The ATM protein is required for sustained activation of NF-κB following DNA damage
Abstract
Cells lacking an intact ATM gene are hypersensitive to ionizing radiation and show multiple defects in the cell cycle-coupled checkpoints. DNA damage usually triggers cell cycle arrest through, among other things, the activation of p53. Another DNA-damage responsive factor is NF-kappaB. It is activated by various stress situations, including oxidative stress, and by DNA-damaging compounds such as topoisomerase poisons. We found that cells from Ataxia Telangiectasia patients exhibit a defect in NF-kappaB activation in response to treatment with camptothecin, a topoisomerase I poison. In AT cells, this activation is shortened or suppressed, compared to that observed in normal cells. Ectopic expression of the ATM protein in AT cells increases the activation of NF-kappaB in response to camptothecin. MO59J glioblastoma cells that do not express the DNA-PK catalytic subunit respond normally to camptothecin. These results support the hypothesis that NF-kappaB is a DNA damage-responsive transcription factor and that its activation pathway by DNA damage shares some components with the one leading to p53 activation.
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In AT fibroblasts, NF-kB is activated in an ATM-dependent manner following treatment with a radiomimetic, ionizing radiation, or topoisomerase inhibitor.
“Previous work with AT fibroblasts had shown that the canonical immune transcription factor NF‐kB is activated in an ATM‐dependent manner following treatment with a radiomimetic, ionizing radiation, or topoisomerase inhibitor (Lee et al, 1998; Piret et al, 1999; Li et al, 2001).”
From Mechanisms of DNA damage-mediated neurotoxicity in neurodegenerative disease (2022) · cites this paper as Piret et al, 1999
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BackgroundIκB kinase complexes: gateways to NF-κB activation and transcription
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“In transfected cells, CYLD interacts with NEMO and TRAFs, selectively degrades UbLys63 chains from NEMO, TRAF2, TRAF6 or TRAF7, and represses activation of IKK and NF-kB by various stimuli.”
BackgroundInfluentialPoly(ADP-ribose) polymerase-1: what have we learned from the deficient mouse model?
Shall, S., & de MURCIA, G. (2000) · Mutation Research/DNA Repair · doi:10.1016/s0921-8777(00)00016-1 · Cited by 534 · see citing works
Molecular Linkage Between the Kinase ATM and NF-κB Signaling in Response to Genotoxic Stimuli
Wu, Z., Shi, Y., Tibbetts, R. S., & Miyamoto, S. (2006) · Science · doi:10.1126/science.1121513 · Cited by 515 · see citing works
Li, F., & Sethi, G. (2010) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2010.01.002 · Cited by 402 · see citing works
“acts as a DNA damage sensor, is required for IKK activation [16,17].”
BackgroundIrinotecan in the Treatment of Colorectal Cancer: Clinical Overview
Vanhoefer, U. J., Harstrick, A., Achterrath, W., Cao, S., Seeber, S., & Rustum, Y. M. (2001) · Journal of Clinical Oncology · doi:10.1200/jco.2001.19.5.1501 · Cited by 327 · see citing works
Signals from within: the DNA-damage-induced NF-κB response
Janssens, S., & Tschopp, J. (2006) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4401843 · Cited by 321 · see citing works
“Furthermore, also CPT and doxorubicin appear to induce NF-kB activation via an ATM-dependent pathway.(27,39,42) Importantly, anthracyclinlike molecules that do not cause DNA breaks but activate NF-kB via unrelated pathways (presumably through the activation of PKC-d) do not need ATM.”
PIDD Mediates NF-κB Activation in Response to DNA Damage
Janssens, S., Tinel, A., Lippens, S., & Tschopp, J. (2005) · Cell · doi:10.1016/j.cell.2005.09.036 · Cited by 319 · see citing works
Repair of and checkpoint response to topoisomerase I-mediated DNA damage
Pommier, Y. G., Redon, C., Rao, V. A., Seiler, J. A., Sordet, O., Takemura, H., Antony, S., Meng, L., Liao, Z., Kohlhagen, G., et al. (2003) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2003.08.016 · Cited by 299 · see citing works
ATM: Genome stability, neuronal development, and cancer cross paths
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The DNA damage-induced cell death response: a roadmap to kill cancer cells
Matt, S., & Hofmann, T. G. (2016) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-016-2130-4 · Cited by 288 · see citing works
“Following DNA damage, ATM can activate the NF-jB pathway to promote cell survival [155] [156, 157].”
