Cited by 313DNA Repair MechanismsEffects of Radiation ExposurePARP inhibition in cancer therapy

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The controlling role of ATM in homologous recombinational repair of DNA damage

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Morrison, Ciaran, Sonoda, Eiichiro, Takao, Noriaki, Shinohara, Akira, Yamamoto, Ken‐ichi, Takeda, Shunichi·2000·The EMBO Journal

DOI 10.1093/emboj/19.3.463PMC PMC305583

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Abstract

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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International System for Human Cytogenetic Nomenclature
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Method
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The ATM gene and ataxia telangiectasia.
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Ionizing radiation-induced Rad51 nuclear focus formation is cell cycle-regulated and defective in both ATM−/− and c-Abl−/− cells
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ATM Is Not Required in Somatic Hypermutation of VH, but Is Involved in the Introduction of Mutations in the Switch μ Region
Pan‐Hammarström, Q., Dai, S.-J., Zhao, Y., van Dijk-Härd, I. F., Gatti, R. A., Børresen‐Dale, A., & Hammarström, L. L. G. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.170.7.3707 · Cited by 86
“ATM is essential for repair of the DNA DSBs induced by gamma irradiation and is involved in homologous endjoining pathways (30).”
Background
Differential and collaborative actions of Rad51 paralog proteins in cellular response to DNA damage
Yonetani, Y. (2005) · Nucleic Acids Research · doi:10.1093/nar/gki766 · Cited by 86
ATM is required for the cellular response to thymidine induced replication fork stress
Bolderson, E., Scorah, J., Helleday, T., Smythe, C., & Meuth, M. (2004) · Human Molecular Genetics · doi:10.1093/hmg/ddh316 · Cited by 86
“ATM2/2 DT40 chicken cells show altered kinetics of RAD51 foci formation and ATM2/2 RAD542/2 double mutants have only slightly higher levels of chromosome aberrations relative to ATM2/2 cells (12).”
BackgroundInfluential
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
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ATM Mutations in Sporadic Lymphoid Tumours
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“both NHEJ and HEJ repair pathways are defective in the absence of ATM [43,44].”
Background
Regulators of homologous recombination repair as novel targets for cancer treatment
Krajewska, M., Fehrmann, R. S. N., de Vries, E. G. E., & van Vugt, M. A. T. M. (2015) · Frontiers in Genetics · doi:10.3389/fgene.2015.00096 · Cited by 81
“…Netherlands m.vugt@umcg.nl Specialty section: This article was submitted to Cancer Genetics, a section of the journal Frontiers in Genetics Received: 14 January 2015 Paper pending published: 03 February 2015 Accepted: 23 February 2015 Published: 20 March 2015 Citation: Krajewska M, Fehrmann RSN, de”
Background
Dancing on Damaged Chromatin: Functions of ATM and the RAD50/MRE11/NBS1 Complex in Cellular Responses to DNA Damage
Iijima, K., Ohara, M., Seki, R., & Tauchi, H. (2008) · Journal of Radiation Research · doi:10.1269/jrr.08065 · Cited by 77
Homologous Recombination and Its Role in Carcinogenesis
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Background
DNA damage checkpoint inactivation: Adaptation and recovery
Clémenson, C., & Marsolier‐Kergoat, M. (2009) · DNA repair · doi:10.1016/j.dnarep.2009.04.008 · Cited by 75
Defects in homologous recombination repair in mismatch-repair-deficient tumour cell lines
Mohindra, A. (2002) · Human Molecular Genetics · doi:10.1093/hmg/11.18.2189 · Cited by 76
“possibility, Takeda and co-workers (50) have presented evidence that supports the hypothesis that ATM and HRR are on the same damage response pathway.”
The S-phase checkpoint and its regulation in Saccharomyces cerevisiae
Longhese, M. P., Clerici, M., & Lucchini, G. (2003) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2003.08.009 · Cited by 74
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“reverse genetics failed to see potentiation in cell death arising from the conditional loss of RAD54 in ATM / cells, suggesting an inherent HR defect in ATM / cells (46).”
Background
ATM‐dependent DNA damage surveillance in T‐cell development and leukemogenesis: the DSB connection
Matei, I. R., Guidos, C. J., & Danska, J. S. (2006) · Immunological Reviews · doi:10.1111/j.0105-2896.2006.00361.x · Cited by 77
“An alternative but not exclusive explanation, supported by several in vitro studies, is that ATM is directly involved in HR (93).”
