The DOI matches its Crossref record; 37 of the 37 references it cites were found in a registry or an index.
Sensing DNA Damage Through ATRIP Recognition of RPA-ssDNA Complexes
Abstract
The function of the ATR (ataxia-telangiectasia mutated– and Rad3-related)–ATRIP (ATR-interacting protein) protein kinase complex is crucial for the cellular response to replication stress and DNA damage. Here, we show that replication protein A (RPA), a protein complex that associates with single-stranded DNA (ssDNA), is required for the recruitment of ATR to sites of DNA damage and for ATR-mediated Chk1 activation in human cells. In vitro, RPA stimulates the binding of ATRIP to ssDNA. The binding of ATRIP to RPA-coated ssDNA enables the ATR-ATRIP complex to associate with DNA and stimulates phosphorylation of the Rad17 protein that is bound to DNA. Furthermore, Ddc2, the budding yeast homolog of ATRIP, is specifically recruited to double-strand DNA breaks in an RPA-dependent manner. A checkpoint-deficient mutant of RPA, rfa1-t11 , is defective for recruiting Ddc2 to ssDNA both in vivo and in vitro. Our data suggest that RPA-coated ssDNA is the critical structure at sites of DNA damage that recruits the ATR-ATRIP complex and facilitates its recognition of substrates for phosphorylation and the initiation of checkpoint signaling.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“ATR in complex with its nuclear binding partner ATR-interacting protein (ATRIP) binds to this RPA-coated ssDNA via an ATRIP-RPA interaction. ATRIP also serves to activate the checkpoint kinase activity of ATR 4, 27–30.”
From Xeroderma Pigmentosa Group A (XPA), Nucleotide Excision Repair and Regulation by ATR in Response to Ultraviolet Irradiation (2017) · cites this paper as [29]
In the citing paper
“In addition, during S phase, replication forks encounter the CPD and 6-4PP lesions that provoke stalling of the replication forks at the single-strand breaks (SSBs).”
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 [18]
In the citing paper
“These breaks are processed to long ssDNA, where RPA binds and initiates the recruitment of a complex array of DNA damage response (DDR) proteins, including ATRIP-ATR complex, TopBP1, MRE11, Rad50, Rad17, and 9-1-1 complex [17–19].”
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 [18]
In the citing paper
“ATR is the primary sensor of single-stranded (ssDNA) breaks (SSB) caused by UV damage and replication stress.”
From NER initiation factors, DDB2 and XPC, regulate UV radiation response by recruiting ATR and ATM kinases to DNA damage sites (2013) · cites this paper as [16]
In the citing paper
“It has been shown that DNA damage and replication intermediates increase the unwinding of DNA, leading to the accumulation of RPA-coated ss-DNA, which recruits ATR [15, 16].”
From NER initiation factors, DDB2 and XPC, regulate UV radiation response by recruiting ATR and ATM kinases to DNA damage sites (2013) · cites this paper as [16]
In the citing paper
“It has been shown that in response to UV irradiation, RPA-coated single-stranded DNA (ssDNA) recruits ATR to the UV damage site [15, 16].”
From NER initiation factors, DDB2 and XPC, regulate UV radiation response by recruiting ATR and ATM kinases to DNA damage sites (2013) · cites this paper as [16]
In the citing paper
“Given the variety of DNA lesions the cell has to deal with, it was hypothesized that the first responders, among checkpoint factors, had to be recruited to a common DNA intermediate, which was later identified as long regions of ssDNA covered by RPA [44].”
From Mind the gap: keeping UV lesions in check (2011) · cites this paper as [44]
In the citing paper
“While ATRIP and Ddc2 directly bind RPA-covered ssDNA [44], loading of the 9-1-1 complex requires the activity of an RFC-like complex, that places it at the junction between dsDNA and 5′ ssDNA [45].”
