ATR‐dependent phosphorylation and activation of ATM in response to UV treatment or replication fork stalling
Open accessAbstract
The phosphatidyl inositol 3-kinase-like kinases (PIKKs), ataxia-telangiectasia mutated (ATM) and ATM- and Rad3-related (ATR) regulate parallel damage response signalling pathways. ATM is reported to be activated by DNA double-strand breaks (DSBs), whereas ATR is recruited to single-stranded regions of DNA. Although the two pathways were considered to function independently, recent studies have demonstrated that ATM functions upstream of ATR following exposure to ionising radiation (IR) in S/G2. Here, we show that ATM phosphorylation at Ser1981, a characterised autophosphorylation site, is ATR-dependent and ATM-independent following replication fork stalling or UV treatment. In contrast to IR-induced ATM-S1981 phosphorylation, UV-induced ATM-S1981 phosphorylation does not require the Nbs1 C-terminus or Mre11. ATR-dependent phosphorylation of ATM activates ATM phosphorylation of Chk2, which has an overlapping function with Chk1 in regulating G2/M checkpoint arrest. Our findings provide insight into the interplay between the PIKK damage response pathways.
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
Cites
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.
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?
Unlike ionizing radiation-induced ATM activation, UV-induced ATM phosphorylation at serine 1981 does not require the MRN complex.
“In contrast to the IR situation, UV-induced ATM phosphorylation at Serine 1981 does not require the MRN complex, which is a requirement for ATM activation by DSBs.”
From Functional interplay between ATM/ATR-mediated DNA damage response and DNA repair pathways in oxidative stress (2014) · cites this paper as [144]
ATR-dependent ATM activation promotes Chk2 phosphorylation downstream of checkpoint signaling.
“ATR-dependent ATM activation promotes Chk2 phosphorylation downstream of the checkpoint signaling [144].”
From Functional interplay between ATM/ATR-mediated DNA damage response and DNA repair pathways in oxidative stress (2014) · cites this paper as [144]
ATM autophosphorylation at serine 1981 is ATR-dependent and ATM-independent in response to stalled DNA replication forks or UV-induced DNA damage.
“ATM auto-phosphorylation at Ser1981 is ATR-dependent and ATM-independent in response to stalled DNA replication forks or UV-induced DNA damage [144].”
From Functional interplay between ATM/ATR-mediated DNA damage response and DNA repair pathways in oxidative stress (2014) · cites this paper as [144]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation
Bakkenist, C. J., & Kastan, M. B. (2003) · Nature · doi:10.1038/nature01368 · Cited by 3,466 · see citing works
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 · see citing works
ATM and related protein kinases: safeguarding genome integrity
Shiloh, Y. (2003) · Nature Reviews Cancer · doi:10.1038/nrc1011 · Cited by 2,577 · see citing works
A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage
Paull, T. T., Rogakou, E. P., Yamazaki, V., Kirchgessner, C. U., Gellert, M., & Bonner, W. M. (2000) · Current Biology · doi:10.1016/s0960-9822(00)00610-2 · Cited by 2,098 · see citing works
Genomic Instability in Mice Lacking Histone H2AX
Celeste, A., Petersen, S., Romanienko, P. J., Fernandez-Capetillo, O., Chen, H. T., Sedelnikova, O. A., Reina-San-Martin, B., Coppola, V., Meffre, E., Difilippantonio, M. J., et al. (2002) · Science · doi:10.1126/science.1069398 · Cited by 1,385 · see citing works
Linkage of ATM to Cell Cycle Regulation by the Chk2 Protein Kinase
Matsuoka, S. (1998) · Science · doi:10.1126/science.282.5395.1893 · Cited by 1,322 · see citing works
Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage
Falck, J., Coates, J., & Jackson, S. P. (2005) · Nature · doi:10.1038/nature03442 · Cited by 1,248 · see citing works
Hickson, I., Zhao, Y., Richardson, C. J., Green, S. J., Martin, N. M. B., Orr, A. I., Reaper, P. M., Jackson, S. P., Curtin, N. J., & Smith, G. C. M. (2004) · Cancer Research · doi:10.1158/0008-5472.can-04-2727 · Cited by 1,220 · see citing works
Requirement of the MRN complex for ATM activation by DNA damage
Uziel, T., Lerenthal, Y., Moyal, L., Andegeko, Y., Mittelman, L., & Shiloh, Y. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg541 · Cited by 1,075 · see citing works
ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks
Jazayeri, A., Falck, J., Lukas, C., Bartek, J., Smith, G. C. M., Lukas, J., & Jackson, S. P. (2006) · Nature Cell Biology · doi:10.1038/ncb1337 · Cited by 1,064 · see citing works
Stewart, G. S., Maser, R. S., Stankovic, T., Bressan, D. A., Kaplan, M. I., Jaspers, N. G. J., Raams, A., Byrd, P. J., Petrini, J. H. J., & Taylor, A. M. R. (1999) · Cell · doi:10.1016/s0092-8674(00)81547-0 · Cited by 1,060 · see citing works
ATM and DNA-PK Function Redundantly to Phosphorylate H2AX after Exposure to Ionizing Radiation
Stiff, T., O’Driscoll, M., Rief, N., Iwabuchi, K., Löbrich, M., & Jeggo, P. A. (2004) · Cancer Research · doi:10.1158/0008-5472.can-03-3207 · Cited by 1,010 · see citing works
Self-citationATR 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 · see citing works
O'Driscoll, M., Ruiz-Perez, V. L., Woods, C. G., Jeggo, P. A., & Goodship, J. A. (2003) · Nature Genetics · doi:10.1038/ng1129 · Cited by 794 · see citing works
Self-citationPI 3-kinase related kinases: ‘big’ players in stress-induced signaling pathways
Abraham, R. T. (2004) · DNA repair · doi:10.1016/j.dnarep.2004.04.002 · Cited by 441 · see citing works
Replication protein A-mediated recruitment and activation of Rad17 complexes
Zou, L., Liu, D., & Elledge, S. J. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2336100100 · Cited by 431 · see citing works
Ataxia–telangiectasia, an evolving phenotype
Chun, H. H., & Gatti, R. A. (2004) · DNA repair · doi:10.1016/j.dnarep.2004.04.010 · Cited by 426 · see citing works
p53 Binding Protein 53BP1 Is Required for DNA Damage Responses and Tumor Suppression in Mice
Ward, I. M., Minn, K. T., van Deursen, J., & Chen, J. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.7.2556-2563.2003 · Cited by 412 · see citing works
An ATR- and Cdc7-Dependent DNA Damage Checkpoint that Inhibits Initiation of DNA Replication
Costanzo, V., Shechter, D., Lupardus, P. J., Cimprich, K. A., Gottesman, M. E., & Gautier, J. (2003) · Molecular Cell · doi:10.1016/s1097-2765(02)00799-2 · Cited by 355 · see citing works
Activation of mammalian Chk1 during DNA replication arrest
Feijóo, C. G., Hall-Jackson, C. A., Wu, R., Jenkins, D., Leitch, J., Gilbert, D. M., & Smythe, C. (2001) · The Journal of Cell Biology · doi:10.1083/jcb.200104099 · Cited by 318 · see citing works
Rapid Activation of ATR by Ionizing Radiation Requires ATM and Mre11
Myers, J. S., & Cortez, D. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m513265200 · Cited by 294 · see citing works
Brown, A. L., Lee, C. H., Schwarz, J. K., Mitiku, N., Piwnica-Worms, H. M., & Chung, J. H. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.7.3745 · Cited by 260 · see citing works
Desai-Mehta, A., Cerosaletti, K. M., & Concannon, P. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.6.2184-2191.2001 · Cited by 196 · see citing works
Self-citationSeckel syndrome exhibits cellular features demonstrating defects in the ATR-signalling pathway
Alderton, G. K., Joenje, H., Varon, R., Børglum, A. D., Jeggo, P. A., & O’Driscoll, M. (2004) · Human Molecular Genetics · doi:10.1093/hmg/ddh335 · Cited by 177 · see citing works
Self-citationNbs1 is required for ATR‐dependent phosphorylation events
