The controlling role of ATM in homologous recombinational repair of DNA damage
Open accessAbstract
The human genetic disorder ataxia telangiectasia (A-T), caused by mutation in the ATM gene, is characterized by chromosomal instability, radiosensitivity and defective cell cycle checkpoint activation. DNA double-strand breaks (dsbs) persist in A-T cells after irradiation, but the underlying defect is unclear. To investigate ATM's interactions with dsb repair pathways, we disrupted ATM along with other genes involved in the principal, complementary dsb repair pathways of homologous recombination (HR) or non-homologous end-joining (NHEJ) in chicken DT40 cells. ATM(-/-) cells show altered kinetics of radiation-induced Rad51 and Rad54 focus formation. Ku70-deficient (NHEJ(-)) ATM(-/-) chicken DT40 cells show radiosensitivity and high radiation-induced chromosomal aberration frequencies, while Rad54-defective (HR(-)) ATM(-/-) cells show only slightly elevated aberration levels after irradiation, placing ATM and HR on the same pathway. These results reveal that ATM defects impair HR-mediated dsb repair and may link cell cycle checkpoints to HR activation.
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Both homologous recombination and nonhomologous end-joining double-strand break repair are modulated by the ATM- and Chk2-dependent checkpoint.
“Both homologous recombination and nonhomologous end-joining pathways of double-strand break repair have been shown to be modulated by the ATM-and Chk2-dependent checkpoint (23)(24)(25).”
From Phosphorylation of Nucleotide Excision Repair Factor Xeroderma Pigmentosum Group A by Ataxia Telangiectasia Mutated and Rad3-Related–Dependent Checkpoint Pathway Promotes Cell Survival in Response to UV Irradiation (2006) · cites this paper as [24]
The Discussion (page unavailable) says ATM controls homologous recombinational repair. It describes a link between ATM and nonhomologous end-joining as suggested by yeast data, not as a finding established by this paper. The Introduction (page unavailable) identifies Chk2 as an ATM target, but does not show that a Chk2-dependent checkpoint modulates both repair pathways. (LLM, conf=0.86)
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BackgroundToward Maintaining the Genome: DNA Damage and Replication Checkpoints
Nyberg, K. A., Michelson, R. J., Putnam, C. W., & Weinert, T. A. (2002) · Annual Review of Genetics · doi:10.1146/annurev.genet.36.060402.113540 · Cited by 770 · see citing works
“ATM is linked to the repair of DNA damage by homologous recombination (HR) based on the fact that AT cells defective in HR components ( rad54 mutation) are no more sick than AT cells, whereas AT cells defective for non-homologous end-joining (NHEJ;ku70mutation) show drastic increases in chromosomal instability (134).”
BackgroundInterfaces Between the Detection, Signaling, and Repair of DNA Damage
Rouse, J. W., & Jackson, S. P. (2002) · Science · doi:10.1126/science.1074740 · Cited by 688 · see citing works
ATM and ATR: networking cellular responses to DNA damage
Shiloh, Y. (2001) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(00)00159-3 · Cited by 601 · see citing works
Regulation and mechanisms of mammalian double-strand break repair
Valerie, K. C., & Povirk, L. F. (2003) · Oncogene · doi:10.1038/sj.onc.1206679 · Cited by 572 · see citing works
ATM and Artemis promote homologous recombination of radiation‐induced DNA double‐strand breaks in G2
Beucher, A., Birraux, J., Tchouandong, L., Barton, O., Shibata, A., Conrad, S., Goodarzi, A. A., Krempler, A., Jeggo, P. A., & Löbrich, M. (2009) · The EMBO Journal · doi:10.1038/emboj.2009.276 · Cited by 548 · see citing works
“Previous studies have provided evidence that ATM is required for at least a component of HR (Morrison et al, 2000; Shrivastav et al, 2009), but this has not previously been shown for Artemis.”
