Cited by 318DNA Repair MechanismsCancer-related Molecular PathwaysMicrotubule and mitosis dynamics

The DOI matches its Crossref record; 70 of the 72 references it cites were found in a registry or an index.

Distinct but Concerted Roles of ATR, DNA-PK, and Chk1 in Countering Replication Stress during S Phase

Open access

Buisson, Rémi, Boisvert, Jessica L., Benes, Cyril H., Zou, Lee·2015·Molecular Cell

DOI 10.1016/j.molcel.2015.07.029PMC PMC4575890

Open this paper in CoChat — free account Open PDF

Abstract

The ATR-Chk1 pathway is critical for DNA damage responses and cell-cycle progression. Chk1 inhibition is more deleterious to cycling cells than ATR inhibition, raising questions about ATR and Chk1 functions in the absence of extrinsic replication stress. Here we show that a key role of ATR in S phase is to coordinate RRM2 accumulation and origin firing. ATR inhibitor (ATRi) induces massive ssDNA accumulation and replication catastrophe in a fraction of early S-phase cells. In other S-phase cells, however, ATRi induces moderate ssDNA and triggers a DNA-PK and Chk1-mediated backup pathway to suppress origin firing. The backup pathway creates a threshold such that ATRi selectively kills cells under high replication stress, whereas Chk1 inhibitor induces cell death at a lower threshold. The levels of ATRi-induced ssDNA correlate with ATRi sensitivity in a panel of cell lines, suggesting that ATRi-induced ssDNA could be predictive of ATRi sensitivity in cancer cells.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1016/j.molcel.2015.07.029

Cites

70 of 70 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Lessons from hereditary colorectal cancer
Kinzler, K. W., & Vogelstein, B. (1996) · Cell · doi:10.1016/s0092-8674(00)81333-1 · Cited by 4,919
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
Sensing DNA Damage Through ATRIP Recognition of RPA-ssDNA Complexes
Zou, L., & Elledge, S. J. (2003) · Science · doi:10.1126/science.1083430 · Cited by 2,693
Self-citation
DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis
Bartkova, J., Hořejší, Z., Koed, K., Krämer, A., Tort, F., Zieger, K., Guldberg, P., Sehested, M., Nesland, J. M., Lukas, C., et al. (2005) · Nature · doi:10.1038/nature03482 · Cited by 2,688
Causes and consequences of replication stress
Zeman, M. K., & Cimprich, K. A. (2014) · Nature Cell Biology · doi:10.1038/ncb2897 · Cited by 2,079
Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions
Gorgoulis, V. G., Vassiliou, L.-V. F., Karakaidos, P., Zacharatos, P., Kotsinas, A., Liloglou, T., Venere, M., DiTullio, R. A., Kastrinakis, N. G., Levy, B., et al. (2005) · Nature · doi:10.1038/nature03485 · Cited by 2,009
An inhibitor of NEDD8-activating enzyme as a new approach to treat cancer
Soucy, T. A., Smith, P. G., Milhollen, M. A., Berger, A. J., Gavin, J. M., Adhikari, S., Brownell, J. E., Burke, K. E., Cardin, D. P., Critchley, S., et al. (2009) · Nature · doi:10.1038/nature07884 · Cited by 1,990
Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints
Bartkova, J., Rezaei, N., Liontos, M., Karakaidos, P., Kletsas, D., Issaeva, N., Vassiliou, L.-V. F., Kolettas, E., Niforou, K., Zoumpourlis, V. C., et al. (2006) · Nature · doi:10.1038/nature05268 · Cited by 1,986
ATR: an essential regulator of genome integrity
Cimprich, K. A., & Cortez, D. (2008) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2450 · Cited by 1,798
Chk1 is an essential kinase that is regulated by Atr and required for the G 2 /M DNA damage checkpoint
Liu, Q., Guntuku, S., Cui, X.-S., Matsuoka, S., Cortez, D., Tamai, K., Luo, G., Carattini-Rivera, S., DeMayo, F., Bradley, A., et al. (2000) · Genes & Development · doi:10.1101/gad.14.12.1448 · Cited by 1,625

Flagged first, then by citations

Show all 72 references

2 of the 72 references couldn’t be matched to a known paper.