Background
Analysis of DNA double-strand break repair pathways in mice
Brugmans, L., Kanaar, R., & Essers, J. (2006) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2006.01.022 · Cited by 74
An Overactivated ATR/CHK1 Pathway Is Responsible for the Prolonged G2 Accumulation in Irradiated AT Cells
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DNA-dependent Protein Kinase Regulates DNA End Resection in Concert with Mre11-Rad50-Nbs1 (MRN) and Ataxia Telangiectasia-mutated (ATM)
Zhou, Y., & Paull, T. T. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.514398 · Cited by 76
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“:3) astrocytes were also included as an additional control as they had been reported to be defective in HR (Morrison et al , 2000), although recent data (Kass et al , 2013; Rass et al , 2013), and our current data (Fig 5), show that they are not HR deficient.”
Drosophila ATR in Double-Strand Break Repair
LaRocque, J. R., Jaklevic, B. R., Su, T. T., & Sekelsky, J. J. (2006) · Genetics · doi:10.1534/genetics.106.067330 · Cited by 67
Transient ATM Kinase Inhibition Disrupts DNA Damage–Induced Sister Chromatid Exchange
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“ATM promotes the HR-mediated repair of DSBs in various systems, including in DT40 chicken cells in response to IR (16) and in Chinese hamster cells in response to inhibition of poly(adenosine diphosphate ribose) polymerase (PARP) (17).”
Background
Untargeted mutation of the maternally derived mouse hypervariable minisatellite allele in F 1 mice born to irradiated spermatozoa
Niwa, O., & Kominami, R. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.98.4.1705 · Cited by 67
The RAD6/BRE1 Histone Modification Pathway in Saccharomyces Confers Radiation Resistance Through a RAD51-Dependent Process That Is Independent of RAD18
Game, J. C., Williamson, M. S., Spicakova, T., & Brown, J. M. (2006) · Genetics · doi:10.1534/genetics.106.057794 · Cited by 67
“…indicates that all the IR resistance conferred by Dot1p depends on Rad9p, but on the basis of our data and that of others (Bashkirov et al. 2000; Morrison et al. 2000), RAD9 itself may perhaps be considered a player in HRR as well as a checkpoint gene, since rad9D strains in our hands are as…”
Background
Clastogenicity of the fungicide afugan in cultured human lymphocytes
Yüzbaşıoğlu, D., Çelık, M., Yılmaz, S., Ünal, F. Ş., & Aksoy, H. (2006) · Mutation Research/Genetic Toxicology and Environmental Mutagenesis · doi:10.1016/j.mrgentox.2006.01.001 · Cited by 66
DNA damage repair in breast cancer and its therapeutic implications
Ali, R., Rakha, E. A., Madhusudan, S., & Bryant, H. E. (2016) · Pathology · doi:10.1016/j.pathol.2016.11.002 · Cited by 66
Radiosensitizing effects of miR‐18a‐5p on lung cancer stem‐like cells via downregulating both ATM and HIF ‐1α
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ATM loss leads to synthetic lethality in BRCA1 BRCT mutant mice associated with exacerbated defects in homology-directed repair
Chen, C.-C., Kass, E. M., Yen, W.-F., Ludwig, T., Moynahan, M. E., Chaudhuri, J., & Jasin, M. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1706392114 · Cited by 64
“Whereas some studies have observed a role for ATM in HDR (17, 18), other studies have not (24–27).”
