ATR and H2AX cooperate in maintaining genome stability under replication stress
Open accessAbstract
Chromosomal abnormalities are frequently caused by problems encountered during DNA replication. Although the ATR-Chk1 pathway has previously been implicated in preventing the collapse of stalled replication forks into double-strand breaks (DSB), the importance of the response to fork collapse in ATR-deficient cells has not been well characterized. Herein, we demonstrate that, upon stalled replication, ATR deficiency leads to the phosphorylation of H2AX by ATM and DNA-PKcs and to the focal accumulation of Rad51, a marker of homologous recombination and fork restart. Because H2AX has been shown to play a facilitative role in homologous recombination, we hypothesized that H2AX participates in Rad51-mediated suppression of DSBs generated in the absence of ATR. Consistent with this model, increased Rad51 focal accumulation in ATR-deficient cells is largely dependent on H2AX, and dual deficiencies in ATR and H2AX lead to synergistic increases in chromatid breaks and translocations. Importantly, the ATM and DNA-PK phosphorylation site on H2AX (Ser(139)) is required for genome stabilization in the absence of ATR; therefore, phosphorylation of H2AX by ATM and DNA-PKcs plays a pivotal role in suppressing DSBs during DNA synthesis in instances of ATR pathway failure. These results imply that ATR-dependent fork stabilization and H2AX/ATM/DNA-PKcs-dependent restart pathways cooperatively suppress double-strand breaks as a layered response network when replication stalls.
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?
ATR and ATM allow H2AX phosphorylation and spreading at damage sites, which changes chromatin structure near the damage and executes DNA repair through the HR pathway.
“Additionally, it is well established that ATR and ATM allow H2AX phosphorylation and spreading at the damage site, which changes the chromatin structure near the damage site and executes DNA repair through the HR pathway [21-23, 26, 63].”
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 [63]
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 double-stranded breaks induce histone H2AX phosphorylation on serine 139
Rogakou, E. P., Pilch, D. R., Orr, A. H., Ivanova, V. S., & Bonner, W. M. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.10.5858 · Cited by 5,438 · see citing works
A Third-Generation Lentivirus Vector with a Conditional Packaging System
Dull, T., Zufferey, R., Kelly, M., Mandel, R. J., Nguyen, M., Trono, D., & Naldini, L. (1998) · Journal of Virology · doi:10.1128/jvi.72.11.8463-8471.1998 · Cited by 3,341 · 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
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 · see citing works
Megabase Chromatin Domains Involved in DNA Double-Strand Breaks in Vivo
Rogakou, E. P., Boon, C., Redon, C., & Bonner, W. M. (1999) · The Journal of Cell Biology · doi:10.1083/jcb.146.5.905 · Cited by 2,422 · 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
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 · see citing works
ATM Phosphorylates Histone H2AX in Response to DNA Double-strand Breaks
Burma, S., Chen, B. P., Murphy, M., Kurimasa, A., & Chen, D. J. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.c100466200 · Cited by 1,954 · 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
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
Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress
Ward, I. M., & Chen, J. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.c100569200 · Cited by 1,150 · 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
RNF8 Transduces the DNA-Damage Signal via Histone Ubiquitylation and Checkpoint Protein Assembly
Huen, M. S. Y., Grant, R. A., Manke, I. A., Minn, K. T., Yu, X., Yaffe, M. B., & Chen, J. (2007) · Cell · doi:10.1016/j.cell.2007.09.041 · Cited by 1,027 · 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
<i>ATR</i> disruption leads to chromosomal fragmentation and early embryonic lethality
Brown, E. J., & Baltimore, D. (2000) · Genes & Development · doi:10.1101/gad.14.4.397 · Cited by 951 · see citing works
Self-citationChoreography of the DNA Damage Response
Lisby, M., Barlow, J. H., Burgess, R. C., & Rothstein, R. (2004) · Cell · doi:10.1016/j.cell.2004.08.015 · Cited by 891 · see citing works
Protection of telomeres through independent control of ATM and ATR by TRF2 and POT1
Denchi, E. L., & de Lange, T. (2007) · Nature · doi:10.1038/nature06065 · Cited by 880 · see citing works
Ruzankina, Y., Pinzon‐Guzman, C., Asare, A., Ong, T., Pontano, L. L., Cotsarelis, G., Zediak, V. P., Velez, M., Bhandoola, A., & Brown, E. J. (2007) · Cell stem cell · doi:10.1016/j.stem.2007.03.002 · Cited by 780 · see citing works