From Mind the gap: keeping UV lesions in check (2011) · cites this paper as [44]
In the citing paper
“ATR-interacting protein ATRIP is recruited to ssDNA via direct interaction between RPA and ATRIP, thereby recruiting ATR to RPA-ssDNA [100, 101].”
From Functional interplay between ATM/ATR-mediated DNA damage response and DNA repair pathways in oxidative stress (2014) · cites this paper as [100]
Citations
Cites
The DNA damage response: putting checkpoints in perspective
Zhou, B.-B. S., & Elledge, S. J. (2000) · Nature · doi:10.1038/35044005 · Cited by 3,213
Self-citationCell cycle checkpoint signaling through the ATM and ATR kinases
Abraham, R. T. (2001) · Genes & Development · doi:10.1101/gad.914401 · Cited by 1,966
Wood, R., Mitchell, M., Sgouros, J., & Lindahl, T. (2001) · Science · doi:10.1126/science.1056154 · Cited by 1,719
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
Self-citationWold, M. S. (1997) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.66.1.61 · Cited by 1,445
ATR and ATRIP: Partners in Checkpoint Signaling
Cortez, D., Guntuku, S., Qin, J., & Elledge, S. J. (2001) · Science · doi:10.1126/science.1065521 · Cited by 985
Self-citationFork Reversal and ssDNA Accumulation at Stalled Replication Forks Owing to Checkpoint Defects
Sogo, J. M., Lopes, M., & Foiani, M. (2002) · Science · doi:10.1126/science.1074023 · Cited by 824
Loss of a yeast telomere: Arrest, recovery, and chromosome loss
Sandell, L. J. (1993) · Cell · doi:10.1016/0092-8674(93)90493-a · Cited by 792
Recombinant replication protein A: expression, complex formation, and functional characterization
Henricksen, L. A., Umbricht, C. B., & Wold, M. S. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)78100-9 · Cited by 597
Functional interactions between BRCA1 and the checkpoint kinase ATR during genotoxic stress
Tibbetts, R. S., Cortez, D., Brumbaugh, K. M., Scully, R., Livingston, D., Elledge, S. J., & Abraham, R. T. (2000) · Genes & Development · doi:10.1101/gad.851000 · Cited by 512
Self-citation
Cited by
Sorted by citations
Items 601–700 of 1,014
Checkpoint kinase inhibitor AZD7762 strongly sensitises urothelial carcinoma cells to gemcitabine
Isono, M., Hoffmann, M. J., Pinkerneil, M., Sato, A., Michaelis, M., Cinatl, J. J., Niegisch, G., & Schulz, W. A. (2017) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-016-0473-1 · Cited by 86
Walker, M., Black, E. J., Oehler, V., Gillespie, D. A., & Scott, M. T. (2009) · Oncogene · doi:10.1038/onc.2009.102 · Cited by 90
Modulation of ATR-mediated DNA damage checkpoint response by cryptochrome 1
Kang, T., & Leem, S.-H. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku094 · Cited by 91
Mismatch repair proteins as sensors of alkylation DNA damage
Wang, J. Y. J., & Edelmann, W. (2006) · Cancer Cell · doi:10.1016/j.ccr.2006.05.013 · Cited by 86
RAD51C facilitates checkpoint signaling by promoting CHK2 phosphorylation
Badie, S., Liao, C., Thanasoula, M., Barber, P. R., Hill, M. A., & Tarsounas, M. (2009) · The Journal of Cell Biology · doi:10.1083/jcb.200811079 · Cited by 90
DNA damage, vascular senescence and atherosclerosis
Andreassi, M. G. (2008) · Journal of Molecular Medicine · doi:10.1007/s00109-008-0358-7 · Cited by 86
Qin, J.-L., Shen, W., Chen, Z., Zhao, L., Qin, Q., Yu, Y.-C., & Liang, H. (2017) · Scientific Reports · doi:10.1038/srep46056 · Cited by 87
Ray, A., Milum, K., Battu, A., Wani, G., & Wani, A. A. (2013) · DNA Repair · doi:10.1016/j.dnarep.2013.01.003 · Cited by 85
“As ATR is recruited by the RPA-ATRIP complex [15, 16] and influenced by DDB2 and XPC, it is possible that these NER factors also associate with the RPA-ATRIP complex, and thereby affect ATR and ATM recruitment.”