Background
Chromium (VI) Activates Ataxia Telangiectasia Mutated (ATM) Protein
Ha, L., Ceryak, S. M., & Patierno, S. R. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m210560200 · Cited by 63
Loss of DNA Damage Response in Neuroblastoma and Utility of a PARP Inhibitor
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Sensitization of breast carcinoma cells to ionizing radiation by small molecule inhibitors of DNA-dependent protein kinase and ataxia telangiectsia mutated
Cowell, I. G., Durkacz, B. W., & Tilby, M. J. (2005) · Biochemical Pharmacology · doi:10.1016/j.bcp.2005.09.029 · Cited by 61
Targeting Squalene Epoxidase Interrupts Homologous Recombination via the ER Stress Response and Promotes Radiotherapy Efficacy
Hong, Z., Liu, T., Wan, L., Fa, P., Kumar, P., Cao, Y., Prasad, C. B., Qiu, Z., Liu, J., Wang, H., et al. (2022) · Cancer Research · doi:10.1158/0008-5472.can-21-2229 · Cited by 60
Up-regulation of microRNA-138 induce radiosensitization in lung cancer cells
Yang, H., Tang, Y., Guo, W., Du, Y., Wang, Y., Li, P., Zang, W., Yin, X., Wang, H., Chu, H., et al. (2014) · Tumor Biology · doi:10.1007/s13277-014-1879-z · Cited by 59
Regulation of Ionizing Radiation-induced Rad52 Nuclear Foci Formation by c-Abl-mediated Phosphorylation
Kitao, H., & Yuan, Z.-M. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m208151200 · Cited by 58
Functional characterization connects individual patient mutations in ataxia telangiectasia mutated (ATM) with dysfunction of specific DNA double‐strand break‐repair signaling pathways
Keimling, M., Volčič, M., Csernok, A., Wieland, B., Dörk, T., & Wiesmüller, L. (2011) · The FASEB Journal · doi:10.1096/fj.11-185546 · Cited by 59
Resveratrol modulates DNA double-strand break repair pathways in an ATM/ATR–p53- and –Nbs1-dependent manner
Gatz, S. A., Keimling, M., Baumann, C., Dörk, T., Debatin, K., Fulda, S., & Wiesmüller, L. (2008) · Carcinogenesis · doi:10.1093/carcin/bgm283 · Cited by 59
Two mouse models reveal an actionable PARP1 dependence in aggressive chronic lymphocytic leukemia
Knittel, G., Rehkämper, T., Korovkina, D., Liedgens, P., Fritz, C., Torgovnick, A., Al-Baldawi, Y., Al-Maarri, M., Cun, Y., Fedorchenko, O., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-00210-6 · Cited by 56
The role of DNA damage and repair in atherosclerosis: A review
Shah, N. R., & Mahmoudi, M. (2015) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2015.07.005 · Cited by 56
“Evidence suggests that ATM exerts genomic regulation primarily through HR [91].”
Background
Flavopiridol in the treatment of chronic lymphocytic leukemia
Christian, B. A., Grever, M. R., Byrd, J. C., & Lin, T. S. (2007) · Current Opinion in Oncology · doi:10.1097/cco.0b013e3282efb9da · Cited by 55
Participation of DNA-PKcs in DSB Repair after Exposure to High- and Low-LET Radiation
Anderson, J. A., Harper, J. V., Cucinotta, F. A., & O’Neill, P. (2010) · Radiation Research · doi:10.1667/rr2071.1 · Cited by 55
ATM dependent apoptosis in the nervous system
Lee, Y., & McKinnon, P. J. (2000) · APOPTOSIS · doi:10.1023/a:1009637512917 · Cited by 53
Effects of double-strand break repair proteins on vertebrate telomere structure
Wei, C. (2002) · Nucleic Acids Research · doi:10.1093/nar/gkf396 · Cited by 51
“The Rad54–/–, Rad51–/– and Mre11–/– conditional cell lines contained human Rad54 or chicken Rad51 and Mre11 under control of a tetracycline (tet)-repressible promoter (28, 30 ,32).”
Background
Tyrosine 370 phosphorylation of ATM positively regulates DNA damage response
Lee, H.-J., Lan, L., Peng, G., Chang, W., Hsu, M., Wang, Y., Cheng, C. C., Wei, L., Nakajima, S., Chang, S.-S., et al. (2015) · Cell Research · doi:10.1038/cr.2015.8 · Cited by 57
“To further determine whether EGFR is involved in ATM-mediated homologous recombination repair (Iijima et al., 2008; Morrison et al., 2000), we generated control and EGFR-depleted U2OS cells integrated with DRGFP reporter (Figure 7A) (Peng et al.”