Stiff, T., Reis, C., Alderton, G. K., Woodbine, L. J., O’Driscoll, M., & Jeggo, P. A. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600504 · Cited by 169 · see citing works
Self-citationYu, Q., Rose, J. H. L., Zhang, H., Takemura, H., Kohn, K. W., & Pommier, Y. G. (2002) · PubMed · Cited by 138 · see citing works
Curman, D., Cinel, B., Williams, D. E., Rundle, N. T., Block, W. D., Goodarzi, A. A., Hutchins, J. R. A., Clarke, P. R., Zhou, B.-B., Lees‐Miller, S. P., et al. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m100728200 · Cited by 121 · see citing works
Self-citationMethylator-induced, Mismatch Repair-dependent G2Arrest Is Activated through Chk1 and Chk2
Adamson, A. W., Beardsley, D. I., Kim, W.-J., Gao, Y., Baskaran, R., & Brown, K. D. (2005) · Molecular Biology of the Cell · doi:10.1091/mbc.e04-02-0089 · Cited by 87 · see citing works
Independent Roles for Nibrin and Mre11-Rad50 in the Activation and Function of Atm
Cerosaletti, K. M., & CONCANNON, P. J. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m404294200 · Cited by 82 · see citing works
Self-citationThe clinical and biological overlap between Nijmegen Breakage Syndrome and Fanconi anemia
Gennery, A. R., Slatter, M. A., Bhattacharya, A., Barge, D., Haigh, S., O’Driscoll, M., Coleman, R., Abinun, M., Flood, T. J., Cant, A. J., et al. (2004) · Clinical Immunology · doi:10.1016/j.clim.2004.03.024 · Cited by 58 · see citing works
Self-citationDodson, G. E., & Tibbetts, R. S. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m509577200 · Cited by 34 · see citing works
Flagged first, then by citations
Cited by
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 1,953 · see citing works
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 · see citing works
The ATM protein kinase: regulating the cellular response to genotoxic stress, and more
Shiloh, Y., & Ziv, Y. (2013) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3546 · Cited by 1,649 · see citing works
Bonner, W. M., Redon, C. E., Dickey, J. S., Nakamura, A. J., Sedelnikova, O. A., Solier, S., & Pommier, Y. (2008) · Nature reviews. Cancer · doi:10.1038/nrc2523 · Cited by 1,623 · see citing works
γH2AX: a sensitive molecular marker of DNA damage and repair
Mah, L.-J., El-Osta, A., & Karagiannis, T. C. (2010) · Leukemia · doi:10.1038/leu.2010.6 · Cited by 1,557 · see citing works
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
DNA damage-induced cell death: From specific DNA lesions to the DNA damage response and apoptosis
Roos, W. P., & Kaina, B. (2013) · Cancer Letters · doi:10.1016/j.canlet.2012.01.007 · Cited by 879 · see citing works
DNA double-strand break repair pathway regulates PD-L1 expression in cancer cells
Sato, H., Niimi, A., Yasuhara, T., Permata, T. B. M., Hagiwara, Y., Isono, M., Nuryadi, E., Sekine, R., Oike, T., Kakoti, S., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-01883-9 · Cited by 710 · see citing works
The impact of a negligent G2/M checkpoint on genomic instability and cancer induction
Löbrich, M., & Jeggo, P. A. (2007) · Nature reviews. Cancer · doi:10.1038/nrc2248 · Cited by 627 · see citing works
Self-citationDNA 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
Noon, A. T., Shibata, A., Rief, N., Löbrich, M., Stewart, G. S., Jeggo, P. A., & Goodarzi, A. A. (2010) · Nature Cell Biology · doi:10.1038/ncb2017 · Cited by 339 · see citing works
Self-citationH2AX: functional roles and potential applications
Dickey, J. S., Redon, C. E., Nakamura, A. J., Baird, B. J., Sedelnikova, O. A., & Bonner, W. M. (2009) · Chromosoma · doi:10.1007/s00412-009-0234-4 · Cited by 320 · 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
Histone H2AX-dependent GABAA receptor regulation of stem cell proliferation