Self-citationByun, T. S., Pacek, M., Yee, M.-C., Walter, J. C., & Cimprich, K. A. (2005) · Genes & Development · doi:10.1101/gad.1301205 · Cited by 767 · see citing works
Weinert, T. A., Kiser, G. L., & Hartwell, L. H. (1994) · Genes & Development · doi:10.1101/gad.8.6.652 · Cited by 750 · see citing works
The DNA replication checkpoint response stabilizes stalled replication forks
Lopes, M., Cotta‐Ramusino, C., Pellicioli, A., Liberi, G., Plevani, P., Muzi-Falconi, M., Newlon, C. S., & Foiani, M. (2001) · Nature · doi:10.1038/35087613 · Cited by 749 · see citing works
Regulation of DNA replication fork progression through damaged DNA by the Mec1/Rad53 checkpoint
Tercero, J. A., & Diffley, J. F. X. (2001) · Nature · doi:10.1038/35087607 · Cited by 667 · see citing works
The cell-cycle checkpoint kinase Chk1 is required for mammalian homologous recombination repair
Sørensen, C. S., Hansen, L. T., Dziegielewski, J., Syljuåsen, R. G., Lundin, C., Bartek, J., & Helleday, T. (2005) · Nature Cell Biology · doi:10.1038/ncb1212 · Cited by 666 · see citing works
ATR Regulates Fragile Site Stability
Casper, A. M., Nghiem, P., Arlt, M. F., & Glover, T. W. (2002) · Cell · doi:10.1016/s0092-8674(02)01113-3 · Cited by 559 · see citing works
Cliby, W. A., Roberts, C. J., Cimprich, K. A., Stringer, C. M., Lamb, J. R., Schreiber, S. L., & Friend, S. H. (1998) · The EMBO Journal · doi:10.1093/emboj/17.1.159 · Cited by 534 · see citing works
Increased ionizing radiation sensitivity and genomic instability in the absence of histone H2AX
Bassing, C. H., Chua, K. F., Sekiguchi, J., Suh, H., Whitlow, S. R., Fleming, J. C., Monroe, B., Ciccone, D. N., Yan, C. T., Vlasáková, K., et al. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.122228699 · Cited by 525 · see citing works
Self-citationEssential and dispensable roles of ATR in cell cycle arrest and genome maintenance
Brown, E. J., & Baltimore, D. (2003) · Genes & Development · doi:10.1101/gad.1067403 · Cited by 511 · see citing works
Self-citationBassing, C. H., Suh, H., Ferguson, D. O., Chua, K. F., Manis, J. P., Eckersdorff, M., Gleason, M., Bronson, R. T., Lee, C., & Alt, F. W. (2003) · Cell · doi:10.1016/s0092-8674(03)00566-x · Cited by 480 · see citing works
Self-citationEnoch, T., & Nurse, P. (1990) · Cell · doi:10.1016/0092-8674(90)90669-6 · Cited by 460 · see citing works
Furuta, T., Takemura, H., Liao, Z.-Y., Aune, G. J., Redon, C., Sedelnikova, O. A., Pilch, D. R., Rogakou, E. P., Celeste, A., Chen, H. T., et al. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m300198200 · Cited by 449 · see citing works
Recovery from DNA replicational stress is the essential function of the S-phase checkpoint pathwayPreprint
Desany, B. A., Alcasabas, A. A., Bachant, J. B., & Elledge, S. J. (1998) · Genes & Development · doi:10.1101/gad.12.18.2956 · Cited by 448 · see citing works
ATR Homolog Mec1 Promotes Fork Progression, Thus Averting Breaks in Replication Slow Zones
Rita, S., & Kleckner, N. E. (2002) · Science · doi:10.1126/science.1071398 · Cited by 429 · see citing works
DNA repair mutants defining G2 checkpoint pathways in Schizosaccharomyces pombe.
Al-Khodairy, F. M., & Carr, A. M. (1992) · The EMBO Journal · doi:10.1002/j.1460-2075.1992.tb05179.x · Cited by 414 · see citing works
A Central Role for DNA Replication Forks in Checkpoint Activation and Response
Tercero, J. A., Longhese, M. P., & Diffley, J. F. X. (2003) · Molecular Cell · doi:10.1016/s1097-2765(03)00169-2 · Cited by 394 · see citing works
Fission yeast genes involved in coupling mitosis to completion of DNA replication.Preprint
Enoch, T., Carr, A. M., & Nurse, P. (1992) · Genes & Development · doi:10.1101/gad.6.11.2035 · Cited by 381 · 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
DNA polymerase stabilization at stalled replication forks requires Mec1 and the RecQ helicase Sgs1
Cobb, J. A., Bjergbæk, L., Shimada, K., Frei, C., & Gasser, S. M. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg391 · Cited by 333 · see citing works
Veuger, S. J., Curtin, N. J., Richardson, C. J., Smith, G. C. M., & Durkacz, B. W. (2003) · PubMed · doi:10.25405/ncl.34607331 · Cited by 332 · see citing works
Functional Interaction of Monoubiquitinated FANCD2 and BRCA2/FANCD1 in Chromatin
Wang, X., Andreassen, P. R., & D’Andrea, A. D. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.13.5850-5862.2004 · Cited by 332 · see citing works
Nghiem, P., Park, P. K., Kim, Y.-S., Vaziri, C., & Schreiber, S. L. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.161281798 · Cited by 290 · see citing works
Dysfunctional telomeres activate an ATM‐ATR‐dependent DNA damage response to suppress tumorigenesis
Guo, X., Deng, Y., Lin, Y., Cosme‐Blanco, W., Chan, S., He, H., Yuan, G., Brown, E. J., & Chang, S. (2007) · The EMBO Journal · doi:10.1038/sj.emboj.7601893 · Cited by 258 · see citing works
