj.2013.9 · Cited by 71 · see citing works
DNA replication and cancer: From dysfunctional replication origin activities to therapeutic opportunities
Boyer, A.-S., Walter, D., & Sørensen, C. S. (2016) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2016.01.001 · Cited by 71 · see citing works
Gap-filling and bypass at the replication fork are both active mechanisms for tolerance of low-dose ultraviolet-induced DNA damage in the human genome
Quinet, A., Vessoni, A. T., Rocha, C. R. R., Gottifredi, V., Biard, D., Sarasin, A., Menck, C. F. M., & Stary, A. (2014) · DNA Repair · doi:10.1016/j.dnarep.2013.12.005 · Cited by 70 · see citing works
Regulation of the DNA damage response by ubiquitin conjugation
Brinkmann, K., Schell, M. J., Hoppe, T., & Kashkar, H. (2015) · Frontiers in Genetics · doi:10.3389/fgene.2015.00098 · Cited by 70 · see citing works
APC/CCdh1-dependent proteolysis of USP1 regulates the response to UV-mediated DNA damage
Cotto-Rios, X. M., Jones, M. V., Busino, L., Pagano, M., & Huang, T. T. (2011) · The Journal of Cell Biology · doi:10.1083/jcb.201101062 · Cited by 68 · see citing works
Mechanisms of PARP1 inhibitor resistance and their implications for cancer treatment
Jackson, L. M., & Moldovan, G. (2022) · NAR Cancer · doi:10.1093/narcan/zcac042 · Cited by 66 · see citing works
Integrating DNA damage repair with the cell cycle
Murray, J. M., & Carr, A. M. (2018) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2018.03.006 · Cited by 66 · see citing works
DNA replication stress: from molecular mechanisms to human disease
Muñoz, S., & Méndez, J. (2016) · Chromosoma · doi:10.1007/s00412-016-0573-x · Cited by 65 · see citing works
PrimPol—Prime Time to Reprime
Guilliam, T. A., & Doherty, A. J. (2017) · Genes · doi:10.3390/genes8010020 · Cited by 65 · see citing works
DNA repair factor RAD18 and DNA polymerase Polκ confer tolerance of oncogenic DNA replication stress
Yang, Y., Gao, Y., Mutter-Rottmayer, L., Zlatanou, A., Durando, M., Ding, W., Wyatt, D. W., Ramsden, D. A., Tanoue, Y., Tateishi, S., et al. (2017) · The Journal of Cell Biology · doi:10.1083/jcb.201702006 · Cited by 65 · see citing works
Molecular and physiological consequences of faulty eukaryotic ribonucleotide excision repair
Kellner, V., & Luke, B. (2019) · The EMBO Journal · doi:10.15252/embj.2019102309 · Cited by 65 · see citing works
Strand invasion by HLTF as a mechanism for template switch in fork rescue
Burkovics, P., Šebesta, M., Balogh, D., Haracska, L., & Krejčí, L. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt1040 · Cited by 62 · see citing works
Error-free DNA-damage tolerance in Saccharomyces cerevisiae
Xu, X., Blackwell, S., Lin, A., Li, F., Qin, Z., & Xiao, W. (2015) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2015.02.001 · Cited by 61 · see citing works
DNA bending facilitates the error‐free DNA damage tolerance pathway and upholds genome integrity
González‐Huici, V., Szakál, B., Urulangodi, M., Psakhye, I., Castellucci, F., Menolfi, D., Rajakumara, E., Fumasoni, M., Bermejo, R., Jentsch, S., et al. (2014) · The EMBO Journal · doi:10.1002/embj.201387425 · Cited by 61 · see citing works
Identification of novel DNA-damage tolerance genes reveals regulation of translesion DNA synthesis by nucleophosmin
Ziv, O., Zeisel, A., Mirlas-Neisberg, N., Swain, U., Nevo, R., Ben-Chetrit, N., Martelli, M. P., Rossi, R., Schiesser, S., Canman, C. E., et al. (2014) · Nature Communications · doi:10.1038/ncomms6437 · Cited by 59 · see citing works
Rad5 Plays a Major Role in the Cellular Response to DNA Damage during Chromosome Replication
Ortiz-Bazán, M. Á., Gallo-Fernández, M., Saugar, I., Jiménez-Martín, A., Vázquez, M. V., & Tercero, J. A. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.09.005 · Cited by 59 · see citing works
Targeting the Translesion Synthesis Pathway for the Development of Anti-Cancer Chemotherapeutics
Korzhnev, D. M., & Hadden, M. K. (2016) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.6b00596 · Cited by 58 · see citing works
PRIMPOL ready, set, reprime!
Tirman, S., Cybulla, E., Quinet, A., Meroni, A., & Vindigni, A. (2020) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.1080/10409238.2020.1841089 · Cited by 57 · see citing works
Genetic instability in budding and fission yeast—sources and mechanisms
Skoneczna, A., Kaniak, A., & Skoneczny, M. (2015) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuv028 · Cited by 57 · see citing works
Structure of monoubiquitinated PCNA
Zhang, Z., Zhang, S., Lin, S. H. S., Wang, X., Wu, L., Lee, E. Y. C., & Lee, M. (2012) · Cell Cycle · doi:10.4161/cc.20595 · Cited by 56 · see citing works
PPL2 Translesion Polymerase Is Essential for the Completion of Chromosomal DNA Replication in the African Trypanosome
Rudd, S. G., Glover, L., Jóźwiakowski, S. K., Horn, D., & Doherty, A. J. (2013) · Molecular Cell · doi:10.1016/j.molcel.2013.10.034 · Cited by 55 · see citing works
Mechanisms of Post-Replication DNA Repair
Gao, Y., Mutter‐Rottmayer, E., Zlatanou, A., Vaziri, C., & Yang, Y. (2017) · Genes · doi:10.3390/genes8020064 · Cited by 55 · see citing works
Rad5 Recruits Error-Prone DNA Polymerases for Mutagenic Repair of ssDNA Gaps on Undamaged Templates
Gallo, D., Kim, T. P., Szakál, B., Saayman, X., Narula, A., Park, Y., Branzei, D., Zhang, Z., & Brown, G. W. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.01.001 · Cited by 54 · see citing works
