DNA replication as a target of the DNA damage checkpoint

Zegerman, Philip; Diffley, John F.X.

doi:10.1016/j.dnarep.2009.04.023

Cited by 128DNA Repair MechanismsBacterial Genetics and BiotechnologyCancer-related Molecular Pathways

DNA replication as a target of the DNA damage checkpoint

Zegerman, Philip, Diffley, John F.X.·2009·DNA Repair

DOI 10.1016/j.dnarep.2009.04.023

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Abstract

Faithful inheritance of the genome from mother to daughter cell requires that it is replicated accurately, in its entirety, exactly once. DNA replication not only has to have high fidelity, but also has to cope with exogenous and endogenous agents that damage DNA during the life cycle of a cell. The DNA damage checkpoint, which monitors and responds to defects in the genome, is critical for the completion of replication. The focus of this review is how DNA replication is regulated by the checkpoint response in the presence of DNA damage and fork stalling agents.

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KL cells respond to gemcitabine plus CHK1 inhibition.
“and to combined treatment with gemcitabine - a deoxycytidine analog that inhibits DNA synthesis and further depletes dNTP pools by targeting ribonucleotide reductase159- and CHK1 inhibitors, that abrogate the CHK1-mediated checkpoint response to replicative stress160, 161.”
From Co-occurring genomic alterations in non-small-cell lung cancer biology and therapy (2019) · cites this paper as [161]

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Exo1 Processes Stalled Replication Forks and Counteracts Fork Reversal in Checkpoint-Defective Cells
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Molecular anatomy and regulation of a stable replisome at a paused eukaryotic DNA replication forkPreprint
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MCM2–7 Complexes Bind Chromatin in a Distributed Pattern Surrounding the Origin Recognition Complex inXenopus Egg Extracts
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Cdc7p–Dbf4p kinase binds to chromatin during S phase and is regulated by both the APC and the RAD53 checkpoint pathway
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E2Fs up-regulate expression of genes involved in DNA replication, DNA repair and mitosis
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Gross Chromosomal Rearrangements and Elevated Recombination at an Inducible Site-Specific Replication Fork Barrier
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DNA-replication checkpoint control at the Drosophila midblastula transition
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Xenopus Cdc45‐dependent loading of DNA polymerase α onto chromatin under the control of S‐phase cdk
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Chk1‐deficient tumour cells are viable but exhibit multiple checkpoint and survival defects
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mcm5/cdc46-bob1 bypasses the requirement for the S phase activator Cdc7p
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Differential assembly of Cdc45p and DNA polymerases at early and late origins of DNA replication
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Human Claspin Is Required for Replication Checkpoint Control
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The structural determinants of checkpoint activation
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Mrc1 channels the DNA replication arrest signal to checkpoint kinase Cds1
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Chk1 regulates the density of active replication origins during the vertebrate S phase
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Sld3, which interacts with Cdc45 (Sld4), functions for chromosomal DNA replication in Saccharomyces cerevisiae
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Genomic mapping of single-stranded DNA in hydroxyurea-challenged yeasts identifies origins of replication
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A ribonucleotide reductase gene is a transcriptional target of p53 and p73
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Identification of Mcm2 Phosphorylation Sites by S-phase-regulating Kinases
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Autoradiography of HeLa cell DNA
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Identification of a Preinitiation Step in DNA Replication That Is Independent of Origin Recognition Complex and cdc6, but Dependent on cdk2
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Mcm10 Regulates the Stability and Chromatin Association of DNA Polymerase-α
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Mammalian Cdc7–Dbf4 protein kinase complex is essential for initiation of DNA replication
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Nuclear and cytoplasmic mitotic cycles continue in Drosophila embryos in which DNA synthesis is inhibited with aphidicolin.
