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

Flynn, Rachel Litman; Zou, Lee

doi:10.1016/j.tibs.2010.09.005

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

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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ATR is the main regulator of nucleotide excision repair because it detects replication and transcription stress caused by UV-induced and other bulky DNA adducts.
“Although it functions in multiple DDR processes 21 ATR is the primary regulator of the nucleotide excision repair pathway due to its ability to detect the replicative and transcriptional stresses caused by UV-induced damage and other bulky DNA adducts resulting from chemical toxins and some chemotherapeutic agents 22–25.”
From Xeroderma Pigmentosa Group A (XPA), Nucleotide Excision Repair and Regulation by ATR in Response to Ultraviolet Irradiation (2017) · cites this paper as [23]

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Phosphorylation of FANCD2 on Two Novel Sites Is Required for Mitomycin C Resistance
Ho, G. P. H., Margossian, S. P., Taniguchi, T., & D’Andrea, A. D. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.02018-05 · Cited by 118 · see citing works
ATR, Claspin and the Rad9-Rad1-Hus1 Complex Regulate Chk1 and Cdc25A in the Absence of DNA Damage
Sørensen, C. S., Syljuåsen, R. G., Lukas, J., & Bártek, J. (2004) · Cell Cycle · doi:10.4161/cc.3.7.972 · Cited by 117 · see citing works
Identification of SMARCAL1 as a Component of the DNA Damage Response
Postow, L., Woo, E. M., Chait, B. T., & Funabiki, H. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.048330 · Cited by 112 · 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
DNA Damage Signaling Recruits the Rtt107-Slx4 Scaffolds via Dpb11 to Mediate Replication Stress Response
Ohouo, P. Y., de Oliveira, F. M. B., Almeida, B. S., & Smolka, M. B. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.06.019 · Cited by 101 · see citing works
Checkpoint Signaling from a Single DNA Interstrand Crosslink
Ben‐Yehoyada, M., Wang, L. C., Kozekov, I. D., Rizzo, C. J., Gottesman, M. E., & Gautier, J. (2009) · Molecular Cell · doi:10.1016/j.molcel.2009.08.014 · Cited by 101 · see citing works
Continued primer synthesis at stalled replication forks contributes to checkpoint activation
Van, C., Yan, S., Michael, W. M., Waga, S., & Cimprich, K. A. (2010) · The Journal of Cell Biology · doi:10.1083/jcb.200909105 · Cited by 100 · see citing works
The Chk1-mediated S-phase Checkpoint Targets Initiation Factor Cdc45 via a Cdc25A/Cdk2-independent Mechanism
Liu, P., Barkley, L. R., Day, T. A., Bi, X., Slater, D., Alexandrow, M. G., Nasheuer, H., & Vaziri, C. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m602982200 · Cited by 97 · see citing works
Involvement of a chromatin remodeling complex in damage tolerance during DNA replication
Falbo, K. B., Alabert, C., Katou, Y., Wu, S., Han, J., Wehr, T. S., Xiao, J., He, X., Zhang, Z., Shi, Y., et al. (2009) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1686 · Cited by 91 · see citing works
FANCM regulates DNA chain elongation and is stabilized by S‐phase checkpoint signalling
Luke-Glaser, S., Luke, B., Grossi, S., & Constantinou, A. (2009) · The EMBO Journal · doi:10.1038/emboj.2009.371 · Cited by 91 · see citing works
ATR signaling at a glance
Shiotani, B., & Zou, L. (2009) · Journal of Cell Science · doi:10.1242/jcs.035105 · Cited by 76 · see citing works
Self-citation
Rad3ATR Decorates Critical Chromosomal Domains with γH2A to Protect Genome Integrity during S-Phase in Fission Yeast
Rozenzhak, S., Mejía-Ramírez, E., Williams, J. S., Schaffer, L., Hammond, J. A., Head, S. R., & Russell, P. R. (2010) · PLoS Genetics · doi:10.1371/journal.pgen.1001032 · Cited by 75 · see citing works
