ATR: an essential regulator of genome integrity

Cimprich, Karlene A.; Cortez, David

doi:10.1038/nrm2450

Cited by 1,798DNA Repair MechanismsCancer-related Molecular PathwaysProtein Kinase Regulation and GTPase Signaling

ATR: an essential regulator of genome integrity

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Cimprich, Karlene A., Cortez, David·2008·Nature Reviews Molecular Cell Biology

DOI 10.1038/nrm2450PMC PMC2663384

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Abstract

Genome maintenance is a constant concern for cells, and a coordinated response to DNA damage is required to maintain cellular viability and prevent disease. The ataxia-telangiectasia mutated (ATM) and ATM and RAD3-related (ATR) protein kinases act as master regulators of the DNA-damage response by signalling to control cell-cycle transitions, DNA replication, DNA repair and apoptosis. Recent studies have provided new insights into the mechanisms that control ATR activation, have helped to explain the overlapping but non-redundant activities of ATR and ATM in DNA-damage signalling, and have clarified the crucial functions of ATR in maintaining genome integrity.

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ATR is an essential gene for nucleotide excision repair initiation and regulation and for genome maintenance.
“ATR is an essential gene for the initiation and regulation of NER and for genome maintenance 17, 36, 37.”
From Xeroderma Pigmentosa Group A (XPA), Nucleotide Excision Repair and Regulation by ATR in Response to Ultraviolet Irradiation (2017) · cites this paper as [17]
H2AX is phosphorylated both in G1 and S phases by ATR in response to UV irradiation.
“H2AX is phosphorylated both in G1 and S phases by ATR in response to UV irradiation [26;32–38].”
From ATR- and ATM-Mediated DNA Damage Response Is Dependent on Excision Repair Assembly during G1 but Not in S Phase of Cell Cycle (2016) · cites this paper as [36]
Short single-stranded DNA gaps caused by UV damage result in activation of ATR-dependent repair and checkpoint pathways.
“Several studies implicated that short ssDNA (single-stranded DNA) gaps caused by UV damage results in activation of ATR-dependent repair and checkpoint pathways [14–16].”
From ATR- and ATM-Mediated DNA Damage Response Is Dependent on Excision Repair Assembly during G1 but Not in S Phase of Cell Cycle (2016) · cites this paper as [14]
ATR is predominantly responsible for the DNA damage response upon UVR exposure.
“Previous studies support that ATR is predominantly responsible for DDR upon UVR exposure”
From ATR- and ATM-Mediated DNA Damage Response Is Dependent on Excision Repair Assembly during G1 but Not in S Phase of Cell Cycle (2016) · cites this paper as [36]
ATM-Chk2 and ATR-Chk1 checkpoints are the two main DNA damage response pathways induced by oxidatively damaged DNA to coordinate DNA repair and cell cycle progression.
“Ataxia-telangiectasia mutated (ATM)-Checkpoint kinase 2 (Chk2) and ATM- and Rad3-related (ATR)-Checkpoint kinase 1 (Chk1) checkpoints are the two major DDR pathways induced by oxidatively damaged DNA to coordinate DNA repair process and cell cycle progression (Figs. 2, 7) [31, 32].”