Andäng, M., Hjerling‐Leffler, J., Moliner, A., Lundgren, K. C., Castelo‐Branco, G., Nanou, E., Pozas, E., Bryja, V., Halliez, S., Nishimaru, H., et al. (2008) · Nature · doi:10.1038/nature06488 · Cited by 288 · see citing works
Abuetabh, Y., Wu, H. H., Chai, C., Yousef, H. A., Persad, S., Sergi, C. M., & Leng, R. P. (2022) · Experimental & Molecular Medicine · doi:10.1038/s12276-022-00863-4 · Cited by 275 · see citing works
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
Jin, M. H., & Oh, D. (2019) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2019.07.002 · Cited by 249 · see citing works
Sordet, O., Redon, C. E., Guirouilh‐Barbat, J., Smith, S. H., Solier, S., Douarre, C., Conti, C., Nakamura, A., Das, B. B., Nicolas, E., et al. (2009) · EMBO Reports · doi:10.1038/embor.2009.97 · Cited by 239 · see citing works
Nikitin, P. A., Yan, C. M., Forte, E., Bocedi, A., Tourigny, J. P., White, R. E., Allday, M. J., Patel, A. B., Davé, S. S., Kim, W., et al. (2010) · Cell Host & Microbe · doi:10.1016/j.chom.2010.11.004 · Cited by 235 · see citing works
How DNA lesions are turned into powerful killing structures: Insights from UV-induced apoptosis
Batista, L. F. Z., Kaina, B., Meneghini, R., & Menck, C. F. M. (2009) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2008.09.001 · Cited by 234 · see citing works
Gene regulation under low oxygen: holding your breath for transcription
Rocha, S. (2007) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2007.06.005 · Cited by 219 · see citing works
Hanasoge, S., & Ljungman, M. (2007) · Carcinogenesis · doi:10.1093/carcin/bgm157 · Cited by 216 · see citing works
Collis, S. J., Ciccia, A., Deans, A. J., Hořejšı́, Z., Martin, J. S., Maslen, S., Skehel, M. J., Elledge, S. J., West, S. C., & Boulton, S. J. (2008) · Molecular Cell · doi:10.1016/j.molcel.2008.10.014 · 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
Cremona, C. A., & Behrens, A. (2013) · Oncogene · doi:10.1038/onc.2013.275 · Cited by 206 · 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 Activation and Signaling under Hypoxic Conditions
Bencokova, Z., Kaufmann, M. R., Pires, I. M., Lecane, P. S., Giaccia, A. J., & Hammond, E. M. (2008) · Molecular and Cellular Biology · doi:10.1128/mcb.01301-08 · Cited by 204 · see citing works
Effects of Atmospheric Pressure Plasmas on Isolated and Cellular DNA—A Review
Arjunan, K. P., Sharma, V. K., & Ptasińska, S. (2015) · International Journal of Molecular Sciences · doi:10.3390/ijms16022971 · Cited by 196 · see citing works
Regulation of DNA repair in hypoxic cancer cells
Bindra, R. S., Crosby, M. E., & Glazer, P. M. (2007) · Cancer and Metastasis Reviews · doi:10.1007/s10555-007-9061-3 · Cited by 191 · see citing works
Control of HIPK2 stability by ubiquitin ligase Siah-1 and checkpoint kinases ATM and ATR
Winter, M., Sombroek, D., Dauth, I., Moehlenbrink, J., Scheuermann, K., Crone, J., & Hofmann, T. G. (2008) · Nature Cell Biology · doi:10.1038/ncb1743 · Cited by 190 · see citing works
Marteijn, J. A., Bekker-Jensen, S., Mailand, N., Lans, H., Schwertman, P., Gourdin, A. M., Dantuma, N. P., Lukas, J., & Vermeulen, W. (2009) · Journal of Cell Biology · doi:10.1083/jcb.200902150 · Cited by 184 · see citing works
Lloyd, R. L., Wijnhoven, P. W. G., Ramos‐Montoya, A., Wilson, Z., Illuzzi, G., Falenta, K., Jones, G. N., James, N. H., Chabbert, C. D., Stott, J., et al. (2020) · Oncogene · doi:10.1038/s41388-020-1328-y · Cited by 181 · see citing works
Rizzo, A., Salvati, E., Porru, M., D’Angelo, C., Stevens, M. F. G., D’Incalci, M., Leonetti, C., Gilson, É., Zupi, G., & Biroccio, A. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp582 · Cited by 176 · see citing works
Kim, D. J., Iwasaki, A., Chien, A. L.-L., & Kang, S. (2022) · JCI Insight · doi:10.1172/jci.insight.156344 · Cited by 166 · see citing works