Sorted by citations

ATM, ATR, and DNA-PK: The Trinity at the Heart of the DNA Damage Response
Blackford, A. N., & Jackson, S. P. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.05.015 · Cited by 2,050
Targeting the DNA Damage Response in Cancer
O’Connor, M. J. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.10.040 · Cited by 1,602
The essential kinase ATR: ensuring faithful duplication of a challenging genome
Saldivar, J. C., Cortez, D., & Cimprich, K. A. (2017) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2017.67 · Cited by 866
Targeting DNA Repair in Cancer: Beyond PARP Inhibitors
Brown, J. S., O’Carrigan, B., Jackson, S. P., & Yap, T. A. (2016) · Cancer Discovery · doi:10.1158/2159-8290.cd-16-0860 · Cited by 642
Hallmarks of DNA replication stress
Saxena, S., & Zou, L. (2022) · Molecular Cell · doi:10.1016/j.molcel.2022.05.004 · Cited by 486
Self-citation
Mechanisms of Oncogene-Induced Replication Stress: Jigsaw Falling into Place
Kotsantis, P., Petermann, E., & Boulton, S. J. (2018) · Cancer Discovery · doi:10.1158/2159-8290.cd-17-1461 · Cited by 416
ATR/CHK1 inhibitors and cancer therapy
Qiu, Z., Oleinick, N. L., & Zhang, J. (2017) · Radiotherapy and Oncology · doi:10.1016/j.radonc.2017.09.043 · Cited by 390
Therapy resistance: opportunities created by adaptive responses to targeted therapies in cancer
Labrie, M., Brugge, J. S., Mills, G. B., & Zervantonakis, I. K. (2022) · Nature reviews. Cancer · doi:10.1038/s41568-022-00454-5 · Cited by 410
AZD7648 is a potent and selective DNA-PK inhibitor that enhances radiation, chemotherapy and olaparib activity
Fok, J. H. L., Ramos‐Montoya, A., Vázquez–Chantada, M., Wijnhoven, P. W. G., Follia, V., James, N. H., Farrington, P. M., Karmokar, A., Willis, S. E., Cairns, J., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-12836-9 · Cited by 352
Targeting ATR in cancer
Lecona, E., & Fernández-Capetillo, Ó. (2018) · Nature reviews. Cancer · doi:10.1038/s41568-018-0034-3 · Cited by 341
A mitosis-specific and R loop–driven ATR pathway promotes faithful chromosome segregation
Kabeche, L., Nguyen, H. D., Buisson, R., & Zou, L. (2017) · Science · doi:10.1126/science.aan6490 · Cited by 317
Self-citation
The impact of replication stress on replication dynamics and DNA damage in vertebrate cells
Técher, H., Koundrioukoff, S., Nicolas, A. G., & Debatisse, M. (2017) · Nature Reviews Genetics · doi:10.1038/nrg.2017.46 · Cited by 287
PRIMPOL-Mediated Adaptive Response Suppresses Replication Fork Reversal in BRCA-Deficient Cells
Quinet, A., Tirman, S., Jackson, J., Šviković, S., Lemacon, D. S., Carvajal-Maldonado, D., González‐Acosta, D., Vessoni, A. T., Cybulla, E., Wood, M. D., et al. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.10.008 · Cited by 273
Sequential Therapy with PARP and WEE1 Inhibitors Minimizes Toxicity while Maintaining Efficacy
Fang, Y., McGrail, D. J., Sun, C., Labrie, M., Chen, X., Zhang, D., Ju, Z., Vellano, C. P., Lu, Y., Li, Y., et al. (2019) · Cancer Cell · doi:10.1016/j.ccell.2019.05.001 · Cited by 242
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 245
Exploiting DNA Replication Stress for Cancer Treatment
Ubhi, T., & Brown, G. W. (2019) · Cancer Research · doi:10.1158/0008-5472.can-18-3631 · Cited by 245
Biomarker-Guided Development of DNA Repair Inhibitors
Cleary, J. M., Aguirre, A. J., Shapiro, G. I., & D’Andrea, A. D. (2020) · Molecular Cell · doi:10.1016/j.molcel.2020.04.035 · Cited by 239
ATM, ATR and DNA-PKcs kinases—the lessons from the mouse models: inhibition ≠ deletion
Menolfi, D., & Zha, S. (2020) · Cell & Bioscience · doi:10.1186/s13578-020-0376-x · Cited by 227
Nucleotide imbalance decouples cell growth from cell proliferation
Diehl, F. F., Miettinen, T. P., Elbashir, R., Nabel, C. S., Darnell, A. M., Do, B. T., Manalis, S. R., Lewis, C. A., & Heiden, M. G. V. (2022) · Nature Cell Biology · doi:10.1038/s41556-022-00965-1 · Cited by 218
DNA repair defects in cancer and therapeutic opportunitiesPreprint
Hopkins, J. L., Lan, L., & Zou, L. (2022) · Genes & Development · doi:10.1101/gad.349431.122 · Cited by 212
Self-citation