BackgroundRETRACTED: PKA-Mediated Phosphorylation of ATR Promotes Recruitment of XPA to UV-Induced DNA Damage
Jarrett, S. G., Horrell, E. M. W., Christian, P. A., Vanover, J. C., Boulanger, M. C., Zou, Y., & D’Orazio, J. A. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.05.030 · Cited by 85
RetractedChang, D.-Y., & Lu, A.-L. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m406800200 · Cited by 85
Dynamic binding of replication protein a is required for DNA repair
Chen, R., Subramanyam, S. V., Elcock, A. H., Spies, M., & Wold, M. S. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw339 · Cited by 86
SURVIV for survival analysis of mRNA isoform variation
Shen, S., Wang, Y., Wang, C., Wu, Y. N., & Xing, Y. (2016) · Nature Communications · doi:10.1038/ncomms11548 · Cited by 87
PCNA promotes processive DNA end resection by Exo1
Chen, X., Paudyal, S. C., Chin, R.-I., & You, Z. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt672 · Cited by 86
Protein Phosphatase 5 Is Required for ATR-Mediated Checkpoint Activation
Zhang, J., Bao, S., Furumai, R., Kucera, K. S., Ali, A., Dean, N. M., & Wang, X.-F. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.22.9910-9919.2005 · Cited by 86
Two-stage mechanism for activation of the DNA replication checkpoint kinase Cds1 in fission yeastPreprint
Xu, Y., Davenport, M., & Kelly, T. J. (2006) · Genes & Development · doi:10.1101/gad.1406706 · Cited by 88
New insights into the roles of ATM and DNA-PKcs in the cellular response to oxidative stress
Chen, B. P. C., Li, M., & Asaithamby, A. (2012) · Cancer Letters · doi:10.1016/j.canlet.2011.12.004 · Cited by 84
Unwind and slow down: checkpoint activation by helicase and polymerase uncoupling: Figure 1.
Cortez, D. (2005) · Genes & Development · doi:10.1101/gad.1316905 · Cited by 84
Zhang, S., Zhou, Y., Trusa, S., Xiao, M., Lee, E. Y. C., & Lee, M. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m610356200 · Cited by 86
Human Claspin Is a Ring-shaped DNA-binding Protein with High Affinity to Branched DNA Structures
Sar, F., Lindsey‐Boltz, L. A., Subramanian, D., Croteau, D. L., Hutsell, S. Q., Griffith, J. D., & Sancar, A. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m405793200 · Cited by 86
The role of ATM and ATR in the cellular response to hypoxia and re-oxygenation
Hammond, E. M., & Giaccia, A. J. (2004) · DNA repair · doi:10.1016/j.dnarep.2004.03.035 · Cited by 85
Xeroderma pigmentosum genes: Functions inside and outside DNA repair
Sugasawa, K. (2007) · Carcinogenesis · doi:10.1093/carcin/bgm282 · Cited by 83
Perspectives on the DNA damage and replication checkpoint responses in Saccharomyces cerevisiae
Putnam, C. D., Jaehnig, E. J., & Kolodner, R. D. (2009) · DNA Repair · doi:10.1016/j.dnarep.2009.04.021 · Cited by 83
Tapia-Alveal, C., Calonge, T. M., & O’Connell, M. J. (2009) · Cell Division · doi:10.1186/1747-1028-4-8 · Cited by 88
Richard, D. J., Savage, K. I., Bolderson, E., Cubeddu, L., So, S., Ghita, M., Chen, D. J., White, M. F., Richard, K., Prise, K. M., et al. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq1098 · Cited by 87