The FHA and BRCT domains recognize ADP-ribosylation during DNA damage responsePreprint
Mo, L., Lu, L., Yang, C., Wang, S., & Yu, X. (2013) · Genes & Development · doi:10.1101/gad.226357.113 · Cited by 164 · see citing works
Ataxia telangiectasia and Rad3-related inhibitors and cancer therapy: where we stand
Mei, L., Zhang, J., He, K., & Zhang, J. (2019) · Journal of Hematology & Oncology · doi:10.1186/s13045-019-0733-6 · Cited by 157 · see citing works
γH2AX as a molecular marker of aging and disease
Mah, L.-J., El‐Osta, A., & Karagiannis, T. C. (2010) · Epigenetics · doi:10.4161/epi.5.2.11080 · Cited by 154 · see citing works
Nakamura, A., Rao, V. A., Pommier, Y. G., & Bonner, W. M. (2010) · Cell Cycle · doi:10.4161/cc.9.2.10475 · Cited by 154 · see citing works
Powley, I. R., Kondrashov, A. V., Young, L. A., Dobbyn, H. C., Hill, K., Cannell, I. G., Stoneley, M., Kong, Y. W., Cotes, J. A., Smith, G. C. M., et al. (2009) · Genes & Development · doi:10.1101/gad.516509 · Cited by 150 · see citing works
RetractedRai, P., Parrish, M. C., Tay, I. J. J., Li, N., Ackerman, S., He, F., Kwang, J., Chow, V. T. K., & Engelward, B. P. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1424144112 · Cited by 145 · see citing works
Targeted cancer therapies based on the inhibition of DNA strand break repair
O’Connor, M. J., Martin, N. M. B., & Smith, G. C. M. (2007) · Oncogene · doi:10.1038/sj.onc.1210879 · Cited by 144 · see citing works
Chromatin and the DNA damage response: The cancer connection
Luijsterburg, M. S., & van Attikum, H. (2011) · Molecular Oncology · doi:10.1016/j.molonc.2011.06.001 · Cited by 141 · see citing works
ATM and ATR Signaling Regulate the Recruitment of Human Telomerase to Telomeres
Tong, A. S., Stern, J. L., Sfeir, A. J., Kartawinata, M., de Lange, T., Zhu, X., & Bryan, T. M. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.10.041 · Cited by 136 · see citing works
Harnessing the complexity of DNA-damage response pathways to improve cancer treatment outcomes
Al‐Ejeh, F., Kumar, R., Wiegmans, A. P., Lakhani, S. R., Brown, M. P., & Khanna, K. K. (2010) · Oncogene · doi:10.1038/onc.2010.407 · Cited by 139 · see citing works
XPF-ERCC1 Participates in the Fanconi Anemia Pathway of Cross-Link Repair
Bhagwat, N. R., Olsen, A. L., Wang, A. T., Hanada, K., Stuckert, P., Kanaar, R., D’Andrea, A. D., Niedernhofer, L. J., & McHugh, P. J. (2009) · Molecular and Cellular Biology · doi:10.1128/mcb.00086-09 · Cited by 138 · see citing works
Functional relevance of the histone γH2Ax in the response to DNA damaging agents
Revet, I. M., Feeney, L., Bruguera, S., Wilson, W., Dong, T. K., Oh, D. H., Dankort, D. L., & Cleaver, J. E. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1105866108 · Cited by 133 · see citing works
Nakano, T., Katafuchi, A., Matsubara, M., Terato, H., Tsuboi, T., Masuda, T., Tatsumoto, T., Pack, S. P., Makino, K., Croteau, D. L., et al. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.019174 · Cited by 131 · see citing works
Jazayeri, A. R., Balestrini, A., Garner, E., Haber, J. E., & Costanzo, V. (2008) · The EMBO Journal · doi:10.1038/emboj.2008.128 · Cited by 131 · see citing works
Many faces of NF-κB signaling induced by genotoxic stress
Wu, Z., & Miyamoto, S. (2007) · Journal of Molecular Medicine · doi:10.1007/s00109-007-0227-9 · Cited by 129 · see citing works
Chromatin modifications and DNA repair: beyond double-strand breaks
House, N. C. M., Koch, M. R., & Freudenreich, C. H. (2014) · Frontiers in Genetics · doi:10.3389/fgene.2014.00296 · Cited by 128 · see citing works
Replication fork dynamics and the DNA damage response
Jones, R. M., & Petermann, E. (2012) · Biochemical Journal · doi:10.1042/bj20112100 · Cited by 127 · see citing works
Self-citationFOXM1 targets NBS1 to regulate DNA damage-induced senescence and epirubicin resistance