BackgroundHinz, M., Stilmann, M., Arslan, S. Ç., Khanna, K. K., Dittmar, G., & Scheidereit, C. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.09.008 · Cited by 280 · see citing works
“NF-kB activation requires ATM and PARP-1 (Li et al., 2001; Piret et al., 1999; Stilmann et al., 2009).”
Baldwin, A. S. (2012) · Immunological Reviews · doi:10.1111/j.1600-065x.2012.01095.x · Cited by 277 · see citing works
“Interestingly, ATM is required for NF-jB activation in response to DNA damage (23, 24).”
BackgroundATM: A mediator of multiple responses to genotoxic stress
Rotman, G., & Shiloh, Y. (1999) · Oncogene · doi:10.1038/sj.onc.1203124 · Cited by 272 · see citing works
“The induction by IR of the NF-kB pathway was abrogated in these cells (Basu et al., 1998), whereas normal induction was observed in response to campothecin, a topoisomerase I inhibitor which generates DSBs (Piret et al., 1999).”
BackgroundSenescent cells develop a parp-1 and nuclear factor-κB-associated secretome (PNAS).
Ohanna, M., Giuliano, S., Bonet, C., Imbert, V., Hofman, V., Zangari, J., Bille, K., Robert, C., Bressac-de Paillerets, B., Hofman, P., et al. (2011) · Genes & Development · doi:10.1101/gad.625811 · Cited by 267 · see citing works
NEMO and RIP1 Control Cell Fate in Response to Extensive DNA Damage via TNF-α Feedforward Signaling
Biton, S., & Ashkenazi, A. (2011) · Cell · doi:10.1016/j.cell.2011.02.023 · Cited by 262 · see citing works
“An important signaling cascade activated by ATM is the NF-kB pathway, which regulates genes involved in diverse biological functions, including inhibition of apoptosis and promotion of cell survival (Criswell et al., 2003; Huang et al., 2003; Li et al., 2001; Piret et al., 1999).”
Nuclear initiated NF-κB signaling: nemo and ATM take center stage
Miyamoto, S. (2011) · Cell Research · doi:10.1038/cr.2010.179 · Cited by 253 · see citing works
DNA damage‐dependent NF‐κB activation: NEMO turns nuclear signaling inside out
McCool, K. W., & Miyamoto, S. (2012) · Immunological Reviews · doi:10.1111/j.1600-065x.2012.01101.x · Cited by 251 · see citing works
Mediation of cell death by poly(ADP-ribose) polymerase-1
Koh, D. W., Dawson, T. M., & Dawson, V. L. (2005) · Pharmacological Research · doi:10.1016/j.phrs.2005.02.011 · Cited by 246 · see citing works
The intersection of radiotherapy and immunotherapy: Mechanisms and clinical implications
Spiotto, M. T., Fu, Y., & Weichselbaum, R. R. (2016) · Science Immunology · doi:10.1126/sciimmunol.aag1266 · Cited by 240 · see citing works
“Gasser et al. demonstrated that radiation and other genotoxic stress induced expression of ligands binding NKG2D, which was dependent of ATM, ataxia telangiectasia– and Rad3-related protein, or checkpoint kinase 1 (47).”
BackgroundInfluentialA nuclear poly(ADP-Ribose)-dependent signalosome confers DNA damage-induced IκB kinase activation.
Stilmann, M., Hinz, M., Arslan, S. Ç., Zimmer, A., Schreiber, V., & Scheidereit, C. (2009) · Molecular Cell · doi:10.1016/j.molcel.2009.09.032 · Cited by 232 · see citing works
“DNA damage-induced NF-kB activation depends on activated ATM (Li et al., 2001; Piret et al., 1999), which can phosphorylate IKKg (Wu et al., 2006).”