Self-citationThe ATR pathway: Fine-tuning the fork
PAULSEN, R., & Cimprich, K. A. (2007) · DNA repair · doi:10.1016/j.dnarep.2007.02.015 · Cited by 256 · see citing works
Chk1‐deficient tumour cells are viable but exhibit multiple checkpoint and survival defects
Zachos, G., Rainey, M. D., & Gillespie, D. A. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg060 · Cited by 247 · see citing works
Trenz, K., Smith, E., Smith, S. J., & Costanzo, V. (2006) · The EMBO Journal · doi:10.1038/sj.emboj.7601045 · Cited by 219 · see citing works
A Critical Role for the Ubiquitin-Conjugating Enzyme Ubc13 in Initiating Homologous Recombination
Zhao, G., Sonoda, E., Barber, L. J., Oka, H., Murakawa, Y., Yamada, K., Ikura, T., Wang, X., Kobayashi, M., Yamamoto, K., et al. (2007) · Molecular Cell · doi:10.1016/j.molcel.2007.01.029 · Cited by 218 · see citing works
Control of Sister Chromatid Recombination by Histone H2AX
Xie, A., Puget, N., Shim, I., Odate, S., Jarzyna, I., Bassing, C. H., Alt, F. W., & Scully, R. (2004) · Molecular Cell · doi:10.1016/j.molcel.2004.12.007 · Cited by 208 · see citing works
Self-citationPhosphorylation of the Bloom's Syndrome Helicase and Its Role in Recovery from S-Phase Arrest
Davies, S. L., North, P. S., Dart, D. A., Lakin, N. D., & Hickson, I. D. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.3.1279-1291.2004 · Cited by 208 · see citing works
Cobb, J. A., Schleker, T., Rojas, V., Bjergbæk, L., Tercero, J. A., & Gasser, S. M. (2005) · Genes & Development · doi:10.1101/gad.361805 · Cited by 197 · see citing works
Menoyo, A., Alazzouzi, H., Espín, E., Armengol, M., Yamamoto, H., & Schwartz, S. (2001) · PubMed · Cited by 151 · see citing works
A conserved pathway to activate BRCA1‐dependent ubiquitylation at DNA damage sites
Polanowska, J., Martin, J. S., García‐Muse, T., Petalcorin, M. I. R., & Boulton, S. J. (2006) · The EMBO Journal · doi:10.1038/sj.emboj.7601102 · Cited by 143 · see citing works
Sengupta, S., Robles, A. I., Linke, S. P., Sinogeeva, N. I., Zhang, R., Pedeux, R., Ward, I. M., Celeste, A., Nussenzweig, A., Chen, J., et al. (2004) · The Journal of Cell Biology · doi:10.1083/jcb.200405128 · Cited by 130 · see citing works
Wang, H., Wang, H., Powell, S. N., Iliakis, G., & Wang, Y. (2004) · Cancer Research · doi:10.1158/0008-5472.can-04-1289 · Cited by 130 · see citing works
Histone H2AX and Fanconi anemia FANCD2 function in the same pathway to maintain chromosome stability
Bogliolo, M., Lyakhovich, A., Callén, E., Castellà, M., Cappelli, E., Ramı́rez, M. J., Creus, A., Marcos, R., Kalb, R., Neveling, K., et al. (2007) · The EMBO Journal · doi:10.1038/sj.emboj.7601574 · Cited by 128 · see citing works
Depletion of CHK1, but not CHK2, induces chromosomal instability and breaks at common fragile sites
Durkin, S. G., Arlt, M. F., Howlett, N. G., & Glover, T. W. (2006) · Oncogene · doi:10.1038/sj.onc.1209466 · Cited by 127 · see citing works
ATR functions as a gene dosage‐dependent tumor suppressor on a mismatch repair‐deficient background
Fang, Y., Tsao, C., Goodman, B. K., Furumai, R., Tirado, C. A., Abraham, R. T., & Wang, X.-F. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600315 · Cited by 113 · see citing works
Replication and recombination intersect
Marians, K. J. (2000) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(00)00059-9 · Cited by 91 · see citing works
Rao, V. A., Fan, A. M., Meng, L., Doe, C. F., North, P. S., Hickson, I. D., & Pommier, Y. G. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.20.8925-8937.2005 · Cited by 87 · see citing works
Temporal separation of replication and recombination requires the intra-S checkpoint
Meister, P., Taddei, A., Vernis, L., Poidevin, M., Gasser, S. M., & Baldacci, G. (2005) · The Journal of Cell Biology · doi:10.1083/jcb.200410006 · Cited by 84 · see citing works
Davalos, A. R., Kaminker, P. G., Hansen, R. K., & Campisi, J. (2004) · Cell Cycle · doi:10.4161/cc.3.12.1286 · Cited by 58 · see citing works
Heterozygous ATR Mutations in Mismatch Repair–Deficient Cancer Cells Have Functional Significance
Lewis, K. A., Mullany, S. A., Thomas, B., CHIEN, J. R., Loewen, R. T., Shridhar, V., & Cliby, W. A. (2005) · Cancer Research · doi:10.1158/0008-5472.can-05-1019 · Cited by 58 · see citing works
Collaborative roles of γH2AX and the Rad51 paralog Xrcc3 in homologous recombinational repair
Sonoda, E., Zhao, G. Y., Kohzaki, M., Dhar, P. K., Kikuchi, K., Redon, C., Pilch, D. R., Bonner, W. M., Nakano, A., Watanabe, M., et al. (2007) · DNA Repair · doi:10.1016/j.dnarep.2006.10.025 · Cited by 47 · see citing works
Collaborative roles of gammaH2AX and the Rad51 paralog Xrcc3 in homologous recombinational repair
