RAD6-RAD18-RAD5-pathway-dependent tolerance to chronic low-dose ultraviolet light
Open accessAbstract
In nature, organisms are exposed to chronic low-dose ultraviolet light (CLUV) as opposed to the acute high doses common to laboratory experiments. Analysis of the cellular response to acute high-dose exposure has delineated the importance of direct DNA repair by the nucleotide excision repair pathway and for checkpoint-induced cell cycle arrest in promoting cell survival. Here we examine the response of yeast cells to CLUV and identify a key role for the RAD6-RAD18-RAD5 error-free postreplication repair (RAD6 error-free PRR) pathway in promoting cell growth and survival. We show that loss of the RAD6 error-free PRR pathway results in DNA-damage-checkpoint-induced G2 arrest in CLUV-exposed cells, whereas wild-type and nucleotide-excision-repair-deficient cells are largely unaffected. Cell cycle arrest in the absence of the RAD6 error-free PRR pathway was not caused by a repair defect or by the accumulation of ultraviolet-induced photoproducts. Notably, we observed increased replication protein A (RPA)- and Rad52-yellow fluorescent protein foci in the CLUV-exposed rad18Delta cells and demonstrated that Rad52-mediated homologous recombination is required for the viability of the rad18Delta cells after release from CLUV-induced G2 arrest. These and other data presented suggest that, in response to environmental levels of ultraviolet exposure, the RAD6 error-free PRR pathway promotes replication of damaged templates without the generation of extensive single-stranded DNA regions. Thus, the error-free PRR pathway is specifically important during chronic low-dose ultraviolet exposure to prevent counter-productive DNA checkpoint activation and allow cells to proliferate normally.
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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 [65]
Under very low chronic UV (0.18 J m−2 min−1), the RAD5-dependent branch of PRR is the only pathway necessary and sufficient for budding yeast cell survival.
“An important point in this regard was made by irradiating budding yeast cells with very low (0.18 J m−2 min−1) chronic UV dose (CLUV): the only pathway necessary and sufficient to ensure cell survival was found to be the RAD5-dependent branch of PRR [65].”
From Mind the gap: keeping UV lesions in check (2011) · cites this paper as [65]
NER-deficient (rad14Δ) and checkpoint-deficient (mec1Δ) cells are not particularly sensitive to CLUV, unlike rad18Δ and rad5Δ PRR-deficient cells, which irreversibly activate Mec1 checkpoint and die in G2.
“Indeed, NER deficient cells (rad14Δ) and DNA damage checkpoint deficient cells (mec1Δ) are not particularly sensitive to the CLUV treatment, contrary to the rad18Δ and rad5Δ cells, deficient in PRR [65], which irreversibly activate Mec1 DNA damage checkpoint and die in the G2 phase.”
From Mind the gap: keeping UV lesions in check (2011) · cites this paper as [65]
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Self-citation
- Authors
- Hishida, T., Kubota, Y., Carr, A. M., & Iwasaki, H.
- Affiliations
- Research Institute for Microbial Diseases, The University of Osaka (JP)
- University of Sussex (GB)
- Yokohama City University (JP)
- Corresponding author
- Hishida, Takashi
- Venue
- Nature
- Published
- 2008-12-14
- Volume
- 457
- Issue
- 7229
- Pages
- 612-615
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W1992705983
- Cited by
- 77
- References
- 34
- Citations by year
- 2024: 2 · 2023: 1 · 2022: 2 · 2021: 3 · 2020: 2 · 2019: 5 · 2018: 7 · 2017: 5 · 2016: 4 · 2015: 2 · 2014: 12 · 2013: 8 · 2012: 6
- FWCI
- 2.47
- Type
- journal article
- Language
- en
- Open access
- green
- figshare.com
- Licence
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Sussex Research Online (University of Sussex) (submittedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Figshare (submittedVersion, cc-by)
- Tokyo Tech Research Repository (Tokyo Institute of Technology) (submittedVersion)
- Funders
- Sumitomo Foundation
- 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
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Effects of Radiation Exposure
- Keywords
- postreplication repair, error-free DNA repair, DNA damage tolerance, G2 cell cycle arrest, DNA damage checkpoint, homologous recombination, RAD52, replication protein A, nucleotide excision repair, Saccharomyces cerevisiae, single-stranded DNA, photoproducts
- MeSH terms
- Adenosine Triphosphatases, DNA Damage, DNA Repair, DNA Replication, DNA Helicases, DNA-Binding Proteins, DNA, Fungal, Recombination, Genetic, Saccharomyces cerevisiae, Ultraviolet Rays, G2 Phase, Saccharomyces cerevisiae Proteins, Ubiquitin-Conjugating Enzymes, Replication Protein A, Rad52 DNA Repair and Recombination Protein
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