BackgroundNF-κB modulation and ionizing radiation: mechanisms and future directions for cancer treatment
Magné, N., Toillon, R., Bottero, V., Mirjolet, C., Houtte, P. V., Gérard, J., & Peyron, J. (2005) · Cancer Letters · doi:10.1016/j.canlet.2005.01.022 · Cited by 189 · see citing works
ATM Is Required for IκB Kinase (IKK) Activation in Response to DNA Double Strand Breaks
Li, N., Banin, S., Ouyang, H., Li, G. C., Courtois, G., Shiloh, Y., Karin, M., & Rotman, G. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m009809200 · Cited by 188 · see citing works
Robe, P. A. J. T., Martin, D., Nguyen-Khac, M., Artesi, M., Deprez, M., Albert, A., Vanbelle, S., Califice, S., Bredel, M., & Bours, V. (2009) · BMC Cancer · doi:10.1186/1471-2407-9-372 · Cited by 184 · see citing works
“Inactivation of NF-kappaB blocks glioma growth in in vitro and in vivo models, and increases their response to radiation, chemotherapy and suicide gene therapy [11-13].”
BackgroundS Phase and G2 Arrests Induced by Topoisomerase I Poisons Are Dependent on ATR Kinase Function
Cliby, W. A., Lewis, K. A., Lilly, K. K., & Kaufmann, S. H. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m106287200 · Cited by 205 · see citing works
Hepatic stellate cell senescence in liver fibrosis: Characteristics, mechanisms and perspectives
Zhang, M., Salas, S. S., Damba, T., Borghesan, M., Demaria, M., & Moshage, H. J. (2021) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2021.111572 · Cited by 180 · see citing works
“Following DNA damage, ATM is activated and causes sustained NF-κB activation, independent of p53 signaling (Piret et al., 1999).”
MLL1 is essential for the senescence-associated secretory phenotype
Capell, B. C., Drake, A. M., Zhu, J., Shah, P. P., Dou, Z., Dorsey, J., Simola, D. F., Donahue, G., Sammons, M., Rai, T. S., et al. (2016) · Genes & Development · doi:10.1101/gad.271882.115 · Cited by 156 · see citing works
Chuang, S., Yeh, P.-Y., Lu, Y., Lai, G., Liao, C.-M., Gao, M., & Cheng, A. (2002) · Biochemical Pharmacology · doi:10.1016/s0006-2952(02)00931-0 · Cited by 158 · see citing works
Cellular Stresses and Stress Responses in the Pathogenesis of Insulin Resistance
Onyango, A. N. (2018) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2018/4321714 · Cited by 160 · see citing works
“ATM activates NF-κB following DNA damage [320].”
NF-κB Activation by Camptothecin
Huang, T. T., Wuerzberger‐Davis, S. M., Seufzer, B. J., Shumway, S. D., Kurama, T., Boothman, D. A., & Miyamoto, S. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.13.9501 · Cited by 158 · see citing works
Butein induces G2/M phase arrest and apoptosis in human hepatoma cancer cells through ROS generation
Moon, D.-O., Kim, M.-O., Choi, Y. H., Hyun, J. W., Chang, W. Y., & Kim, G.-Y. (2010) · Cancer Letters · doi:10.1016/j.canlet.2009.07.002 · Cited by 151 · see citing works
“An accumulation of ROS can severely damage cellular macromolecules, especially DNA, and induce G2/M phase arrest through ataxia telangiectasia mutant (ATM) activation [7].”
BackgroundPise-Masison, C. A., Mahieux, R., Jiang, H., Ashcroft, M. A., Radonovich, M. F., Duvall, J. F., Guillerm, C., & Brady, J. N. (2000) · Molecular and Cellular Biology · doi:10.1128/.20.10.3377-3386.2000 · Cited by 143 · see citing works
The Nuclear Factor κB pathway: A link to the immune system in the radiation response
Hellweg, C. E. (2015) · Cancer Letters · doi:10.1016/j.canlet.2015.02.019 · Cited by 139 · see citing works
“ATM was shown to be required for NF-κB activation after DNA damage [92,93,106,108], and NF-κB/RelA translocation and Ser-276 phosphorylation was reduced in ATM(−/−) murine embryonic fibroblasts (MEF) [109].”
BackgroundNF-κB activation by double-strand breaks
Habraken, Y., & Piette, J. G. (2006) · Biochemical Pharmacology · doi:10.1016/j.bcp.2006.07.015 · Cited by 140 · see citing works
Self-citationLi, M., You, L., Xue, J., & Lü, Y. (2018) · Frontiers in Pharmacology · doi:10.3389/fphar.2018.00522 · Cited by 141 · see citing works
“…induces proinflammatory gene expression including IL-1α/β, IL-6, TGF-β, TNF-α, fibroblast growth factor, hepatocyte growth factor, and matrix metalloproteinases et al., which belong to the SASP factors (Piret et al., 1999; Orjalo et al., 2009; Ferrand et al., 2015; Childs et al., 2017) (Figure 1A).”