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ORC and the intra-S-phase checkpoint: a threshold regulates Rad53p activation in S phasePreprint
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Mrc1 and DNA Polymerase ɛ Function Together in Linking DNA Replication and the S Phase Checkpoint
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Human Cdc25 A inactivation in response to S phase inhibition and its role in preventing premature mitosis
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Claspin, a Chk1-Regulatory Protein, Monitors DNA Replication on Chromatin Independently of RPA, ATR, and Rad17
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DNA synthesis at individual replication forks requires the essential initiation factor Cdc45p
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Paradoxes of eukaryotic DNA replication: MCM proteins and the random completion problem
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The N-Terminal Noncatalytic Region of Xenopus RecQ4 Is Required for Chromatin Binding of DNA Polymerase α in the Initiation of DNA Replication
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STRUCTURE, FUNCTION, AND REPLICATION OF SACCHAROMYCES CEREVISIAE TELOMERES
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Phosphorylation of MCM4 by Cdc7 Kinase Facilitates Its Interaction with Cdc45 on the Chromatin
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Mrc1 Is Required for Normal Progression of Replication Forks throughout Chromatin in S. cerevisiae
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Start Sites of Bidirectional DNA Synthesis at the Human Lamin B2 Origin
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Dpb11 Controls the Association between DNA Polymerases α and ɛ and the Autonomously Replicating Sequence Region of Budding Yeast
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Xenopus Mcm10 Binds to Origins of DNA Replication after Mcm2-7 and Stimulates Origin Binding of Cdc45
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Replication fork barriers: pausing for a break or stalling for time?
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Changes in association of the Xenopus origin recognition complex with chromatin on licensing of replication origins
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CLB5-Dependent Activation of Late Replication Origins in S. cerevisiae
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Reconstitution of an ATM-Dependent Checkpoint that Inhibits Chromosomal DNA Replication following DNA Damage
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ORC‐ and Cdc6‐dependent complexes at active and inactive chromosomal replication origins in Saccharomyces cerevisiae.
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Separate roles for the DNA damage checkpoint protein kinases in stabilizing DNA replication forksPreprint
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Checkpoint-mediated control of replisome–fork association and signalling in response to replication pausing
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Checkpoint-dependent phosphorylation of Exo1 modulates the DNA damage response
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Cell Cycle Regulation of the Replication Licensing System: Involvement of a Cdk-dependent Inhibitor
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Human and Xenopus cDNAs encoding budding yeast Cdc7‐related kinases: in vitro phosphorylation of MCM subunits by a putative human homologue of Cdc7
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Specification of Regions of DNA Replication Initiation during Embryogenesis in the 65-Kilobase DNApolα-dE2F Locus of Drosophila melanogaster
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A Novel Human p53 Isoform Is an Essential Element of the ATR-Intra-S Phase Checkpoint
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Characterization of nuclease-dependent functions of Exo1p in Saccharomyces cerevisiae
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Xenopus Cut5 is essential for a CDK‐dependent process in the initiation of DNA replication