A role for chromatin remodellers in replication of damaged DNA
Niimi, A., Chambers, A. L., Downs, J. A., & Lehmann, A. R. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks453 · Cited by 54 · see citing works
Strategic role of the ubiquitin-dependent segregase p97 (VCP or Cdc48) in DNA replication
Ramadan, K., Halder, S., Wiseman, K., & Vaz, B. (2016) · Chromosoma · doi:10.1007/s00412-016-0587-4 · Cited by 54 · see citing works
Monoubiquitylation of histone H2B contributes to the bypass of DNA damage during and after DNA replication
Hung, S.-H., Wong, R. P. C., Ulrich, H. D., & Kao, C.-F. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1612633114 · Cited by 54 · see citing works
Self-citation
Working on Genomic Stability: From the S-Phase to Mitosis
Ovejero, S., Bueno, A., & Sacristán, M. P. (2020) · Genes · doi:10.3390/genes11020225 · Cited by 54 · see citing works
Repriming DNA synthesis: an intrinsic restart pathway that maintains efficient genome replication
Bainbridge, L. J., Teague, R., & Doherty, A. J. (2021) · Nucleic Acids Research · doi:10.1093/nar/gkab176 · Cited by 54 · see citing works
Reversal of PCNA Ubiquitylation by Ubp10 in Saccharomyces cerevisiae
Gallego-Sánchez, A., Andrés, S., Conde, F., San-Segundo, P. A., & Bueno, A. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1002826 · Cited by 52 · see citing works
Ubiquitin and SUMO in DNA repair at a glance
Ulrich, H. D. (2012) · Journal of Cell Science · doi:10.1242/jcs.091801 · Cited by 52 · see citing works
Self-citation
Ubiquitination of PCNA and Its Essential Role in Eukaryotic Translesion Synthesis
Chen, J., Bozza, W. P., & Zhuang, Z. (2011) · Cell Biochemistry and Biophysics · doi:10.1007/s12013-011-9187-3 · Cited by 52 · see citing works
Diverse roles of RAD18 and Y-family DNA polymerases in tumorigenesis
Yang, Y., Gao, Y., Zlatanou, A., Tateishi, S., Yurchenko, V., Rogozin, I. B., & Vaziri, C. (2018) · Cell Cycle · doi:10.1080/15384101.2018.1456296 · Cited by 51 · see citing works
Mechanism of DNA damage tolerance
Bi, X. (2015) · World Journal of Biological Chemistry · doi:10.4331/wjbc.v6.i3.48 · Cited by 51 · see citing works
NMR Mapping of PCNA Interaction with Translesion Synthesis DNA Polymerase Rev1 Mediated by Rev1-BRCT Domain
Pustovalova, Y. E., Maciejewski, M. W., & Korzhnev, D. M. (2013) · Journal of Molecular Biology · doi:10.1016/j.jmb.2013.05.029 · Cited by 50 · see citing works
Eukaryotic Translesion DNA Synthesis on the Leading and Lagging Strands: Unique Detours around the Same Obstacle
Hedglin, M., & Benkovic, S. J. (2017) · Chemical Reviews · doi:10.1021/acs.chemrev.7b00046 · Cited by 50 · see citing works
Spatial separation between replisome‐ and template‐induced replication stress signaling
García‐Rodríguez, N., Morawska, M., Wong, R. P. C., Daigaku, Y., & Ulrich, H. D. (2018) · The EMBO Journal · doi:10.15252/embj.201798369 · Cited by 50 · see citing works
Self-citation
PIP degron proteins, substrates of CRL4Cdt2, and not PIP boxes, interfere with DNA polymerase η and κ focus formation on UV damage
Tsanov, N., Kermi, C., Coulombe, P., van der Laan, S., Hodroj, D., & Maiorano, D. (2014) · Nucleic Acids Research · doi:10.1093/nar/gkt1400 · Cited by 48 · see citing works
Causes and consequences of ribonucleotide incorporation into nuclear DNA
Dalgaard, J. Z. (2012) · Trends in Genetics · doi:10.1016/j.tig.2012.07.008 · Cited by 48 · see citing works
Rev1 promotes replication through UV lesions in conjunction with DNA polymerases η, ι, and κ but not DNA polymerase ζPreprint
Yoon, J.-H., Park, J., Conde, J., Wakamiya, M., Prakash, L., & Prakash, S. (2015) · Genes & Development · doi:10.1101/gad.272229.115 · Cited by 47 · see citing works
Modulation of mutagenesis in eukaryotes by DNA replication fork dynamics and quality of nucleotide pools
Waisertreiger, I. S.-R., Liston, V. G., Menezes, M. R., Kim, H., Lobachev, K. S., Stepchenkova, E. I., Tahirov, T. H., Rogozin, I. B., & Pavlov, Y. I. (2012) · Environmental and Molecular Mutagenesis · doi:10.1002/em.21735 · Cited by 46 · see citing works
Genomic assay reveals tolerance of DNA damage by both translesion DNA synthesis and homology-dependent repair in mammalian cells
Izhar, L., Ziv, O., Cohen, I. S., Geacintov, N. E., & Livneh, Z. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1216894110 · Cited by 46 · see citing works
The Rev1 translesion synthesis polymerase has multiple distinct DNA binding modes
de Groote, F. H., Jansen, J. G., Masuda, Y., Shah, D. M., Kamiya, K., de Wind, N., & Siegal, G. (2011) · DNA repair · doi:10.1016/j.dnarep.2011.04.033 · Cited by 45 · see citing works
Roles of PCNA ubiquitination and TLS polymerases κ and η in the bypass of methyl methanesulfonate-induced DNA damage
Wit, N., Buoninfante, O. A., van den Berk, P. C. M., Jansen, J. G., Hogenbirk, M. A., de Wind, N., & Jacobs, H. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku1301 · Cited by 45 · see citing works
New Functions of Ctf18-RFC in Preserving Genome Stability outside Its Role in Sister Chromatid Cohesion
Gellon, L., Razidlo, D. F., Gleeson, O., Verra, L., Schulz, D., Lahue, R. S., & Freudenreich, C. H. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1001298 · Cited by 44 · see citing works