Khongkow, P., Karunarathna, U., Khongkow, M., Gong, C., Gomes, A., Yagüe, E., Monteiro, L. J., Kongsema, M., Zona, S., Man, E. P. S., et al. (2013) · Oncogene · doi:10.1038/onc.2013.457 · Cited by 127 · see citing works
Hein, J., Boichuk, S., Wu, J., Cheng, Y., Freire, R., Jat, P., Roberts, T. M., & Gjoerup, O. V. (2008) · Journal of Virology · doi:10.1128/jvi.01515-08 · Cited by 124 · see citing works
Chromatin structure and DNA damage repair
Dinant, C., Houtsmuller, A. B., & Vermeulen, W. (2008) · Epigenetics & Chromatin · doi:10.1186/1756-8935-1-9 · Cited by 122 · see citing works
Yajima, H., Lee, K.-J., Zhang, S., Kobayashi, J., & Chen, B. P. C. (2009) · Journal of Molecular Biology · doi:10.1016/j.jmb.2008.11.036 · Cited by 124 · see citing works
ATM Acts Downstream of ATR in the DNA Damage Response Signaling of Bystander Cells
Burdak‐Rothkamm, S., Rothkamm, K., & Prise, K. M. (2008) · Cancer Research · doi:10.1158/0008-5472.can-08-0545 · Cited by 124 · see citing works
Early events in the mammalian response to DNA double-strand breaks
Riches, L. C., Lynch, A. M., & Gooderham, N. J. (2008) · Mutagenesis · doi:10.1093/mutage/gen039 · Cited by 122 · see citing works
Eich, M., Roos, W. P., Nikolova, T., & Kaina, B. (2013) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-13-0136 · Cited by 119 · see citing works
ATM protein kinase: the linchpin of cellular defenses to stress
Bhatti, S., Kozlov, S., Farooqi, A. A., Naqi, A., Lavin, M., & Khanna, K. K. (2011) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-011-0683-9 · Cited by 116 · see citing works
Shibata, A., Barton, O., Noon, A. T., Dahm, K., Deckbar, D., Goodarzi, A. A., Löbrich, M., & Jeggo, P. A. (2010) · Molecular and Cellular Biology · doi:10.1128/mcb.01644-09 · Cited by 114 · see citing works
Self-citationDealing with DNA damage: Relationships between checkpoint and repair pathways
Warmerdam, D. O., & Kanaar, R. (2009) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2009.12.001 · Cited by 113 · see citing works
Replication Stress and Chromatin Context Link ATM Activation to a Role in DNA Replication
Olcina, M. M., Foskolou, I. P., Anbalagan, S., Senra, J. M., Pires, I. M., Jiang, Y., Ryan, A. J., & Hammond, E. M. (2013) · Molecular Cell · doi:10.1016/j.molcel.2013.10.019 · Cited by 110 · see citing works
γH2Ax: Biomarker of Damage or Functional Participant in DNA Repair “All that Glitters Is not Gold!”
Cleaver, J. E. (2011) · Photochemistry and Photobiology · doi:10.1111/j.1751-1097.2011.00995.x · Cited by 112 · see citing works
gamma-H2AX: Can it be established as a classical cancer prognostic factor?
Palla, V., Karaolanis, G., Katafigiotis, I. S., Anastasiou, I. P., Patapis, P., Dimitroulis, D., & Perrea, D. N. (2017) · Tumor Biology · doi:10.1177/1010428317695931 · Cited by 108 · see citing works
Bitomsky, N., & Hofmann, T. G. (2009) · FEBS Journal · doi:10.1111/j.1742-4658.2009.07331.x · Cited by 107 · see citing works
Targeting Hypoxic Cells through the DNA Damage Response
Olcina, M. M., Lecane, P. S., & Hammond, E. M. (2010) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-10-0286 · Cited by 109 · see citing works
Chk2-dependent phosphorylation of XRCC1 in the DNA damage response promotes base excision repair
Chou, W., Wang, H., Wong, F., Ding, S., Wu, P., Shieh, S., & Shen, C. (2008) · The EMBO Journal · doi:10.1038/emboj.2008.229 · Cited by 104 · see citing works
Targeting DNA repair in cancer: current state and novel approaches
Klinakis, A., Karagiannis, D., & Rampias, T. N. (2019) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-019-03299-8 · Cited by 105 · see citing works
NRF2 preserves genomic integrity by facilitating ATR activation and G2 cell cycle arrest
Sun, X., Wang, Y., Ji, K., Liu, Y., Kong, Y., Nie, S., Li, N., Hao, J., Xie, Y., Xu, C., et al. (2020) · Nucleic Acids Research · doi:10.1093/nar/gkaa631 · Cited by 102 · see citing works