Rad17 Plays a Central Role in Establishment of the Interaction between TopBP1 and the Rad9-Hus1-Rad1 Complex at Stalled Replication Forks
Lee, J., & Dunphy, W. G. (2010) · Molecular Biology of the Cell · doi:10.1091/mbc.e09-11-0958 · Cited by 70 · see citing works
The Role of Dbf4/Drf1-Dependent Kinase Cdc7 in DNA-Damage Checkpoint Control
Tsuji, T., Lau, E. K., Chiang, G. G., & Jiang, W. B. (2008) · Molecular Cell · doi:10.1016/j.molcel.2008.12.005 · Cited by 62 · see citing works
Postreplication gaps at UV lesions are signals for checkpoint activation
Callegari, A. J., Clark, E., Pneuman, A., & Kelly, T. J. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1003449107 · Cited by 54 · see citing works
Mrc1 phosphorylation in response to DNA replication stress is required for Mec1 accumulation at the stalled fork
Naylor, M. L., Li, J.-M., Osborn, A. J., & Elledge, S. J. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0904623106 · Cited by 47 · see citing works

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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
Self-citation
DNA repair dysregulation from cancer driver to therapeutic target
Curtin, N. J. (2012) · Nature Reviews Cancer · doi:10.1038/nrc3399 · Cited by 1,051 · see citing works
Homologous Recombination Deficiency: Exploiting the Fundamental Vulnerability of Ovarian Cancer
Konstantinopoulos, P. A., Ceccaldi, R., Shapiro, G. I., & D'Andrea, A. D. (2015) · Cancer Discovery · doi:10.1158/2159-8290.cd-15-0714 · Cited by 945 · see citing works
Clinical and translational advances in ovarian cancer therapy
Konstantinopoulos, P. A., & Matulonis, U. A. (2023) · Nature Cancer · doi:10.1038/s43018-023-00617-9 · Cited by 399 · see citing works
Smarcal1-Mediated Fork Reversal Triggers Mre11-Dependent Degradation of Nascent DNA in the Absence of Brca2 and Stable Rad51 Nucleofilaments
Kolinjivadi, A. M., Sannino, V., Antoni, A. D., Zadorozhny, K., Kilkenny, M. L., Técher, H., Baldi, G., Shen, R., Ciccia, A., Pellegrini, L., et al. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.07.001 · Cited by 366 · see citing works
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
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
Self-citation
Chemotherapy induced DNA damage response: Convergence of drugs and pathways
Woods, D., & Turchi, J. J. (2013) · Cancer Biology & Therapy · doi:10.4161/cbt.23761 · Cited by 296 · 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
Self-citation
ATM and ATR signaling at a glance
Awasthi, P., Foiani, M., & Kumar, A. (2015) · Journal of Cell Science · doi:10.1242/jcs.169730 · Cited by 277 · see citing works
Molecular Pathways: Overcoming Radiation Resistance by Targeting DNA Damage Response Pathways
Morgan, M. A., & Lawrence, T. S. (2015) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-13-3229 · Cited by 252 · see citing works
PRP19 Transforms into a Sensor of RPA-ssDNA after DNA Damage and Drives ATR Activation via a Ubiquitin-Mediated Circuitry
Maréchal, A., Li, J.-M., Ji, X. Y., Wu, C.-S. P., Yazinski, S. A., Nguyen, H. D., Liu, S., Jiménez, A. E., Jin, J., & Zou, L. (2013) · Molecular Cell · doi:10.1016/j.molcel.2013.11.002 · Cited by 246 · see citing works
Self-citation
Replication Catastrophe: When a Checkpoint Fails because of Exhaustion
Toledo, L. I., Neelsen, K. J., & Lukas, J. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.05.001 · Cited by 228 · see citing works
Berzosertib plus gemcitabine versus gemcitabine alone in platinum-resistant high-grade serous ovarian cancer: a multicentre, open-label, randomised, phase 2 trial
Konstantinopoulos, P. A., Cheng, S., Hendrickson, A. E. W., Penson, R. T., Schumer, S., Doyle, L. A., Lee, E. K., Kohn, E. C., Duska, L., Crispens, M. A., et al. (2020) · The Lancet Oncology · doi:10.1016/s1470-2045(20)30180-7 · Cited by 226 · see citing works
The intersection between DNA damage response and cell death pathways.