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Regulation of replication timing in fission yeast
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The role of Cdc6 in ensuring complete genome licensing and S phase checkpoint activation
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Stability, chromatin association and functional activity of mammalian pre‐replication complex proteins during the cell cycle
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The nuclear envelope prevents reinitiation of replication by regulating the binding of MCM3 to chromatin in Xenopus egg extracts
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Purification of Hsk1, a Minichromosome Maintenance Protein Kinase from Fission Yeast
Brown, G. W., & Kelly, T. J. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.34.22083 · Cited by 116 · see citing works
Claspin Promotes Normal Replication Fork Rates in Human Cells
Petermann, E., Helleday, T., & Caldecott, K. W. (2008) · Molecular Biology of the Cell · doi:10.1091/mbc.e07-10-1035 · Cited by 116 · see citing works
Human Minichromosome Maintenance Proteins and Human Origin Recognition Complex 2 Protein on Chromatin
Ritzi, M., Baack, M., Musahl, C., Romanowski, P., Laskey, R. A., & Knippers, R. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.38.24543 · Cited by 113 · see citing works
A Fission Yeast Gene, him1 + /dfp1 + , Encoding a Regulatory Subunit for Hsk1 Kinase, Plays Essential Roles in S-Phase Initiation as Well as in S-Phase Checkpoint Control and Recovery from DNA Damage
Takeda, T., Ogino, K., Matsui, E., Cho, M. K., Kumagai, H., Miyake, T., Arai, K., & Masai, H. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.8.5535 · Cited by 112 · see citing works
Characterization of mec1 Kinase-Deficient Mutants and of New Hypomorphic mec1 Alleles Impairing Subsets of the DNA Damage Response Pathway
Paciotti, V., Clerici, M., Scotti, M., Lucchini, G., & Longhese, M. P. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.12.3913-3925.2001 · Cited by 112 · see citing works
A CDK‐catalysed regulatory phosphorylation for formation of the DNA replication complex Sld2–Dpb11
Tak, Y., Tanaka, Y., Endo, S., Kamimura, Y., & Araki, H. (2006) · The EMBO Journal · doi:10.1038/sj.emboj.7601075 · Cited by 108 · see citing works
Dif1 Is a DNA-Damage-Regulated Facilitator of Nuclear Import for Ribonucleotide Reductase
Lee, Y. D., Wang, J., Stubbe, J., & Elledge, S. J. (2008) · Molecular Cell · doi:10.1016/j.molcel.2008.08.018 · Cited by 107 · see citing works
swi1 - and swi3 -dependent and independent replication fork arrest at the ribosomal DNA of Schizosaccharomyces pombe
Krings, G., & Bastia, D. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0406037101 · Cited by 106 · see citing works
Tyrosine Phosphorylation of Cdc2 Is Required for the Replication Checkpoint in Schizosaccharomyces pombe
Rhind, N., & Russell, P. R. (1998) · Molecular and Cellular Biology · doi:10.1128/mcb.18.7.3782 · Cited by 106 · see citing works
The Chinese Hamster Dihydrofolate Reductase Origin Consists of Multiple Potential Nascent-Strand Start Sites
Dijkwel, P. A., & Hamlin, J. L. (1995) · Molecular and Cellular Biology · doi:10.1128/mcb.15.6.3023 · Cited by 103 · see citing works
NORF5/HUG1 Is a Component of the MEC1-Mediated Checkpoint Response to DNA Damage and Replication Arrest in Saccharomyces cerevisiae
Basrai, M. A., Velculescu, V. E., Kinzler, K. W., & Hieter, P. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.10.7041 · Cited by 100 · see citing works

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Control of cell cycle transcription during G1 and S phases
Bertoli, C., Skotheim, J. M., & de Bruin, R. A. M. (2013) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3629 · Cited by 1,509 · see citing works
Co-occurring genomic alterations in non-small-cell lung cancer biology and therapy
Skoulidis, F., & Heymach, J. V. (2019) · Nature Reviews Cancer · doi:10.1038/s41568-019-0179-8 · Cited by 1,019 · see citing works
Maintaining genome stability at the replication fork
Branzei, D., & Foiani, M. (2010) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2852 · Cited by 786 · see citing works