趙, 光. (2007) · Medical Entomology and Zoology · Cited by 39 · see citing works
Zhu, M., & Weiss, R. S. (2007) · Molecular Biology of the Cell · doi:10.1091/mbc.e06-10-0957 · Cited by 34 · see citing works
Flagged first, then by citations
Research works printed but not linked: 2
- Nghiem, P., Park, P. K., Kim, Y., Vaziri, C., and Schreiber, S. L. (2001) Proc. Natl. Acad. Sci. U. S. A. 98, 9092-9097
- Bassing, C. H., Chua, K. F., Sekiguchi, J., Suh, H., Whitlow, S. R., Fleming, J. C., Monroe, B. C., Ciccone, D. N., Yan, C., Vlasakova, K., Livingston, D. M., Ferguson, D. O., Scully, R., and Alt, F. W. (2002) Proc. Natl. Acad. Sci. U. S. A. 99, 8173-8178
Cited by
Sorted by citations
Causes and consequences of replication stress
Zeman, M. K., & Cimprich, K. A. (2014) · Nature Cell Biology · doi:10.1038/ncb2897 · Cited by 2,079 · 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
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 829 · see citing works
Buisson, R., Boisvert, J. L., Benes, C. H., & Zou, L. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.07.029 · Cited by 316 · see citing works
Replication Catastrophe: When a Checkpoint Fails because of Exhaustion
Toledo, L. I., Neelsen, K. J., & Lukas, J. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.05.001 · Cited by 228 · see citing works
Gilad, O., Nabet, B. Y., Ragland, R. L., Schoppy, D. W., Smith, K. D., Durham, A. C., & Brown, E. J. (2010) · Cancer Research · doi:10.1158/0008-5472.can-10-2286 · Cited by 225 · see citing works
Self-citationHuman CST promotes telomere duplex replication and general replication restart after fork stalling
Stewart, J. A., Wang, F., Fedor‐Chaiken, M., Kasbek, C., Chastain, P. D., Wright, W. E., & Price, C. M. (2012) · The EMBO Journal · doi:10.1038/emboj.2012.215 · Cited by 206 · see citing works
Potentiation of tumor responses to DNA damaging therapy by the selective ATR inhibitor VX-970
Hall, A. B., Newsome, D., Wang, Y., Boucher, D. M., Eustace, B. K., Gu, Y., Hare, B. J., Johnson, M., Li, H. Y., Milton, S., et al. (2014) · Oncotarget · doi:10.18632/oncotarget.2158 · Cited by 198 · see citing works
Targeting ATR in DNA damage response and cancer therapeutics
Fokas, E., Prevo, R., Hammond, E. M., Brunner, T. B., McKenna, W. G., & Muschel, R. J. (2013) · Cancer Treatment Reviews · doi:10.1016/j.ctrv.2013.03.002 · Cited by 192 · see citing works
Oncogenic stress sensitizes murine cancers to hypomorphic suppression of ATR
Schoppy, D. W., Ragland, R. L., Gilad, O., Shastri, N., Peters, A. A., Murga, M., Fernández-Capetillo, Ó., Diehl, J. A., & Brown, E. J. (2011) · Journal of Clinical Investigation · doi:10.1172/jci58928 · Cited by 180 · see citing works
Self-citationJossé, R., Martin, S. E., Guha, R., Ormanoglu, P., Pfister, T. D., Reaper, P. M., Barnes, C. S., Jones, J. L., Charlton, P., Pollard, J. R., et al. (2014) · Cancer Research · doi:10.1158/0008-5472.can-13-3369 · Cited by 173 · see citing works
Ammazzalorso, F., Pirzio, L. M., Bignami, M., Franchitto, A., & Pichierri, P. (2010) · The EMBO Journal · doi:10.1038/emboj.2010.205 · Cited by 171 · see citing works
Histone Modifiers in Cancer: Friends or Foes?
Cohen, I., Poręba, E., Kamieniarz-Gdula, K., & Schneider, R. (2011) · Genes & Cancer · doi:10.1177/1947601911417176 · Cited by 171 · see citing works
Fu, S., Li, Z., Xiao, L., Hu, W., Zhang, L., Xie, B., Zhou, Q., He, J., Qiu, Y., Wen, M., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.07.002 · Cited by 169 · see citing works
An, J., Huang, Y.-C., Xu, Q.-Z., Zhou, L.-J., Shang, Z., Huang, B., Wang, Y., Liu, X.-D., Wu, D.-C., & Zhou, P. (2010) · BMC Molecular Biology · doi:10.1186/1471-2199-11-18 · Cited by 163 · see citing works
Wip1 Directly Dephosphorylates γ-H2AX and Attenuates the DNA Damage Response
Cha, H., Lowe, J. M., Li, H., Lee, J., Belova, G. I., Bulavin, D. V., & Fornace, A. J. (2010) · Cancer Research · doi:10.1158/0008-5472.can-09-4244 · Cited by 151 · see citing works
Trial Watch: Targeting ATM–CHK2 and ATR–CHK1 pathways for anticancer therapy
Manic, G., Obrist, F., Sistigu, A., & Vitale, I. (2015) · Molecular & Cellular Oncology · doi:10.1080/23723556.2015.1012976 · Cited by 147 · see citing works
More forks on the road to replication stress recovery
Allen, C., Ashley, A. K., Hromas, R., & Nickoloff, J. A. (2011) · Journal of Molecular Cell Biology · doi:10.1093/jmcb/mjq049 · Cited by 147 · see citing works
Firsanov, D., Solovjeva, L. V., & Svetlova, M. (2011) · Clinical Epigenetics · doi:10.1007/s13148-011-0044-4 · Cited by 139 · see citing works
Efficacy of CHK inhibitors as single agents in MYC-driven lymphoma cells
Ferrao, P. T., Bukczynska, E. P., Johnstone, R. W., & McArthur, G. A. (2012) · Oncogene · doi:10.1038/onc.2011.358 · Cited by 133 · see citing works