Nowsheen, S., & Yang, E. S.-H. (2012) · PubMed · Cited by 219 · see citing works
Genotoxic Anti-Cancer Agents and Their Relationship to DNA Damage, Mitosis, and Checkpoint Adaptation in Proliferating Cancer Cells
Swift, L. H., & Golsteyn, R. M. (2014) · International Journal of Molecular Sciences · doi:10.3390/ijms15033403 · Cited by 214 · see citing works
Beyond ATM: The protein kinase landscape of the DNA damage response
Bensimon, A., Aebersold, R. H., & Shiloh, Y. (2011) · FEBS Letters · doi:10.1016/j.febslet.2011.05.013 · Cited by 206 · see citing works
ATM‐mediated phosphorylation of SOG1 is essential for the DNA damage response in Arabidopsis
Yoshiyama, K., Kobayashi, J., Ogita, N., Ueda, M., Kimura, S., Maki, H., & Umeda, M. (2013) · EMBO Reports · doi:10.1038/embor.2013.112 · Cited by 173 · see citing works
Functions, Regulation, and Therapeutic Implications of the ATR Checkpoint Pathway
Yazinski, S. A., & Zou, L. (2016) · Annual Review of Genetics · doi:10.1146/annurev-genet-121415-121658 · Cited by 173 · see citing works
Self-citation
Targeting the S and G2 checkpoint to treat cancer
Chen, T., Stephens, P., Middleton, F. K., & Curtin, N. J. (2011) · Drug Discovery Today · doi:10.1016/j.drudis.2011.12.009 · Cited by 168 · see citing works
Elucidating Role of Reactive Oxygen Species (ROS) in Cisplatin Chemotherapy: A Focus on Molecular Pathways and Possible Therapeutic Strategies
Mirzaei, S., Hushmandi, K., Zabolian, A., Saleki, H., Torabi, S. M., Ranjbar, A., SeyedSaleh, S., Sharifzadeh, S. O., Khan, H. Z., Ashrafizadeh, M., et al. (2021) · Molecules · doi:10.3390/molecules26082382 · Cited by 150 · see citing works
Genome maintenance in pluripotent stem cells
Weissbein, U., Benvenisty, N., & Ben‐David, U. (2014) · The Journal of Cell Biology · doi:10.1083/jcb.201310135 · Cited by 143 · see citing works
Trial Watch: Targeting ATM–CHK2 and ATR–CHK1 pathways for anticancer therapy
Manic, G., Obrist, F., Sistigu, A., & Vitale, I. (2015) · Molecular & Cellular Oncology · doi:10.1080/23723556.2015.1012976 · Cited by 147 · see citing works
A regulatory module controlling stress-induced cell cycle arrest in Arabidopsis
Takahashi, N., Ogita, N., Takahashi, T., Taniguchi, S., Tanaka, M., Seki, M., & Umeda, M. (2019) · eLife · doi:10.7554/elife.43944 · Cited by 134 · see citing works
Role of AKT signaling in DNA repair and clinical response to cancer therapy
Liu, Q., Turner, K. M., Yung, W. K. A., Chen, K., & Zhang, W. (2014) · Neuro-Oncology · doi:10.1093/neuonc/nou058 · Cited by 140 · see citing works
Two Distinct Modes of ATR Activation Orchestrated by Rad17 and Nbs1
Shiotani, B., Nguyen, H. D., Håkansson, P., Maréchal, A., Tse, A., Tahara, H., & Zou, L. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.04.018 · Cited by 137 · see citing works
Self-citation
Identification of small molecule proliferating cell nuclear antigen (PCNA) inhibitor that disrupts interactions with PIP-box proteins and inhibits DNA replication
Punchihewa, C., Inoue, A., Hishiki, A., Fujikawa, Y., Connelly, M., Evison, B., Shao, Y., Heath, R., Kuraoka, I., Rodrigues, P., et al. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.353201 · Cited by 135 · see citing works
HPV 5 and 8 E6 Abrogate ATR Activity Resulting in Increased Persistence of UVB Induced DNA Damage
Wallace, N. A., Robinson, K. L., Howie, H. L., & Galloway, D. A. (2012) · PLoS Pathogens · doi:10.1371/journal.ppat.1002807 · Cited by 131 · see citing works
Progress towards a clinically-successful ATR inhibitor for cancer therapy
Barnieh, F. M., Loadman, P. M., & Falconer, R. A. (2021) · Current Research in Pharmacology and Drug Discovery · doi:10.1016/j.crphar.2021.100017 · Cited by 130 · see citing works
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