BackgroundResultThe Human LINE-1 Retrotransposon Creates DNA Double-strand Breaks
Gasior, S. L., Wakeman, T. P., Xu, B., & Deininger, P. L. (2006) · Journal of Molecular Biology · doi:10.1016/j.jmb.2006.01.089 · Cited by 519 · see citing works
Homologous recombinational repair of DNA ensures mammalian chromosome stability
Thompson, L. H., & Schild, D. (2001) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/s0027-5107(01)00115-4 · Cited by 426 · see citing works
Recombinational DNA repair and human disease
Thompson, L. H., & Schild, D. (2002) · Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis · doi:10.1016/s0027-5107(02)00224-5 · Cited by 417 · see citing works
Mismatch repair and DNA damage signalling
Stojic, L., Brun, R., & Jiricny, J. (2004) · DNA Repair · doi:10.1016/j.dnarep.2004.06.006 · Cited by 396 · see citing works
Genotoxic Stress Abrogates Renewal of Melanocyte Stem Cells by Triggering Their Differentiation
Inomata, K., Aoto, T., Binh, N. T., Okamoto, N., Tanimura, S., Wakayama, T., Iseki, S., Hara, E., Masunaga, T., Shimizu, H., et al. (2009) · Cell · doi:10.1016/j.cell.2009.03.037 · Cited by 368 · see citing works
“As DDR is affected by Atm deficiency (Kuhne et al., 2004; McKinnon, 2004; Morrison et al., 2000; Takubo et al., 2008), our data indicate that ATM efficiently protects MSCs from their differentiation in the niche by activating the downstream DDR pathways.”
Thompson, L. H. (2012) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2012.06.002 · Cited by 357 · see citing works
DNA repair deficiency in neurodegeneration
Jeppesen, D. K., Bohr, V. A., & Stevnsner, T. (2011) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2011.04.013 · Cited by 349 · see citing works
“ATM together with the MRN complex may also function in DSBR via HR (Kobayashi, 2004; Morrison et al., 2000).”
Biomarkers for Homologous Recombination Deficiency in Cancer
Hoppe, M. M., Sundar, R., Tan, D. S. P., & Jeyasekharan, A. D. (2018) · JNCI: Journal of the National Cancer Institute · doi:10.1093/jnci/djy085 · Cited by 329 · see citing works
“Cells with loss of the upstream DDR components of the MRN complex (114) and ATM form RAD51 foci in vitro, but display defects in homologous recombination (115,116).”
BackgroundChen, C.-C., Feng, W., Lim, P. X., Kass, E. M., & Jasin, M. (2017) · Annual Review of Cancer Biology · doi:10.1146/annurev-cancerbio-030617-050502 · Cited by 313 · see citing works
“…HDR. Loss of ATM reduces HDR in some contexts but not in others (AlvarezQuilon et al. 2014, Beucher et al. 2009, Chen et al. 2017, Kass et al. 2013, Morrison et al. 2000, Rass et al. 2013, White et al. 2010), possibly due in part to redundancy of substrate phosphorylation by other PI3K-related…”
BackgroundThe combined status of ATM and p53 link tumor development with therapeutic responsePreprint
Jiang, H., Reinhardt, H. C., Bártková, J., Tommiska, J., BLOMQVIST, C. P., Nevanlinna, H. A., Bártek, J., Yaffe, M. B., & Hemann, M. T. (2009) · Genes & Development · doi:10.1101/gad.1815309 · Cited by 303 · see citing works
“It has been suggested that ATM deficiency primarily impairs HR-mediated DSB repair with less effect on NHEJ-mediated DSB repair (Morrison et al. 2000; Yuan et al. 2003; Riballo et al. 2004).”
BackgroundDNA Strand Break Repair and Human Genetic Disease
McKinnon, P. J., & Caldecott, K. W. (2007) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev.genom.7.080505.115648 · Cited by 303 · see citing works
Weston, V., Oldreive, C., Skowrońska, A., Oscier, D. G., Pratt, G., Dyer, M. J. S., Smith, G. C. M., Powell, J. E., Rudzki, Z., Kearns, P. R., et al. (2010) · Blood · doi:10.1182/blood-2010-01-265769 · Cited by 300 · see citing works
ATM: Genome stability, neuronal development, and cancer cross paths
(2001) · Advances in Cancer Research · doi:10.1016/s0065-230x(01)83007-4 · Cited by 299 · see citing works
DNA double-strand break repair by homologous recombination
Dudáš, A., & Chovanec, M. (2003) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2003.07.001 · Cited by 268 · see citing works
Quantitation of DNA double-strand break resection intermediates in human cells
Zhou, Y., Caron, P., Legube, G., & Paull, T. T. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt1309 · Cited by 266 · see citing works
The role of Alu repeat clusters as mediators of recurrent chromosomal aberrations in tumors
Kolomietz, E., Meyn, M. S., Pandita, A., & Squire, J. A. (2002) · Genes Chromosomes and Cancer · doi:10.1002/gcc.10111 · Cited by 263 · see citing works
“The controlling role of ATM in HR-mediated repair (Morrison et al., 2000) provides the link between the recombinational repair machinery and the DNA damage checkpoint apparatus.”