BackgroundBottero, V., Busuttil, V., Loubat, A., Magné, N., Fischel, J., Milano, G. A., & Peyron, J. (2001) · PubMed · Cited by 132 · see citing works
Many faces of NF-κB signaling induced by genotoxic stress
Wu, Z., & Miyamoto, S. (2007) · Journal of Molecular Medicine · doi:10.1007/s00109-007-0227-9 · Cited by 129 · see citing works
“Interestingly, all AT cell lines also activated NF-κB in response to the anticancer drug daunomycin, a Topo II poison that also stimulates generation of free radicals and ceramide [49].”
Mechanisms of DNA damage-mediated neurotoxicity in neurodegenerative disease
Welch, G., & Tsai, L. (2022) · The EMBO Reports · doi:10.15252/embr.202154217 · Cited by 129 · see citing works
“Previous work with AT fibroblasts had shown that the canonical immune transcription factor NF-kB is activated in an ATM-dependent manner following treatment with a radiomimetic, ionizing radiation, or topoisomerase inhibitor (Lee et al , 1998; Piret et al , 1999; Li et al , 2001).”
Panta, G. R., Kaur, S., Cavin, L. G., Cortés, M. L., Mercurio, F., Lothstein, L., Sweatman, T. W., Israel, M., & Arsura, M. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.5.1823-1835.2004 · Cited by 127 · see citing works
Yeh, P.-Y., Yeh, K., Chuang, S., Song, Y., & Cheng, A. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m402362200 · Cited by 119 · see citing works
Schmitt, E., Paquet, C., Beauchemin, M., & Bertrand, R. (2007) · Journal of Zhejiang University SCIENCE B · doi:10.1631/jzus.2007.b0377 · Cited by 114 · see citing works
Klammer, H., Mladenov, E., Li, F., & Iliakis, G. E. (2013) · Cancer Letters · doi:10.1016/j.canlet.2013.12.017 · Cited by 111 · see citing works
Nuclear Factor-κB Modulates the p53 Response in Neurons Exposed to DNA Damage
Aleyasin, H., Cregan, S. P., Iyirhiaro, G. O., O'Hare, M. J., Callaghan, S. M., Slack, R. S., & Park, D. S. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.0155-04.2004 · Cited by 108 · see citing works
“, 2003), also is reported to regulate NF- B activity (Piret et al., 1999).”
BackgroundDNA damage-induced nuclear factor-kappa B activation and its roles in cancer progression
Wang, W., Mani, A. M., & Wu, Z. (2017) · Journal of Cancer Metastasis and Treatment · doi:10.20517/2394-4722.2017.03 · Cited by 109 · see citing works
“Later Piret et al.[56] reported that decreased NF-kB activation by the chemotherapeutic drug CPT in A-T cells could be restored by complementation with ATM.”
BackgroundJin, H., Lee, D.-H., Kim, D., Chung, J.-H., Lee, S.-J., & Lee, T. H. (2009) · Cancer Research · doi:10.1158/0008-5472.can-08-2256 · Cited by 102 · see citing works
Mabb, A. M., & Miyamoto, S. (2007) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-007-7005-2 · Cited by 100 · see citing works
DNA-dependent protein kinase inhibitors as drug candidates for the treatment of cancer.
Kashishian, A., Douangpanya, H., Clark, D., Schlachter, S. T., Eary, C. T., Schiro, J. G., Huang, H., Burgess, L. E., Kesicki, E. A., & Halbrook, J. (2003) · PubMed · Cited by 95 · see citing works
Buchholz, T. A., Garg, A. K., Chakravarti, N., Aggarwal, B. B., Esteva, F. J., Kuerer, H. M., Singletary, S. E., Hortobágyi, G. N., Pusztai, L., Cristofanilli, M., et al. (2005) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-05-0885 · Cited by 94 · see citing works
Necrosis Is an Active and Controlled Form of Programmed Cell Death
Proskuryakov, S. Y., Gabai, V. L., & Konoplyannikov, A. (2002) · Biochemistry (Moscow) · doi:10.1023/a:1015289521275 · Cited by 94 · see citing works
Pamment, J., Ramsay, E., Kelleher, M., Dornan, D., & Ball, K. L. (2002) · Oncogene · doi:10.1038/sj.onc.1205981 · Cited by 88 · see citing works
“For example ATM is required, in some cell types, for the activation of NF-kB in response to IR (Li et al., 2001; Piret et al., 1999).”