Method
Roles of Vertebrate Smc5 in Sister Chromatid Cohesion and Homologous Recombinational Repair
Stephan, A. K., Kliszczak, M., Dodson, H., Cooley, C., & Morrison, C. G. (2011) · Molecular and Cellular Biology · doi:10.1128/mcb.00786-10 · Cited by 51
“Rad54 (32), anti-chicken Smc1 8232 and anti-chicken Scc1 2110 at 1:1000, af-”
Self-citation
The dominant role of proofreading exonuclease activity of replicative polymerase ε in cellular tolerance to cytarabine (Ara-C)
Tsuda, M., Terada, K., Ooka, M., Kobayashi, K., Sasanuma, H., Fujisawa, R., Tsurimoto, T., Yamamoto, J., Iwai, S., Kadoda, K., et al. (2017) · Oncotarget · doi:10.18632/oncotarget.16508 · Cited by 49
“ATM-/Chicken DT40 NEOR, PUROR Checkpoint control [46]”
Self-citation
Reverse genetic studies of homologous DNA recombination using the chicken B–lymphocyte line, DT40
Sonoda, E., Morrison, C. G., Yamashita, Y. M., Takata, M., & Takeda, S. (2001) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2000.0755 · Cited by 51
Self-citation
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
Self-citation
ATM deficiency disrupts Tcra locus integrity and the maturation of CD4+CD8+ thymocytes
Matei, I. R., Gladdy, R. A., Nutter, L. M. J., Canty, A. J., Guidos, C. J., & Danska, J. S. (2006) · Blood · doi:10.1182/blood-2006-05-020917 · Cited by 52
The Radioresistance to Killing of A1–5 Cells Derives from Activation of the Chk1 Pathway
Hu, B., Zhou, X.-Y., Wang, X., Zeng, Z., Iliakis, G. E., & Wang, Y. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m009340200 · Cited by 49
Radiation-induced double-strand breaks require ATM but not Artemis for homologous recombination during S-phase
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 49
Critical Roles for Polymerase ζ in Cellular Tolerance to Nitric Oxide–Induced DNA Damage
Wu, X., Takenaka, K., Sonoda, E., Hochegger, H., Kawanishi, S., Kawamoto, T., Takeda, S., & Yamazoe, M. (2006) · Cancer Research · doi:10.1158/0008-5472.can-05-2884 · Cited by 47
“Such marked divergence in the extent of G2 arrest among individual cells was not found following other genotoxic stressors such as ionizing radiation (36).”
BackgroundInfluentialSelf-citation
The WRN and MUS81 proteins limit cell death and genome instability following oncogene activation
Murfuni, I., Nicolai, S., Baldari, S., Crescenzi, M., Bignami, M., Franchitto, A., & Pichierri, P. (2012) · Oncogene · doi:10.1038/onc.2012.80 · Cited by 48
Therapeutic applications of PARP inhibitors in ovarian cancer
Xie, H., Wang, W., Xia, B., Jin, W., & Lou, G. (2020) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2020.110204 · Cited by 47
Loss of atm sensitises p53-deficient cells to topoisomerase poisons and antimetabolites
Fedier, A., Schlamminger, M., Schwarz, V. A., Haller, U., Howell, S. B., & Fink, D. A. (2003) · Annals of Oncology · doi:10.1093/annonc/mdg240 · Cited by 45
“It serves a surveillance function that helps maintain genomic integrity by promoting cell cycle arrest and damage repair, and possibly by recruiting repair proteins to the site of damage to prevent double-strand break repair from entering an error-prone pathway [10].”
Background
Regulation of ATM in DNA double strand break repair accounts for the radiosensitivity in human cells exposed to high linear energy transfer ionizing radiation
Xue, L., Yu, D. S., Furusawa, Y., Okayasu, R., Tong, J., Cao, J., & Fan, S. (2009) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2009.06.016 · Cited by 45
“decreased and delayed formation of Rad51 foci-containing nuclei is observed in AT cells upon radiation, a finding which reveals that ATM is also a major player in the HRR pathway [12–14].”
Background
Critical role for chicken Rad17 and Rad9 in the cellular response to DNA damage and stalled DNA replication
Kobayashi, M., Hirano, A., Kumano, T., Xiang, S., Mihara, K. L., Haseda, Y., Matsui, O., Shimizu, H., & Yamamoto, K. (2004) · Genes to Cells · doi:10.1111/j.1356-9597.2004.00728.x · Cited by 45
“These results are also consistent with those derived from radiation sensitivity analysis: while ATM−/− DT40 cells were highly X-ray sensitive, as we reported previously (Morrison et al. 2000; Takao et al. 1999, 2000), Rad17−/− and Rad9−/− cells were only moderately sensitive to X-rays (Fig.”