BackgroundATM, a central controller of cellular responses to DNA damage
Khanna, K. K., Lavin, M. F., Jackson, S. P., & Mulhern, T. D. (2001) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4400874 · Cited by 251 · see citing works
“The recent knockout of ATM in chicken DT-40 cells has provided evidence for the involvement of ATM in the HR pathway of repair of DSBs in that disruption of the ATM gene caused altered kinetics of radiation-induced RAD51 and RAD54 foci formation.(171) Furthermore ATMKu70 double mutant DT-40 cells show more radiosensit…”
BackgroundPaciotti, V., Clerici, M., Lucchini, G., & Longhese, M. P. (2000) · Genes & Development · doi:10.1101/gad.14.16.2046 · Cited by 246 · see citing works
ATM and the Molecular Pathogenesis of Ataxia Telangiectasia
McKinnon, P. J. (2011) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev-pathol-011811-132509 · Cited by 239 · see citing works
Chromosome instability syndromes
Taylor, A. M. R., Rothblum‐Oviatt, C., Ellis, N. A., Hickson, I. D., Meyer, S., Crawford, T. O., Smogorzewska, A., Pietrucha, B. M., Weemaes, C. M. R., & Stewart, G. S. (2019) · Nature Reviews Disease Primers · doi:10.1038/s41572-019-0113-0 · Cited by 227 · see citing works
Bryant, H. E. (2006) · Nucleic Acids Research · doi:10.1093/nar/gkl108 · Cited by 208 · see citing works
“A controlling role for ATM in HR has been suggested (41) and we previously showed that ATM is required for HRR at slowed replication forks (37).”
BackgroundCentrosome amplification induced by DNA damage occurs during a prolonged G2 phase and involves ATM
Dodson, H., Bourke, E., Jeffers, L. J., Vagnarelli, P., Sonoda, E., Takeda, S., Earnshaw, W. C., Merdes, A., & Morrison, C. G. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600393 · Cited by 202 · see citing works
“Phenotypes we describe here were similar in both the tetracycline-repressible Rad54 (Morrison et al, 2000) and constitutive Rad54 null (Bezzubova et al, 1997) lines.”
BackgroundMethodInfluentialSelf-citationStudying Gene Function in Eukaryotes by Conditional Gene Inactivation
Gossen, M., & Bujard, H. (2002) · Annual Review of Genetics · doi:10.1146/annurev.genet.36.041002.120114 · Cited by 199 · see citing works
Golding, S. E., Rosenberg, E., Neill, S. J., Dent, P., Povirk, L. F., & Valerie, K. C. (2007) · Cancer Research · doi:10.1158/0008-5472.can-06-2371 · Cited by 190 · see citing works
“Using this system, previous studies by our group and others have shown that ATM is important for HRR (6, 21).”
ResultOrii, K. E., Lee, Y., Kondo, N., & McKinnon, P. J. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0602436103 · Cited by 181 · see citing works
PARP inhibitors in ovarian cancer: Sensitivity prediction and resistance mechanisms
Jiang, X., Li, X., Li, W., Bai, H., & Zhang, Z. (2019) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.14133 · Cited by 178 · see citing works
“Hence, ATM defects impair HR‐mediated DSB repair.(59) Low ATM expression was demonstrated”
BackgroundKennedy, R. D., Chen, C. C., Stuckert, P., Archila, E. M., la Vega, M. A. D., Moreau, L. A., Shimamura, A., & D’Andrea, A. D. (2007) · Journal of Clinical Investigation · doi:10.1172/jci31245 · Cited by 174 · see citing works
“Recent data also suggest that ATM may have a direct signaling role to NHEJ (45) or a role in HR (46).”