Eukaryotic DNA replication origins: many choices for appropriate answers
Méchali, M. (2010) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2976 · Cited by 441 · see citing works
An overview of Cdk1-controlled targets and processes
Enserink, J. M., & Kolodner, R. D. (2010) · Cell Division · doi:10.1186/1747-1028-5-11 · Cited by 409 · 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
Break-Induced Replication Is Highly Inaccurate
Deem, A. K., Keszthelyi, A., Blackgrove, T., Vayl, A., Coffey, B. M., Mathur, R., Chabes, A., & Malkova, A. (2011) · PLoS Biology · doi:10.1371/journal.pbio.1000594 · Cited by 297 · see citing works
dNTP pools determine fork progression and origin usage under replication stress
Poli, J., Tsaponina, O., Crabbé, L., Keszthelyi, A., Pantesco, V., Chabes, A., Lengronne, A., & Pasero, P. (2012) · The EMBO Journal · doi:10.1038/emboj.2011.470 · Cited by 292 · see citing works
The impact of replication stress on replication dynamics and DNA damage in vertebrate cells
Técher, H., Koundrioukoff, S., Nicolas, A. G., & Debatisse, M. (2017) · Nature Reviews Genetics · doi:10.1038/nrg.2017.46 · Cited by 271 · see citing works
Eukaryotic DNA replication control: Lock and load, then fire
Remus, D., & Diffley, J. F. X. (2009) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2009.08.002 · Cited by 245 · see citing works
Self-citation
Involvement of Matrin 3 and SFPQ/NONO in the DNA damage response
Salton, M., Lerenthal, Y., Wang, S., Chen, D. J., & Shiloh, Y. (2010) · Cell Cycle · doi:10.4161/cc.9.8.11298 · Cited by 209 · see citing works
A Ctf4 trimer couples the CMG helicase to DNA polymerase α in the eukaryotic replisome
Simon, A. C., Zhou, J. C., Perera, R. L., van Deursen, F. J., Evrin, C., Ivanova, M. E., Kilkenny, M. L., Renault, L. L. R., Kjaer, S., Matak‐Vinković, D., et al. (2014) · Nature · doi:10.1038/nature13234 · Cited by 206 · see citing works
Extensive DNA Damage-Induced Sumoylation Contributes to Replication and Repair and Acts in Addition to the Mec1 Checkpoint
Cremona, C. A., Sarangi, P., Yang, Y., Hang, L. E., Rahman, S., & Zhao, X. (2012) · Molecular Cell · doi:10.1016/j.molcel.2011.11.028 · Cited by 197 · see citing works
Repeat instability during DNA repair: Insights from model systems
Usdin, K., House, N. C. M., & Freudenreich, C. H. (2015) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.3109/10409238.2014.999192 · Cited by 168 · see citing works
Mec1 Is One of Multiple Kinases that Prime the Mcm2-7 Helicase for Phosphorylation by Cdc7
Randell, J. C. W., Fan, A., Chan, C., Francis, L. I., Heller, R. C., Galani, K., & Bell, S. P. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.10.017 · Cited by 169 · see citing works
Highly mutagenic and severely imbalanced dNTP pools can escape detection by the S-phase checkpoint
Kumar, D., Viberg, J., Nilsson, A. K., & Chabes, A. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq128 · Cited by 145 · see citing works
Controlling DNA replication origins in response to DNA damage – inhibit globally, activate locally
Yekezare, M., Gómez‐González, B., & Diffley, J. F. X. (2013) · Journal of Cell Science · doi:10.1242/jcs.096701 · Cited by 134 · see citing works
Self-citation
Analysis of replication profiles reveals key role of RFC-Ctf18 in yeast replication stress response
Crabbé, L., Thomas, A., Pantesco, V., Vos, J. D., Pasero, P., & Lengronne, A. (2010) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1932 · Cited by 136 · see citing works
Post-licensing Specification of Eukaryotic Replication Origins by Facilitated Mcm2-7 Sliding along DNA
Gros, J., Kumar, C., Lynch, G., Yadav, T., Whitehouse, I., & Remus, D. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.10.022 · Cited by 134 · see citing works
Eukaryotic DNA damage checkpoint activation in response to double-strand breaks
Finn, K., Lowndes, N. F., & Grenon, M. (2012) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-011-0875-3 · Cited by 127 · see citing works
Preclinical Development of the Novel Chk1 Inhibitor SCH900776 in Combination with DNA-Damaging Agents and Antimetabolites
