Maintaining genome stability at the replication fork

Branzei, Dana; Foiani, Marco

doi:10.1038/nrm2852

Cited by 786DNA Repair MechanismsTelomeres, Telomerase, and SenescenceDNA and Nucleic Acid Chemistry

Maintaining genome stability at the replication fork

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Branzei, Dana, Foiani, Marco·2010·Nature Reviews Molecular Cell Biology

DOI 10.1038/nrm2852

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Abstract

Aberrant DNA replication is a major source of the mutations and chromosome rearrangements that are associated with pathological disorders. When replication is compromised, DNA becomes more prone to breakage. Secondary structures, highly transcribed DNA sequences and damaged DNA stall replication forks, which then require checkpoint factors and specialized enzymatic activities for their stabilization and subsequent advance. These mechanisms ensure that the local DNA damage response, which enables replication fork progression and DNA repair in S phase, is coupled with cell cycle transitions. The mechanisms that operate in eukaryotic cells to promote replication fork integrity and coordinate replication with other aspects of chromosome maintenance are becoming clear.

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Crossref · 10.1038/nrm2852

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H2AX is phosphorylated both in G1 and S phases by ATR in response to UV irradiation.
“H2AX is phosphorylated both in G1 and S phases by ATR in response to UV irradiation [26;32–38].”
From ATR- and ATM-Mediated DNA Damage Response Is Dependent on Excision Repair Assembly during G1 but Not in S Phase of Cell Cycle (2016) · cites this paper as [35]
ATR is predominantly responsible for the DNA damage response upon UVR exposure.
“Previous studies support that ATR is predominantly responsible for DDR upon UVR exposure”
From ATR- and ATM-Mediated DNA Damage Response Is Dependent on Excision Repair Assembly during G1 but Not in S Phase of Cell Cycle (2016) · cites this paper as [35]
DNA damage response pathways are conserved surveillance mechanisms that coordinate DNA repair, cell cycle progression, transcription, apoptosis, and senescence.
“To maintain genome stability, the DDR pathways are conserved surveillance mechanisms coordinating DNA repair, cell cycle progression, transcription, apoptosis, and senescence [19, 39–41].”
From Functional interplay between ATM/ATR-mediated DNA damage response and DNA repair pathways in oxidative stress (2014) · cites this paper as [41]
RPA-coated 5'-primed single-stranded DNA is the determinant DNA structure for ATR activation in response to stalled replication forks or DNA damage.
“5′-primed ssDNA coated with RPA (RPA-ssDNA) is the determinant DNA structure for ATR activation in response to stalled DNA replication forks or DNA damage [41, 94–96].”
From Functional interplay between ATM/ATR-mediated DNA damage response and DNA repair pathways in oxidative stress (2014) · cites this paper as [41]