Ogi, T., Walker, S., Stiff, T., Hobson, E., Limsirichaikul, S., Carpenter, G., Prescott, K., Suri, M., Byrd, P. J., Matsuse, M., et al. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1002945 · Cited by 117 · see citing works
RNF4 and PLK1 are required for replication fork collapse in ATR-deficient cellsPreprint
Ragland, R. L., Patel, S., Rivard, R. S., Smith, K. D., Peters, A. A., Bielinsky, A., & Brown, E. J. (2013) · Genes & Development · doi:10.1101/gad.223180.113 · Cited by 113 · see citing works
Self-citationEstrogen receptor α-mediated transcription induces cell cycle-dependent DNA double-strand breaks
Williamson, L. M., & Lees‐Miller, S. P. (2010) · Carcinogenesis · doi:10.1093/carcin/bgq255 · Cited by 111 · see citing works
Lee, W. T. C., Yin, Y., Morten, M. J., Tonzi, P., Gwo, P. P., Odermatt, D. C., Modesti, M., Cantor, S. B., Gari, K., Huang, T. T., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-22830-9 · Cited by 107 · see citing works
TopBP1/Dpb11 binds DNA anaphase bridges to prevent genome instability
Germann, S. M., Schramke, V., Pedersen, R. T., Gallina, I., Eckert‐Boulet, N., Oestergaard, V. H., & Lisby, M. (2013) · The Journal of Cell Biology · doi:10.1083/jcb.201305157 · Cited by 106 · see citing works
Ruzankina, Y., Schoppy, D. W., Asare, A., Clark, C. E., Vonderheide, R. H., & Brown, E. J. (2009) · Nature Genetics · doi:10.1038/ng.441 · Cited by 104 · see citing works
Self-citationTargeting 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
Chiu, C., Haung, J.-W., Chang, F., Huang, K.-J., Huang, H.-M., Huang, H., Chou, C., Wu, Y., & Chang, H. (2013) · PLoS ONE · doi:10.1371/journal.pone.0064739 · Cited by 98 · see citing works
Smith, K. D., Fu, M. A., & Brown, E. J. (2009) · The Journal of Cell Biology · doi:10.1083/jcb.200905006 · Cited by 92 · see citing works
Self-citationXu, L. H., Huang, M., Fang, S. G., & Liu, D. X. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.242206 · Cited by 91 · see citing works
Wang, J., He, J., Su, F., Ding, N., Hu, W., Yao, B. W., Wang, W., & Zhou, G. (2013) · Cell Death and Disease · doi:10.1038/cddis.2013.227 · Cited by 92 · see citing works
Fulka, J., & Langerová, A. (2014) · Development · doi:10.1242/dev.105940 · Cited by 87 · see citing works
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 · see citing works
“Additionally, it is well established that ATR and ATM allow H2AX phosphorylation and spreading at the damage site, which changes the chromatin structure near the damage site and executes DNA repair through the HR pathway [21-23, 26, 63].”
BackgroundSrivastava, N., Manvati, S., Srivastava, A., Pal, R., Ponnusamy, K., Chattopadhyay, S., Gochhait, S., Dua, R., & Bamezai, R. N. K. (2011) · Breast Cancer Research · doi:10.1186/bcr2861 · Cited by 82 · see citing works
Hammack, C., Ogden, S. C., Madden, J. C., Medina, A., Xu, C., Phillips, E. O. N., Son, Y., Cone, A. S., Giovinazzi, S., Didier, R., et al. (2019) · Journal of Virology · doi:10.1128/jvi.00638-19 · Cited by 73 · see citing works
Wangsa, D., Quintanilla, I., Torabi, K., Vila-Casadesús, M., Ercilla, A., Klus, G. T., Yüce, Z., Galofré, C., Cuatrecasas, M., Lozano, J. J., et al. (2018) · The FASEB Journal · doi:10.1096/fj.201700247rr · Cited by 70 · see citing works
Her, J., Ray, C., Altshuler, J., Zheng, H., & Bunting, S. F. (2018) · Molecular and Cellular Biology · doi:10.1128/mcb.00472-17 · Cited by 67 · see citing works
Walters, D. K., Wu, X., Tschumper, R. C., Arendt, B. K., Huddleston, P. M., Henderson, K. J., Dispenzieri, A. A., & Jelinek, D. F. (2011) · Leukemia · doi:10.1038/leu.2011.94 · Cited by 67 · see citing works
DNA Damage and Repair in Atherosclerosis: Current Insights and Future Perspectives
Cervelli, T., Borghini, A., Galli, A., & Andreassi, M. G. (2012) · International Journal of Molecular Sciences · doi:10.3390/ijms131216929 · Cited by 66 · see citing works
RhoJ Regulates Melanoma Chemoresistance by Suppressing Pathways That Sense DNA Damage
Ho, H., Aruri, J., Kapadia, R., Mehr, H., White, M. A., & Ganesan, A. K. (2012) · Cancer Research · doi:10.1158/0008-5472.can-12-0775 · Cited by 64 · see citing works
Histone H2A variants: Diversifying chromatin to ensure genome integrity
Oberdoerffer, P., & Miller, K. M. (2022) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2022.03.011 · Cited by 61 · see citing works
The Werner syndrome protein: linking the replication checkpoint response to genome stability
Pichierri, P., Ammazzalorso, F., Bignami, M., & Franchitto, A. (2011) · Aging · doi:10.18632/aging.100293 · Cited by 58 · see citing works
Svetlova, M., Solovjeva, L., & Tomilin, N. V. (2009) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2009.08.001 · Cited by 59 · see citing works
Loss of Slug Compromises DNA Damage Repair and Accelerates Stem Cell Aging in Mammary Epithelium