BackgroundNovel functional requirements for non‐homologous DNA end joining in Schizosaccharomyces pombe
Manolis, K. G., Nimmo, E. R., Hartsuiker, E., Carr, A. M., Jeggo, P. A., & Allshire, R. C. (2001) · The EMBO Journal · doi:10.1093/emboj/20.1.210 · Cited by 171 · 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
“…that formation of RAD51 foci after replication inhibition is mediated by ATR through CHK1-dependent phosphorylation of the RAD51 protein (Sorensen et al, 2005), whereas, after IR or treatment with radiomimetic drugs, RAD51 foci are under the control of ATM (Morrison et al, 2000; Yuan et al, 2003).”
BackgroundImmunoglobulin Class Switch Recombination Is Impaired in Atm-deficient Mice
Lumsden, J. M., McCarty, T. C., Petiniot, L. K., Shen, R., Barlow, C., Wynn, T. A., Morse, H. C., Gearhart, P. J., Wynshaw-Boris, A. J., Max, E. E., et al. (2004) · The Journal of Experimental Medicine · doi:10.1084/jem.20041074 · Cited by 172 · see citing works
“ATM plays a critical role in pathways for repair of DNA DSBs induced by insults such as gamma irradiation (46).”
BackgroundMukherjee, B., Tomimatsu, N., Amancherla, K. V., Camacho, C. V., Pichamoorthy, N., & Burma, S. (2012) · Neoplasia · doi:10.1593/neo.111512 · Cited by 170 · see citing works
“As expected, NU7026 and KU55933 treatments resulted in attenuated DSB repair, consistent with the role of DNA-PKcs in NHEJ [30] and the role of ATM in promoting HR [31] and heterochromatic DSB repair [32] (Figure 2B).”
DNA damage response pathway in radioadaptive response
Sasaki, M. S., Ejima, Y., Tachibana, A., Yamada, T., Ishizaki, K., Shimizu, T., & Nomura, T. (2002) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/s0027-5107(02)00084-2 · Cited by 166 · see citing works
Chromosome instability syndromes
Taylor, A. M. R. (2001) · Best Practice & Research Clinical Haematology · doi:10.1053/beha.2001.0158 · Cited by 170 · see citing works
Interactive competition between homologous recombination and non-homologous end joining.
Allen, C., Halbrook, J., & Nickoloff, J. A. (2003) · PubMed · Cited by 171 · see citing works
DNA Double-Strand Break Repair by Homologous Recombination
van den Bosch, M., Lohman, P. H. M., & Pastink, A. (2002) · Biological Chemistry · doi:10.1515/bc.2002.095 · Cited by 169 · see citing works
“These observations indicate that ATM acts in concert with NHEJ to preserve the genome, through HR pathways (Morrison et al., 2000).”
BackgroundThe chicken as a model for large-scale analysis of vertebrate gene function
Brown, W., Hubbard, S., Tickle, C., & Wilson, S. (2003) · Nature reviews genetics · doi:10.1038/nrg998 · Cited by 192 · see citing works
Linking DNA damage and neurodegeneration
Rolig, R. L., & McKinnon, P. J. (2000) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01625-8 · Cited by 167 · see citing works
DNA repair protein Rad55 is a terminal substrate of the DNA damage checkpoints
Bashkirov, V. I., King, J. S., Bashkirova, E. V., Schmuckli-Maurer, J., & Heyer, W.-D. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.12.4393-4404.2000 · Cited by 164 · see citing works
“This observation is consistent with the phenotypes of ATM-deficient chicken DT40 cells, which also suggested a positive role of ATM in the homologous recombination pathway (54, 80).”