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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 activation regulates mutagenic translesion synthesisPreprint
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The FANCM Ortholog Fml1 Promotes Recombination at Stalled Replication Forks and Limits Crossing Over during DNA Double-Strand Break Repair
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Large-scale expansions of Friedreich’s ataxia GAA repeats in yeast
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Cycles of chromosome instability are associated with a fragile site and are increased by defects in DNA replication and checkpoint controls in yeastPreprint
Admire, A. A., Shanks, L., Danzl, N. M., Wang, M., Weier, U., Stevens, W. R., Hunt, E. G., & Weinert, T. A. (2005) · Genes & Development · doi:10.1101/gad.1392506 · Cited by 141 · see citing works
Telomere length regulation: coupling DNA end processing to feedback regulation of telomerase
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Stability, chromatin association and functional activity of mammalian pre‐replication complex proteins during the cell cycle
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Replisome stalling and stabilization at CGG repeats that are responsible for chromosomal fragility
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Nearby inverted repeats fuse to generate acentric and dicentric palindromic chromosomes by a replication template exchange mechanismPreprint
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DNA replication as a target of the DNA damage checkpoint
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Tof1p Regulates DNA Damage Responses During S Phase in Saccharomyces cerevisiae
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DDB1 Targets Chk1 to the Cul4 E3 Ligase Complex in Normal Cycling Cells and in Cells Experiencing Replication Stress
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A DNA replication-arrest site RTS1 regulates imprinting by determining the direction of replication at mat1 in S. pombePreprint
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The 9-1-1 Checkpoint Clamp Physically Interacts with Polζ and Is Partially Required for Spontaneous Polζ-dependent Mutagenesis in Saccharomyces cerevisiae
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Genome-Organizing Factors Top2 and Hmo1 Prevent Chromosome Fragility at Sites of S phase Transcription
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BRCA1 participates in DNA decatenation
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Replicon Dynamics, Dormant Origin Firing, and Terminal Fork Integrity after Double-Strand Break Formation
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Characterization of a High Mobility Group 1/2 Homolog in Yeast
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FANCL Replaces BRCA1 as the Likely Ubiquitin Ligase Responsible for FANCD2 Monoubiquitination
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The Saccharomyces cerevisiae Esc2 and Smc5-6 Proteins Promote Sister Chromatid Junction-mediated Intra-S Repair
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Interplay between the Smc5/6 complex and the Mph1 helicase in recombinational repair
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Involvement of a chromatin remodeling complex in damage tolerance during DNA replication
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Fanconi Anemia Proteins Are Required To Prevent Accumulation of Replication-Associated DNA Double-Strand Breaks
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Requirement of RAD52 Group Genes for Postreplication Repair of UV-Damaged DNA in Saccharomyces cerevisiae
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FANCM regulates DNA chain elongation and is stabilized by S‐phase checkpoint signalling
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DNA Repeat Rearrangements Mediated by DnaK-Dependent Replication Fork Repair
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DNA Knotting Caused by Head-on Collision of Transcription and Replication
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Enigmatic Variations
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The Amino-Terminal TPR Domain of Dia2 Tethers SCFDia2 to the Replisome Progression Complex
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Fusion of nearby inverted repeats by a replication-based mechanism leads to formation of dicentric and acentric chromosomes that cause genome instability in budding yeastPreprint
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Replication origins in the eucaryotic chromosome
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The involvement of Srs2 in post-replication repair and homologous recombination in fission yeast
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GETTING STARTED: Regulating the Initiation of DNA Replication in Yeast
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Top3 Processes Recombination Intermediates and Modulates Checkpoint Activity after DNA Damage
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Flexibility and governance in eukaryotic DNA replication
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Novel Control of S Phase of the Cell Cycle by Ubiquitin-conjugating Enzyme H7
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Schizosaccharomyces pombe Rtf2 mediates site-specific replication termination by inhibiting replication restart
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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
Targeting hypoxia in cancer therapy
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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
DNA breaks and chromosome pulverization from errors in mitosis
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DNA Replication Stress as a Hallmark of Cancer
Macheret, M., & Halazonetis, T. D. (2015) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev-pathol-012414-040424 · Cited by 816 · see citing works
53BP1 nuclear bodies form around DNA lesions generated by mitotic transmission of chromosomes under replication stress
Lukas, C., Savic, V., Bekker‐Jensen, S., Doil, C., Neumann, B., Pedersen, R. S., Grøfte, M., Chan, K., Hickson, I. D., Bártek, J., et al. (2011) · Nature Cell Biology · doi:10.1038/ncb2201 · Cited by 658 · see citing works