Montano, R. E., Chung, I., Garner, K. M., Parry, D., & Eastman, A. R. (2011) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-11-0406 · Cited by 125 · see citing works
Cell cycle-dependent regulation of the nuclease activity of Mus81–Eme1/Mms4
Gallo-Fernández, M., Saugar, I., Ortiz-Bazán, M. Á., Vázquez, M. V., & Tercero, J. A. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks599 · Cited by 119 · see citing works
CDK targeting of NBS1 promotes DNA‐end resection, replication restart and homologous recombination
Falck, J., Forment, J. V., Coates, J., Mistrík, M., Lukas, J., Bártek, J., & Jackson, S. P. (2012) · EMBO Reports · doi:10.1038/embor.2012.58 · Cited by 108 · see citing works
TheArabidopsis thalianaCheckpoint Kinase WEE1 Protects against Premature Vascular Differentiation during Replication Stress
Cools, T., Iantcheva, A., Weimer, A. K. K., Boens, S., Takahashi, N., Maes, S., den Daele, H. V., Isterdael, G. V., Schnittger, A., & Veylder, L. D. (2011) · The Plant Cell · doi:10.1105/tpc.110.082768 · Cited by 91 · see citing works
Polyphosphate is involved in cell cycle progression and genomic stability in Saccharomyces cerevisiae
Bru, S., Martínez‐Láinez, J. M., Hernández‐Ortega, S., Quandt, E., Torres‐Torronteras, J., Martí, R., Canadell, D., Ariño, J., Sharma, S., Jiménez, J., et al. (2016) · Molecular Microbiology · doi:10.1111/mmi.13396 · Cited by 83 · see citing works
The DNA damage checkpoint response to replication stress: A Game of Forks
Jossen, R., & Bermejo, R. (2013) · Frontiers in Genetics · doi:10.3389/fgene.2013.00026 · Cited by 81 · see citing works
Ixr1 Is Required for the Expression of the Ribonucleotide Reductase Rnr1 and Maintenance of dNTP Pools
Tsaponina, O., Barsoum, E., Åström, S. U., & Chabes, A. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1002061 · Cited by 81 · see citing works
Xbp1 Directs Global Repression of Budding Yeast Transcription during the Transition to Quiescence and Is Important for the Longevity and Reversibility of the Quiescent State
Miles, S., Li, L., Davison, J., & Breeden, L. L. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003854 · Cited by 81 · see citing works
Sensitization of human cancer cells to gemcitabine by the Chk1 inhibitor MK-8776: cell cycle perturbation and impact of administration schedule in vitro and in vivo
Montano, R. E., Thompson, R. H., Chung, I., Hou, H. G., Khan, N. I., & Eastman, A. R. (2013) · BMC Cancer · doi:10.1186/1471-2407-13-604 · Cited by 77 · see citing works
The interface between transcription and mechanisms maintaining genome integrity
Svejstrup, J. Q. (2010) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2010.02.001 · Cited by 73 · see citing works
The fork and the kinase: A DNA replication tale from a CHK1 perspective
Besteiro, M. A. G., & Gottifredi, V. (2014) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2014.10.003 · Cited by 71 · see citing works
A Common Telomeric Gene Silencing Assay Is Affected by Nucleotide Metabolism
Rossmann, M. P., Luo, W., Tsaponina, O., Chabes, A., & Stillman, B. (2011) · Molecular Cell · doi:10.1016/j.molcel.2011.03.007 · Cited by 67 · see citing works
Neurogenesis requires TopBP1 to prevent catastrophic replicative DNA damage in early progenitors
Lee, Y., Katyal, S., Downing, S. M., Zhao, J., Russell, H. R., & McKinnon, P. J. (2012) · Nature Neuroscience · doi:10.1038/nn.3097 · Cited by 59 · see citing works
Replication Checkpoint: Tuning and Coordination of Replication Forks in S Phase
Hustedt, N., Gasser, S. M., & Shimada, K. (2013) · Genes · doi:10.3390/genes4030388 · Cited by 57 · see citing works
Spatholobus suberectus inhibits cancer cell growth by inducing apoptosis and arresting cell cycle at G2/M checkpoint
Wang, Z., Wang, D., Loo, T. Y., Cheng, Y., Chen, L., Shen, J.-G., Yang, D.-P., Chow, L. W., Guan, X., & Chen, J. (2010) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2010.11.004 · Cited by 56 · see citing works
Chaperoning HMGA2 Protein Protects Stalled Replication Forks in Stem and Cancer Cells
Yu, H., Lim, H. H., Tjokro, N. O., Sathiyanathan, P., Natarajan, S., Chew, T. W., Klonisch, T. C., Goodman, S. D., Surana, U., & Dröge, P. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.01.014 · Cited by 55 · see citing works