Arabidopsis RETINOBLASTOMA RELATED directly regulates DNA damage responses through functions beyond cell cycle control
Horváth, B. M., Kourová, H., Nagy, S. K., Németh, E., Magyar, Z., Papdi, C., Ahmad, Z., Sanchez‐Perez, G. F., Perilli, S., Blilou, I., et al. (2017) · The EMBO Journal · doi:10.15252/embj.201694561 · Cited by 113 · see citing works
The Intra-S Checkpoint Responses to DNA Damage
Iyer, D., & Rhind, N. (2017) · Genes · doi:10.3390/genes8020074 · Cited by 113 · see citing works
Targeting ATR in patients with cancer
Ngoi, N. Y. L., Pilie, P. G., McGrail, D. J., Zimmermann, M., Schlacher, K., & Yap, T. A. (2024) · Nature Reviews Clinical Oncology · doi:10.1038/s41571-024-00863-5 · Cited by 114 · see citing works
DNA damage-induced nuclear factor-kappa B activation and its roles in cancer progression
Wang, W., Mani, A. M., & Wu, Z. (2017) · Journal of Cancer Metastasis and Treatment · doi:10.20517/2394-4722.2017.03 · Cited by 109 · see citing works
Selective Targeting of the G2/M Cell Cycle Checkpoint to Improve the Therapeutic Index of Radiotherapy
Dillon, M. T., Good, J., & Harrington, K. J. (2014) · Clinical Oncology · doi:10.1016/j.clon.2014.01.009 · Cited by 103 · see citing works
Role of Cyclin B1 Levels in DNA Damage and DNA Damage-Induced Senescence
Nakayama, Y., & Yamaguchi, N. (2013) · International review of cytology · doi:10.1016/b978-0-12-407695-2.00007-x · Cited by 101 · see citing works
Novel DNA Damage Checkpoints Mediating Cell Death Induced by the NEDD8-Activating Enzyme Inhibitor MLN4924
Blank, J. L., Liu, X. J., Cosmopoulos, K., Bouck, D. C., Garcia, K., Bernard, H., Tayber, O., Hather, G., Liu, R., Narayanan, U., et al. (2012) · Cancer Research · doi:10.1158/0008-5472.can-12-1729 · Cited by 101 · see citing works
Arabidopsis R1R2R3-Myb proteins are essential for inhibiting cell division in response to DNA damage
Chen, P., Takatsuka, H., Takahashi, N., Kurata, R., Fukao, Y., Kobayashi, K., Ito, M. A., & Umeda, M. (2017) · Nature Communications · doi:10.1038/s41467-017-00676-4 · Cited by 101 · see citing works
Repair of naturally occurring mismatches can induce mutations in flanking DNA
Chen, J., Miller, B., & Furano, A. V. (2014) · eLife · doi:10.7554/elife.02001 · Cited by 95 · see citing works
Repression of ATR pathway by miR-185 enhances radiation-induced apoptosis and proliferation inhibition
Wang, J., He, J., Su, F., Ding, N., Hu, W., Yao, B. W., Wang, W., & Zhou, G. (2013) · Cell Death and Disease · doi:10.1038/cddis.2013.227 · Cited by 92 · see citing works
Sensing R-Loop-Associated DNA Damage to Safeguard Genome Stability
Rinaldi, C., Pizzul, P., Longhese, M. P., & Bonetti, D. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.618157 · Cited by 91 · see citing works
Human CST facilitates genome-wide RAD51 recruitment to GC-rich repetitive sequences in response to replication stress
Chastain, M., Zhou, Q., Shiva, O., Fadri-Moskwik, M., Whitmore, L. S., Jia, P., Dai, X., Huang, C.-H., Ye, P., & Chai, W.-H. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.06.077 · Cited by 79 · see citing works
MiR-126 negatively regulates PLK-4 to impact the development of hepatocellular carcinoma via ATR/CHEK1 pathway
Bao, J., Yu, Y. H., Chen, J., He, Y., Chen, X., Ren, Z., Xue, C., Liu, L., Hu, Q., Li, J., et al. (2018) · Cell Death and Disease · doi:10.1038/s41419-018-1020-0 · Cited by 88 · see citing works
MicroRNA and signal transduction pathways in tumor radiation response
Zhao, L., Lu, X., & Cao, Y. (2013) · Cellular Signalling · doi:10.1016/j.cellsig.2013.04.004 · Cited by 87 · see citing works
Untangling the ATR‐CHEK1 network for prognostication, prediction and therapeutic target validation in breast cancer