Replication stress is a potent driver of functional decline in ageing haematopoietic stem cells
Flach, J., Bakker, S. T., Mohrin, M., Conroy, P. C., Pietras, E. M., Reynaud, D., Alvarez, S., Diolaiti, M. E., Ugarte, F., Forsberg, E. C., et al. (2014) · Nature · doi:10.1038/nature13619 · Cited by 650 · 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
Rad51 protects nascent DNA from Mre11-dependent degradation and promotes continuous DNA synthesis
Hashimoto, Y., Chaudhuri, A. R., Lopes, M., & Costanzo, V. (2010) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1927 · Cited by 537 · see citing works
Double-Strand Breaks in Heterochromatin Move Outside of a Dynamic HP1a Domain to Complete Recombinational Repair
Chiolo, I., Minoda, A., Colmenares, S. U., Polyzos, A. A., Costes, S. V., & Karpen, G. H. (2011) · Cell · doi:10.1016/j.cell.2011.02.012 · Cited by 516 · see citing works
Heterochromatin: Guardian of the Genome
Janssen, A., Colmenares, S. U., & Karpen, G. H. (2018) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100617-062653 · Cited by 500 · see citing works
Replication fork reversal in eukaryotes: from dead end to dynamic response
Neelsen, K. J., & Lopes, M. (2015) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3935 · Cited by 494 · see citing works
p53 induces formation of NEAT1 lncRNA-containing paraspeckles that modulate replication stress response and chemosensitivity
Adriaens, C., Standaert, L., Barra, J., Latil, M., Verfaillie, A., Kalev, P., Boeckx, B., Wijnhoven, P. W. G., Radaelli, E., Vermi, W., et al. (2016) · Nature Medicine · doi:10.1038/nm.4135 · Cited by 468 · see citing works
Nucleotide-resolution DNA double-strand break mapping by next-generation sequencing
Crosetto, N., Mitra, A., Silva, M. J., Bienko, M., Dojer, N., Wang, Q., Karaca, E., Chiarle, R., Skrzypczak, M., Ginalski, K., et al. (2013) · Nature Methods · doi:10.1038/nmeth.2408 · Cited by 465 · see citing works
Break-Induced Replication Repair of Damaged Forks Induces Genomic Duplications in Human Cells
Costantino, L., Sotiriou, S. K., Rantala, J., Magin, S., Mladenov, E., Helleday, T., Haber, J. E., Iliakis, G. E., Kallioniemi, O., & Halazonetis, T. D. (2013) · Science · doi:10.1126/science.1243211 · Cited by 451 · see citing works
Cell-type-specific replication initiation programs set fragility of the FRA3B fragile site
Letessier, A., Millot, G. A., Koundrioukoff, S., Lachagès, A.-M., Vogt, N., Hansen, R. S., Malfoy, B., Brison, O., & Debatisse, M. (2011) · Nature · doi:10.1038/nature09745 · Cited by 414 · see citing works
ATR phosphorylates SMARCAL1 to prevent replication fork collapsePreprint
Couch, F. B., Bansbach, C. E., Driscoll, R., Luzwick, J. W., Glick, G. G., Betous, R., Carroll, C. M., Jung, S. Y., Qin, J., Cimprich, K. A., et al. (2013) · Genes & Development · doi:10.1101/gad.214080.113 · Cited by 409 · see citing works
The Replication Checkpoint Prevents Two Types of Fork Collapse without Regulating Replisome Stability
Dungrawala, H., Rose, K. L., Bhat, K. P., Mohni, K. N., Glick, G. G., Couch, F. B., & Cortez, D. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.07.030 · Cited by 376 · see citing works
Translocation-Capture Sequencing Reveals the Extent and Nature of Chromosomal Rearrangements in B Lymphocytes
Klein, I. A., Resch, W., Janković, M., Oliveira, T. Y., Yamane, A., Nakahashi, H., Virgilio, M. D., Bothmer, A., Nussenzweig, A., Robbiani, D. F., et al. (2011) · Cell · doi:10.1016/j.cell.2011.07.048 · Cited by 353 · 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
Replication stress induces 53BP1-containing OPT domains in G1 cells
Harrigan, J. A., Belotserkovskaya, R., Coates, J., Dimitrova, D. S., Polo, S. E., Bradshaw, C. R., Fraser, P., & Jackson, S. P. (2011) · The Journal of Cell Biology · doi:10.1083/jcb.201011083 · Cited by 336 · see citing works
EZH2 promotes degradation of stalled replication forks by recruiting MUS81 through histone H3 trimethylation
Rondinelli, B., Gogola, E., Yücel, H., Duarte, A. A., van de Ven, M., van der Sluijs, R., Konstantinopoulos, P. A., Jonkers, J., Ceccaldi, R., Rottenberg, S., et al. (2017) · Nature Cell Biology · doi:10.1038/ncb3626 · Cited by 332 · see citing works
DNA Methylation, Its Mediators and Genome Integrity
Meng, H., Cao, Y., Qin, J., Song, X., Zhang, Q., Shi, Y. S., & Cao, L. (2015) · International Journal of Biological Sciences · doi:10.7150/ijbs.11218 · Cited by 327 · 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
ATR signalling: more than meeting at the fork
Nam, E. A., & Cortez, D. (2011) · Biochemical Journal · doi:10.1042/bj20102162 · Cited by 316 · see citing works
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Authors: Branzei, D., & Foiani, M.
Affiliations: IFOM (IT)
University of Milan (IT)
ORCID: Branzei, Dana
Foiani, Marco
Venue: Nature Reviews Molecular Cell Biology
Publisher: Springer Science and Business Media LLC
Published: 2010-03
Volume: 11
Issue: 3
Pages: 208-219
ISSN: 1471-0072 (ISSN-L)
1471-0080
DOI: 10.1038/nrm2852
OpenAlex: W2063979868
Cited by: 786
References: 155
Citations by year: 2026: 16 · 2025: 15 · 2024: 27 · 2023: 22 · 2022: 30 · 2021: 36 · 2020: 51 · 2019: 48 · 2018: 38 · 2017: 56 · 2016: 70 · 2015: 67 · 2014: 73 · 2013: 82 · 2012: 73
FWCI: 6.60
Type: journal article
Language: en
Open access: green
zenodo.org
Licence: other-oa
www.springer.com/tdm (tdm)
Locations: Nature Reviews Molecular Cell Biology (publishedVersion)
PubMed (publishedVersion)
Universitätsbibliographie, Universität Duisburg-Essen (submittedVersion)
Zenodo (CERN European Organization for Nuclear Research) (submittedVersion, other-oa)
Funders: Associazione Italiana per la Ricerca sul Cancro
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
Health Sciences › Medicine › Physiology › Telomeres, Telomerase, and Senescence
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA and Nucleic Acid Chemistry
Keywords: genome stability, DNA replication, replication fork, replication fork stalling, DNA secondary structure, DNA damage response, DNA repair, S phase, chromosome maintenance, genetic mutations, chromosomal rearrangements
MeSH terms: Animals, DNA, DNA Damage, DNA Repair, DNA Replication, Humans, Models, Biological, Nucleic Acid Conformation, Replication Origin, Genomic Instability

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Maintaining genome stability at the replication fork

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