Srs2: The “Odd-Job Man” in DNA repair
Marini, V., & Krejčí, L. (2010) · DNA repair · doi:10.1016/j.dnarep.2010.01.007 · Cited by 83
DNA double-strand break signaling and human disorders
Bohgaki, T., Bohgaki, M., & Hakem, R. (2010) · Genome Integrity · doi:10.1186/2041-9414-1-15 · Cited by 95
Peterson, S., Li, Y., Chait, B. T., Gottesman, M. E., Baer, R. J., & Gautier, J. (2011) · The Journal of Cell Biology · doi:10.1083/jcb.201103103 · Cited by 83
SUMOylation and de‐SUMOylation in response to DNA damage
Dou, H., Huang, C., Nguyen, T. V., Lu, L., & Yeh, E. T. H. (2011) · FEBS Letters · doi:10.1016/j.febslet.2011.04.002 · Cited by 88
How Cells Respond to DNA Breaks in Mitosis
Blackford, A. N., & Stucki, M. (2020) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2019.12.010 · Cited by 83
The Cytolethal Distending Toxin Effects on Mammalian Cells: A DNA Damage Perspective
Bezine, E., Vignard, J., & Mirey, G. (2014) · Cells · doi:10.3390/cells3020592 · Cited by 92
Hong, S., Cheng, S., Iovane, A., & Laimins, L. A. (2015) · mBio · doi:10.1128/mbio.02006-15 · Cited by 82
Cdc45 is limiting for replication initiation in humans
Köhler, C., Koalick, D., Fabricius, A., Parplys, A. C., Borgmann, K., Pospiech, H., & Große, F. (2016) · Cell Cycle · doi:10.1080/15384101.2016.1152424 · Cited by 82
Kim, K., Dimitrova, D. D., Carta, K. M., Saxena, A. D., Daras, M., & Borowiec, J. A. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.6.2463-2474.2005 · Cited by 86
Wu, X., Yang, Z., Liu, Y., & Zou, Y. (2005) · Biochemical Journal · doi:10.1042/bj20050379 · Cited by 81
The DNA damage checkpoint response to replication stress: A Game of Forks
Jossen, R., & Bermejo, R. (2013) · Frontiers in Genetics · doi:10.3389/fgene.2013.00026 · Cited by 88
Targeting the checkpoint kinase Chk1 in cancer therapy
Merry, C. R., Fu, K., Wang, J., Yeh, I., & Zhang, Y. (2010) · Cell Cycle · doi:10.4161/cc.9.2.10445 · Cited by 82
Karimian, A., Mir, S. M., Parsian, H., Refieyan, S., Mirza‐Aghazadeh‐Attari, M., Yousefi, B., & Majidinia, M. (2018) · Journal of Cellular Biochemistry · doi:10.1002/jcb.28309 · Cited by 84
Olson, E. E., Nievera, C. J., Lee, A. Y., Chen, L., & Wu, X. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m702162200 · Cited by 86
DNA strand break repair and neurodegeneration
Rulten, S. L., & Caldecott, K. W. (2013) · DNA repair · doi:10.1016/j.dnarep.2013.04.008 · Cited by 85
Lemmens, B. B. L. G., Johnson, N. M., & Tijsterman, M. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003276 · Cited by 85
Miz1 and HectH9 regulate the stability of the checkpoint protein, TopBP1
Herold, S., Hock, A., Herkert, B., Berns, K., Mullenders, J., Beijersbergen, R. L., Bernards, R., & Eilers, M. (2008) · The EMBO Journal · doi:10.1038/emboj.2008.200 · Cited by 84
Filtering of Ineffective siRNAs and Improved siRNA Design Tool
Yiu, S., Wong, P. W. H., Lam, T., Mui, Y.-C., Kung, H. F., Lin, M. C. M., & Cheung, Y.-T. (2004) · Bioinformatics · doi:10.1093/bioinformatics/bth498 · Cited by 81