ResultSekiguchi, J., Ferguson, D. O., Chen, H. T., Yang, E. M., Earle, J., Frank, K., Whitlow, S., Gu, Y., Xu, Y., Nussenzweig, A., et al. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.051632098 · Cited by 156 · see citing works
Homologous DNA recombination in vertebrate cells
Sonoda, E., Takata, M., Yamashita, Y. M., Morrison, C. G., & Takeda, S. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.111006398 · Cited by 151 · see citing works
Self-citationEkumi, K. M., Paculová, H., Lenasi, T., Pospíchalová, V., Bösken, C. A., Rybaříková, J., Bryja, V., Geyer, M., Blažek, D., & Barborič, M. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv101 · Cited by 145 · see citing works
Shima, N., Munroe, R. J., & Schimenti, J. C. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.23.10381-10389.2004 · Cited by 144 · see citing works
DNA repair in murine embryonic stem cells and differentiated cells
Tichy, E. D., & Stambrook, P. J. (2008) · Experimental Cell Research · doi:10.1016/j.yexcr.2008.02.007 · Cited by 143 · see citing works
“This pathway is active predominantly in the late S to G2 phases of the cell cycle, where sister chromatids are available to serve as templates [13–15].”
BackgroundWhite, D. E., Negorev, D., Peng, H.-Z., Ivanov, A., Maul, G., & Rauscher, F. (2006) · Cancer Research · doi:10.1158/0008-5472.can-06-4138 · Cited by 152 · see citing works
“Further studies have revealed that ATM is a key DNA damage responsive kinase required for the homologous recombination double-stranded break repair pathway (2).”
BackgroundHenning, W., & Stürzbecher, H.-W. (2003) · Toxicology · doi:10.1016/s0300-483x(03)00291-9 · Cited by 141 · see citing works
DNA-PKcs and ATM co-regulate DNA double-strand break repair
Shrivastav, M., Miller, C. A., Haro, L. P. D., Durant, S. T., Chen, B. P. C., Chen, D. J., & Nickoloff, J. A. (2009) · DNA repair · doi:10.1016/j.dnarep.2009.05.006 · Cited by 138 · see citing works
“Several lines of evidence suggest that ATM promotes DSB repair by HR [22,25-27].”
BackgroundChistiakov, D. A., Voronova, N. V., & Chistiakov, P. A. (2008) · Acta Oncologica · doi:10.1080/02841860801885969 · Cited by 137 · see citing works
“The ATM-deficient cells are highly sensitive to DNA damage induced by ionizing radiation [25].”
Ashley, A. K., Shrivastav, M., Nie, J., Amerin, C. L., Troksa, K. A., Glanzer, J. G., Liu, S., Opiyo, S. O., Dimitrova, D. D., Le, P. N., et al. (2014) · DNA repair · doi:10.1016/j.dnarep.2014.04.008 · Cited by 132 · see citing works
Rad54 and DNA Ligase IV cooperate to maintain mammalian chromatid stabilityPreprint
Mills, K. D., Ferguson, D. O., Essers, J., Eckersdorff, M., Kanaar, R., & Alt, F. W. (2004) · Genes & Development · doi:10.1101/gad.1204304 · Cited by 136 · see citing works
“Consistent with this interpretation, ATM and Rad54 have been placed in the same genetic pathway with respect to repair of IR-induced DNA damage (Morrison et al. 2000), and ATM deficient cells show abnormal kinetics of Rad54 focus formation following IR exposure (Morrison et al. 2000).”
BackgroundInfluentialThe XRCC genes: expanding roles in DNA double-strand break repair
Thacker, J., & Zdzienicka, M. Z. (2004) · DNA repair · doi:10.1016/j.dnarep.2004.04.012 · Cited by 135 · 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
“The role of ATM in cellular radiosensitivity is linked to HRR (11, 12), but which pathway, HRR or NHEJ or both, is responsible for the effects of ATR on the sensitivity of cells to IR remains unclear.”
BackgroundThe interplay between DNA repair and autophagy in cancer therapy
Zhang, D., Tang, B., Xie, X., Xiao, Y., Yang, S., & Zhang, J. (2015) · Cancer Biology & Therapy · doi:10.1080/15384047.2015.1046022 · Cited by 131 · see citing works
The chicken B cell line DT40: a novel tool for gene disruption experiments
Winding, P., & Berchtold, M. W. (2001) · Journal of Immunological Methods · doi:10.1016/s0022-1759(00)00333-1 · Cited by 132 · see citing works
Bakr, A., Oing, C., Köcher, S., Borgmann, K., Dornreiter, I., Petersen, C., Dikomey, E., & Mansour, W. Y. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv160 · Cited by 131 · see citing works
“The later function was described to specifically depend on its ATPase activity (39), which is also required for its own displacement from the ends (40).”
