Cited by 291DNA Repair MechanismsCancer-related Molecular PathwaysDNA and Nucleic Acid Chemistry

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ATR: a master conductor of cellular responses to DNA replication stress

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Flynn, Rachel Litman, Zou, Lee·2011·Trends in Biochemical Sciences

DOI 10.1016/j.tibs.2010.09.005PMC PMC3024454

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Abstract

The integrity of the genome is constantly challenged by intrinsic and extrinsic genotoxic stresses that damage DNA. The cellular responses to DNA damage are orchestrated by DNA damage signaling pathways, also known as DNA damage checkpoints. These signaling pathways play crucial roles in detecting DNA damage, regulating DNA repair and coordinating DNA repair with other cellular processes. In vertebrates, the ATM- and Rad3-related (ATR) kinase plays a key role in the response to a broad spectrum of DNA damage and DNA replication stress. Here, we will discuss the recent findings on how ATR is activated by DNA damage and how it protects the genome against interference with DNA replication.

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Peng, C.-Y., Graves, P. R., Thoma, R. S., Wu, Z., Shaw, A. S., & Piwnica-Worms, H. (1997) · Science · doi:10.1126/science.277.5331.1501 · Cited by 1,341
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Sanchez, Y., Wong, C., Thoma, R. S., Richman, R., Wu, Z., Piwnica-Worms, H., & Elledge, S. J. (1997) · Science · doi:10.1126/science.277.5331.1497 · Cited by 1,320
ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks
Jazayeri, A., Falck, J., Lukas, C., Bartek, J., Smith, G. C. M., Lukas, J., & Jackson, S. P. (2006) · Nature Cell Biology · doi:10.1038/ncb1337 · Cited by 1,064
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Recognition, signaling, and repair of DNA double-strand breaks produced by ionizing radiation in mammalian cells: the molecular choreography
Thompson, L. H. (2012) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2012.06.002 · Cited by 357
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Liu, S., Shiotani, B., Lahiri, M., Maréchal, A., Tse, A., Leung, C. C. Y., Glover, J. N. M., Yang, X. H., & Zou, L. (2011) · Molecular Cell · doi:10.1016/j.molcel.2011.06.019 · Cited by 281
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Berzosertib plus gemcitabine versus gemcitabine alone in platinum-resistant high-grade serous ovarian cancer: a multicentre, open-label, randomised, phase 2 trial
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ATM‐mediated phosphorylation of SOG1 is essential for the DNA damage response in Arabidopsis
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Authors: Flynn, R. L., & Zou, L.
Affiliations: Harvard University (US)
Corresponding author: Zou, Lee
ORCID: Flynn, Rachel Litman
Zou, Lee
Venue: Trends in Biochemical Sciences
Publisher: Elsevier BV
Published: 2011-03
Volume: 36
Issue: 3
Pages: 133-140
ISSN: 0968-0004 (ISSN-L)
DOI: 10.1016/j.tibs.2010.09.005
PMC: PMC3024454
OpenAlex: W2050293032
Cited by: 290
References: 100
Citations by year: 2026: 6 · 2025: 8 · 2024: 14 · 2023: 14 · 2022: 17 · 2021: 16 · 2020: 20 · 2019: 19 · 2018: 21 · 2017: 19 · 2016: 22 · 2015: 23 · 2014: 29 · 2013: 29 · 2012: 19
FWCI: 1.74
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Trends in Biochemical Sciences (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of General Medical Sciences (R01GM076388, GM076388)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
Health Sciences › Medicine › Oncology › Cancer-related Molecular Pathways
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA and Nucleic Acid Chemistry
Keywords: ATR kinase, replication stress, DNA damage checkpoint, DNA damage signaling, genome stability, DNA repair, genotoxic stress
MeSH terms: DNA Damage, DNA Repair, DNA Replication, Humans, Models, Biological, Protein Serine-Threonine Kinases, Cell Cycle Proteins, Ataxia Telangiectasia Mutated Proteins

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ATR: a master conductor of cellular responses to DNA replication stress

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