BackgroundAblation of XP-V gene causes adipose tissue senescence and metabolic abnormalities
Chen, Y.-W., Harris, R. A., Hatahet, Z., & Chou, K.-M. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1506954112 · Cited by 86 · see citing works
“The primary antibodies used for Western blotting were the following antimouse antibodies: anti-ATM, anti–phospho-γ-H2AX, and anti–Parp-1 antibodies from Cell Signaling Technology; anti–phospho-ATM (Ser1981) and anti–Ki-67 antibodies from Millipore; anti-p53, anti–phospho-p53 (Ser15), anti-p21, anti–phospho-p21, anti–P…”
BackgroundInfluentialLinking JNK Activity to the DNA Damage Response
Picco, V., & Pagès, G. (2013) · Genes & Cancer · doi:10.1177/1947601913486347 · Cited by 84 · see citing works
“A fundamental development confirming the existence of a nucleus-to-cytoplasm signaling pathway came from extending the results obtained with UV radiation activation of NF-κB to a variety of other DNAdamaging agents such as etoposide or camptothecin.(36,37) Another convincing line of evidence comes from an experiment u…”
BackgroundWu, Z., & Miyamoto, S. (2008) · The EMBO Journal · doi:10.1038/emboj.2008.127 · Cited by 82 · see citing works
Wuerzberger‐Davis, S. M., Nakamura, Y., Seufzer, B. J., & Miyamoto, S. (2006) · Oncogene · doi:10.1038/sj.onc.1209815 · Cited by 82 · see citing works
“…different signaling events are implicated in NF-kB activation, such as the ataxia telangiectasia mutated (ATM) protein kinase (Lee et al., 1998; Piret et al., 1999; Li et al., 2001; Huang et al., 2003) and multiple cytoplasmic signaling components (Romashkova and Makarov, 1999; Habraken et…”
BackgroundRole of nuclear factor κB in liver health and disease
Robinson, S. M., & Mann, D. A. (2010) · Clinical Science · doi:10.1042/cs20090549 · Cited by 81 · see citing works
Atm deficiency causes an increased frequency of intrachromosomal homologous recombination in mice.
Bishop, A. J. R., Barlow, C., Wynshaw-Boris, A. J., & Schiestl, R. H. (2000) · PubMed · Cited by 75 · see citing works
The role of ATM in breast cancer development
Prokopcova, J., Kleibl, Z., Banwell, C. M., & Pohlreich, P. (2006) · Breast Cancer Research and Treatment · doi:10.1007/s10549-006-9406-6 · Cited by 76 · see citing works
“Phosphorylated IjB is released from NFjB, and activated NFjB is translocated to the nucleus where it acts as a transcriptional regulator of antiapoptotic genes [37].”
BackgroundRashi‐Elkeles, S., Elkon, R., Weizman, N., Linhart, C., Amariglio, N., Sternberg, G., Rechavi, G., Barzilai, A., Ron Shamir, A., & Shiloh, Y. (2005) · Oncogene · doi:10.1038/sj.onc.1209189 · Cited by 75 · see citing works
“These results are in agreement with previous studies that reported compromised IR-induced activation of both NF-kB and p53 in murine Atm-deficient tissues and in cell lines derived from A-T patients (Banin et al., 1998; Piret et al., 1999; Li et al., 2001; Saito et al., 2002).”