BackgroundCaretaker tumour suppressor genes that defend genome integrity
Levitt, N. C., & Hickson, I. D. (2002) · Trends in Molecular Medicine · doi:10.1016/s1471-4914(02)02298-0 · Cited by 130 · see citing works
Golding, S. E., Rosenberg, E., Khalil, A. A., McEwen, A., Holmes, M., Neill, S. J., Povirk, L. F., & Valerie, K. C. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m314191200 · Cited by 124 · see citing works
ATM directs DNA damage responses and proteostasis via genetically separable pathways
Lee, J., Mand, M. R., Kao, C.-H., Zhou, Y., Ryu, S. W., Richards, A., Coon, J. J., & Paull, T. T. (2018) · Science Signaling · doi:10.1126/scisignal.aan5598 · Cited by 118 · see citing works
“MRN-mediated ATM stimulation regulates DNA end resection ATM activity is important for homologous recombination (35), which initiates with DNA end resection.”
BackgroundBaroni, E., Viscardi, V., Cartagena‐Lirola, H., Lucchini, G., & Longhese, M. P. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.10.4151-4165.2004 · Cited by 116 · see citing works
“Finally, ATM is required for homologous-recombination-mediated repair of DSBs and is a member of the recombinational repair epistasis group (11, 13, 37, 50, 51, 74).”
BackgroundNakamura, K. M., Sakai, W., Kawamoto, T., Bree, R. T., Lowndes, N. F., Takeda, S., & Taniguchi, Y. (2006) · DNA repair · doi:10.1016/j.dnarep.2006.03.008 · Cited by 111 · see citing works
Self-citationRole of the spindle pole body of yeast in mediating assembly of the prospore membrane during meiosis
Knop, M., & Strasser, K. (2000) · The EMBO Journal · doi:10.1093/emboj/19.14.3657 · Cited by 116 · see citing works
Role of homologous recombination in carcinogenesis
Bishop, A. J. R., & Schiestl, R. H. (2003) · Experimental and Molecular Pathology · doi:10.1016/s0014-4800(03)00010-8 · Cited by 114 · see citing works
Exploiting synthetic lethal interactions for targeted cancer therapy
Reinhardt, H. C., Jiang, H., Hemann, M. T., & Yaffe, M. B. (2009) · Cell Cycle · doi:10.4161/cc.8.19.9626 · Cited by 110 · see citing works
“There is strong evidence for a role of ATM in HR-mediated DSB repair,(77-80) with a less pronounced effect on NHEJ-mediated DSB repair.(78,80-84) Since ATM-deficient cancer cells with preserved p53 function must repair doxorubicin-induced DSBs to ensure longterm survival, they likely rely extensively on alternative, e…”
BackgroundPaciotti, V., Clerici, M., Scotti, M., Lucchini, G., & Longhese, M. P. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.12.3913-3925.2001 · Cited by 112 · see citing works
“The findings that ATM is required for homologous recombination-mediated repair of DSBs and is a member of the recombinational repair epistasis group (33) clearly indicate that ATM has a role not only in preventing cells from propagating damaged DNA but also in the processing and repair of DSBs.”
BackgroundMultiple Roles of Vertebrate REV Genes in DNA Repair and Recombination
Okada, T., Sonoda, E., Yoshimura, M., Kawano, Y., Saya, H., Kohzaki, M., & Takeda, S. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.14.6103-6111.2005 · Cited by 112 · see citing works
“(atm) and rad18 cells were described previously (27, 47).”
Self-citationIdentification and characterization of FUS/TLS as a new target of ATM
Gardiner, M., Toth, R., Vandermoere, F., Morrice, N. A., & Rouse, J. (2008) · Biochemical Journal · doi:10.1042/bj20081135 · Cited by 111 · see citing works
Reverse genetic studies of the DNA damage response in the chicken B lymphocyte line DT40.
