Multiple mechanisms control chromosome integrity after replication fork uncoupling and restart at irreparable UV lesions
Open accessAbstract
DNA replication forks pause in front of lesions on the template, eventually leading to cytotoxic chromosomal rearrangements. The in vivo structure of damaged eukaryotic replication intermediates has been so far elusive. Combining electron microscopy (EM) and two-dimensional (2D) gel electrophoresis, we found that UV-irradiated S. cerevisiae cells uncouple leading and lagging strand replication at irreparable UV lesions, thus generating long ssDNA regions on one side of the fork. Furthermore, small ssDNA gaps accumulate along replicated duplexes, likely resulting from repriming events downstream of the lesions on both leading and lagging strands. Translesion synthesis and homologous recombination counteract gap accumulation, without affecting fork progression. The DNA damage checkpoint contributes to gap repair and maintains a replication-competent fork structure. We propose that the coordinated action of checkpoint, recombination, and translesion synthesis-mediated processes at the fork and behind the fork preserves the integrity of replicating chromosomes by allowing efficient replication restart and filling the resulting ssDNA gaps.
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Such ssDNA gaps have been detected by electron microscopy on replicating UV-damaged DNA and are likely responsible for the rapid and sensitive response in UV-irradiated S phase cells.
“Such structures have been detected by electron microscopy on replicating UV-damaged DNA and are likely responsible for the rapid and sensitive response observed in UV-irradiated S phase cells [51].”
From Mind the gap: keeping UV lesions in check (2011) · cites this paper as [51]
When replication forks collide with UV lesions in S phase, re-priming downstream leaves ssDNA gaps behind the fork.
“Since UV lesions are bulky and block the progression of replicative DNA polymerases, when the replication forks collide with UV-induced lesions during the S phase of the cell cycle re-priming events may take place downstream of the lesions, leaving ssDNA gaps behind the fork.”
From Mind the gap: keeping UV lesions in check (2011) · cites this paper as [51]
In S phase cells, replicative polymerases blocked by bulky UV lesions re-initiate DNA synthesis downstream of the lesions, leaving a single-stranded DNA tract.
“In S phase cells, on the other hand, the replicative polymerases, blocked by bulky UV lesions, re-initiate DNA synthesis downstream of the lesions, leaving behind a ssDNA tract.”
From Mind the gap: keeping UV lesions in check (2011) · cites this paper as [51]
Blocked polymerases can leave the lesion and PCNA behind and re-initiate downstream via re-priming, generating numerous ssDNA gaps behind forks that likely cause strong Mec1 activation during S phase in UV-irradiated cells.
“Blocked polymerase can leave the lesion and PCNA behind and re-initiate downstream of the lesion via a re-priming mechanism, generating numerous ssDNA gaps behind the forks, which are likely responsible for the strong activation of Mec1 during S phase in UV-irradiated cells [51,82–85].”
From Mind the gap: keeping UV lesions in check (2011) · cites this paper as [51]
UV irradiation in G1 of cycling rad14Δ cells causes strong arrest at the beginning of S phase, accompanied by accumulation of replication-dependent ssDNA regions.
“Such results are also consistent with the finding that UV irradiation in G1 of a cycling rad14Δ strain results in a strong arrest at the beginning of S phase [58], accompanied by the accumulation of replication-dependent ssDNA regions [51].”
From Mind the gap: keeping UV lesions in check (2011) · cites this paper as [51]
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“Such structures have been detected by elecron microscopy on replicating UV-damaged DNA and are likely esponsible for the rapid and sensitive response observed in UVrradiated S phase cells [51].”
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- Authors
- Lopes, M., Foiani, M., & Sogo, J. M.
- Affiliations
- ETH Zurich (CH)
- University of Milan (IT)
- Corresponding author
- Lopes, Massimo
- Sogo, José M.
- Venue
- Molecular Cell
- Publisher
- Elsevier BV
- Published
- 2006-01
- Volume
- 21
- Issue
- 1
- Pages
- 15-27
- ISSN
- 1097-2765 (ISSN-L)
- OpenAlex
- W2085866527
- Cited by
- 563
- References
- 45
- Citations by year
- 2026: 5 · 2025: 11 · 2024: 18 · 2023: 12 · 2022: 20 · 2021: 35 · 2020: 26 · 2019: 23 · 2018: 23 · 2017: 24 · 2016: 24 · 2015: 28 · 2014: 22 · 2013: 36 · 2012: 33
- FWCI
- 20.78
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Molecular Cell (publishedVersion)
- PubMed (publishedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion)
- Zurich Open Repository and Archive (University of Zurich)
- Funders
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Keywords
- replication restart, UV-induced DNA damage, single-stranded DNA gaps, translesion synthesis, homologous recombination, DNA damage checkpoint, chromosome integrity, Saccharomyces cerevisiae, replication intermediates
- MeSH terms
- Chromosomes, DNA Damage, DNA Repair, DNA Replication, DNA, Fungal, DNA, Single-Stranded, Recombination, Genetic, Saccharomyces cerevisiae, Templates, Genetic, Ultraviolet Rays, Saccharomyces cerevisiae Proteins
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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 ›
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