A Genome-wide CRISPR Screen Identifies CDC25A as a Determinant of Sensitivity to ATR Inhibitors
Ruiz, S., Mayor‐Ruiz, C., Lafarga, V., Murga, M., Vega-Sendino, M., Ortega, S., & Fernández-Capetillo, Ó. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.03.006 · Cited by 202
Overcoming Platinum and PARP-Inhibitor Resistance in Ovarian Cancer
McMullen, M., Karakasis, K., Madariaga, A., & Oza, A. M. (2020) · Cancers · doi:10.3390/cancers12061607 · Cited by 199
Mechanisms for stalled replication fork stabilization: new targets for synthetic lethality strategies in cancer treatments
Liao, H., Ji, F., Helleday, T., & Ying, S. (2018) · EMBO Reports · doi:10.15252/embr.201846263 · Cited by 197
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 178
Self-citation
Checkpoint Responses to DNA Double-Strand Breaks
Waterman, D. P., Haber, J. E., & Smolka, M. B. (2020) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-011520-104722 · Cited by 184
DNA damage response inhibitors: Mechanisms and potential applications in cancer therapy
Carrassa, L., & Damia, G. L. M. (2017) · Cancer Treatment Reviews · doi:10.1016/j.ctrv.2017.08.013 · Cited by 178
Defining and Modulating ‘BRCAness’
Byrum, A. K., Vindigni, A., & Mosammaparast, N. (2019) · Trends in Cell Biology · doi:10.1016/j.tcb.2019.06.005 · Cited by 164
DNA-PKcs: A Multi-Faceted Player in DNA Damage Response
Yue, X., Bai, C., Xie, D., Ma, T., & Zhou, P. (2020) · Frontiers in Genetics · doi:10.3389/fgene.2020.607428 · Cited by 170
Targeting the replication stress response in cancer
Forment, J. V., & O’Connor, M. J. (2018) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2018.03.005 · Cited by 161
DNA Replication Stress and Chromosomal Instability: Dangerous Liaisons
Wilhelm, T., Said, M., & Naim, V. (2020) · Genes · doi:10.3390/genes11060642 · Cited by 161
Cancer-Specific Synthetic Lethality between ATR and CHK1 Kinase Activities
Sanjiv, K., Hagenkort, A., Calderón‐Montaño, J. M., Koolmeister, T., Reaper, P. M., Mortusewicz, O., Jacques, S. A., Kuiper, R., Schultz, N., Scobie, M., et al. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.12.032 · Cited by 147
ATR Protects the Genome against R Loops through a MUS81-Triggered Feedback Loop
Matos, D. A., Zhang, J., Ouyang, J., Nguyen, H. D., Genois, M., & Zou, L. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.10.010 · Cited by 149
Self-citation
Hydroxyurea—The Good, the Bad and the Ugly
Musiałek, M. W., & Rybaczek, D. (2021) · Genes · doi:10.3390/genes12071096 · Cited by 140
cGAS suppresses genomic instability as a decelerator of replication forks
Chen, H., Chen, H., Zhang, J., Wang, Y., Simoneau, A., Yang, H., Levine, A. S., Zou, L., Chen, Z. J., & Lan, L. (2020) · Science Advances · doi:10.1126/sciadv.abb8941 · Cited by 146
Self-citation
Leveraging the replication stress response to optimize cancer therapy
Cybulla, E., & Vindigni, A. (2022) · Nature reviews. Cancer · doi:10.1038/s41568-022-00518-6 · Cited by 144
Targeting DNA repair pathway in cancer: Mechanisms and clinical application
Wang, M., Chen, S., & Ao, D. (2021) · MedComm · doi:10.1002/mco2.103 · Cited by 140
APOBEC3A and APOBEC3B Activities Render Cancer Cells Susceptible to ATR Inhibition
Buisson, R., Lawrence, M. S., Benes, C. H., & Zou, L. (2017) · Cancer Research · doi:10.1158/0008-5472.can-16-3389 · Cited by 132
Self-citation
The synthetic lethality of targeting cell cycle checkpoints and PARPs in cancer treatment
Li, S., Wang, L., Wang, Y., Zhang, C., Hong, Z., & Han, Z. (2022) · Journal of Hematology & Oncology · doi:10.1186/s13045-022-01360-x · Cited by 141
Discovery of ATR kinase inhibitor berzosertib (VX-970, M6620): Clinical candidate for cancer therapy
Górecki, L., Andrš, M., Řezáčová, M., & Korábečný, J. (2020) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2020.107518 · Cited by 123
Synthetically Lethal Interactions of ATM, ATR, and DNA-PKcs
Kantidze, O. L., Velichko, A. K., Luzhin, A. V., Petrova, N. V., & Razin, S. V. (2018) · Trends in cancer · doi:10.1016/j.trecan.2018.09.007 · Cited by 112
Camonsertib in DNA damage response-deficient advanced solid tumors: phase 1 trial results