Yamazoe, M., Sonoda, E., Hochegger, H., & Takeda, S. (2004) · DNA Repair · doi:10.1016/j.dnarep.2004.03.039 · Cited by 116 · see citing works
Self-citationKass, E. M., Helgadottir, H. R., Chen, C.-C., Barbera, M. A., Wang, R., Westermark, U., Ludwig, T., Moynahan, M. E., & Jasin, M. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1216824110 · Cited by 107 · see citing works
“Although some studies using transformed cell lines have reported that ATM is not required for HDR (44), others have suggested that ATM plays a critical role (45, 46).”
BackgroundATM Deficiency Is Associated with Sensitivity to PARP1- and ATR Inhibitors in Lung Adenocarcinoma
Schmitt, A., Knittel, G., Welcker, D., Yang, T.-P., George, J., Nowak, M., Leeser, U., Büttner, R., Perner, S., Peifer, M., et al. (2017) · Cancer Research · doi:10.1158/0008-5472.can-16-3398 · Cited by 107 · see citing works
“One of the first steps of HRmediated DSB repair is the resection of the DSB leading to the generation of a single-stranded (ss) 3′-overhang, which is immediately coated by the singlestrand-binding protein RPA (15, 36-39).”
BackgroundWang, H., Chou, W., Shieh, S.-Y., & Shen, C. (2006) · Cancer Research · doi:10.1158/0008-5472.can-05-3270 · Cited by 105 · see citing works
Ralhan, R., Kaur, J., Kreienberg, R., & Wiesmüller, L. (2006) · Cancer Letters · doi:10.1016/j.canlet.2006.06.004 · Cited by 104 · see citing works
“It preserves the genome integrity mainly through HRR rather than NHEJ pathways in addition to its critical role in linking cell cycle checkpoints to HRR activation [21,22].”
BackgroundResponding to DNA double strand breaks in the nervous system
Lee, Y., & McKinnon, P. J. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.07.026 · Cited by 104 · see citing works
Therapeutic Targeting of a Robust Non-Oncogene Addiction to PRKDC in ATM -Defective Tumors
Riabinska, A., Daheim, M., Herter-Sprie, G. S., Winkler, J., Fritz, C., Hallek, M. J., Thomas, R. K., Kreuzer, K., Frenzel, L. P., Monfared, P., et al. (2013) · Science Translational Medicine · doi:10.1126/scitranslmed.3005814 · Cited by 99 · see citing works
“Cells derived from A-T patients show a DSB repair defect, which is due to impaired assembly and functioning of the RAD51-associated protein complexes in the HR arm of DSB repair (16, 18, 19).”
ATM-Mediated Transcriptional and Developmental Responses to γ-rays in Arabidopsis
Ricaud, L., Proux, C., Renou, J., Pichon, O., Fochesato, S., Ortet, P., & Montané, M. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000430 · Cited by 102 · see citing works
“ATM kinase also mediates cell cycle checkpoints and DSB repair by HR or NHEJ, depending on the DSB end structure and on the cell cycle at the time of damage [13,14].”
BackgroundAsaad, N. A., Zeng, Z., Guan, J., Thacker, J., & Iliakis, G. E. (2000) · Oncogene · doi:10.1038/sj.onc.1203953 · Cited by 99 · see citing works
“Indeed, evidence has been recently presented that ATM is such a regulatory kinase (Morrison et al., 2000).”
BackgroundKarlsson, K. H., & Stenerlöw, B. (2004) · Radiation Research · doi:10.1667/rr3171 · Cited by 99 · see citing works
Herzberg, K., Bashkirov, V. I., Rolfsmeier, M., Haghnazari, E., McDonald, W. H., Anderson, S., Bashkirova, E. V., Yates, J. R., & Heyer, W.-D. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.01317-06 · Cited by 95 · see citing works
“Genetic analyses in budding yeast and vertebrate cells have shown that Mec1 and ATM, two pivotal DNA damage checkpoint kinases, control HR (4, 21, 48).”