Abdel-Fatah, T. M. A., Middleton, F. K., Arora, A., Agarwal, D., Chen, T., Moseley, P. M., Perry, C., Doherty, R. E., Chan, S. Y. T., Green, A. R., et al. (2014) · Molecular Oncology · doi:10.1016/j.molonc.2014.10.013 · Cited by 86 · see citing works
BRCA2 functions: from DNA repair to replication fork stabilization
Fradet‐Turcotte, A., Sitz, J., Grapton, D., & Orthwein, A. (2016) · Endocrine Related Cancer · doi:10.1530/erc-16-0297 · Cited by 82 · see citing works
Insights into a Crucial Role of TRIP13 in Human Cancer
Lu, S., Qian, J., Guo, M., Gu, C., & Yang, Y. (2019) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2019.06.005 · Cited by 83 · see citing works
Fanconi anaemia: genetics, molecular biology, and cancer – implications for clinical management in children and adults
Schneider, M., Chandler, K., Tischkowitz, M. D., & Meyer, S. (2014) · Clinical Genetics · doi:10.1111/cge.12517 · Cited by 83 · see citing works
ATM pathway activation limits R-loop-associated genomic instability in Werner syndrome cells
Marabitti, V., Lillo, G., Malacaria, E., Palermo, V., Sanchez, M., Pichierri, P., & Franchitto, A. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz025 · Cited by 78 · see citing works
DNA-damage-induced degradation of EXO1 exonuclease limits DNA end resection to ensure accurate DNA repair
Tomimatsu, N., Mukherjee, B., Harris, J. L., Boffo, F. L., Hardebeck, M. C., Potts, P. R., Khanna, K. K., & Burma, S. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.m116.772475 · Cited by 80 · see citing works
Impaired replication elongation in Tetrahymena mutants deficient in histone H3 Lys 27 monomethylationPreprint
Gao, S., Xiong, J., Zhang, C., Berquist, B. R., Yang, R., Zhao, M., Molascon, A. J., Kwiatkowski, S., Yuan, D., Qin, Z. S., et al. (2013) · Genes & Development · doi:10.1101/gad.218966.113 · Cited by 76 · see citing works
HERC2-USP20 axis regulates DNA damage checkpoint through Claspin
Yuan, J., Luo, K., Deng, M., Li, Y., Yin, P., Gao, B., Fang, Y., Wu, P., Liu, T., & Lou, Z. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku1034 · Cited by 78 · see citing works
DNA damage and repair in Parkinson's disease: Recent advances and new opportunities
González-Hunt, C. P., & Sanders, L. H. (2020) · Journal of Neuroscience Research · doi:10.1002/jnr.24592 · Cited by 77 · see citing works
DUOXA1-mediated ROS production promotes cisplatin resistance by activating ATR-Chk1 pathway in ovarian cancer
Meng, Y., Chen, C., Yung, M. M. H., Sun, W., Sun, J. F., Li, Z., Li, J., Li, Z., Zhou, W., Liu, S. S., et al. (2018) · Cancer Letters · doi:10.1016/j.canlet.2018.04.029 · Cited by 77 · see citing works
ATM and ATR signaling at a glance
Awasthi, P., Foiani, M., & Kumar, A. (2016) · Journal of Cell Science · doi:10.1242/jcs.188631 · Cited by 76 · see citing works
Nek1 kinase associates with ATR–ATRIP and primes ATR for efficient DNA damage signaling
Liu, S., Ho, C. K., Ouyang, J., & Zou, L. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1217781110 · Cited by 75 · see citing works
Self-citation
DNA damage response in renal ischemia–reperfusion and ATP-depletion injury of renal tubular cells
Ma, Z., Wei, Q., Dong, G., Huo, Y., & Dong, Z. (2014) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2014.04.002 · Cited by 76 · see citing works
Inhibiting the DNA damage response as a therapeutic manoeuvre in cancer
Curtin, N. J. (2013) · British Journal of Pharmacology · doi:10.1111/bph.12244 · Cited by 76 · see citing works
RNF20–RNF40: A ubiquitin‐driven link between gene expression and the DNA damage response
Shiloh, Y., Shema, E., Moyal, L., & Oren, M. (2011) · FEBS Letters · doi:10.1016/j.febslet.2011.07.034 · Cited by 75 · see citing works
Parvovirus B19 Infection of Human Primary Erythroid Progenitor Cells Triggers ATR-Chk1 Signaling, Which Promotes B19 Virus Replication