From Functional interplay between ATM/ATR-mediated DNA damage response and DNA repair pathways in oxidative stress (2014) · cites this paper as [32]

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Architecture of the Replication Fork Stalled at the 3′ End of Yeast Ribosomal Genes
Gruber, M., Wellinger, R. E., & Sogo, J. M. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.15.5777-5787.2000 · Cited by 64 · see citing works
Phosphorylation of Chk1 by ATM- and Rad3-related (ATR) in Xenopus Egg Extracts Requires Binding of ATRIP to ATR but Not the Stable DNA-binding or Coiled-coil Domains of ATRIP
Kim, S.-M., Kumagai, A., Lee, J., & Dunphy, W. G. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m508673200 · Cited by 58 · see citing works
Direct requirement for Xmus101 in ATR-mediated phosphorylation of Claspin bound Chk1 during checkpoint signaling
Yan, S., Lindsay, H. D., & Michael, W. M. (2006) · The Journal of Cell Biology · doi:10.1083/jcb.200601076 · Cited by 56 · see citing works
Electron microscopy and 3D reconstructions reveal that human ATM kinase uses an arm-like domain to clamp around double-stranded DNA
Llorca, Ó., Rivera-Calzada, Á., Grantham, J., et al. (2003) · Oncogene · doi:10.1038/sj.onc.1206649 · Cited by 52 · see citing works
Absence of BLM leads to accumulation of chromosomal DNA breaks during both unperturbed and disrupted S phases
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Checkpoint independence of most DNA replication origins in fission yeast
Mickle, K. L., Ramanathan, S., Rosebrock, A. P., Oliva, A., Chaudari, A., Yompakdee, C., Scott, D., Leatherwood, J., & Huberman, J. A. (2007) · BMC Molecular Biology · doi:10.1186/1471-2199-8-112 · Cited by 39 · see citing works
Cdc18 Enforces Long-Term Maintenance of the S Phase Checkpoint by Anchoring the Rad3-Rad26 Complex to Chromatin
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Dimerization of the ATRIP Protein through the Coiled-Coil Motif and Its Implication to the Maintenance of Stalled Replication Forks
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Phosphorylation ofXenopusRad1 and Hus1 Defines a Readout for ATR Activation That Is Independent of Claspin and the Rad9 Carboxy Terminus
Lupardus, P. J., & Cimprich, K. A. (2006) · Molecular Biology of the Cell · doi:10.1091/mbc.e05-09-0865 · Cited by 33 · see citing works
Self-citation
Activation of a DNA Damage Checkpoint Response in a TAF1-Defective Cell Line
Buchmann, A. M., Skaar, J. R., & DeCaprio, J. A. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.12.5332-5339.2004 · Cited by 30 · see citing works
Different requirements for the association of ATR–ATRIP and 9-1-1 to the stalled replication forks
Kanoh, Y., Tamai, K., & Shirahige, K. (2006) · Gene · doi:10.1016/j.gene.2006.03.019 · Cited by 29 · see citing works
ATR-dependent phosphorylation of ATRIP in response to genotoxic stress
Itakura, E., Umeda, K., Sekoguchi, E., Takata, H., Ohsumi, M., & Matsuura, A. (2004) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2004.08.228 · Cited by 29 · see citing works
Phosphorylation of replication protein A by S-phase checkpoint kinases
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A Ddc2-Rad53 Fusion Protein Can Bypass the Requirements forRAD9andMRC1in Rad53 Activation
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Phosphorylation of ATR-Interacting Protein on Ser239 Mediates an Interaction with Breast-Ovarian Cancer Susceptibility 1 and Checkpoint Function
Venere, M., Snyder, A. R., Zgheib, O., & Halazonetis, T. D. (2007) · Cancer Research · doi:10.1158/0008-5472.can-07-0369 · Cited by 25 · see citing works
Regulation of ATR-dependent pathways by the FHA domain containing protein SNIP1
Roche, K. C., Rocha, S., Bracken, C. P., & Perkins, N. D. (2007) · Oncogene · doi:10.1038/sj.onc.1210233 · Cited by 23 · see citing works
Function of the ATR N-terminal domain revealed by an ATM/ATR chimera