Effects of Selective Checkpoint Kinase 1 Inhibition on Cytarabine Cytotoxicity in Acute Myelogenous Leukemia Cells In Vitro
Schenk, E. L., Koh, B. D., Flatten, K. S., Peterson, K. L., Parry, D., Hess, A. D., Smith, B. D., Karp, J. E., Karnitz, L. M., & Kaufmann, S. H. (2012) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-12-0961 · Cited by 55 · see citing works
Modulation of cell cycle control during oocyte‐to‐embryo transitions
Hörmanseder, E., Tischer, T., & Mayer, T. U. (2013) · The EMBO Journal · doi:10.1038/emboj.2013.164 · Cited by 54 · see citing works
Cdc45 Protein-Single-stranded DNA Interaction Is Important for Stalling the Helicase during Replication Stress
Bruck, I., & Kaplan, D. L. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.440941 · Cited by 53 · see citing works
Dephosphorylation of γH2A by Glc7/Protein Phosphatase 1 Promotes Recovery from Inhibition of DNA Replication
Bazzi, M., Mantiero, D., Trovesi, C., Lucchini, G., & Longhese, M. P. (2009) · Molecular and Cellular Biology · doi:10.1128/mcb.01000-09 · Cited by 53 · see citing works
The combination of CHK1 inhibitor with G-CSF overrides cytarabine resistance in human acute myeloid leukemia
Tullio, A. D., Rouault‐Pierre, K., Abarrategi, A., Mian, S., Grey, W. E., Gribben, J. G., Stewart, A., Blackwood, E. R., & Bonnet, D. A. (2017) · Nature Communications · doi:10.1038/s41467-017-01834-4 · Cited by 50 · see citing works
On the Interplay of the DNA Replication Program and the Intra-S Phase Checkpoint Pathway
Ciardo, D., Goldar, A., & Marheineke, K. (2019) · Genes · doi:10.3390/genes10020094 · Cited by 47 · see citing works
Small-molecule screen reveals synergy of cell cycle checkpoint kinase inhibitors with DNA-damaging chemotherapies in medulloblastoma
Endersby, R., Whitehouse, J. P., Pribnow, A. K., Kuchibhotla, M., Hii, H. L., Carline, B., Gande, S., Stripay, J. L., Ancliffe, M., Howlett, M., et al. (2021) · Science Translational Medicine · doi:10.1126/scitranslmed.aba7401 · Cited by 47 · see citing works
Elevated dNTP levels suppress hyper-recombination in Saccharomyces cerevisiae S-phase checkpoint mutants
Fasullo, M., Tsaponina, O., Sun, M., & Chabes, A. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp1064 · Cited by 44 · see citing works
Helicase Subunit Cdc45 Targets the Checkpoint Kinase Rad53 to Both Replication Initiation and Elongation Complexes after Fork Stalling
Can, G., Kauerhof, A. C., Macak, D., & Zegerman, P. (2018) · Molecular Cell · doi:10.1016/j.molcel.2018.11.025 · Cited by 45 · see citing works
Self-citation
Mathematical Modelling of DNA Replication Reveals a Trade-off between Coherence of Origin Activation and Robustness against Rereplication
Brümmer, A., Salazar, C., Zinzalla, V., Alberghina, L., & Höfer, T. (2010) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000783 · Cited by 41 · see citing works
Replication Fork Collapse and Genome Instability in a Deoxycytidylate Deaminase Mutant
Sánchez, A., Sharma, S., Rozenzhak, S., Roguev, A., Krogan, N. J., Chabes, A., & Russell, P. R. (2012) · Molecular and Cellular Biology · doi:10.1128/mcb.01062-12 · Cited by 40 · see citing works
Structural Analysis of Replication Protein A Recruitment of the DNA Damage Response Protein SMARCAL1
Feldkamp, M. D., Mason, A. C., Eichman, B. F., & Chazin, W. (2014) · Biochemistry · doi:10.1021/bi500252w · Cited by 38 · see citing works
The evolutionary plasticity of chromosome metabolism allows adaptation to constitutive DNA replication stress
Fumasoni, M., & Murray, A. W. (2020) · eLife · doi:10.7554/elife.51963 · Cited by 36 · see citing works
Arabidopsis thaliana RNase H2 Deficiency Counteracts the Needs for the WEE1 Checkpoint Kinase but Triggers Genome Instability
Kalhorzadeh, P., Hu, Z., Cools, T., Amiard, S., Willing, E., Winne, N. D., Gevaert, K., Jaeger, G. D., Schneeberger, K., White, C. I., et al. (2014) · The Plant Cell · doi:10.1105/tpc.114.128108 · Cited by 34 · see citing works
H2B Mono-ubiquitylation Facilitates Fork Stalling and Recovery during Replication Stress by Coordinating Rad53 Activation and Chromatin Assembly