BackgroundDNA damage responses and their many interactions with the replication fork
Andreassen, P. R., Ho, G. P. H., & D’Andrea, A. D. (2006) · Carcinogenesis · doi:10.1093/carcin/bgi319 · Cited by 97 · see citing works
“It is important to note that ATM, NBS1, and BRCA1 have all been implicated in homologous recombination (HR) in vertebrate cells [60-62] and that recent experimental evidence suggests the slowing of the replication fork by HR in mammalian cells [63].”
BackgroundThe mTOR Inhibitor Rapamycin Suppresses DNA Double-Strand Break Repair
Chen, H., Ma, Z., Vanderwaal, R. P., Feng, Z., González-Suárez, I., Wang, S., Zhang, J., Roti, J. L. R., Gonzalo, S., & Zhang, J. (2010) · Radiation Research · doi:10.1667/rr2323.1 · Cited by 97 · see citing works
“HR is a slower and typically error-free repair process and takes place predominantly in S- and G2/M-phase cells (21, 22).”
BackgroundMurcia, J. M., Mark, M. P., Wendling, O., Wynshaw-Boris, A. J., & de MURCIA, G. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.5.1828-1832.2001 · Cited by 96 · see citing works
“As noted above, homologous recombination is defective in Atm cells (21) and mice (4).”
BackgroundBelli, M., Sapora, O., & Tabocchini, M. A. (2002) · Journal of Radiation Research · doi:10.1269/jrr.43.s13 · Cited by 93 · see citing works
Heitzeberg, F., Chen, I.-P., Hartung, F., Orel, N., Angelis, K. J., & Puchta, H. (2004) · The Plant Journal · doi:10.1111/j.1365-313x.2004.02097.x · Cited by 89 · see citing works
- Authors
- Morrison, C., Sonoda, E., Takao, N., Shinohara, A., Yamamoto, K., & Takeda, S.
- Affiliations
- Kyoto University (JP)
- Kanazawa University (JP)
- University of Chicago (US)
- Corresponding author
- Takeda, Shunichi
- ORCID
- Morrison, Ciaran
- Venue
- The EMBO Journal
- Published
- 2000-02-01
- Volume
- 19
- Issue
- 3
- Pages
- 463-471
- ISSN
- 0261-4189 (ISSN-L)
- 1460-2075
- PMC
- PMC305583
- OpenAlex
- W2017297714
- Cited by
- 312
- References
- 76
- Citations by year
- 2026: 6 · 2025: 1 · 2024: 10 · 2023: 2 · 2022: 8 · 2021: 6 · 2020: 9 · 2019: 8 · 2018: 9 · 2017: 9 · 2016: 1 · 2015: 12 · 2014: 9 · 2013: 8 · 2012: 15
- FWCI
- 10.74
- Type
- journal article
- Language
- en
- Update notices
- erratum (2000-02-15)
- Open access
- bronze
- doi.org
- Locations
- The EMBO Journal (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Wellcome Trust
- QIMR Berghofer Medical Research Institute
- University of Cambridge
- University of Sussex
- Mochida Memorial Foundation for Medical and Pharmaceutical Research
- Bayer Yakuhin
- Medical Research Council
- Japan Society for the Promotion of Science (CREST)
- Core Research for Evolutional Science and Technology
- 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
- Health Sciences › Medicine › Oncology › PARP inhibition in cancer therapy
- Keywords
- ATM kinase, ataxia telangiectasia, homologous recombination, non-homologous end joining, DNA double-strand break repair, radiosensitivity, chromosomal instability, cell cycle checkpoints, RAD51, Rad54, Ku70, DT40 cells, chromosomal abnormalities
- MeSH terms
- Ku Autoantigen, Animals, Ataxia Telangiectasia, Cell Division, Cell Line, Chickens, Chromosome Aberrations, DNA Damage, DNA Repair, DNA Helicases, DNA-Binding Proteins, Fluorescent Antibody Technique, Fungal Proteins, Humans, Nuclear Proteins, Radiation Tolerance, Recombination, Genetic, Immunoblotting, Protein Serine-Threonine Kinases, Gene Targeting, Cell Cycle Proteins, Tumor Suppressor Proteins, Saccharomyces cerevisiae Proteins, Avian Proteins, Antigens, Nuclear, DNA Repair Enzymes, Rad51 Recombinase, Ataxia Telangiectasia Mutated Proteins
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