ResultSelf-citation
FANCD2 associated with sporadic breast cancer risk
Barroso, E. (2006) · Carcinogenesis · doi:10.1093/carcin/bgl062 · Cited by 45
Exploiting Synthetic Lethal Interactions Between DNA Damage Signaling, Checkpoint Control, and p53 for Targeted Cancer Therapy
Morandell, S., & Yaffe, M. B. (2012) · Progress in molecular biology and translational science · doi:10.1016/b978-0-12-387665-2.00011-0 · Cited by 45
A long noncoding RNA sensitizes genotoxic treatment by attenuating ATM activation and homologous recombination repair in cancers
Zhao, K., Wang, X., Xue, X., Li, L., & Hu, Y. (2020) · PLoS Biology · doi:10.1371/journal.pbio.3000666 · Cited by 44
Genetic analysis of homologous DNA recombination in vertebrate somatic cells
Morrison, C. G., & Takeda, S. (2000) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/s1357-2725(00)00033-9 · Cited by 43
Self-citation
DNA-PK: the Major Target for Wortmannin-mediated Radiosensitization by the Inhibition of DSB Repair via NHEJ Pathway.
HASHIMOTO, M. W., Rao, B. S. S., Tokuno, O., Yamamoto, K.-I., Takata, M., Takeda, S., & Utsumi, H. (2003) · Journal of Radiation Research · doi:10.1269/jrr.44.151 · Cited by 42
Self-citation
Inhibition of DNA repair by Pentoxifylline and related methylxanthine derivatives
Böhm, L., Roos, W. P., & Serafin, A. M. (2003) · Toxicology · doi:10.1016/s0300-483x(03)00294-4 · Cited by 42
Caffeine Could Not Efficiently Sensitize Homologous Recombination Repair-Deficient Cells to Ionizing Radiation-Induced Killing
Wang, H., Wang, X., Iliakis, G. E., & Wang, Y. (2003) · Radiation Research · doi:10.1667/0033-7587(2003)159[0420:ccnesh]2.0.co;2 · Cited by 42
MST-312 Alters Telomere Dynamics, Gene Expression Profiles and Growth in Human Breast Cancer Cells
Gurung, R. L., Lim, S. N., Low, G. K. M., & Hande, M. P. (2014) · Lifestyle Genomics · doi:10.1159/000381346 · Cited by 39
Human MutL-complexes monitor homologous recombination independently of mismatch repair
Siehler, S. Y., Schrauder, M. G., Gerischer, U. C., Cantor, S. B., Marra, G., & Wiesmüller, L. (2008) · DNA repair · doi:10.1016/j.dnarep.2008.10.011 · Cited by 41
A Role for the Fanconi Anemia C Protein in Maintaining the DNA Damage-induced G2 Checkpoint
Freie, B. W., Ciccone, S. L. M., Li, X., Plett, P. A., Orschell, C. M., Srour, E. F., Hanenberg, H., Schindler, D., Lee, S., & Clapp, D. W. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m407160200 · Cited by 40
Targeting senescence pathways to reverse drug resistance in cancer
Rebbaa, A. (2004) · Cancer Letters · doi:10.1016/j.canlet.2004.08.011 · Cited by 41
“[62] C.”
Background
Variations in ATM Protein Expression During Normal Lymphoid Differentiation and Among B-Cell-Derived Neoplasias
Starczynski, J., Simmons, W., Flavell, J. R., Byrd, P. J., Stewart, G. S., Kullar, H. S., Groom, A., Crocker, J., Moss, P. A. H., Reynolds, G. M., et al. (2003) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)63672-3 · Cited by 39
“Furthermore, both NHEJ and HEJ repair pathways are found to be defective in the absence of ATM.(9,10) The precise mechanism of DNA repair regulation by ATM, however, is yet to be elucidated.”
BackgroundInfluential
A Novel Host Cell Reactivation Assay to Assess Homologous Recombination Capacity in Human Cancer Cell Lines
Slebos, R. J. C., & Taylor, J. A. (2001) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.2001.4335 · Cited by 39
Trifluorothymidine exhibits potent antitumor activity via the induction of DNA double-strand breaks
SUZUKI, N., Nakagawa, F., Nukatsuka, M., & Fukushima, M. (2011) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2011.244 · Cited by 39
“Furthermore, the ATM signals induce the association of homologous recombination repair components, such as Rad51, Xrcc3, BRCA2 and H2AX (22,23).”
