The mismatch repair system is required for S-phase checkpoint activation

Brown, Kevin D.; Rathi, Abhilasha; Kamath, Ravindra; Beardsley, Dillon I.; Zhan, Qimin; Mannino, Jennifer L.; Baskaran, R

doi:10.1038/ng1052

Cited by 206DNA Repair MechanismsGenetic factors in colorectal cancerCancer-related Molecular Pathways

The mismatch repair system is required for S-phase checkpoint activation

Brown, Kevin D., Rathi, Abhilasha, Kamath, Ravindra, Beardsley, Dillon I., Zhan, Qimin, Mannino, Jennifer L., Baskaran, R·2003·Nature Genetics

DOI 10.1038/ng1052

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Abstract

Defective S-phase checkpoint activation results in an inability to downregulate DNA replication following genotoxic insult such as exposure to ionizing radiation. This 'radioresistant DNA synthesis' (RDS) is a phenotypic hallmark of ataxia-telangiectasia, a cancer-prone disorder caused by mutations in ATM. The mismatch repair system principally corrects nucleotide mismatches that arise during replication. Here we show that the mismatch repair system is required for activation of the S-phase checkpoint in response to ionizing radiation. Cells deficient in mismatch repair proteins showed RDS, and restoration of mismatch repair function restored normal S-phase checkpoint function. Catalytic activation of ATM and ATM-mediated phosphorylation of the protein NBS1 (also called nibrin) occurred independently of mismatch repair. However, ATM-dependent phosphorylation and activation of the checkpoint kinase CHK2 and subsequent degradation of its downstream target, CDC25A, was abrogated in cells lacking mismatch repair. In vitro and in vivo approaches both show that MSH2 binds to CHK2 and that MLH1 associates with ATM. These findings indicate that the mismatch repair complex formed at the sites of DNA damage facilitates the phosphorylation of CHK2 by ATM, and that defects in this mechanism form the molecular basis for the RDS observed in cells deficient in mismatch repair.

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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 [196]
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 [196]
Interactions between MSH2 and Chk2 and between MLH1 and ATM promote recruitment of DDR proteins to IR-damaged sites and help ATM phosphorylate Chk2.
“The interactions between MMR and DDR proteins (i.e., MSH2-Chk2 and MLH1-ATM) promote the recruitment of DDR proteins to IR-damaged sites and facilitate Chk2 phosphorylation by ATM [196]”
From Functional interplay between ATM/ATR-mediated DNA damage response and DNA repair pathways in oxidative stress (2014) · cites this paper as [196]
MSH2 binds Chk2, and MLH1 associates with ATM.
“MSH2 binds to Chk2 and that MLH1 associates with ATM”
From Functional interplay between ATM/ATR-mediated DNA damage response and DNA repair pathways in oxidative stress (2014) · cites this paper as [196]

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Authors: Brown, K. D., Rathi, A., Kamath, R., Beardsley, D. I., Zhan, Q., Mannino, J. L., & Baskaran, R.
Affiliations: Louisiana State University Health Sciences Center New Orleans (US)
University of Pittsburgh Medical Center (US)
Corresponding author: Baskaran, R
ORCID: Brown, Kevin D.
Zhan, Qimin
Baskaran, R
Venue: Nature Genetics
Publisher: Springer Science and Business Media LLC
Published: 2002-11-25
Volume: 33
Issue: 1
Pages: 80-84
ISSN: 1061-4036 (ISSN-L)
1546-1718
DOI: 10.1038/ng1052
OpenAlex: W2092282016
Cited by: 206
References: 31
Citations by year: 2026: 3 · 2025: 5 · 2024: 3 · 2023: 2 · 2022: 4 · 2021: 6 · 2020: 5 · 2019: 1 · 2018: 3 · 2017: 2 · 2016: 5 · 2015: 6 · 2014: 3 · 2013: 10 · 2012: 6
FWCI: 7.53
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Nature Genetics (publishedVersion)
PubMed (publishedVersion)
Funders: American Cancer Society
National Institutes of Health
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
Health Sciences › Medicine › Pathology and Forensic Medicine › Genetic factors in colorectal cancer
Health Sciences › Medicine › Oncology › Cancer-related Molecular Pathways
Keywords: DNA mismatch repair, S-phase checkpoint, radioresistant DNA synthesis, ataxia telangiectasia, ATM, NBS1, Chk2, CDC25A, MSH2, MLH1, ionizing radiation, DNA replication, DNA damage response, checkpoint kinase
MeSH terms: MutL Protein Homolog 1, Carrier Proteins, DNA Repair, DNA Replication, DNA-Binding Proteins, Enzyme Activation, Humans, Models, Biological, Neoplasm Proteins, Nuclear Proteins, Phosphorylation, Protein Kinases, Proto-Oncogene Proteins, Radiation Tolerance, Radiation, Ionizing, Tumor Cells, Cultured, S Phase, Protein Serine-Threonine Kinases, Gene Deletion, Cell Cycle Proteins, Base Pair Mismatch, cdc25 Phosphatases, Tumor Suppressor Proteins, Adaptor Proteins, Signal Transducing, MutS Homolog 2 Protein, Ataxia Telangiectasia Mutated Proteins, Checkpoint Kinase 2

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The mismatch repair system is required for S-phase checkpoint activation

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