ATR Kinase Activation Mediated by MutSα and MutLα in Response to Cytotoxic O6-Methylguanine Adducts

Yoshioka, Ken-ichi; Yoshioka, Yoshiko; Hsieh, Peggy

doi:10.1016/j.molcel.2006.04.023

Cited by 288DNA Repair MechanismsGenetic factors in colorectal cancerDNA and Nucleic Acid Chemistry

ATR Kinase Activation Mediated by MutSα and MutLα in Response to Cytotoxic O6-Methylguanine Adducts

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Yoshioka, Ken-ichi, Yoshioka, Yoshiko, Hsieh, Peggy·2006·Molecular Cell

DOI 10.1016/j.molcel.2006.04.023PMC PMC2423943

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Abstract

S(N)1-type alkylating agents that produce cytotoxic O(6)-methyl-G (O(6)-meG) DNA adducts induce cell cycle arrest and apoptosis in a manner requiring the DNA mismatch repair (MMR) proteins MutSalpha and MutLalpha. Here, we show that checkpoint signaling in response to DNA methylation occurs during S phase and requires DNA replication that gives rise to O(6)-meG/T mispairs. DNA binding studies reveal that MutSalpha specifically recognizes O(6)-meG/T mispairs, but not O(6)-meG/C. In an in vitro assay, ATR-ATRIP, but not RPA, is preferentially recruited to O(6)-meG/T mismatches in a MutSalpha- and MutLalpha-dependent manner. Furthermore, ATR kinase is activated to phosphorylate Chk1 in the presence of O(6)-meG/T mispairs and MMR proteins. These results suggest that MMR proteins can act as direct sensors of methylation damage and help recruit ATR-ATRIP to sites of cytotoxic O(6)-meG adducts to initiate ATR checkpoint signaling.

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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 [197]
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 [197]
SN1-type DNA alkylating agents produce DNA adducts such as O6-methylguanine and activate the ATR-Chk1 pathway.
“SN1-type DNA alkylating agents induce DNA adducts, such as O6-meG (O6-methylguanine), and activate the ATR-Chk1 pathway.”
From Functional interplay between ATM/ATR-mediated DNA damage response and DNA repair pathways in oxidative stress (2014) · cites this paper as [197]
MutSα acts upstream in ATR checkpoint signaling.
“indicating MutSα plays an upstream role for ATR checkpoint signaling [197]”
From Functional interplay between ATM/ATR-mediated DNA damage response and DNA repair pathways in oxidative stress (2014) · cites this paper as [197]
MutSα recruits ATR-ATRIP to O6-methylguanine:thymine mismatches.
“MutSα also recruits ATR-ATRIP to O6-meG:T”
From Functional interplay between ATM/ATR-mediated DNA damage response and DNA repair pathways in oxidative stress (2014) · cites this paper as [197]

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Authors: Yoshioka, K.-I., Yoshioka, Y., & Hsieh, P.
Affiliations: National Institutes of Health (US)
Corresponding author: Hsieh, Peggy
Venue: Molecular Cell
Publisher: Elsevier BV
Published: 2006-05
Volume: 22
Issue: 4
Pages: 501-510
ISSN: 1097-2765 (ISSN-L)
DOI: 10.1016/j.molcel.2006.04.023
PMC: PMC2423943
OpenAlex: W2163529853
Cited by: 288
References: 49
Citations by year: 2026: 7 · 2025: 4 · 2024: 12 · 2023: 4 · 2022: 14 · 2021: 15 · 2020: 8 · 2019: 9 · 2018: 6 · 2017: 7 · 2016: 13 · 2015: 15 · 2014: 9 · 2013: 15 · 2012: 13
FWCI: 11.68
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 2634 d)
Locations: Molecular Cell (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: Massachusetts General Hospital
National Institutes of Health
National Institute of Diabetes and Digestive and Kidney Diseases (Z01DK052029)
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
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA and Nucleic Acid Chemistry
Keywords: MutSα, MutLα, DNA mismatch repair, DNA replication checkpoint, S phase, Chk1 phosphorylation, DNA damage recognition
MeSH terms: Animals, Base Sequence, Carrier Proteins, Cell Line, DNA, DNA Damage, DNA Repair, DNA-Binding Proteins, Enzyme Activation, Exodeoxyribonucleases, Guanine, HeLa Cells, Humans, Nuclear Proteins, Phosphoproteins, Signal Transduction, S Phase, Protein Serine-Threonine Kinases, DNA Adducts, Cell Cycle Proteins, Base Pair Mismatch, Adaptor Proteins, Signal Transducing, Mice, MutS DNA Mismatch-Binding Protein, Ataxia Telangiectasia Mutated Proteins

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ATR Kinase Activation Mediated by MutSα and MutLα in Response to Cytotoxic O6-Methylguanine Adducts

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