Lin, C., Wu, M., Gay, S., Marjavaara, L., Lai, M. S., Hsiao, W.-C., Hung, S.-H., Tseng, H.-Y., Wright, D. E., Wang, C., et al. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004667 · Cited by 34 · see citing works
Dpb11/TopBP1 plays distinct roles in DNA replication, checkpoint response and homologous recombination
Germann, S. M., Oestergaard, V. H., Haas, C., Salis, P., Motegi, A., & Lisby, M. (2010) · DNA repair · doi:10.1016/j.dnarep.2010.11.001 · Cited by 35 · see citing works
Concerted activities of Mcm4, Sld3, and Dbf4 in control of origin activation and DNA replication fork progressionPreprint
Sheu, Y.-J., Kinney, J. B., & Stillman, B. (2016) · Genome Research · doi:10.1101/gr.195248.115 · Cited by 35 · see citing works
DNA replication: Failures and inverted fusions
Carr, A. M., Paek, A. L., & Weinert, T. A. (2011) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2011.10.008 · Cited by 34 · see citing works
The CRL2LRR-1 ubiquitin ligase regulates cell cycle progression during C. elegans development
Merlet, J., Burger, J., Tavernier, N., Richaudeau, B., Gomes, J., & Pintard, L. (2010) · Development · doi:10.1242/dev.054866 · Cited by 34 · see citing works
Temporal regulation of the Mus81-Mms4 endonuclease ensures cell survival under conditions of DNA damage
Saugar, I., Vázquez, M. V., Gallo-Fernández, M., Ortiz-Bazán, M. Á., Segurado, M., Calzada, A., & Tercero, J. A. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt645 · Cited by 32 · see citing works
Stability of blocked replication forks in vivo
Mettrick, K. A., & Grainge, I. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv1079 · Cited by 31 · see citing works
Epigenetic Control of Expression Homeostasis during Replication Is Stabilized by the Replication Checkpoint
Voichek, Y., Mittelman, K., Gordon, Y., Bar‐Ziv, R., Smit, D. L., Shenhav, R., & Barkai, N. (2018) · Molecular Cell · doi:10.1016/j.molcel.2018.05.015 · Cited by 30 · see citing works
Replication origins: determinants or consequences of nuclear organization?
Marks, A. B., Smith, O. K., & Aladjem, M. I. (2016) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2015.11.008 · Cited by 26 · see citing works
Molecular Basis of the Essential S Phase Function of the Rad53 Checkpoint Kinase
Hoch, N. C., Chen, E. S.-W., Buckland, R. J., Wang, S., Fazio, A., Hammet, A., Pellicioli, A., Chabes, A., Tsai, M., & Heierhorst, J. (2013) · Molecular and Cellular Biology · doi:10.1128/mcb.00474-13 · Cited by 25 · see citing works
The Role of the Transcriptional Response to DNA Replication Stress
Herlihy, A. E., & de Bruin, R. A. M. (2017) · Genes · doi:10.3390/genes8030092 · Cited by 23 · see citing works
The CDK-PLK1 axis targets the DNA damage checkpoint sensor protein RAD9 to promote cell proliferation and tolerance to genotoxic stress
Wakida, T., Ikura, M., Kuriya, K., Ito, S., Shiroiwa, Y., Habu, T., Kawamoto, T., Okumura, K., Ikura, T., & Furuya, K. (2017) · eLife · doi:10.7554/elife.29953 · Cited by 25 · see citing works
The DNA replication checkpoint prevents PCNA/RFC depletion to protect forks from HLTF-induced collapse in human cells
Bertolin, A. P., Canal, B., Yekezare, M., Early, A. E., Zeng, J., Instrell, R., Howell, M., & Diffley, J. F. X. (2025) · Molecular Cell · doi:10.1016/j.molcel.2025.06.002 · Cited by 27 · see citing works
Self-citation
Regulation of cell cycle and stress responses under nitrosative stress in Schizosaccharomyces pombe
Majumdar, U., Biswas, P., Sarkar, T. S., Maiti, D., & Ghosh, S. (2012) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2012.03.026 · Cited by 24 · see citing works
Replication stress in hematopoietic stem cells in mouse and man
Flach, J., & Milyavsky, M. (2017) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2017.10.001 · Cited by 23 · see citing works
Diallyl disulfide selectively causes checkpoint kinase-1 mediated G2/M arrest in human MGC803 gastric cancer cell line
Ling, H. Y., Li-Feng, L., He, J., XIAO, G.-H., Jiang, H., & Su, Q. (2014) · Oncology Reports · doi:10.3892/or.2014.3417 · Cited by 23 · see citing works