Despras, E., Daboussi, F., Hyrien, O., Marheineke, K., & Kannouche, P. L. (2010) · Human Molecular Genetics · doi:10.1093/hmg/ddq046 · Cited by 80
Sertic, S., Pizzi, S., Cloney, R., Lehmann, A. R., Marini, F., Plevani, P., & Muzi-Falconi, M. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1108547108 · Cited by 80
RPA Phosphorylation Inhibits DNA Resection
Soniat, M. M., Myler, L. R., Kuo, H., Paull, T. T., & Finkelstein, I. J. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.05.005 · Cited by 80
Evidence of sex differences in cellular senescence
Ng, M., & Hazrati, L. (2022) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2022.08.014 · Cited by 85
Groth, P., Ausländer, S., Majumder, M. M., Schultz, N., Johansson, F., Petermann, E., & Helleday, T. (2010) · Journal of Molecular Biology · doi:10.1016/j.jmb.2010.07.010 · Cited by 86
Quanz, M., Chassoux, D., Berthault, N., Agrario, C., Sun, J., & Dutreix, M. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006298 · Cited by 92
Structural mechanism of RPA loading on DNA during activation of a simple pre‐replication complex
Jiang, X., Klimovich, V., Arunkumar, A. I., Hysinger, E. B., Wang, Y., Ott, R. D., Guler, G. D., Weiner, B., Chazin, W., & Fanning, E. (2006) · The EMBO Journal · doi:10.1038/sj.emboj.7601432 · Cited by 80
Budding Yeast Sae2 is an In Vivo Target of the Mec1 and Tel1 Checkpoint Kinases During Meiosis
Cartagena‐Lirola, H., Guerini, I., Viscardi, V., Lucchini, G., & Longhese, M. P. (2006) · Cell Cycle · doi:10.4161/cc.5.14.2916 · Cited by 85
Roberts, T. M., Kobor, M. S., Bastin-Shanower, S. A., Ii, M., Horte, S. A., Gin, J., Emili, A., Rine, J., Brill, S. J., & Brown, G. W. (2005) · Molecular Biology of the Cell · doi:10.1091/mbc.e05-08-0785 · Cited by 82
Role of Deubiquitinating Enzymes in DNA Repair
Kee, Y., & Huang, T. T. (2015) · Molecular and Cellular Biology · doi:10.1128/mcb.00847-15 · Cited by 81
Effects of hyperthermia as a mitigation strategy in DNA damage-based cancer therapies
Mantso, T., Goussetis, G., Franco, R., Botaitis, S., Pappa, A., & Panayiotidis, M. I. (2016) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2016.03.004 · Cited by 80
Cell cycle-dependent inhibition of 53BP1 signaling by BRCA1
Feng, L., Li, N., Li, Y., Wang, J., Gao, M., Wang, W., & Chen, J. (2015) · Cell Discovery · doi:10.1038/celldisc.2015.19 · Cited by 86
Lin, H.-P., Lin, C., Huo, C., Hsiao, P.-H., Su, L., Jiang, S. S., Chan, T.-M., Chang, C.-H., Chen, L., Kung, H.-J., et al. (2015) · Oncotarget · doi:10.18632/oncotarget.3246 · Cited by 82
Fahrer, J., Huelsenbeck, J., Jaurich, H., Dörsam, B., Frisan, T., Eich, M., Roos, W. P., Kaina, B., & Fritz, G. (2014) · DNA repair · doi:10.1016/j.dnarep.2014.03.002 · Cited by 84
γH2A binds Brc1 to maintain genome integrity during S‐phase
Williams, J. S., Williams, R. S., Dovey, C. L., Guenther, G., Tainer, J. A., & Russell, P. R. (2010) · The EMBO Journal · doi:10.1038/emboj.2009.413 · Cited by 79