Loss of ATM sensitizes against O6-methylguanine triggered apoptosis, SCEs and chromosomal aberrations
Dębiak, M., Nikolova, T., & Kaina, B. (2004) · DNA repair · doi:10.1016/j.dnarep.2003.11.013 · Cited by 39
Caffeine-Induced Radiosensitization is Independent of Nonhomologous End Joining of DNA Double-Strand Breaks
Wang, X., Wang, H., Iliakis, G. E., & Wang, Y. (2003) · Radiation Research · doi:10.1667/0033-7587(2003)159[0426:ciriio]2.0.co;2 · Cited by 38
“Results published previously strongly support the link between ATM and HRR (51, 52), suggesting that ATM is an NHEJ-independent checkpoint regulator.”
Background
Phenotypic effects of heterozygosity for a BRCA2 mutation
Warren, M. V. (2003) · Human Molecular Genetics · doi:10.1093/hmg/ddg277 · Cited by 37
Checkpoint and DNA-repair proteins are associated with the cores of mammalian meiotic chromosomes
Tarsounas, M., & Møens, P. B. (2001) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/s0070-2153(01)51004-2 · Cited by 36
Adenovirus-mediated wild-type p53 radiosensitizes human tumor cells by suppressing DNA repair capacity.
Sah, N. K., Munshi, A., Nishikawa, T., Mukhopadhyay, T., Roth, J. A., & Meyn, R. E. (2003) · PubMed · Cited by 35
Targeting ATM-deficient CLL through interference with DNA repair pathways
Knittel, G., Liedgens, P., & Reinhardt, H. C. (2015) · Frontiers in Genetics · doi:10.3389/fgene.2015.00207 · Cited by 34
“…DNA repair, specifically HR-mediated DSB repair, with a less well-characterized role in NHEJ (Luo et al., 1996; Dar et al., 1997; Chen et al., 1999; Morrison et al., 2000; Yuan et al., 2003; Kuhne et al., 2004; Riballo et al., 2004; Xie et al., 2004; Frontiers in Genetics | www.frontiersin.org 3…”
BackgroundInfluential
Level of cdk5 expression predicts the survival of relapsed multiple myeloma patients
Levacque, Z., Rosales, J. L., & Lee, K. (2012) · Cell Cycle · doi:10.4161/cc.21886 · Cited by 33
NUCKS1 promotes RAD54 activity in homologous recombination DNA repair
Maranon, D. G., Sharma, N., Huang, Y., Selemenakis, P., Wang, M., Altina, N. H., Zhao, W., & Wiese, C. (2020) · The Journal of Cell Biology · doi:10.1083/jcb.201911049 · Cited by 30
A miR-590/Acvr2a/Rad51b Axis Regulates DNA Damage Repair during mESC Proliferation
Liu, Q., Wang, G., Chen, Y., Li, G., Yang, D., & Kang, J. (2014) · Stem Cell Reports · doi:10.1016/j.stemcr.2014.10.006 · Cited by 31
“During HRR, DSB damage repair uses a template containing hundreds of base pairs of sequence homology, and usually the sister chromatids are available to serve as templates (Haber, 2000; Morrison et al., 2000; Takata et al., 1998).”
Background
Caspase cleavage of transcription factor Sp1 enhances apoptosis
Torabi, B., Flashner, S. P., Beishline, K., Sowash, A., Donovan, K., Bassett, G., & Azizkhan‐Clifford, J. (2017) · APOPTOSIS · doi:10.1007/s10495-017-1437-4 · Cited by 31
Deubiquitinase USP47-stabilized splicing factor IK regulates the splicing of ATM pre-mRNA
Ka, H. I., Lee, S., Han, S., Jeong, A. L., Park, J. Y., Joo, H. J., Soh, S., Park, D., & Yang, Y. D. (2020) · Cell Death Discovery · doi:10.1038/s41420-020-0268-1 · Cited by 30
Assessment of the genotoxic effects of organophosphorus insecticides phorate and trichlorfon in human lymphocytes
Timoroğlu, İ., Yüzbaşıoğlu, D., Ünal, F., Yılmaz, S., Aksoy, H., & Çelık, M. (2012) · Environmental Toxicology · doi:10.1002/tox.21783 · Cited by 30
“Clastogenic agents may induce DNA double-strand breaks and lead to either cellcycle arrest or apoptosis by a mechanism that includes activation of the TP53 and p21 proteins (Kastan et al., 1991; Bunz et al., 1998; Rotman and Shiloh, 1998; Morrison et al., 2000, Obe and Durante, 2010).”