Składanowski, A., Bozko, P. M., & Sabisz, M. (2009) · Chemical Reviews · doi:10.1021/cr900026u · Cited by 71 · see citing works
Ciceroni, C., Bonelli, M., Mastrantoni, E., Niccolini, C., Laurenza, M., Larocca, L. M., D, R. P. M., Traficante, A., Spinsanti, P., Ricci‐Vitiani, L., et al. (2012) · Cell Death and Differentiation · doi:10.1038/cdd.2012.150 · Cited by 71 · see citing works
ATM-NF-κB Connection as a Target for Tumor Radiosensitization
Ahmed, K. M., & Li, J. J. (2007) · Current Cancer Drug Targets · doi:10.2174/156800907780809769 · Cited by 64 · see citing works
Pan-cancer analysis distinguishes transcriptional changes of aneuploidy from proliferationPreprint
Buccitelli, C., Salgueiro, L., Rowald, K., Sotillo, R., Mardin, B. R., & Korbel, J. O. (2017) · Genome Research · doi:10.1101/gr.212225.116 · Cited by 61 · see citing works
“The “ up ” gene set was enriched especially for targets of MYC but also NFKB1 , the latter having been previously implicated in the regulation of senescence in response to DNA damage (Mercurio and Manning 1999; Piret et al. 1999; Chien et al. 2011; Kang et al. 2015; Voce et al. 2015).”
BackgroundSchön, M., Wienrich, B. G., Kneitz, S., Sennefelder, H., Amschler, K., Voehringer, V., Weber, O., Stiewe, T., Ziegelbauer, K. B., & Schön, M. P. (2008) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djn174 · Cited by 59 · see citing works
Poly-ADP-ribosylation in health and disease
Koh, D. W., Dawson, T. M., & Dawson, V. L. (2005) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-004-4508-y · Cited by 59 · see citing works
Signals from the Nucleus: Activation of NF-κB by Cytosolic ATM in the DNA Damage Response
Hadian, K., & Krappmann, D. (2011) · Science Signaling · doi:10.1126/scisignal.2001712 · Cited by 57 · see citing works
Kang, N., Jian, J.-F., Cao, S., Zhang, Q., Mao, Y.-W., Huang, Y., Peng, Y., Qiu, F., & Gao, X. (2016) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-016-2686-1 · Cited by 56 · see citing works
“An accumulation of ROS can severely damage cellular macromolecules, especially DNA, and induce cell cycle arrest [17].”
BackgroundThe many interactions between the innate immune system and the response to radiation
Candéias, S. M., & Testard, I. (2015) · Cancer Letters · doi:10.1016/j.canlet.2015.02.007 · Cited by 54 · see citing works
“Indeed, IκB-α [77,78] or NEMO [80] phosphorylation allows the nuclear translocation of NF-κB and the activation of its DNA binding activity.”
BackgroundFu, K., Sun, X., Wier, E. M., Hodgson, A., Liu, Y., Sears, C. L., & Wan, F. (2016) · eLife · doi:10.7554/elife.15018 · Cited by 53 · see citing works
“(Li et al., 2001; Piret et al., 1999), poly (ADP-ribose) polymerase 1 (PARP1) was recently revealed”
BackgroundInfluentialActivation of Nuclear Factor κB by Different Agents
Hellweg, C. E., Arenz, A., Bogner, S., Schmitz, C., & Baumstark‐Khan, C. (2006) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1378.066 · Cited by 49 · see citing works
Van, P. L., Yim, K.-W., Jin, D., Dapolito, G., Kurimasa, A., & Jeang, K. (2001) · Journal of Virology · doi:10.1128/jvi.75.1.396-407.2001 · Cited by 49 · see citing works
DNA double-strand breaks: a potential therapeutic target for neurodegenerative diseases
Thadathil, N., Hori, R. T., Xiao, J., & Khan, M. M. (2019) · Chromosome Research · doi:10.1007/s10577-019-09617-x · Cited by 48 · see citing works
IκB kinase β phosphorylates Dok1 serines in response to TNF, IL-1, or γ radiation
Lee, S., Andrieu‐Soler, C., Saltel, F., Destaing, O., Auclair, J., Pouchkine, V., Michelon, J., Salaun, B., Kobayashi, R., Jurdic, P., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0408061101 · Cited by 48 · see citing works
Reddy, B. V., & Prasad, N. R. (2012) · Tumor Biology · doi:10.1007/s13277-012-0545-6 · Cited by 47 · see citing works
“These cells also display a defect in NF-κB activation that could explain in part their enhanced apoptotic responses to DNA damaging agents [52].”
BackgroundGudipaty, S. A., McNamara, R. P., Morton, E. L., & D’Orso, I. (2015) · Molecular and Cellular Biology · doi:10.1128/mcb.00226-15 · Cited by 45 · see citing works
“Since inhibition of ATM blocks the PPM1G-7SK RNA interaction as well as the activation of NF- B transcription in response to DNA damage (48, 57, 62), it appears that both molecular events are intimately coupled and that the role of ATM in promoting the PPM1G-7SK RNA interaction relies on NF- B signaling.”