Liu, S., Chu, J., Yucer, N., Leng, M., Wang, S., Chen, B. P. C., Hittelman, W. N., & Wáng, Y. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.222802 · Cited by 82
Regulators of homologous recombination repair as novel targets for cancer treatment
Krajewska, M., Fehrmann, R. S. N., de Vries, E. G. E., & van Vugt, M. A. T. M. (2015) · Frontiers in Genetics · doi:10.3389/fgene.2015.00096 · Cited by 81
Nuss, J. E., Patrick, S. M., Oakley, G. G., Alter, G. M., Robison, J. G., Dixon, K., & Turchi, J. J. (2005) · Biochemistry · doi:10.1021/bi0480584 · Cited by 79
How ATR turns on: TopBP1 goes on ATRIP with ATR: Figure 1.Preprint
Burrows, A. E., & Elledge, S. J. (2008) · Genes & Development · doi:10.1101/gad.1685108 · Cited by 79
Self-citationInteractions of Human Mismatch Repair Proteins MutSα and MutLα with Proteins of the ATR-Chk1 Pathway
Liu, Y., Fang, Y., Shao, H., Lindsey-Boltz, L., Sancar, A., & Modrich, P. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.076109 · Cited by 78
An N‐terminal acidic region of Sgs1 interacts with Rpa70 and recruits Rad53 kinase to stalled forks
Hegnauer, A. M., Hustedt, N., Shimada, K., Pike, B. L., Vogel, M., Amsler, P., Rubin, S. M., van Leeuwen, F., Guénolé, A., van Attikum, H., et al. (2012) · The EMBO Journal · doi:10.1038/emboj.2012.195 · Cited by 82
Orba, Y., Suzuki, T., Makino, Y., Kubota, K., Tanaka, S., Kimura, T., & Sawa, H. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.064311 · Cited by 81
Cdc7-Dbf4 and the Human S Checkpoint Response to UVC
Heffernan, T. P., Ünsal-Kaçmaz, K., Heinloth, A. N., Simpson, D. A., Paules, R. S., Sancar, A., Cordeiro‐Stone, M., & Kaufmann, W. K. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m611292200 · Cited by 81
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
RAD6-RAD18-RAD5-pathway-dependent tolerance to chronic low-dose ultraviolet light
Hishida, T., Kubota, Y., Carr, A. M., & Iwasaki, H. (2009) · Nature · doi:10.1038/nature07580 · Cited by 77
DNA replication stress differentially regulates G1/S genes via Rad53‐dependent inactivation of Nrm1
Travesa, A., Kuo, D., de Bruin, R. A. M., Kalashnikova, T. I., Guaderrama, M., Thai, K. E., Aslanian, A., Smolka, M. B., Yates, J. R., Ideker, T., et al. (2012) · The EMBO Journal · doi:10.1038/emboj.2012.28 · Cited by 79
Mirza‐Aghazadeh‐Attari, M., Darband, S. G., Kaviani, M., Mihanfar, A., Aghazadeh-Attari, J., Yousefi, B., & Majidinia, M. (2018) · DNA repair · doi:10.1016/j.dnarep.2018.07.005 · Cited by 79
Persistent repair intermediates induce senescence
Feringa, F. M., Raaijmakers, J. A., Hadders, M. A., Vaarting, C., Macůrek, L., Heitink, L. S., Krenning, L., & Medema, R. H. (2018) · Nature Communications · doi:10.1038/s41467-018-06308-9 · Cited by 79
Chromatin Remodeling and Epigenetic Regulation in Plant DNA Damage Repair
Kim, J. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20174093 · Cited by 79
Curtis, M. J., & Hays, J. B. (2007) · DNA repair · doi:10.1016/j.dnarep.2007.03.004 · Cited by 80
Structure and function of the Rad9-binding region of the DNA-damage checkpoint adaptor TopBP1