Kerzendorfer, C., & O’Driscoll, M. (2009) · DNA Repair · doi:10.1016/j.dnarep.2009.04.018 · Cited by 97 · see citing works
Self-citationMislocalization of the MRN complex prevents ATR signaling during adenovirus infection
Carson, C. T., Orazio, N. I., Lee, D. V., Suh, J., Bekker‐Jensen, S., Araujo, F. D., Lakdawala, S. S., Lilley, C. E., Bártek, J., Lukas, J., et al. (2009) · The EMBO Journal · doi:10.1038/emboj.2009.15 · Cited by 93 · see citing works
Sivasubramaniam, S., Sun, X., Pan, Y.-R., Wang, S., & Lee, E. Y.-H. P. (2008) · Genes & Development · doi:10.1101/gad.1627708 · Cited by 91 · see citing works
Auclair, Y., Rouget, R., Affar, E. B., & Drobetsky, E. A. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0801585105 · Cited by 91 · see citing works
Kozlov, S., Waardenberg, A. J., Engholm‐Keller, K., Arthur, J. W., Graham, M. E., & Lavin, M. F. (2016) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m115.055723 · Cited by 89 · see citing works
Al-Aamri, H. M., Ku, H., Irving, H. R., Tucci, J., Meehan-Andrews, T., & Bradley, C. (2019) · BMC Cancer · doi:10.1186/s12885-019-5377-y · Cited by 88 · see citing works
Göder, A., Emmerich, C., Nikolova, T., Kiweler, N., Schreiber, M., Kühl, T., Imhof, D., Christmann, M., Heinzel, T., Schneider, G., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-03096-0 · Cited by 86 · see citing works
Shahabi, S., Kumaran, V., Castillo, J., Cong, Z., Nandagopal, G., Mullen, D. J., Alvarado, A., Correa, M. R., Saizan, A., Goel, R., et al. (2019) · Cancer Research · doi:10.1158/0008-5472.can-18-2034 · Cited by 85 · see citing works
Wu, Z., & Miyamoto, S. (2008) · The EMBO Journal · doi:10.1038/emboj.2008.127 · Cited by 82 · see citing works
Expression and functionality of histone H2A variants in cancer
Monteiro, F. L., Baptista, T., Amado, F. M. L., Vitorino, R. M. P., Jerónimo, C., & Helguero, L. A. (2014) · Oncotarget · doi:10.18632/oncotarget.2007 · Cited by 82 · see citing works
Telomerase Regulation from Beginning to the End
MacNeil, D., Bensoussan, H., & Autexier, C. (2016) · Genes · doi:10.3390/genes7090064 · Cited by 82 · see citing works
Chen, Y., Chen, C., Riley, D. J., & Chen, P. (2011) · Cell Cycle · doi:10.4161/cc.10.4.14814 · Cited by 82 · see citing works
ATR-dependent pathways control hEXO1 stability in response to stalled forks
El‐Shemerly, M., Heß, D., Pyakurel, A., Moselhy, S. S., & Ferrari, S. M. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm1052 · Cited by 82 · see citing works
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 81 · see citing works
Hastak, K., Paul, R. K., Agarwal, M. K., Thakur, V. S., Amin, A. R. M. R., Agrawal, S., Sramkoski, R. M., Jacobberger, J. W., Jackson, M. W., Stark, G. R., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0802080105 · Cited by 79 · see citing works
Cheng, W., Muftic, D., Müftüoğlu, M., Dawut, L., Morris, C., Helleday, T., Shiloh, Y., & Bohr, V. A. (2008) · Molecular Biology of the Cell · doi:10.1091/mbc.e07-07-0698 · Cited by 78 · see citing works
Cellular senescence: a hitchhiker’s guide
Aravinthan, A. D. (2015) · Human Cell · doi:10.1007/s13577-015-0110-x · Cited by 73 · see citing works
Selenium Compounds Activate Early Barriers of Tumorigenesis
Wu, M., Kang, M. M., Schoene, N. W., & Cheng, W. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.088781 · Cited by 73 · see citing works
Polo-Like Kinase 1 Depletion Induces DNA Damage in Early S Prior to Caspase Activation
Yim, H., & Erikson, R. L. (2009) · Molecular and Cellular Biology · doi:10.1128/mcb.01277-08 · Cited by 73 · see citing works
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
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 72 · see citing works