Gross, K. M., Zhou, W., Breindel, J. L., Ouyang, J., Jin, D. X., Sokol, E. S., Gupta, P. B., Huber, K., Zou, L., & Kuperwasser, C. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.06.043 · Cited by 58 · see citing works
Metnase promotes restart and repair of stalled and collapsed replication forks
Haro, L. P. D., Wray, J. W., Williamson, E. A., Durant, S. T., Corwin, L. K., Gentry, A. C., Osheroff, N., Lee, S., Hromas, R., & Nickoloff, J. A. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq339 · Cited by 58 · see citing works
Maxwell, T., Lee, K. E., Kim, S. Y., & Nam, K. (2018) · International Journal of Oncology · doi:10.3892/ijo.2018.4271 · Cited by 58 · see citing works
Feng, Z., & Zhang, J. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr748 · Cited by 48 · see citing works
Köcher, S., Rieckmann, T., Rohaly, G., Mansour, W. Y., Dikomey, E., Dornreiter, I., & Dahm‐Daphi, J. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks604 · Cited by 47 · see citing works
Saxena, S., Dixit, S., Somyajit, K., & Nagaraju, G. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.09.008 · Cited by 49 · see citing works
Vandersickel, V., Depuydt, J., BOCKSTAELE, B. V., Perletti, G., Philippé, J., Thierens, H., & Vral, A. (2010) · Journal of Radiation Research · doi:10.1269/jrr.10033 · Cited by 45 · see citing works
Replication stress response in cancer stem cells as a target for chemotherapy
Manic, G., Sistigu, A., Corradi, F., Musella, M., Maria, R. D., & Vitale, I. (2018) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2018.08.003 · Cited by 43 · see citing works
Tiwari, M. K., Adaku, N., Peart, N. J., & Rogers, F. A. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw515 · Cited by 42 · see citing works
Hromas, R., Kim, H.-S., Sidhu, G. S., Williamson, E. A., Jaiswal, A. S., Totterdale, T. A., Nole, J., Lee, S., Nickoloff, J. A., & Kong, K. Y. (2017) · Breast Cancer Research · doi:10.1186/s13058-017-0912-8 · Cited by 40 · see citing works
Mimmler, M., Peter, S., Kraus, A., Stroh, S., Nikolova, T., Seiwert, N., Hasselwander, S., Neitzel, C., Haub, J., Monien, B. H., et al. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw791 · Cited by 39 · see citing works
Sobanski, T., Suraweera, A., Burgess, J. T., Richard, I. A., Cheong, C. M., Dave, K. A., Rose, M., Adams, M. N., O'Byrne, K. J., Richard, D. J., et al. (2023) · Scientific Reports · doi:10.1038/s41598-023-41133-1 · Cited by 38 · see citing works
Sherman, M. Y., Le, M., Stampfer, M. R., Gabai, V. L., & Yaglom, J. A. (2011) · Aging Cell · doi:10.1111/j.1474-9726.2011.00736.x · Cited by 37 · see citing works
ATR inhibition rewires cellular signaling networks induced by replication stress
Wagner, S., Oehler, H., Voigt, A., Dalic, D., Freiwald, A., Serve, H. L., & Beli, P. (2015) · PROTEOMICS · doi:10.1002/pmic.201500172 · Cited by 38 · see citing works
ATR Mutations Promote the Growth of Melanoma Tumors by Modulating the Immune Microenvironment
Chen, C., Ruiz, R., Vasudeva, P., Espitia, F., Krasieva, T. B., de Feraudy, S. M., Tromberg, B. J., Huang, S., Garner, C. P., Wu, J., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.02.040 · Cited by 37 · see citing works
Replication Stress: A Lifetime of Epigenetic Change
Khurana, S., & Oberdoerffer, P. (2015) · Genes · doi:10.3390/genes6030858 · Cited by 36 · see citing works
Pelletier, J., Riaño‐Canalias, F., Almacellas, E., Mauvezin, C., Samino, S., Feu, S., Menoyo, S., Domostegui, A., Garcia‐Cajide, M., Salazar, R., et al. (2020) · The EMBO Journal · doi:10.15252/embj.2019103838 · Cited by 35 · see citing works
Kay, J. E., Corrigan, J. J., Armijo, A. L., Nazari, I. S., Kohale, I. N., Torous, D. K., Avlasevich, S. L., Croy, R. G., Wadduwage, D. N., Carrasco, S. E., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.108864 · Cited by 34 · see citing works
Gu, L., Chu, P. G., Lingeman, R. G., McDaniel, H., Kechichian, S., Hickey, R. J., Liu, Z., Yuan, Y., Sandoval, J. A., Fields, G. B., et al. (2015) · EBioMedicine · doi:10.1016/j.ebiom.2015.11.016 · Cited by 32 · see citing works
Evaluation of ATM Kinase Inhibitor KU-55933 as Potential Anti-Toxoplasma gondii Agent
Lopez, J. M., Ganuza, A., Bogado, S. S., Muñoz, D., Ruiz, D. M., Sullivan, W. J., Vanagas, L., & Angel, S. O. (2019) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2019.00026 · Cited by 32 · see citing works
DNA Damage Response and Repair in Boron Neutron Capture Therapy
Mechetin, G. V., & Zharkov, D. O. (2023) · Genes · doi:10.3390/genes14010127 · Cited by 30 · see citing works
Ip, L. R. H., Poulogiannis, G., Cia, F., Sasaki, J., Kofuji, S., Spanswick, V. J., Hochhauser, D., Hartley, J. A., Sasaki, T., & Gewinner, C. A. (2015) · Oncotarget · doi:10.18632/oncotarget.3307 · Cited by 30 · see citing works