Rappas, M., Oliver, A. W., & Pearl, L. H. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq743 · Cited by 78
Zeng, X., Yan, T., Schupp, J. E., Seo, Y., & Kinsella, T. J. (2007) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-06-1517 · Cited by 77
ATR maintains select progenitors during nervous system development
Lee, Y., Shull, E. R. P., Frappart, P., Katyal, S., Enriquez-Rios, V. D., Zhao, J., Russell, H. R., Brown, E. J., & McKinnon, P. J. (2012) · The EMBO Journal · doi:10.1038/emboj.2011.493 · Cited by 78
ATRIP Oligomerization Is Required for ATR-dependent Checkpoint Signaling
Ball, H. L., & Cortez, D. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m504961200 · Cited by 78
The Response to DNA Damage at Telomeric Repeats and Its Consequences for Telomere Function
Doksani, Y. (2019) · Genes · doi:10.3390/genes10040318 · Cited by 83
Eukaryotic Single-Stranded DNA Binding Proteins: Central Factors in Genome Stability
Broderick, S., Rehmet, K., Concannon, C., & Nasheuer, H. (2009) · Sub-cellular biochemistry/Subcellular biochemistry · doi:10.1007/978-90-481-3471-7_8 · Cited by 78
RPA Inhibition Increases Replication Stress and Suppresses Tumor Growth
Glanzer, J. G., Liu, S., Wang, L., Mosel, A., Peng, A., & Oakley, G. G. (2014) · Cancer Research · doi:10.1158/0008-5472.can-14-0306 · Cited by 79
Ogiwara, H., Ui, A., Shiotani, B., Zou, L., Yasui, A., & Kohno, T. (2013) · Carcinogenesis · doi:10.1093/carcin/bgt240 · Cited by 76
Self-citationShiotani, B., & Zou, L. (2009) · Journal of Cell Science · doi:10.1242/jcs.035105 · Cited by 82
Self-citationGao, 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
STAT3 interrupts ATR-Chk1 signaling to allow oncovirus-mediated cell proliferation
Koganti, S. R. K., Hui‐Yuen, J. S., McAllister, S. C., Gardner, B., Grässer, F. A., Palendira, U., Tangye, S. G., Freeman, A. F., & Bhaduri‐McIntosh, S. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1400683111 · Cited by 76
Predicting breast cancer risk using interacting genetic and demographic factors and machine learning
Behravan, H., Hartikainen, J. M., Tengström, M., Kosma, V., & Mannermaa, A. (2020) · Scientific Reports · doi:10.1038/s41598-020-66907-9 · Cited by 77
Targeting ATM and ATR for cancer therapeutics: Inhibitors in clinic
Priya, B., Ravi, S., & Kirubakaran, S. (2023) · Drug Discovery Today · doi:10.1016/j.drudis.2023.103662 · Cited by 77
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 76
Self-citationAdenovirus 12 E4orf6 inhibits ATR activation by promoting TOPBP1 degradation
Blackford, A. N., Patel, R. N., Forrester, N. A., Theil, K., Groitl, P., Stewart, G. S., Taylor, A. M. R., Morgan, I. M., Dobner, T., Grand, R. J. A., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0914605107 · Cited by 77
Deficient DNA Damage Signaling Leads to Chemoresistance to Cisplatin in Oral Cancer
Wang, L., Mosel, A., Oakley, G. G., & Peng, A. (2012) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-12-0448 · Cited by 78
The DNA-polymerase-X family: controllers of DNA quality?