Ubiquitin-dependent DNA damage bypass is separable from genome replication. Nature. 2010; 465:951–5. [PubMed: 20453836
Daigaku, Y., Davies, A. A., & Ulrich, H. D. (2016)
Self-citation
Timing and spacing of ubiquitin‐dependent DNA damage bypass
Ulrich, H. D. (2011) · FEBS Letters · doi:10.1016/j.febslet.2011.05.028 · Cited by 73 · see citing works
Self-citation
Activation of Ubiquitin-Dependent DNA Damage Bypass Is Mediated by Replication Protein A
Davies, A. A., Huttner, D., Daigaku, Y., Chen, S., & Ulrich, H. D. (2008) · Molecular Cell · doi:10.1016/j.molcel.2007.12.016 · Cited by 281 · see citing works
Self-citation
PCNA Modifications for Regulation of Post-Replication Repair Pathways
Lee, K., & Myung, K. (2008) · Molecules and Cells · doi:10.1016/s1016-8478(23)13956-2 · Cited by 141 · see citing works
Post-replication repair: ubiquitin throws the switch
Swaminathan, S. (2004) · Nature Cell Biology · doi:10.1038/ncb0704-578 · Cited by 2 · see citing works

Authors: Daigaku, Y., Davies, A. A., & Ulrich, H. D.
Affiliations: Cancer Research UK (GB)
Corresponding author: Ulrich, Helle D.
ORCID: Daigaku, Yasukazu
Ulrich, Helle D.
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2010-05-09
Volume: 465
Issue: 7300
Pages: 951-955
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature09097
PMC: PMC2888004
OpenAlex: W2080574942
Cited by: 259
References: 30
Citations by year: 2026: 8 · 2025: 8 · 2024: 9 · 2023: 4 · 2022: 6 · 2021: 15 · 2020: 15 · 2019: 13 · 2018: 21 · 2017: 16 · 2016: 26 · 2015: 15 · 2014: 18 · 2013: 22 · 2012: 27
FWCI: 11.08
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Funders: Cancer Research UK (A7123, A10152)
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
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Keywords: DNA damage bypass, translesion synthesis, error-free bypass, genome replication, S phase, Saccharomyces cerevisiae, replication fork, DNA polymerase, monoubiquitylation, polyubiquitination, template switching, sister chromatids, cell cycle synchronization
MeSH terms: Cell Cycle, Chromatin, DNA Damage, DNA Replication, Saccharomyces cerevisiae, Time Factors, Ultraviolet Rays, Genome, Proliferating Cell Nuclear Antigen, Ubiquitin, Saccharomyces cerevisiae Proteins, Ubiquitin-Conjugating Enzymes

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Ubiquitin-dependent DNA damage bypass is separable from genome replication

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Self-check

Cites

Cited by

Related

Record

About these checks