Yap, T. A., Fontana, E., Lee, E. K., Spigel, D. R., Højgaard, M., Lheureux, S., Mettu, N. B., Carneiro, B. A., Carter, L., Plummer, R., et al. (2023) · Nature Medicine · doi:10.1038/s41591-023-02399-0 · Cited by 123
Improving anticancer drug development begins with cell culture: misinformation perpetrated by the misuse of cytotoxicity assays
Eastman, A. R. (2016) · Oncotarget · doi:10.18632/oncotarget.12673 · Cited by 115
Mechanisms by which HPV Induces a Replication Competent Environment in Differentiating Keratinocytes
Moody, C. A. (2017) · Viruses · doi:10.3390/v9090261 · Cited by 121
ATM Deficiency Generating Genomic Instability Sensitizes Pancreatic Ductal Adenocarcinoma Cells to Therapy-Induced DNA Damage
Perkhofer, L., Schmitt, A., Carrasco, M. C. R., Ihle, M., Hampp, S., Ruess, D. A., Heßmann, E., Russell, R., Lechel, A., Azoitei, N., et al. (2017) · Cancer Research · doi:10.1158/0008-5472.can-17-0634 · Cited by 113
The ATR Inhibitor AZD6738 Synergizes with Gemcitabine In Vitro and In Vivo to Induce Pancreatic Ductal Adenocarcinoma Regression
Wallez, Y., Dunlop, C. R., Johnson, T. I., Koh, S., Fornari, C., Yates, J. W. T., Fernández, S. B. D. Q., Lau, A., Richards, F. M., & Jodrell, D. I. (2018) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-18-0010 · Cited by 114
CARM1 regulates replication fork speed and stress response by stimulating PARP1
Genois, M., Gagné, J., Yasuhara, T., Jackson, J., Saxena, S., Langelier, M.-F., Ahel, I., Bedford, M. T., Pascal, J. M., Vindigni, A., et al. (2021) · Molecular Cell · doi:10.1016/j.molcel.2020.12.010 · Cited by 114
Self-citation
A consensus set of genetic vulnerabilities to ATR inhibition
Hustedt, N., Álvarez-Quilón, A., McEwan, A., Yuan, J. Y., Cho, T., Koob, L., Hart, T., & Durocher, D. (2019) · Open Biology · doi:10.1098/rsob.190156 · Cited by 107
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 119
Participation of the ATR/CHK1 pathway in replicative stress targeted therapy of high-grade ovarian cancer
Gralewska, P., Gajek, A., Marczak, A., & Rogalska, A. (2020) · Journal of Hematology & Oncology · doi:10.1186/s13045-020-00874-6 · Cited by 107
Clinical Candidates Targeting the ATR–CHK1–WEE1 Axis in Cancer
Górecki, L., Andrš, M., & Korábečný, J. (2021) · Cancers · doi:10.3390/cancers13040795 · Cited by 107
Integrative multi-omics networks identify PKCδ and DNA-PK as master kinases of glioblastoma subtypes and guide targeted cancer therapy
Migliozzi, S., Oh, Y. T., Hasanain, M., Garofano, L., D’Angelo, F., Najac, R. D., Pïcca, A., Bielle, F., Stefano, A. L. D., Lerond, J., et al. (2023) · Nature Cancer · doi:10.1038/s43018-022-00510-x · Cited by 102
Efficient Pre-mRNA Cleavage Prevents Replication-Stress-Associated Genome Instability
Teloni, F., Michelena, J., Lezaja, A., Kilic, S., Ambrosi, C. M., Menon, S., Dobrovolná, J., Imhof, R., Janščák, P., Baubec, T., et al. (2019) · Molecular Cell · doi:10.1016/j.molcel.2018.11.036 · Cited by 97
Targeting the replication stress response through synthetic lethal strategies in cancer medicine
Ngoi, N. Y. L., Pham, M. M., Tan, D. S. P., & Yap, T. A. (2021) · Trends in cancer · doi:10.1016/j.trecan.2021.06.002 · Cited by 95
Inhibition of the ATR–CHK1 Pathway in Ewing Sarcoma Cells Causes DNA Damage and Apoptosis via the CDK2-Mediated Degradation of RRM2
Koppenhafer, S. L., Goss, K. L., Terry, W. W., & Gordon, D. J. (2019) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-19-0585 · Cited by 96
Ca2+-Stimulated AMPK-Dependent Phosphorylation of Exo1 Protects Stressed Replication Forks from Aberrant Resection
Li, S., Lavagnino, Z., Lemacon, D. S., Kong, L., Ustione, A., Ng, X. W., Zhang, Y., Wang, Y., Zheng, B., Piwnica-Worms, H. M., et al. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.04.003 · Cited by 90
Linker histone H1 prevents R-loop accumulation and genome instability in heterochromatin
Bayona‐Feliú, A., Casas-Lamesa, A., Reina, Ó., Bernués, J., & Azorı́n, F. (2017) · Nature Communications · doi:10.1038/s41467-017-00338-5 · Cited by 90
Signaling from Mus81-Eme2-Dependent DNA Damage Elicited by Chk1 Deficiency Modulates Replication Fork Speed and Origin Usage