Ramadan, K., Shevelev, I., & Hübscher, U. (2004) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1530 · Cited by 75
Kapoor, A., Agarwal, M., Andreucci, A. C., Zheng, X., Gong, Z., Hasegawa, P. M., Bressan, R. A., & Zhu, J. (2005) · Current Biology · doi:10.1016/j.cub.2005.09.013 · Cited by 75
The human checkpoint sensor Rad9–Rad1–Hus1 interacts with and stimulates NEIL1 glycosylase
Guan, X., Bai, H., Shi, G., Theriot, C. A., Hazra, T. K., Mitra, S., & Lu, A.-L. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm075 · Cited by 74
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-citationRSC Functions as an Early Double-Strand-Break Sensor in the Cell's Response to DNA Damage
Liang, B., Qiu, J., Ratnakumar, K., & Laurent, B. C. (2007) · Current Biology · doi:10.1016/j.cub.2007.07.035 · Cited by 83
Regulation of the DNA Damage Response by Cyclin-Dependent Kinases
Trovesi, C., Manfrini, N., Falcettoni, M., & Longhese, M. P. (2013) · Journal of Molecular Biology · doi:10.1016/j.jmb.2013.04.013 · Cited by 79
McGee, J. S., Phillips, J. A., Chan, A., Sabourin, M., Paeschke, K., & Zakian, V. A. (2010) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1947 · Cited by 74
Differential arrival of leading and lagging strand DNA polymerases at fission yeast telomeres
Moser, B. A., Subramanian, L., Chang, Y.-T., Noguchi, C., Noguchi, E., & Nakamura, T. (2009) · The EMBO Journal · doi:10.1038/emboj.2009.31 · Cited by 74
p53 Mediates Senescence-Like Arrest Induced by Chronic Replicational Stress
Marusyk, A., Wheeler, L. J., Mathews, C. K., & DeGregori, J. V. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.01316-06 · Cited by 74
The Emerging Role of Cohesin in the DNA Damage Response
Litwin, I., Pilarczyk, E., & Wysocki, R. (2018) · Genes · doi:10.3390/genes9120581 · Cited by 80
DNA single-strand breaks and neurodegeneration
Caldecott, K. W. (2004) · DNA repair · doi:10.1016/j.dnarep.2004.04.011 · Cited by 74
The S-phase checkpoint and its regulation in Saccharomyces cerevisiae
Longhese, M. P., Clerici, M., & Lucchini, G. (2003) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2003.08.009 · Cited by 74
Metadata
- Authors
- Zou, L., & Elledge, S. J.
- Affiliations
- Howard Hughes Medical Institute (US)
- Corresponding author
- Elledge, Stephen J.
- Venue
- Science
- Published
- 2003-06-06
- Volume
- 300
- Issue
- 5625
- Pages
- 1542-1548
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W2043895957
- Cited by
- 2,693
- References
- 37
- Citations by year
- 2026: 64 · 2025: 65 · 2024: 114 · 2023: 98 · 2022: 112 · 2021: 136 · 2020: 111 · 2019: 116 · 2018: 106 · 2017: 114 · 2016: 130 · 2015: 139 · 2014: 117 · 2013: 144 · 2012: 121
- FWCI
- 41.94
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of General Medical Sciences (GM-44664)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Keywords
- replication protein A, single-stranded DNA, DNA damage recognition, DNA damage checkpoint, Chk1 activation, DNA double-strand breaks, replication stress
- MeSH terms
- Checkpoint Kinase 1, Cell Nucleus, DNA Damage, DNA Repair, DNA Replication, DNA-Binding Proteins, DNA, Fungal, DNA, Single-Stranded, Enzyme Activation, Exodeoxyribonucleases, HeLa Cells, Humans, Mutation, Phosphoproteins, Phosphorylation, Protein Binding, Protein Kinases, Radiation, Ionizing, Recombination, Genetic, Saccharomyces cerevisiae, Transcription Factors, Transfection, Tumor Cells, Cultured, Ultraviolet Rays, Signal Transduction, Protein Serine-Threonine Kinases, Cell Cycle Proteins, Saccharomyces cerevisiae Proteins, RNA, Small Interfering, Adaptor Proteins, Signal Transducing, Replication Protein A, 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