Background
Differential Requirement for H2AX and 53BP1 in Organismal Development and Genome Maintenance in the Absence of Poly(ADP)ribosyl Polymerase 1
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 34
“However, ATM may also facilitate HR via H2AX-independent mechanisms, including activation of cell cycle checkpoints and endprocessing activities (5, 33, 48).”
Background
Homologous recombination as a resistance mechanism to replication-induced double-strand breaks caused by the antileukemia agent CNDAC
Liu, X., Wang, Y., Benaissa, S., Matsuda, A., Kantarjian, H. M., Estrov, Z. E., & Plunkett, W. K. (2010) · Blood · doi:10.1182/blood-2009-05-220376 · Cited by 28
Targeting DNA Repair Proteins: A Promising Avenue for Cancer Gene Therapy
Belzile, J.-P., Choudhury, S. A., Cournoyer, D., & Chow, T. Y.-K. (2006) · Current Gene Therapy · doi:10.2174/156652306775515538 · Cited by 28
“It is generally agreed that HRR plays a more prominent role in late S and G2 stages of the cell cycle when sister chromatids are available for homologous pairing [Haber, 2000;Morrison et al., 2000], whereas the majority of DSBs are rejoined by NHEJ in G1/G0 and early S stages [Lee et al.”
Background
Inhibition of novel GCN5–ATM axis restricts the onset of acquired drug resistance in leukemia
Salunkhe, S. J., Mishra, S. V., Nair, J., Ghosh, S., Choudhary, N., Kaur, E., Shah, S. G., Patkar, K., Anand, D., Khattry, N., et al. (2018) · International Journal of Cancer · doi:10.1002/ijc.31242 · Cited by 29
“3a), these data are in agreement with previous reports where ATM is shown to prefer resolution of DNA DSBs via HR pathway.(22)”
Result
Epstein-Barr Virus (EBV)-Related Lymphoproliferative Disorders in Ataxia Telangiectasia: Does ATM Regulate EBV Life Cycle?
Tatfi, M., Hermine, O., & Suárez, F. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2018.03060 · Cited by 28
“The repair mechanism involves non-homologous end joining, an error-prone process occurring in G1/S phase (19), or homologous recombination, a faithful process in G2/M when sister chromatid is available (20).”
Background
A role for Xrcc2 in the early stages of mouse development
Adam, J., Deans, B., & Thacker, J. (2006) · DNA repair · doi:10.1016/j.dnarep.2006.10.024 · Cited by 26
Ku affects the ATM-dependent S phase checkpoint following ionizing radiation
Zhou, X.-Y., Wang, X., Wang, H., Chen, D. J., Li, G. C., Iliakis, G. E., & Wang, Y. (2002) · Oncogene · doi:10.1038/sj.onc.1205782 · Cited by 27
“…telangiectasia (AT) cells of which ATM is mutant showed deficient fast response of S checkpoint (Painter and Young, 1980; Xu et al., 2001; Zhou et al., 2002) as well as abnormal G1 and G2 checkpoint responses and deficient DNA homologous recombination (HR) repair (Morrison et al., 2000) after IR.”
Background
A nervous predisposition to unrepaired DNA double strand breaks
Reynolds, J. J., & Stewart, G. S. (2013) · DNA Repair · doi:10.1016/j.dnarep.2013.04.011 · Cited by 26
“However, it has been proposed that the slow’ component of DSB repair is mediated by the HRR machinry, suggesting that HRR functions to repair DSBs in regions of eterochromatin.”
BackgroundInfluential
Alpha particles induce pan-nuclear phosphorylation of H2AX in primary human lymphocytes mediated through ATM
Horn, S., Brady, D., & Prise, K. M. (2015) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2015.06.010 · Cited by 29
“ATMs role appears to be more subtle, with suggestions that this kinase is involved in the repair of DSBs that require re-sectioning and those breaks lying within heterochromatic regions [28, 29], along with its critical role in DNA damage signalling [30] and apoptosis [31].”