Técher, H., Koundrioukoff, S., Carignon, S., Wilhelm, T., Millot, G. A., Lopez, B. S., Brison, O., & Debatisse, M. (2016) · Cell Reports · doi:10.1016/j.celrep.2015.12.093 · Cited by 88
RP-3500: A Novel, Potent, and Selective ATR Inhibitor that is Effective in Preclinical Models as a Monotherapy and in Combination with PARP Inhibitors
Roulston, A., Zimmermann, M., Papp, R., Skeldon, A. M., Pellerin, C., Dumas-Bérube, É., Dumais, V., Dorich, S., Fader, L. D., Fournier, S., et al. (2021) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-21-0615 · Cited by 86
Acetylation regulates ribonucleotide reductase activity and cancer cell growth
Chen, G., Luo, Y., Warncke, K., Sun, Y., Yu, D. S., Fu, H., Behera, M., Ramalingam, S. S., Doetsch, P. W., Duong, D. M., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-11214-9 · Cited by 82
A Surveillance Mechanism Ensures Repair of DNA Lesions during Zygotic Reprogramming
Ladstätter, S., & Tachibana-Konwalski, K. (2016) · Cell · doi:10.1016/j.cell.2016.11.009 · Cited by 77
53BP1 and BRCA1 control pathway choice for stalled replication restart
Xu, Y., Ning, S., Zheng, W., Xu, R., Xu, X., Xing, M., Guo, R., & Xu, D. (2017) · eLife · doi:10.7554/elife.30523 · Cited by 79
SLFN11 promotes CDT1 degradation by CUL4 in response to replicative DNA damage, while its absence leads to synthetic lethality with ATR/CHK1 inhibitors
Jo, U., Murai, Y., Chakka, S., Chen, L., Cheng, K. C.-C., Murai, J., Saha, L. K., Jenkins, L. M. M., & Pommier, Y. G. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2015654118 · Cited by 76
An extending ATR–CHK1 circuitry: the replication stress response and beyond
Simoneau, A., & Zou, L. (2021) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2021.07.003 · Cited by 74
Self-citation
Identification of a Molecularly-Defined Subset of Breast and Ovarian Cancer Models that Respond to WEE1 or ATR Inhibition, Overcoming PARP Inhibitor Resistance
Serra, V., Wang, A. T., Castroviejo‐Bermejo, M., Polanska, U. M., Palafox, M., Herencia-Ropero, A., Jones, G. N., Lai, Z., Armenia, J., Michopoulos, F., et al. (2022) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-22-0568 · Cited by 74
Targeting Wee1 kinase as a therapeutic approach in Hematological Malignancies
Vakili‐Samiani, S., Jalil, A. T., Abdelbasset, W. K., Yumashev, A. V., Karpisheh, V., Jalali, P., Adibfar, S., Ahmadi, M., Feizi, A. A. H., & Jadidi‐Niaragh, F. (2021) · DNA repair · doi:10.1016/j.dnarep.2021.103203 · Cited by 74
Targeting the kinase activities of ATR and ATM exhibits antitumoral activity in mouse models of MLL -rearranged AML
Morgado-Palacin, I., Day, A., Murga, M., Lafarga, V., Antón, M. E., Tubbs, A., Chen, H.-T., Ergen, A. V., Anderson, R., Bhandoola, A., et al. (2016) · Science Signaling · doi:10.1126/scisignal.aad8243 · Cited by 73
Key Proteins of Replication Stress Response and Cell Cycle Control as Cancer Therapy Targets
Khamidullina, A. I., Abramenko, Y. E., Bruter, A. V., & Tatarskiy, V. V. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25021263 · Cited by 73
Modulation of the DNA damage response during the life cycle of human papillomaviruses
Anacker, D. C., & Moody, C. A. (2016) · Virus Research · doi:10.1016/j.virusres.2016.11.006 · Cited by 70
A patient-derived-xenograft platform to study BRCA-deficient ovarian cancers
George, E. M., Kim, H., Krepler, C., Wenz, B. M., Makvandi, M., Tanyi, J. L., Brown, E. J., Zhang, R., Brafford, P. A., Jean, S., et al. (2017) · JCI Insight · doi:10.1172/jci.insight.89760 · Cited by 71
53BP1 Mediates ATR-Chk1 Signaling and Protects Replication Forks under Conditions of Replication Stress
Her, J., Ray, C., Altshuler, J., Zheng, H., & Bunting, S. F. (2018) · Molecular and Cellular Biology · doi:10.1128/mcb.00472-17 · Cited by 70
Differential Activity of ATR and WEE1 Inhibitors in a Highly Sensitive Subpopulation of DLBCL Linked to Replication Stress
Young, L. A., O’Connor, L. O., de Renty, C., Veldman-Jones, M. H., Dorval, T., Wilson, Z., Jones, D. R., Lawson, D., Odedra, R., Maya‐Mendoza, A., et al. (2019) · Cancer Research · doi:10.1158/0008-5472.can-18-2480 · Cited by 71