Chen, X., Zhao, R., Glick, G. G., & Cortez, D. (2007) · Experimental Cell Research · doi:10.1016/j.yexcr.2007.02.015 · Cited by 19 · see citing works
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The DNA-damage response in human biology and disease
Jackson, S. P., & Bartek, J. (2009) · Nature · doi:10.1038/nature08467 · Cited by 6,092 · see citing works
The DNA Damage Response: Making It Safe to Play with Knives
Ciccia, A., & Elledge, S. J. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.09.019 · Cited by 4,368 · see citing works
Cell cycle, CDKs and cancer: a changing paradigm
Malumbres, M., & Barbacid, M. (2009) · Nature Reviews Cancer · doi:10.1038/nrc2602 · Cited by 3,957 · see citing works
The ATM protein kinase: regulating the cellular response to genotoxic stress, and more
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DNA Damage Sensing by the ATM and ATR Kinases
Marechal, A., & Zou, L. (2013) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a012716 · Cited by 1,514 · see citing works
Ataxia-telangiectasia: from a rare disorder to a paradigm for cell signalling and cancer
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Shelterin-Mediated Telomere Protection
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Tumor Exome Analysis Reveals Neoantigen-Specific T-Cell Reactivity in an Ipilimumab-Responsive Melanoma
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Systems biology of cisplatin resistance: past, present and future
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The MRE11 complex: starting from the ends
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Selective killing of ATM- or p53-deficient cancer cells through inhibition of ATR
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ARID1A Deficiency Impairs the DNA Damage Checkpoint and Sensitizes Cells to PARP Inhibitors
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RPA-coated single-stranded DNA as a platform for post-translational modifications in the DNA damage response
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Roles of Chk1 in cell biology and cancer therapy
Zhang, Y., & Hunter, T. (2014) · International Journal of Cancer · doi:10.1002/ijc.28226 · Cited by 462 · see citing works
Causes of genome instability
Aguilera, A., & García-Muse, T. (2013) · Annual Review of Genetics · doi:10.1146/annurev-genet-111212-133232 · Cited by 476 · see citing works
A cell-based screen identifies ATR inhibitors with synthetic lethal properties for cancer-associated mutations
Toledo, L. I., Murga, M., Zur, R., Soria, R., Rodriguez, A., Martinez, S., Oyarzabal, J., Pastor, J., Bischoff, J. R., & Fernandez-Capetillo, O. (2011) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2076 · Cited by 465 · see citing works
DNA damage during S-phase mediates the proliferation-quiescence decision in the subsequent G1 via p21 expression
Barr, A. R., Cooper, S., Heldt, F. S., Butera, F., Stoy, H., Mansfeld, J., Novák, B., & Bakal, C. (2017) · Nature Communications · doi:10.1038/ncomms14728 · Cited by 403 · see citing works
DNA damage checkpoints in stem cells, ageing and cancer
Sperka, T., Wang, J., & Rudolph, K. L. (2012) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3420 · Cited by 393 · see citing works
Exploiting oncogene-induced replicative stress for the selective killing of Myc-driven tumors
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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 · see citing works
Checkpoint kinase 1 in DNA damage response and cell cycle regulation
Patil, M., Pabla, N., & Dong, Z. (2013) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-013-1307-3 · Cited by 317 · see citing works
DNA repair deficiency and neurological disease
McKinnon, P. J. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2559 · Cited by 323 · see citing works
ATR signalling: more than meeting at the fork
