Expanded CAG/CTG Repeat DNA Induces a Checkpoint Response That Impacts Cell Proliferation in Saccharomyces cerevisiae
Open accessAbstract
Repetitive DNA elements are mutational hotspots in the genome, and their instability is linked to various neurological disorders and cancers. Although it is known that expanded trinucleotide repeats can interfere with DNA replication and repair, the cellular response to these events has not been characterized. Here, we demonstrate that an expanded CAG/CTG repeat elicits a DNA damage checkpoint response in budding yeast. Using microcolony and single cell pedigree analysis, we found that cells carrying an expanded CAG repeat frequently experience protracted cell division cycles, persistent arrests, and morphological abnormalities. These phenotypes were further exacerbated by mutations in DSB repair pathways, including homologous recombination and end joining, implicating a DNA damage response. Cell cycle analysis confirmed repeat-dependent S phase delays and G2/M arrests. Furthermore, we demonstrate that the above phenotypes are due to the activation of the DNA damage checkpoint, since expanded CAG repeats induced the phosphorylation of the Rad53 checkpoint kinase in a rad52Δ recombination deficient mutant. Interestingly, cells mutated for the MRX complex (Mre11-Rad50-Xrs2), a central component of DSB repair which is required to repair breaks at CAG repeats, failed to elicit repeat-specific arrests, morphological defects, or Rad53 phosphorylation. We therefore conclude that damage at expanded CAG/CTG repeats is likely sensed by the MRX complex, leading to a checkpoint response. Finally, we show that repeat expansions preferentially occur in cells experiencing growth delays. Activation of DNA damage checkpoints in repeat-containing cells could contribute to the tissue degeneration observed in trinucleotide repeat expansion diseases.
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Previous studies suggest an inverse correlation between repetitive sequence expression and cell cycle progression and a positive correlation with immune responses.
“Previous studies suggest an inverse correlation between repetitive sequence expression and cell cycle progression14,15 and a positive correlation with immune responses16,17.”
From Multi-omics analysis identifies glioblastoma dependency on H3K9me3 methyltransferase activity (2025) · cites this paper as [15]
The Results section ('Damage at expanded CAG/CTG repeats elicits frequent S phase and post-replication G2/M delays'; page unavailable) reports that yeast cells carrying expanded CAG repeats experience cell-cycle arrests and longer division times. This supports the cell-cycle portion of the claim, but the study attributes those effects to expanded repeat DNA, not to repetitive-sequence expression. The immune-response portion has separate citations in the citing sentence and is not attributed to this source. (LLM, conf=0.86)
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- Authors
- Sundararajan, R., & Freudenreich, C. H.
- Affiliations
- Tufts University (US)
- Corresponding author
- Freudenreich, Catherine H.
- Venue
- PLoS Genetics
- Publisher
- Public Library of Science (PLoS)
- Published
- 2011-03-17
- Volume
- 7
- Issue
- 3
- Pages
- e1001339
- ISSN
- 1553-7390 (ISSN-L)
- 1553-7404
- PMC
- PMC3060079
- OpenAlex
- W2134987903
- Semantic Scholar
- e50b132bfa9443c823bc2087cb281ff9dc76daf1
- Cited by
- 36
- References
- 55
- Citations by year
- 2025: 4 · 2024: 1 · 2023: 1 · 2022: 5 · 2021: 1 · 2020: 1 · 2019: 1 · 2018: 1 · 2017: 3 · 2016: 3 · 2015: 3 · 2014: 4 · 2013: 2 · 2012: 4
- FWCI
- 1.56
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS Genetics (publishedVersion, cc-by)
- PubMed Central (publishedVersion, other-oa)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Funders
- National Institutes of Health
- National Institute of General Medical Sciences (GM063006, R01GM063066)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Genetic Neurodegenerative Diseases
- Health Sciences › Medicine › Pathology and Forensic Medicine › Genetic factors in colorectal cancer
- Keywords
- CAG/CTG repeat expansion, trinucleotide repeat instability, DNA damage checkpoint, DNA double-strand break repair, MRX complex, Rad53 phosphorylation, homologous recombination, non-homologous end joining, G2/M cell cycle arrest, S phase delay, cell cycle arrest, Saccharomyces cerevisiae, growth delay
- MeSH terms
- Cell Cycle, DNA Damage, DNA Repair, DNA Replication, Endodeoxyribonucleases, Exodeoxyribonucleases, Hydroxyurea, Phenotype, Saccharomyces cerevisiae, Protein Serine-Threonine Kinases, Cell Cycle Proteins, Nucleic Acid Synthesis Inhibitors, Trinucleotide Repeat Expansion, Saccharomyces cerevisiae Proteins, Cell Proliferation, Checkpoint Kinase 2
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