Chk1 inhibition significantly potentiates activity of nucleoside analogs in TP53-mutated B-lymphoid cells
Zemanová, J., Hylse, O., Čolláková, J., Veselý, P., Oltová, A., Borský, M., Zápražná, K., Kasparkova, M., Janovská, P., Verner, J., et al. (2016) · Oncotarget · doi:10.18632/oncotarget.11388 · Cited by 23 · see citing works
Targeting Chk1 in the replicative stress response
Dai, Y., & Grant, S. (2010) · Cell Cycle · doi:10.4161/cc.9.6.11155 · Cited by 22 · see citing works
Checkpoint-dependent RNR induction promotes fork restart after replicative stress
Morafraile, E. C., Diffley, J. F. X., Tercero, J. A., & Segurado, M. (2015) · Scientific Reports · doi:10.1038/srep07886 · Cited by 21 · see citing works
Self-citation
The Role of Dbf4-Dependent Protein Kinase in DNA Polymerase ζ-Dependent Mutagenesis in Saccharomyces cerevisiae
Brandão, L., Ferguson, R. L., Santoro, I. Μ., Jinks-Robertson, S., & Sclafani, R. A. (2014) · Genetics · doi:10.1534/genetics.114.165308 · Cited by 21 · see citing works
Long-range heterochromatin association is mediated by silencing and double-strand DNA break repair proteins
Kirkland, J. G., & Kamakaka, R. T. (2013) · The Journal of Cell Biology · doi:10.1083/jcb.201211105 · Cited by 20 · see citing works
‘AND’ logic gates at work: Crystal structure of Rad53 bound to Dbf4 and Cdc7
Almawi, A. W., Matthews, L. A., Larasati, Myrox, P., Boulton, S., Lai, C. C.-L., Moraes, T. F., Melacini, G., Ghirlando, R., Duncker, B. P., et al. (2016) · Scientific Reports · doi:10.1038/srep34237 · Cited by 19 · see citing works
Structural studies of RFCCtf18 reveal a novel chromatin recruitment role for Dcc1
Wade, B. O., Liu, H. W., Samora, C. P., Uhlmann, F., & Singleton, M. R. (2017) · EMBO Reports · doi:10.15252/embr.201642825 · Cited by 18 · see citing works
Insights into the Initiation of Eukaryotic DNA Replication
Bruck, I., Pérez-Arnaiz, P., Colbert, M. K., & Kaplan, D. L. (2015) · Nucleus · doi:10.1080/19491034.2015.1115938 · Cited by 18 · see citing works
The checkpoint transcriptional response: Make sure to turn it off once you are satisfied
Smolka, M. B., de Oliveira, F. M. B., Harris, M. R., & de Bruin, R. A. M. (2012) · Cell Cycle · doi:10.4161/cc.21197 · Cited by 14 · see citing works
Replicating Damaged DNA in EukaryotesPreprint
Chatterjee, N., & Siede, W. (2013) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a019836 · Cited by 17 · see citing works
Transgene Expression of Drosophila melanogaster Nucleoside Kinase Reverses Mitochondrial Thymidine Kinase 2 Deficiency
Krishnan, S., Zhou, X., Paredes, J. A., Kuiper, R., Curbo, S., & Karlsson, A. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.437152 · Cited by 15 · see citing works
Nuclear DNA replication and repair in parasites of the genusLeishmania: Exploiting differences to develop innovative therapeutic approaches
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Authors: Zegerman, P., & Diffley, J. F. X.
Affiliations: Cancer Research UK (GB)
Corresponding author: Diffley, John F.X.
ORCID: Zegerman, Philip
Diffley, John F.X.
Venue: DNA Repair
Publisher: Elsevier BV
Published: 2009-09-02
Volume: 8
Issue: 9
Pages: 1077-1088
ISSN: 1568-7856 (ISSN-L)
1568-7864
DOI: 10.1016/j.dnarep.2009.04.023
OpenAlex: W2056492477
Cited by: 128
References: 240
Citations by year: 2025: 2 · 2024: 4 · 2023: 1 · 2022: 1 · 2021: 2 · 2020: 3 · 2019: 6 · 2018: 5 · 2017: 7 · 2016: 9 · 2015: 7 · 2014: 11 · 2013: 18 · 2012: 17
FWCI: 6.99
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: DNA repair (publishedVersion)
PubMed (publishedVersion)
Funders: Cancer Research UK
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Health Sciences › Medicine › Oncology › Cancer-related Molecular Pathways
Keywords: DNA replication, DNA damage checkpoint, replication fork stalling, replication fork restart, DNA damage response, replication regulation
MeSH terms: Replisomes, Animals, Cell Cycle, DNA Damage, DNA-Directed DNA Polymerase, DNA Replication, Eukaryotic Cells, Humans, Multienzyme Complexes, Replication Origin

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DNA replication as a target of the DNA damage checkpoint

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