Pontano, L. L., Aggarwal, P., Barbash, O., Brown, E. J., Bassing, C. H., & Diehl, J. A. (2008) · Molecular and Cellular Biology · doi:10.1128/mcb.01085-08 · Cited by 71 · see citing works
ATM inhibitor KU-55933 increases the TMZ responsiveness of only inherently TMZ sensitive GBM cells
Nadkarni, A., Shrivastav, M., Mladek, A. C., Schwingler, P. M., Grogan, P. T., Chen, J., & Sarkaria, J. N. (2012) · Journal of Neuro-Oncology · doi:10.1007/s11060-012-0979-0 · Cited by 68 · see citing works
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
Role of homologous recombination in DNA interstrand crosslink repair
Hinz, J. M. (2010) · Environmental and Molecular Mutagenesis · doi:10.1002/em.20577 · Cited by 66 · see citing works
DNA damage responses in cells exposed to sulphur mustard
Jowsey, P. A., Williams, F. M., & Blain, P. G. (2011) · Toxicology Letters · doi:10.1016/j.toxlet.2011.11.009 · Cited by 65 · see citing works
Li‐Weber, M. (2014) · International Journal of Cancer · doi:10.1002/ijc.29013 · Cited by 63 · see citing works
Severe hypoxia induces complete antifolate resistance in carcinoma cells due to cell cycle arrest
Raz, S., Sheban, D., Gonen, N., Stark, M., Berman, B., & Assaraf, Y. G. (2014) · Cell Death and Disease · doi:10.1038/cddis.2014.39 · Cited by 64 · see citing works
Interplay between ATM and ATR in the regulation of common fragile site stability
Ozeri-Galai, E., Schwartz, M., Rahat, A., & Kerem, B. (2007) · Oncogene · doi:10.1038/sj.onc.1210849 · Cited by 64 · see citing works
Recruitment and activation of the ATM kinase in the absence of DNA-damage sensors
Hartlerode, A. J., Morgan, M. J., Wu, Y., Buis, J. M., & Ferguson, D. O. (2015) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.3072 · Cited by 63 · see citing works
Oh, K.-S., Bustin, M., Mazur, S. J., Appella, E., & Kraemer, K. H. (2011) · DNA Repair · doi:10.1016/j.dnarep.2010.09.004 · Cited by 60 · see citing works
- Authors
- Stiff, T., Walker, S. A., Cerosaletti, K., Goodarzi, A. A., Petermann, E., Concannon, P., O'Driscoll, M., & Jeggo, P. A.
- Affiliations
- University of Sussex (GB)
- Benaroya Research Institute (US)
- Corresponding author
- Jeggo, Penny A
- Venue
- The EMBO Journal
- Published
- 2006-11-23
- Volume
- 25
- Issue
- 24
- Pages
- 5775-5782
- ISSN
- 0261-4189 (ISSN-L)
- 1460-2075
- PMC
- PMC1698893
- OpenAlex
- W2018458310
- Cited by
- 360
- References
- 31
- Citations by year
- 2026: 4 · 2025: 5 · 2024: 7 · 2023: 6 · 2022: 10 · 2021: 12 · 2020: 11 · 2019: 18 · 2018: 11 · 2017: 17 · 2016: 14 · 2015: 20 · 2014: 20 · 2013: 29 · 2012: 27
- FWCI
- 13.20
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- Locations
- The EMBO Journal (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Figshare (submittedVersion, cc-by)
- University of Birmingham Research Portal (University of Birmingham) (submittedVersion)
- Sussex Research Online (University of Sussex) (submittedVersion)
- Funders
- National Cancer Institute (CA 57569, R01CA057569)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Effects of Radiation Exposure
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Kinase Regulation and GTPase Signaling
- Keywords
- ATM, ATR, ATM phosphorylation, replication fork stalling, UV-induced DNA damage, Chk2 phosphorylation, NBS1, MRE11, DNA double-strand breaks, single-stranded DNA
- MeSH terms
- Checkpoint Kinase 1, Animals, DNA Replication, DNA-Binding Proteins, Enzyme Activation, Fibroblasts, Histones, Humans, Hydroxyurea, Mitosis, Models, Biological, Nuclear Proteins, Phosphoproteins, Phosphorylation, Phosphoserine, Protein Kinases, Ultraviolet Rays, G2 Phase, Protein Serine-Threonine Kinases, Protein Structure, Tertiary, Cell Cycle Proteins, Tumor Suppressor Proteins, Mice, Ataxia Telangiectasia Mutated Proteins, Checkpoint Kinase 2
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