S-phase checkpoint regulations that preserve replication and chromosome integrity upon dNTP depletion
Giannattasio, M., & Branzei, D. (2017) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-017-2474-4 · Cited by 67
ATR inhibition facilitates targeting of leukemia dependence on convergent nucleotide biosynthetic pathways
Le, T. M., Poddar, S., Capri, J. R., Abt, E. R., Kim, W., Liu, W., Uong, N. T., Cheng, C., Braas, D., Nikanjam, M., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-00221-3 · Cited by 67
Radiation-dose-dependent functional synergisms between ATM, ATR and DNA-PKcs in checkpoint control and resection in G2-phase
Mladenov, E., Fan, X., Dueva, R., Soni, A., & Iliakis, G. E. (2019) · Scientific Reports · doi:10.1038/s41598-019-44771-6 · Cited by 67
ATR promotes clearance of damaged DNA and damaged cells by rupturing micronuclei
Joo, Y. K., Black, E. M., Trier, I., Haakma, W. E., Zou, L., & Kabeche, L. (2023) · Molecular Cell · doi:10.1016/j.molcel.2023.09.003 · Cited by 69
Self-citation
Sustained E2F-Dependent Transcription Is a Key Mechanism to Prevent Replication-Stress-Induced DNA Damage
Bertoli, C., Herlihy, A. E., Pennycook, B. R., Kriston-Vizi, J., & de Bruin, R. A. M. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.04.036 · Cited by 67
Checkpoint Kinase Rad53 Couples Leading- and Lagging-Strand DNA Synthesis under Replication Stress
Gan, H., Yu, C., Devbhandari, S., Sharma, S., Han, J., Chabes, A., Remus, D., & Zhang, Z. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.09.018 · Cited by 62
A wake-up call for cancer DNA damage: the role of Schlafen 11 (SLFN11) across multiple cancers
Zhang, B., Ramkumar, K., Cardnell, R. J., Gay, C. M., Stewart, C. A., Wang, W., Fujimoto, J., Wistuba, I. I., & Byers, L. A. (2021) · British Journal of Cancer · doi:10.1038/s41416-021-01476-w · Cited by 61
Mec1 Is Activated at the Onset of Normal S Phase by Low-dNTP Pools Impeding DNA Replication
Forey, R., Poveda, A., Sharma, S., Barthe, A., Padioleau, I., Renard, C., Lambert, R., Skrzypczak, M., Ginalski, K., Lengronne, A., et al. (2019) · Molecular Cell · doi:10.1016/j.molcel.2020.02.021 · Cited by 64
HPV31 utilizes the ATR-Chk1 pathway to maintain elevated RRM2 levels and a replication-competent environment in differentiating Keratinocytes
Anacker, D. C., Aloor, H. L., Shepard, C., Lenzi, G. M., Johnson, B. A., Kim, B., & Moody, C. A. (2016) · Virology · doi:10.1016/j.virol.2016.09.028 · Cited by 58
Mechanisms responsible for the synergistic antileukemic interactions between ATR inhibition and cytarabine in acute myeloid leukemia cells
Ma, J., Li, X., Su, Y., Zhao, J., Luedtke, D. A., Epshteyn, V., Edwards, H. J., Wang, G., Wang, Z., Chu, R. L., et al. (2017) · Scientific Reports · doi:10.1038/srep41950 · Cited by 60
hDNA2 nuclease/helicase promotes centromeric DNA replication and genome stability
Li, Z., Liu, B., Jin, W., Wu, X., Zhou, M., Liu, V., Goel, A., Shen, Z., Zheng, L., & Shen, B. (2018) · The EMBO Journal · doi:10.15252/embj.201796729 · Cited by 59
Checkpoint Kinase 1 Inhibition Enhances Cisplatin Cytotoxicity and Overcomes Cisplatin Resistance in SCLC by Promoting Mitotic Cell Death
Hsu, W., Zhao, X., Zhu, J., Kim, I., Rao, G., McCutcheon, J. N., Hsu, S.-T., Teicher, B. A., Kallakury, B., Dowlati, A., et al. (2019) · Journal of Thoracic Oncology · doi:10.1016/j.jtho.2019.01.028 · Cited by 59
A landscape of response to drug combinations in non-small cell lung cancer
Nair, N. U., Greninger, P., Zhang, X., Friedman, A. A., Amzallag, A., Cortez, E., Sahu, A. D., Lee, J. S., Dastur, A., Egan, R. K., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-39528-9 · Cited by 63
Self-citation
E2F1 proteolysis via SCF‐cyclin F underlies synthetic lethality between cyclin F loss and Chk1 inhibition
Burdová, K., Yang, H., Faedda, R., Hume, S., Chauhan, J. S., Ebner, D. V., Kessler, B. M., Vendrell, I., Drewry, D. H., Wells, C. I., et al. (2019) · The EMBO Journal · doi:10.15252/embj.2018101443 · Cited by 54
Combined ATR and DNA-PK Inhibition Radiosensitizes Tumor Cells Independently of Their p53 Status