Orsburn, B. C., Escudero, B., Prakash, M., Gesheva, S. I., Liu, G., Huso, D. L., & Franco, S. (2010) · Molecular and Cellular Biology · doi:10.1128/mcb.00091-10 · Cited by 30 · see citing works
Ye, W., & Blain, S. W. (2010) · Brain · doi:10.1093/brain/awq139 · Cited by 30 · see citing works
Targeting DNA Damage Response as a Strategy to Treat HPV Infections
Banerjee, N. S., Moore, D. W., Parker, C. J., Broker, T. R., & Chow, L. T. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20215455 · Cited by 29 · see citing works
Development of pharmacodynamic biomarkers for ATR inhibitors
Chen, T., Middleton, F. K., Falcon, S. C., Reaper, P. M., Pollard, J. R., & Curtin, N. J. (2014) · Molecular Oncology · doi:10.1016/j.molonc.2014.09.012 · Cited by 27 · see citing works
Thakur, V., Zhang, K., Savadelis, A., Zmina, P. M., Aguila, B., Welford, S. M., Abdul‐Karim, F. W., Bonk, K. W., Keri, R. A., & Bedogni, B. (2018) · Cancer Letters · doi:10.1016/j.canlet.2018.11.031 · Cited by 26 · see citing works
Li, X., Dean, D. C., Cote, G. M., Zou, L., Hornicek, F. J., Yu, S., & Duan, Z. (2020) · Therapeutic Advances in Medical Oncology · doi:10.1177/1758835920956900 · Cited by 25 · see citing works
TACC3 deregulates the DNA damage response and confers sensitivity to radiation and PARP inhibition
Ha, G., Kim, J.-L., Petersson, A., Oh, S. H., Denning, M. F., Patel, T., & Breuer, E.-K. (2014) · Oncogene · doi:10.1038/onc.2014.105 · Cited by 24 · see citing works
Sokòl, A. M., Cruet-Hennequart, S., Pasero, P., & Carty, M. P. (2013) · Scientific Reports · doi:10.1038/srep03277 · Cited by 23 · see citing works
Rybaczek, D., & Kowalewicz‐Kulbat, M. (2011) · Histochemistry and Cell Biology · doi:10.1007/s00418-011-0793-3 · Cited by 24 · see citing works
Ikezu, T., Chen, C.-D., DeLeo, A. M., Zeldich, E., Fallin, M. D., Kanaan, N. M., Lunetta, K. L., Abraham, C. R., Logue, M. W., & Farrer, L. A. (2018) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-018-9781-x · Cited by 22 · see citing works
Paths from DNA damage and signaling to genome rearrangements via homologous recombination
Nickoloff, J. A. (2017) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2017.07.008 · Cited by 21 · see citing works
The relationship between histone posttranslational modification and DNA damage signaling and repair
Sharma, A. K., & Hendzel, M. J. (2018) · International Journal of Radiation Biology · doi:10.1080/09553002.2018.1516911 · Cited by 20 · see citing works
Age-Dependent Changes in DNA Repair in Radiation-Exposed Mice
Kovalchuk, I., Golubov, A., Koturbash, I. V., Kutanzi, K. R., Martin, O. A., & Kovalchuk, O. (2014) · Radiation Research · doi:10.1667/rr13697.1 · Cited by 21 · see citing works
Evison, B. J., Actis, M. L., Wu, S. Z., Shao, Y., Heath, R. J., Yang, L., & Fujii, N. (2014) · Bioorganic & Medicinal Chemistry · doi:10.1016/j.bmc.2014.09.058 · Cited by 19 · see citing works
Chen, S., Pan, C., Huang, J., & Liu, T. (2024) · The EMBO Journal · doi:10.1038/s44318-024-00066-9 · Cited by 18 · see citing works
XLF and H2AX function in series to promote replication fork stability
Chen, B.-R., Quinet, A., Byrum, A. K., Jackson, J., Berti, M., Thangavel, S., Bredemeyer, A. L., Hindi, I., Mosammaparast, N., Tyler, J. K., et al. (2019) · The Journal of Cell Biology · doi:10.1083/jcb.201808134 · Cited by 18 · see citing works
Quantitative profiling of adaptation to cyclin E overproduction
Limas, J. C., Littlejohn, A. N., House, A. M., Kedziora, K. M., Mouery, B. L., Ma, B., Fleifel, D., Walens, A., Aleman, M. M., Dominguez, D., et al. (2022) · Life Science Alliance · doi:10.26508/lsa.202201378 · Cited by 17 · see citing works
Marrero, A. M., Lawrence, S. M., Wilsker, D. F., Voth, A. R., & Kinders, R. J. (2016) · Seminars in Oncology · doi:10.1053/j.seminoncol.2016.06.003 · Cited by 17 · see citing works
Chromatin as a Platform for Modulating the Replication Stress Response
Fournier, L.-A., Kumar, A., & Stirling, P. C. (2018) · Genes · doi:10.3390/genes9120622 · Cited by 17 · see citing works
ATR Suppresses Endogenous DNA Damage and Allows Completion of Homologous Recombination Repair
Brown, A., Sager, B. W., Gorthi, A., Tonapi, S. S., Brown, E. J., & Bishop, A. J. R. (2014) · PLoS ONE · doi:10.1371/journal.pone.0091222 · Cited by 17 · see citing works
Self-citationVillicaña, C., Cruz‐Becerra, G., & Zurita, M. (2013) · Journal of Cell Science · doi:10.1242/jcs.122721 · Cited by 17 · see citing works
SAF-A promotes origin licensing and replication fork progression to ensure robust DNA replication
Connolly, C., Takahashi, S., Miura, H., Hiratani, I., Gilbert, N., Donaldson, A. D., & Hiraga, S. (2021) · Journal of Cell Science · doi:10.1242/jcs.258991 · Cited by 16 · see citing works