Luo, Y., Lou, S., Deng, X., Liu, Z., Li, Y., Kleiboeker, S. B., & Qiu, J. (2011) · Journal of Virology · doi:10.1128/jvi.00831-11 · Cited by 74 · see citing works
SUMOylation of ATRIP potentiates DNA damage signaling by boosting multiple protein interactions in the ATR pathwayPreprint
Wu, C.-S. P., Ouyang, J., Mori, E., Nguyen, H. D., Maréchal, A., Hallet, A., Chen, D. J., & Zou, L. (2014) · Genes & Development · doi:10.1101/gad.238535.114 · Cited by 73 · see citing works
Self-citation
A Replication stress biomarker is associated with response to gemcitabine versus combined gemcitabine and ATR inhibitor therapy in ovarian cancer
Konstantinopoulos, P. A., da Costa, A. A. B. A., Gulhan, D., Lee, E. K., Cheng, S., Hendrickson, A. E. W., Kochupurakkal, B. S., Kolin, D. L., Kohn, E. C., Liu, J. F., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-25904-w · Cited by 69 · see citing works
Bridging the gap between in vitro and in vivo: Dose and schedule predictions for the ATR inhibitor AZD6738
Checkley, S., MacCallum, L., Yates, J. W. T., Jasper, P., Luo, H., Tolsma, J., & Bendtsen, C. (2015) · Scientific Reports · doi:10.1038/srep13545 · Cited by 68 · see citing works
ATR–ATRIP Kinase Complex Triggers Activation of the Fanconi Anemia DNA Repair Pathway
Shigechi, T., Tomida, J., Sato, K., Kobayashi, M., Eykelenboom, J. K., Pessina, F., Zhang, Y., Uchida, E., Ishiai, M., Lowndes, N. F., et al. (2012) · Cancer Research · doi:10.1158/0008-5472.can-11-2904 · Cited by 67 · see citing works
Manipulation of cellular DNA damage repair machinery facilitates propagation of human papillomaviruses
Wallace, N. A., & Galloway, D. A. (2014) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2013.12.003 · Cited by 66 · see citing works
ATM- and ATR-Mediated Phosphorylation of XRCC3 Regulates DNA Double-Strand Break-Induced Checkpoint Activation and Repair
Somyajit, K., Basavaraju, S., Scully, R., & Nagaraju, G. (2013) · Molecular and Cellular Biology · doi:10.1128/mcb.01521-12 · Cited by 66 · see citing works
Telomere Lengthening and Other Functions of Telomerase
Rubtsova, M. P., Vasilkova, D. P., Malyavko, A. N., Нарайкина, Ю. В., Zvereva, M. I., & Донцова, О. А. (2012) · Acta Naturae · doi:10.32607/20758251-2012-4-2-44-61 · Cited by 66 · see citing works
'BRCAness' and its implications for platinum action in gynecologic cancer.
Muggia, F. M., & Safra, T. (2014) · PubMed · Cited by 65 · see citing works
Novel Functions of the Human Papillomavirus E6 Oncoproteins
Wallace, N. A., & Galloway, D. A. (2015) · Annual Review of Virology · doi:10.1146/annurev-virology-100114-055021 · Cited by 63 · see citing works
Novel regulation of checkpoint kinase 1: Is checkpoint kinase 1 a good candidate for anti‐cancer therapy?
Goto, H., Izawa, I., Li, P., & Inagaki, M. (2012) · Cancer Science · doi:10.1111/j.1349-7006.2012.02280.x · Cited by 64 · see citing works
Human CST complex protects stalled replication forks by directly blocking MRE11 degradation of nascent‐strand DNA
Lyu, X., Lei, K.-H., Sang, P. B., Shiva, O., Chastain, M., Chi, P., & Chai, W.-H. (2020) · EMBO Journal · doi:10.15252/embj.2019103654 · Cited by 54 · see citing works
Targeting the DNA Damage Response and DNA Repair Pathways to Enhance Radiosensitivity in Colorectal Cancer
Deng, S., Vlatkovic, T., Li, M., Zhan, T., Veldwijk, M. R., & Herskind, C. (2022) · Cancers · doi:10.3390/cancers14194874 · Cited by 62 · see citing works
ATM, ATR and DNA-PKcs expressions correlate to adverse clinical outcomes in epithelial ovarian cancers
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Opposing role of condensin hinge against replication protein A in mitosis and interphase through promoting DNA annealing
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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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