Nam, E. A., & Cortez, D. (2011) · Biochemical Journal · doi:10.1042/bj20102162 · Cited by 316 · see citing works
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Distinct but Concerted Roles of ATR, DNA-PK, and Chk1 in Countering Replication Stress during S Phase
Buisson, R., Boisvert, J. L., Benes, C. H., & Zou, L. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.07.029 · Cited by 316 · see citing works
RNF4, a SUMO-targeted ubiquitin E3 ligase, promotes DNA double-strand break repair
Galanty, Y., Belotserkovskaya, R., Coates, J., & Jackson, S. P. (2012) · Genes & Development · doi:10.1101/gad.188284.112 · Cited by 314 · see citing works
ATR: a master conductor of cellular responses to DNA replication stress
Flynn, R. L., & Zou, L. (2011) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2010.09.005 · Cited by 290 · see citing works
ATR autophosphorylation as a molecular switch for checkpoint activation
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 · see citing works
Common mechanisms of PIKK regulation
Lovejoy, C. A., & Cortez, D. (2009) · DNA Repair · doi:10.1016/j.dnarep.2009.04.006 · Cited by 277 · see citing works
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DNA Damage Response: Three Levels of DNA Repair Regulation
Sirbu, B. M., & Cortez, D. (2013) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a012724 · Cited by 272 · see citing works
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Functional interplay between ATM/ATR-mediated DNA damage response and DNA repair pathways in oxidative stress
Yan, S., Sorrell, M., & Berman, Z. (2014) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-014-1666-4 · Cited by 247 · see citing works
Preventing replication fork collapse to maintain genome integrity
Cortez, D. (2015) · DNA Repair · doi:10.1016/j.dnarep.2015.04.026 · Cited by 223 · see citing works
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Maintaining genome stability in the nervous system
McKinnon, P. J. (2013) · Nature Neuroscience · doi:10.1038/nn.3537 · Cited by 229 · see citing works
CtIP Links DNA Double-Strand Break Sensing to Resection
You, Z., Shi, L. Z., Zhu, Q., Wu, P., Zhang, Y.-W., Basilio, A., Tonnu, N., Verma, I. M., Berns, M. W., & Hunter, T. (2009) · Molecular Cell · doi:10.1016/j.molcel.2009.12.002 · Cited by 231 · see citing works
A genetic screen identifies the Triple T complex required for DNA damage signaling and ATM and ATR stability
Hurov, K. E., Cotta-Ramusino, C., & Elledge, S. J. (2010) · Genes & Development · doi:10.1101/gad.1934210 · Cited by 210 · see citing works
Impact of genomic damage and ageing on stem cell function
Behrens, A., van Deursen, J. M., Rudolph, K. L., & Schumacher, B. (2014) · Nature Cell Biology · doi:10.1038/ncb2928 · Cited by 207 · see citing works
Nucleotide metabolism, oncogene-induced senescence and cancer
Aird, K. M., & Zhang, R. (2015) · Cancer Letters · doi:10.1016/j.canlet.2014.01.017 · Cited by 166 · see citing works
The Good, the Bad, and the Ugly of ROS: New Insights on Aging and Aging‐Related Diseases from Eukaryotic and Prokaryotic Model Organisms
Santos, A. L., Sinha, S., & Lindner, A. B. (2018) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2018/1941285 · Cited by 168 · see citing works
Mechanisms of replication fork protection: a safeguard for genome stability
Errico, A., & Costanzo, V. (2012) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.3109/10409238.2012.655374 · Cited by 159 · see citing works
A Role for the MRN Complex in ATR Activation via TOPBP1 Recruitment
Duursma, A. M., Driscoll, R., Elias, J. E., & Cimprich, K. A. (2013) · Molecular Cell · doi:10.1016/j.molcel.2013.03.006 · Cited by 153 · see citing works
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ATR/Mec1: coordinating fork stability and repair
Friedel, A. M., Pike, B. L., & Gasser, S. M. (2009) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2009.01.017 · Cited by 157 · see citing works