Hafsi, H., Dillon, M. T., Barker, H. E., Kyula, J., Schick, U., Paget, J. T.-E. H., Smith, H. G., Pedersen, M., McLaughlin, M., & Harrington, K. J. (2018) · Frontiers in Oncology · doi:10.3389/fonc.2018.00245 · Cited by 53
Harnessing DNA Replication Stress for Novel Cancer Therapy
Zhu, H., Swami, U., Preet, R., & Zhang, J. (2020) · Genes · doi:10.3390/genes11090990 · Cited by 56
Progerin sequestration of PCNA promotes replication fork collapse and mislocalization of XPA in laminopathy‐related progeroid syndromes
Hilton, B. A., Liu, J., Cartwright, B. M., Liu, Y., Breitman, M., Wang, Y., Jones, R., Tang, H., Rusinol, A., Musich, P. R., et al. (2017) · The FASEB Journal · doi:10.1096/fj.201700014r · Cited by 52
Replication Stress Defines Distinct Molecular Subtypes Across Cancers
Takahashi, N., Kim, S. H., Schultz, C. W., Rajapakse, V. N., Zhang, Y., Redon, C. E., Fu, H., Pongor, L. S., Kumar, S., Pommier, Y. G., et al. (2021) · Cancer Research Communications · doi:10.1158/2767-9764.crc-22-0168 · Cited by 64
ATR-mediated proteome remodeling is a major determinant of homologous recombination capacity in cancer cells
Kim, D.-S., Liu, Y., Oberly, S., Freire, R., & Smolka, M. B. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky625 · Cited by 53
Impact of Replication Stress in Human Papillomavirus Pathogenesis
Moody, C. A. (2018) · Journal of Virology · doi:10.1128/jvi.01012-17 · Cited by 50
SMARCA4 deficiency-associated heterochromatin induces intrinsic DNA replication stress and susceptibility to ATR inhibition in lung adenocarcinoma
Kurashima, K., Kashiwagi, H., Shimomura, I., Suzuki, A., Takeshita, F., Mazevet, M., Harata, M., Yamashita, T., Yamamoto, Y., Kohno, T., et al. (2020) · NAR Cancer · doi:10.1093/narcan/zcaa005 · Cited by 53
MMB-FOXM1-driven premature mitosis is required for CHK1 inhibitor sensitivity
Branigan, T. B., Kozono, D., Schade, A. E., Deraska, P. V., Rivas, H. G., Sambel, L. A., Reavis, H. D., Shapiro, G. I., D’Andrea, A. D., & DeCaprio, J. A. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.108808 · Cited by 48
Kinase-dead ATR differs from ATR loss by limiting the dynamic exchange of ATR and RPA
Menolfi, D., Jiang, W., Lee, B. J., Moiseeva, T. N., Shao, Z., Estes, V. M., Frattini, M. G., Bakkenist, C. J., & Zha, S. (2018) · Nature Communications · doi:10.1038/s41467-018-07798-3 · Cited by 50
RRM2 enhances MYCN-driven neuroblastoma formation and acts as a synergistic target with CHK1 inhibition
Nunes, C., Depestel, L., Mus, L. M., Keller, K. M., Delhaye, L., Louwagie, A., Rishfi, M., Whale, A. J., Kara, N., Andrews, S., et al. (2022) · Science Advances · doi:10.1126/sciadv.abn1382 · Cited by 51
The mTOR pathway: Implications for DNA replication
Lamm, N., Rogers, S., & Cesare, A. J. (2019) · Progress in Biophysics and Molecular Biology · doi:10.1016/j.pbiomolbio.2019.04.002 · Cited by 51
Co-regulation and function of FOXM1/RHNO1 bidirectional genes in cancer
Barger, C. J., Chee, L., Albahrani, M., Muñoz-Trujillo, C., Boghean, L., Branick, C., Odunsi, K. O., Drapkin, R., Zou, L., & Karpf, A. R. (2021) · eLife · doi:10.7554/elife.55070 · Cited by 46
Self-citation
ATR protects ongoing and newly assembled DNA replication forks through distinct mechanisms
Leung, W., Simoneau, A., Saxena, S., Jackson, J., Patel, P. S., Limbu, M., Vindigni, A., & Zou, L. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112792 · Cited by 45
Self-citation
Inhibition of ATR acutely sensitizes acute myeloid leukemia cells to nucleoside analogs that target ribonucleotide reductase
Fordham, S. E., Blair, H. J., Elstob, C. J., Plummer, R., Drew, Y., Curtin, N. J., Heidenreich, O. T., Pal, D., Jamieson, D., Park, C., et al. (2018) · Blood Advances · doi:10.1182/bloodadvances.2017015214 · Cited by 45
RB1 loss overrides PARP inhibitor sensitivity driven by RNASEH2B loss in prostate cancer
Miao, C., Tsujino, T., Takai, T., Gui, F., Tsutsumi, T., Sztupinszki, Z. M., Wang, Z., Azuma, H., Szállási, Z., Mouw, K. W., et al. (2022) · Science Advances · doi:10.1126/sciadv.abl9794 · Cited by 46
Self-citation