Background
Roles of DNA-dependent protein kinase and ATM in cell-cycle-dependent radiation sensitivity in human cells
Yoshida, M., Hosoi, Y., Miyachi, H., Ishii, N., Matsumoto, Y., Enomoto, A., Nakagawa, K., Yamada, S., Suzuki, N., & Ono, T. (2002) · International Journal of Radiation Biology · doi:10.1080/095530002317577321 · Cited by 26
“After the hydroxyurea treatment, cells were washed with phos-1998, Chen et al. 1999, Cortez et al. 1999, Morrison et al. 2000) .”
BackgroundMethod
Sapacitabine for cancer
Liu, X., Kantarjian, H. M., & Plunkett, W. K. (2012) · Expert Opinion on Investigational Drugs · doi:10.1517/13543784.2012.660249 · Cited by 25
“The NHEJ pathway is dependent on DNA-PK [33], where as HR is initiated by ATM [34,35].”
Background
Increased sister chromatid cohesion and DNA damage response factor localization at an enzyme-induced DNA double-strand break in vertebrate cells
Dodson, H., & Morrison, C. G. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp684 · Cited by 26
“Wild type, Ku70 / (23), ATM / (24) and H2AX / (25) clones of the chicken lymphoma B-cell line DT40 were cultured as described (23).”
InfluentialSelf-citation
7‐hydroxy‐staurosporine, UCN‐01, induces DNA damage response, and autophagy in human osteosarcoma U2‐OS cells
Lien, W., Chen, T., Sheu, S., Lin, T., Kang, F., Yu, C., Kuan, T., Huang, B., & Wang, C. (2017) · Journal of Cellular Biochemistry · doi:10.1002/jcb.26652 · Cited by 25
“Among these proteins, ATM, which belongs to the superfamily of phosphatidylinositol 3-kinase-related kinases, participates in the repair of DNA double-strand breaks via homologous recombination.(9,10) In the presence of DNA double-strand breaks, ATM is activated and phosphorylated at Ser1981, thus activating the downs…”
Expression of DNA repair and apoptosis genes in mitochondrial mutant and normal cells following exposure to ionizing radiation
Kulkarni, R. M., Thomas, R. A., & Tucker, J. D. (2010) · Environmental and Molecular Mutagenesis · doi:10.1002/em.20605 · Cited by 24
“It is generally believed that during late S phase and in G2 phase of the cell cycle, HRR plays a more prominent role, whereas NHEJ predominates during G1 and early S phases [Lee et al., 1997; Takata et al., 1998; Haber, 2000; Morrison et al., 2000; Wu et al., 2008].”
Background
Dysregulated G2 phase checkpoint recovery pathway reduces DNA repair efficiency and increases chromosomal instability in a wide range of tumours
Fernando, M., Duijf, P. H. G., Proctor, M. A., Stevenson, A. J., Ehmann, A., Vora, S., Škalamera, D., Adams, M. N., & Gabrielli, B. G. (2021) · Oncogenesis · doi:10.1038/s41389-021-00329-8 · Cited by 25
Mammalian meiosis involves DNA double-strand breaks with 3′ overhangs
Zenvirth, D., Richler, C., Bardhan, A., Baudat, F., Barzilai, A., Wahrman, J., & Simchen, G. (2003) · Chromosoma · doi:10.1007/s00412-002-0223-3 · Cited by 23
Screening breast cancer patients for ATM mutations and polymorphisms by using denaturing high‐performance liquid chromatography
Atencio, D. P., Iannuzzi, C. M., Green, S., Stock, R. G., Bernstein, J. L., & Rosenstein, B. S. (2001) · Environmental and Molecular Mutagenesis · doi:10.1002/em.1072 · Cited by 23
“…Kharbanda et al., 1996] and NF-kB [Lee et al., 1998; Piret et al., 1999; Li et al., 2001] as well as BRCA1 [Gatei et al., 2000; Cortez et al., 1999], all of which are involved in DNA surveillance and repair (both homologous and nonhomologous) processes [Morrison et al., 2000; Kanaar et al., 1998].”

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
Publisher: Springer Science and Business Media LLC
Published: 2000-02-01
Volume: 19
Issue: 3
Pages: 463-471
ISSN: 0261-4189 (ISSN-L)
1460-2075
DOI: 10.1093/emboj/19.3.463
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
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
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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The controlling role of ATM in homologous recombinational repair of DNA damage

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