BACH1/FANCJ Acts with TopBP1 and Participates Early in DNA Replication Checkpoint Control
Gong, Z., Kim, J.-E., Leung, C. C. Y., Glover, J. N. M., & Chen, J. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.01.002 · Cited by 160 · see citing works
Optimal function of the DNA repair enzyme TDP1 requires its phosphorylation by ATM and/or DNA‐PK
Das, B. B., Antony, S., Gupta, S., Dexheimer, T. S., Redon, C. E., Garfield, S., Shiloh, Y., & Pommier, Y. (2009) · The EMBO Journal · doi:10.1038/emboj.2009.302 · Cited by 151 · see citing works
Roles of UVA radiation and DNA damage responses in melanoma pathogenesis
Khan, A. Q., Travers, J. B., & Kemp, M. G. (2018) · Environmental and Molecular Mutagenesis · doi:10.1002/em.22176 · Cited by 152 · see citing works
The MMS22L-TONSL Complex Mediates Recovery from Replication Stress and Homologous Recombination
O'Donnell, L., Panier, S., Wildenhain, J., Tkach, J. M., Al-Hakim, A., Landry, M.-C., Escribano-Diaz, C., Szilard, R. K., Young, J. T. F., Munro, M., et al. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.10.024 · Cited by 149 · see citing works
Cell fitness screens reveal a conflict between LINE-1 retrotransposition and DNA replication
Ardeljan, D., Steranka, J. P., Liu, C., Li, Z., Taylor, M. S., Payer, L. M., Gorbounov, M., Sarnecki, J. S., Deshpande, V., Hruban, R. H., et al. (2020) · Nature Structural & Molecular Biology · doi:10.1038/s41594-020-0372-1 · Cited by 135 · see citing works
DNA damage-induced cell death relies on SLFN11-dependent cleavage of distinct type II tRNAs
Li, M., Kao, E., Malone, D., Gao, X., Wang, J. Y. J., & David, M. (2018) · Nature Structural & Molecular Biology · doi:10.1038/s41594-018-0142-5 · Cited by 136 · see citing works
Eukaryotic DNA damage checkpoint activation in response to double-strand breaks
Finn, K., Lowndes, N. F., & Grenon, M. (2012) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-011-0875-3 · Cited by 127 · see citing works
Dpb11 activates the Mec1-Ddc2 complex
Mordes, D. A., Nam, E. A., & Cortez, D. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0806621105 · Cited by 121 · see citing works
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Complex DNA repair pathways as possible therapeutic targets to overcome temozolomide resistance in glioblastoma
Yoshimoto, K., Mizoguchi, M., Hata, N., Murata, H., Hatae, R., Amano, T., Nakamizo, A., & Sasaki, T. (2012) · Frontiers in Oncology · doi:10.3389/fonc.2012.00186 · Cited by 126 · see citing works
MDC1 collaborates with TopBP1 in DNA replication checkpoint control
Wang, J., Gong, Z., & Chen, J. (2011) · Journal of Cell Biology · doi:10.1083/jcb.201010026 · Cited by 118 · see citing works
Genomic instability and DNA damage responses in progeria arising from defective maturation of prelamin A
Musich, P. R., & Zou, Y. (2009) · Aging · doi:10.18632/aging.100012 · Cited by 117 · see citing works
Hypoxia signaling in cancer: Implications for therapeutic interventions
Zhuang, Y., Liu, K., He, Q., Gu, X., Jiang, C., & Wu, J. (2023) · MedComm · doi:10.1002/mco2.203 · Cited by 119 · see citing works
hMSH2 Recruits ATR to DNA Damage Sites for Activation during DNA Damage-induced Apoptosis
Pabla, N., Ma, Z., McIlhatton, M. A., Fishel, R., & Dong, Z. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.210989 · Cited by 107 · see citing works
TopBP1 and DNA polymerase-α directly recruit the 9-1-1 complex to stalled DNA replication forks
Yan, S., & Michael, W. M. (2009) · Journal of Cell Biology · doi:10.1083/jcb.200810185 · Cited by 107 · see citing works
Mitotic catastrophe and cancer drug resistance: A link that must to be broken
Denisenko, T. V., Sorokina, I. V., Gogvadze, V., & Zhivotovsky, B. (2016) · Drug Resistance Updates · doi:10.1016/j.drup.2015.11.002 · Cited by 108 · see citing works
Rejuvenating the immune system in rheumatoid arthritis.