Authors: Buisson, R., Boisvert, J. L., Benes, C. H., & Zou, L.
Affiliations: Harvard University (US)
Corresponding author: Zou, Lee
ORCID: Buisson, Rémi
Benes, Cyril H.
Zou, Lee
Venue: Molecular Cell
Publisher: Elsevier BV
Published: 2015-09
Volume: 59
Issue: 6
Pages: 1011-1024
ISSN: 1097-2765 (ISSN-L)
DOI: 10.1016/j.molcel.2015.07.029
PMC: PMC4575890
OpenAlex: W1855851918
Cited by: 316
References: 72
Citations by year: 2026: 27 · 2025: 14 · 2024: 16 · 2023: 27 · 2022: 33 · 2021: 37 · 2020: 38 · 2019: 30 · 2018: 38 · 2017: 29 · 2016: 25 · 2015: 2
FWCI: 13.61
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, 382 d)
Locations: Molecular Cell (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
eScholarship (California Digital Library) (submittedVersion)
Funders: Wellcome Trust (102696)
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 › Cell Biology › Microtubule and mitosis dynamics
Keywords: ATR, DNA-dependent protein kinase, Chk1, replication stress, S phase, DNA damage response, RRM2, replication origin firing, single-stranded DNA, replication catastrophe, cancer cell lines
MeSH terms: Checkpoint Kinase 1, DNA Damage, DNA Replication, DNA, Single-Stranded, Humans, Nuclear Proteins, Phosphorylation, Protein Kinases, Protein Processing, Post-Translational, Ribonucleoside Diphosphate Reductase, Stress, Physiological, S Phase, Replication Origin, Cell Line, Tumor, DNA-Activated Protein Kinase, Ataxia Telangiectasia Mutated Proteins

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Distinct but Concerted Roles of ATR, DNA-PK, and Chk1 in Countering Replication Stress during S Phase

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks