Exo1 competes with repair synthesis, converts NER intermediates to long ssDNA gaps, and promotes checkpoint activation
Open accessAbstract
Ultraviolet (UV) light induces DNA-damage checkpoints and mutagenesis, which are involved in cancer protection and tumorigenesis, respectively. How cells identify DNA lesions and convert them to checkpoint-activating structures is a major question. We show that during repair of UV lesions in noncycling cells, Exo1-mediated processing of nucleotide excision repair (NER) intermediates competes with repair DNA synthesis. Impediments of the refilling reaction allow Exo1 to generate extended ssDNA gaps, detectable by electron microscopy, which drive Mec1 kinase activation and will be refilled by long-patch repair synthesis, as shown by DNA combing. We provide evidence that this mechanism may be stimulated by closely opposing UV lesions, represents a strategy to redirect problematic repair intermediates to alternative repair pathways, and may also be extended to physically different DNA damages. Our work has significant implications for understanding the coordination between repair of DNA lesions and checkpoint pathways to preserve genome stability.
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DNA polymerase κ directly participates in NER repair synthesis in human cells, and loss of TLS activity greatly potentiates the checkpoint response to UV in yeast G1 cells, suggesting closely opposing UV lesions may be at least partly responsible for checkpoint activation.
“Interestingly, it was recently shown that DNA polymerase κ directly participates to NER repair synthesis in human cells [70,71] and that loss of TLS activity greatly potentiates the checkpoint response to UV irradiation in yeast G1 cells [61], suggesting that closely opposing UV lesions may indeed be at least partly responsible for checkpoint activation.”
From Mind the gap: keeping UV lesions in check (2011) · cites this paper as [61]
G1 synchronized yeast mutants lacking TLS polymerases are more sensitive to UV than asynchronous cultures, while TLS-proficient strains are not.
“Moreover, a role for TLS in G1-irradiated cells is also supported by the finding that G1 synchronized cultures of yeast mutants lacking TLS polymerases are more sensitive to UV light than asynchronous cultures, while this is not the case for strains that are TLS proficient [61].”
From Mind the gap: keeping UV lesions in check (2011) · cites this paper as [61]
Translesion DNA polymerase activities seem to counteract the generation of the UV-induced checkpoint signal.
“Interestingly, translesion DNA polymerase activities (TLS) seem to counteract the generation of the UV-induced checkpoint signal [61,69].”
From Mind the gap: keeping UV lesions in check (2011) · cites this paper as [61]
Normal NER intermediates are not directly responsible for activating checkpoint kinases.
“Recent work shed light on these problems, showing that normal NER-intermediates are not directly responsible for activating checkpoint kinases.”
From Mind the gap: keeping UV lesions in check (2011) · cites this paper as [61]
In non-cycling yeast, full and prompt checkpoint activity after UV requires NER and also Exo1 nuclease activity.
“In order to achieve a full and prompt checkpoint activity after UV irradiation in non cycling yeast cells, NER is necessary but not sufficient: in fact, the nuclease activity of Exo1 is also required [60,61].”
From Mind the gap: keeping UV lesions in check (2011) · cites this paper as [61]
UV irradiation causes accumulation of long ssDNA regions in yeast chromosomes that depend on NER and Exo1 and correlate with Mec1 kinase activation.
“This work shows that UV irradiation causes the accumulation, in yeast chromosomes, of long ssDNA regions that are dependent upon NER and Exo1 and correlate with Mec1 kinase activation.”
From Mind the gap: keeping UV lesions in check (2011) · cites this paper as [61]
Very low UV doses do not appear to activate the G1 checkpoint.
“This is consistent with the observation that very low UV doses do not seem to activate the G1 checkpoint [61,64,65]”
From Mind the gap: keeping UV lesions in check (2011) · cites this paper as [61]
Once the checkpoint is active, PRR refills the gaps and the lesions are removed from chromosomes.
“This event has a clear relevance since checkpoint mutants will die in this situation, and only after checkpoint activation the gaps are refilled by PRR and the lesions are actually removed from the chromosomes [61].”
From Mind the gap: keeping UV lesions in check (2011) · cites this paper as [61]
Checkpoint mutants die in this situation.
“This event has a clear relevance since checkpoint mutants will die in this situation, and only after checkpoint activation the gaps are refilled by PRR and the lesions are actually removed from the chromosomes [61].”
From Mind the gap: keeping UV lesions in check (2011) · cites this paper as [61]
Long single-stranded DNA can be generated by uncoupling MCM helicase and DNA polymerase during replication stress, by CtIP-mediated double-strand break end resection, by Exo1-mediated processing of nucleotide excision repair intermediates after UV, and by APE2-mediated single-strand break end resection in oxidative stress.
“A long stretch of ssDNA can be generated through the functional uncoupling of minichromosome maintenance (MCM) helicase and DNA polymerase in DNA replication stress, the DSB end resection by DNA exonuclease such as CtIP in DSB response, the Exo1-mediated processing of NER intermediates after UV radiation, and the SSB end resection by AP endonuclease 2 (APE2) in oxidative stress [86, 97–99]”
From Functional interplay between ATM/ATR-mediated DNA damage response and DNA repair pathways in oxidative stress (2014) · cites this paper as [99]
DNA repair proteins, including DNA nucleases, can convert DNA damage into structures that recruit DDR proteins or can directly recruit DDR proteins to damaged sites through protein-protein interactions.
“DNA repair proteins (such as DNA nucleases) may process DNA damage into structures for DDR protein recruitment or recruit DDR proteins to damaged sites via direct protein–protein interactions.”
From Functional interplay between ATM/ATR-mediated DNA damage response and DNA repair pathways in oxidative stress (2014) · cites this paper as [99]
DNA repair proteins may regulate the DDR pathway either directly or indirectly.
“This suggests DNA repair proteins may regulate the DDR pathway directly or indirectly [99, 196, 197].”
From Functional interplay between ATM/ATR-mediated DNA damage response and DNA repair pathways in oxidative stress (2014) · cites this paper as [99]
Exo1 localizes with XPA at damage sites after local UV irradiation in non-replicating cells and converts NER intermediates into single-stranded DNA to promote DDR signaling.
“Exo1 localizes with XPA to damage sites after local UV irradiation in non-replicating cells and converts NER intermediates into ssDNA to promote DDR signaling [99, 205]”
From Functional interplay between ATM/ATR-mediated DNA damage response and DNA repair pathways in oxidative stress (2014) · cites this paper as [99]
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- Authors
- Giannattasio, M., Follonier, C., Tourrière, H., Puddu, F., Lazzaro, F., Pasero, P., Lopes, M., Plevani, P., & Muzi-Falconi, M.
- Affiliations
- University of Milan (IT)
- University of Zurich (CH)
- Centre National de la Recherche Scientifique (FR)
- Corresponding author
- Plevani, Paolo
- Muzi-Falconi, Marco
- ORCID
- Venue
- Molecular Cell
- Publisher
- Elsevier BV
- Published
- 2010-10
- Volume
- 40
- Issue
- 1
- Pages
- 50-62
- ISSN
- 1097-2765 (ISSN-L)
- OpenAlex
- W2029361378
- Cited by
- 121
- References
- 51
- Citations by year
- 2026: 7 · 2025: 6 · 2024: 4 · 2023: 1 · 2022: 6 · 2021: 4 · 2020: 3 · 2019: 5 · 2018: 6 · 2017: 13 · 2016: 11 · 2015: 7 · 2014: 12 · 2013: 16 · 2012: 6
- FWCI
- 4.69
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 1020 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Molecular Cell (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA and Nucleic Acid Chemistry
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Keywords
- EXO1, nucleotide excision repair, UV-induced DNA damage, DNA damage checkpoint, Mec1 kinase, single-stranded DNA gaps, repair synthesis, long-patch repair, DNA damage tolerance, genome stability, DNA combing, electron microscopy of DNA
- MeSH terms
- Cell Cycle, DNA Damage, DNA Repair, DNA, Fungal, DNA, Single-Stranded, Dose-Response Relationship, Radiation, Enzyme Activation, Exodeoxyribonucleases, Saccharomyces cerevisiae, Time Factors, Ultraviolet Rays, Chromosomes, Fungal, Gene Expression Regulation, Fungal, Protein Serine-Threonine Kinases, Saccharomyces cerevisiae Proteins, Genomic Instability, Intracellular Signaling Peptides and Proteins
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