Weyand, C. M., Fujii, H., Shao, L., & Goronzy, J. J. (2009) · Nature Reviews Rheumatology · doi:10.1038/nrrheum.2009.180 · Cited by 112 · see citing works
A Synthetic Lethal Screen Identifies DNA Repair Pathways that Sensitize Cancer Cells to Combined ATR Inhibition and Cisplatin Treatments
Mohni, K. N., Thompson, P. S., Luzwick, J. W., Glick, G. G., Pendleton, C. S., Lehmann, B. D., Pietenpol, J. A., & Cortez, D. (2015) · PLOS ONE · doi:10.1371/journal.pone.0125482 · Cited by 108 · see citing works
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Caspase-2 deficiency promotes aberrant DNA-damage response and genetic instability
Dorstyn, L., Puccini, J., Wilson, C. H., Shalini, S., Nicola, M., Moore, S., & Kumar, S. (2012) · Cell Death & Differentiation · doi:10.1038/cdd.2012.36 · Cited by 104 · see citing works
Increased Neural Progenitor Proliferation in a hiPSC Model of Autism Induces Replication Stress-Associated Genome Instability
Wang, M., Wei, P.-C., Lim, C. K., Gallina, I. S., Marshall, S., Marchetto, M. C., Alt, F. W., & Gage, F. H. (2020) · Cell Stem Cell · doi:10.1016/j.stem.2019.12.013 · Cited by 105 · see citing works
Cdk2 is required for p53-independent G2/M checkpoint control
Chung, J. H., & Bunz, F. (2010) · PLoS Genetics · doi:10.1371/journal.pgen.1000863 · Cited by 105 · see citing works
APE2 is required for ATR-Chk1 checkpoint activation in response to oxidative stress
Willis, J., Patel, Y., Lentz, B. L., & Yan, S. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1301445110 · Cited by 100 · see citing works
A Shld1-Controlled POT1a Provides Support for Repression of ATR Signaling at Telomeres through RPA Exclusion
Gong, Y., & de Lange, T. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.10.016 · Cited by 102 · see citing works
Checkpoint mechanisms at the intersection between DNA damage and repair
Lazzaro, F., Giannattasio, M., Puddu, F., Granata, M., Pellicioli, A., Plevani, P., & Muzi-Falconi, M. (2009) · DNA Repair · doi:10.1016/j.dnarep.2009.04.022 · Cited by 94 · see citing works
Treating ARID1A mutated cancers by harnessing synthetic lethality and DNA damage response
Mandal, J., Mandal, P., Wang, T.-L., & Shih, I.-M. (2022) · Journal of Biomedical Science · doi:10.1186/s12929-022-00856-5 · Cited by 84 · see citing works
The MMS22L–TONSL heterodimer directly promotes RAD51-dependent recombination upon replication stress
Piwko, W., Mlejnkova, L. J., Mutreja, K., Ranjha, L., Stafa, D., Smirnov, A., Brodersen, M. M., Zellweger, R., Sturzenegger, A., Janscak, P., et al. (2016) · The EMBO Journal · doi:10.15252/embj.201593132 · Cited by 87 · see citing works
New insights into the roles of ATM and DNA-PKcs in the cellular response to oxidative stress
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ATR/Chk1 pathway is essential for resumption of DNA synthesis and cell survival in UV-irradiated XP variant cells
Despras, E., Daboussi, F., Hyrien, O., Marheineke, K., & Kannouche, P. L. (2010) · Human Molecular Genetics · doi:10.1093/hmg/ddq046 · Cited by 80 · see citing works
Oxidative Stress, Bone Marrow Failure, and Genome Instability in Hematopoietic Stem Cells
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CHK1 as a therapeutic target to bypass chemoresistance in AML
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Human SNF5/INI1, a component of the human SWI/SNF chromatin remodeling complex, promotes nucleotide excision repair by influencing ATM recruitment and downstream H2AX phosphorylation
Ray, A., Mir, S. N., Wani, G., Zhao, Q., Battu, A., Zhu, Q., Wang, Q.-E., & Wani, A. A. (2009) · Molecular and Cellular Biology · doi:10.1128/mcb.00503-09 · Cited by 71 · see citing works
Significance of the melanocortin 1 receptor in the DNA damage response of human melanocytes to ultraviolet radiation