Histone dynamics during DNA replication stress
Hsu, C.-L., Chong, S. Y., Lin, C., & Kao, C.-F. (2021) · Journal of Biomedical Science · doi:10.1186/s12929-021-00743-5 · Cited by 15 · see citing works
Wakabayashi, M., Ishii, C., Hatakeyama, S., Inoue, H., & Tanaka, S. (2010) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2010.05.010 · Cited by 13 · see citing works
Guggulsterone-Mediated Enhancement of Radiosensitivity in Human Tumor Cell Lines
Choudhuri, R., DeGraff, W., Gamson, J., Mitchell, J. B., & Cook, J. A. (2011) · Frontiers in Oncology · doi:10.3389/fonc.2011.00019 · Cited by 14 · see citing works
Lebel, E. A., Boukamp, P., & Tafrov, S. T. (2010) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-010-0390-0 · Cited by 14 · see citing works
Core and Linker Histone Modifications Involved in the DNA Damage Response
Chubb, J. E., & Rea, S. (2009) · Sub-cellular biochemistry/Subcellular biochemistry · doi:10.1007/978-90-481-3471-7_2 · Cited by 12 · see citing works
Redundant and Nonredundant Functions of ATM and H2AX in αβ T-Lineage Lymphocytes
Yin, B., Lee, B.-S., Yang-Iott, K. S., Sleckman, B. P., & Bassing, C. H. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.1200829 · Cited by 10 · see citing works
Self-citationNew human ATM variants are able to regain ATM functions in ataxia telangiectasia disease
Ricci, A., Biancucci, F., Morganti, G., Magnani, M., & Menotta, M. (2022) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-022-04625-3 · Cited by 9 · see citing works
ATRX loss inhibits DDR to strengthen radio-sensitization in p53-deficent HCT116 cells
Qin, L., Tang, G., Gui, R., Yang, Y., Li, W., Xu, W., Tian, H., Yu, L., Yang, X., & Wang, Z. (2025) · Scientific Reports · doi:10.1038/s41598-024-85085-6 · Cited by 7 · see citing works
Targeting extracellular matrix remodeling sensitizes glioblastoma to ionizing radiation
Thakur, V., Thakur, V. S., Aguila, B., Slepak, T. I., Wang, M., Song, W., Konai, M. M., Mobashery, S., Chang, M., Rana, A. B., et al. (2022) · Neuro-Oncology Advances · doi:10.1093/noajnl/vdac147 · Cited by 6 · see citing works
Structural insights into γH2Ax containing nucleosomes
Panigrahi, R., Edwards, R. A., Islam, M. T., Lu, J., Kulepa, A., Kim, T., & Glover, J. N. M. (2025) · Nucleic Acids Research · doi:10.1093/nar/gkaf1028 · Cited by 5 · see citing works
Targeting DNA Repair and Chromatin Crosstalk in Cancer Therapy
Johnson, D. P., Chandrasekharan, M. B., Dutreix, M., & Bhaskara, S. (2021) · Cancers · doi:10.3390/cancers13030381 · Cited by 5 · see citing works
Cristaldi, C., Cartagena, A. M. S., Ganuza, A., Sullivan, W. J., Angel, S. O., & Vanagas, L. (2023) · International Journal for Parasitology Drugs and Drug Resistance · doi:10.1016/j.ijpddr.2023.11.004 · Cited by 4 · see citing works
Yin, H., Zheng, Y., Chen, M., Ding, M., Zhang, L., Wang, R., Wang, C., Jia, J. F., & Liu, X. (2024) · Environmental Pollution · doi:10.1016/j.envpol.2024.125377 · Cited by 4 · see citing works
- Authors
- Chanoux, R. A., Yin, B., Urtishak, K. A., Asare, A., Bassing, C. H., & Brown, E. J.
- Affiliations
- University of Pennsylvania (US)
- Children's Hospital of Philadelphia (US)
- Corresponding author
- Brown, Eric J.
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2009-02
- Volume
- 284
- Issue
- 9
- Pages
- 5994-6003
- ISSN
- 0021-9258 (ISSN-L)
- PMC
- PMC2645842
- OpenAlex
- W2091890593
- Cited by
- 130
- References
- 63
- Citations by year
- 2026: 3 · 2025: 8 · 2024: 3 · 2023: 5 · 2022: 4 · 2021: 6 · 2020: 4 · 2019: 10 · 2018: 12 · 2017: 5 · 2016: 4 · 2015: 7 · 2014: 10 · 2013: 14 · 2012: 6
- FWCI
- 3.98
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Cancer Research Institute
- Pennsylvania Department of Health
- National Institutes of Health
- National Institute on Aging (R01AG027376)
- National Cancer Institute (R01CA125195)
- Abramson Family Cancer Research Institute
- 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 › Genetics › Bacterial Genetics and Biotechnology
- Keywords
- ATR, H2AX, replication stress, genome stability, replication fork collapse, DNA double-strand breaks, ATM, DNA-PKcs, RAD51, homologous recombination, fork restart, chromatid breaks, translocation, checkpoint signaling
- MeSH terms
- Animals, Cells, Cultured, DNA Replication, DNA-Binding Proteins, Embryo, Mammalian, Fibroblasts, Histones, Metaphase, Mitosis, Nuclear Proteins, Phosphorylation, Radiation, Ionizing, RNA, Messenger, S Phase, Protein Serine-Threonine Kinases, Mice, Knockout, Cell Cycle Proteins, Reverse Transcriptase Polymerase Chain Reaction, Tumor Suppressor Proteins, Spectral Karyotyping, RNA, Small Interfering, Genomic Instability, Rad51 Recombinase, Mice, DNA-Activated Protein Kinase, DNA Breaks, Double-Stranded, 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