Swope, V., Alexander, C., Starner, R., Schwemberger, S., Babcock, G., & Abdel‐Malek, Z. A. (2014) · Pigment Cell & Melanoma Research · doi:10.1111/pcmr.12252 · Cited by 67 · see citing works
Replication protein A availability during DNA replication stress is a major determinant of cisplatin resistance in ovarian cancer cells
Bélanger, F., Fortier, E., Dubé, M., Lemay, J.-F., Buisson, R., Masson, J.-Y., Elsherbiny, A., Costantino, S., Carmona, E., Mes-Masson, A.-M., et al. (2018) · Cancer Research · doi:10.1158/0008-5472.can-18-0618 · Cited by 58 · see citing works
Lycopene inhibits Helicobacter pylori-induced ATM/ATR-dependent DNA damage response in gastric epithelial AGS cells
Jang, S. H., Lim, J. W., Morio, T., & Kim, H. (2012) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2011.11.010 · Cited by 62 · see citing works
Coordinated regulation of XPA stability by ATR and HERC2 during nucleotide excision repair
Lee, T.-H., Park, J.-M., Leem, S.-H., & Kang, T.-H. (2014) · Oncogene · doi:10.1038/onc.2012.539 · Cited by 61 · see citing works
Coupling of Human DNA Excision Repair and the DNA Damage Checkpoint in a Defined in Vitro System
Lindsey-Boltz, L. A., Kemp, M. G., Reardon, J. T., DeRocco, V., Iyer, R. R., Modrich, P., & Sancar, A. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.542787 · Cited by 59 · see citing works
Defining the Contribution of MC1R Physiological Ligands to ATR Phosphorylation at Ser435, a Predictor of DNA Repair in Melanocytes
Jarrett, S. G., Wolf Horrell, E. M., Boulanger, M. C., & D'Orazio, J. A. (2015) · Journal of Investigative Dermatology · doi:10.1038/jid.2015.280 · Cited by 54 · see citing works
Nucleotide excision repair-dependent DNA double-strand break formation and ATM signaling activation in mammalian quiescent cells
Wakasugi, M., Sasaki, T., Matsumoto, M., Nagaoka, M., Inoue, K., Inobe, M., Horibata, K., Tanaka, K., & Matsunaga, T. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.589747 · Cited by 48 · see citing works
Significance of the melanocortin 1 and endothelin B receptors in melanocyte homeostasis and prevention of sun-induced genotoxicity
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Progeroid Syndromes and UV-Induced Oxidative DNA Damage
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Authors: Cimprich, K. A., & Cortez, D.
Affiliations: Stanford Medicine (US)
Vanderbilt University (US)
ORCID: Cimprich, Karlene A.
Cortez, David
Venue: Nature Reviews Molecular Cell Biology
Publisher: Springer Science and Business Media LLC
Published: 2008-07-02
Volume: 9
Issue: 8
Pages: 616-627
ISSN: 1471-0072 (ISSN-L)
1471-0080
DOI: 10.1038/nrm2450
PMC: PMC2663384
OpenAlex: W1967630574
Cited by: 1,798
References: 189
Citations by year: 2026: 55 · 2025: 63 · 2024: 67 · 2023: 86 · 2022: 67 · 2021: 98 · 2020: 102 · 2019: 67 · 2018: 87 · 2017: 106 · 2016: 105 · 2015: 130 · 2014: 144 · 2013: 134 · 2012: 127
FWCI: 9.25
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature Reviews Molecular Cell Biology (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Cancer Institute (R01CA102729, R21CA132010)
National Institute of General Medical Sciences (R01GM099825, R01GM067735)
National Institute of Environmental Health Sciences (R01ES016486)
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 › Protein Kinase Regulation and GTPase Signaling
Keywords: ATR kinase, ATM kinase, DNA damage response, genome stability, DNA replication, cell cycle regulation, DNA repair, apoptosis, protein phosphorylation, ataxia telangiectasia
MeSH terms: Animals, Carrier Proteins, DNA Damage, DNA-Binding Proteins, Humans, Models, Biological, Nuclear Proteins, Protein Processing, Post-Translational, Signal Transduction, Protein Serine-Threonine Kinases, Cell Cycle Proteins, Genomic Instability, Ataxia Telangiectasia Mutated Proteins

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ATR: an essential regulator of genome integrity

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