BackgroundTranscription Factors in the Cellular Response to Charged Particle Exposure
Hellweg, C. E., Spitta, L. F., Henschenmacher, B., Diegeler, S., & Baumstark‐Khan, C. (2016) · Frontiers in Oncology · doi:10.3389/fonc.2016.00061 · Cited by 44 · see citing works
The Molecular Basis and Clinical Management of Ataxia Telangiectasia
Spacey, S. D., Gatti, R. A., & Bebb, G. D. (2000) · Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques · doi:10.1017/s0317167100000822 · Cited by 42 · see citing works
Yeh, P.-Y., Chuang, S., Yeh, K., Song, Y., & Cheng, A. (2003) · Biochemical Pharmacology · doi:10.1016/s0006-2952(03)00250-8 · Cited by 41 · see citing works
Yin, K., Chen, S., Lee, J., Xu, J., & Hsu, C. Y. (2002) · Stroke · doi:10.1161/01.str.0000030316.79601.03 · Cited by 41 · see citing works
Sabatel, H., Valentin, E. D., Gloire, G., Dequiedt, F., Piette, J. G., & Habraken, Y. (2012) · PLoS ONE · doi:10.1371/journal.pone.0038246 · Cited by 40 · see citing works
“The primordial role of ATM kinase in NF-kB activation by DSB was demonstrated some years ago [25,26], but the different molecular mechanisms by which it controls this signaling cascade are continuously uncovered.”
BackgroundSelf-citationSignalling loops and linear pathways: NF- B activation in response to genotoxic stress
Brzóska, K., & Szumiel, I. (2008) · Mutagenesis · doi:10.1093/mutage/gen056 · Cited by 40 · see citing works
TSG101 associates with PARP1 and is essential for PARylation and DNA damage‐induced NF‐κB activation
Tufan, A. B., Lazarow, K., Kolesnichenko, M., Sporbert, A., von Kries, J. P., & Scheidereit, C. (2022) · The EMBO Journal · doi:10.15252/embj.2021110372 · Cited by 38 · see citing works
“Following activation, auto-modified PARP1 forms a transient nuclear complex with IKK c , PIASy, and ATM (Stilmann et al , 2009).”
InfluentialImportance of PIKKs in NF-κB activation by genotoxic stress
Sabatel, H., Pirlot, C., Piette, J. G., & Habraken, Y. (2011) · Biochemical Pharmacology · doi:10.1016/j.bcp.2011.07.105 · Cited by 39 · see citing works
“AT cells\IR\20 Gy [10] AT cells\CPT\10 mM [113]”
BackgroundMethodSelf-citationSinha, S., Ghildiyal, R., Mehta, V., & Sen, E. (2013) · Cell Death and Disease · doi:10.1038/cddis.2013.128 · Cited by 41 · see citing works
“Also, ATM sustains NFkB activation following DNA damage.(20) As we have shown that inhibition of NFkB by chemotherapeutics sensitizes glioma cells to TNFa-induced apoptosis,(21,22) we investigated whether TNFa effects the responsiveness of glioma cell to NCS by fine tuning the”
BackgroundThe Molecular Mechanisms in Senescent Cells Induced by Natural Aging and Ionizing Radiation
Ibragimova, M., Kussainova, A., Aripova, A., Bersimbaev, R. I., & Bulgakova, O. (2024) · Cells · doi:10.3390/cells13060550 · Cited by 36 · see citing works
Huguet, F., Fernet, M., Giocanti, N., Favaudon, V., & Larsen, A. K. (2015) · Targeted Oncology · doi:10.1007/s11523-015-0403-8 · Cited by 36 · see citing works
Williams, E. J., Baines, K. J., Berthon, B. S., & Wood, L. G. (2017) · Nutrients · doi:10.3390/nu9020116 · Cited by 35 · see citing works
Sustained elevation of NF‐ κ B DNA binding activity in radiation‐induced lung damage in rats
Haase, M., Klawitter, A., Geyer, P., Alheit, H., Baumann, M. A., Kriegel, T. M., Kasper, M. E., & Baretton, G. B. (2003) · International Journal of Radiation Biology · doi:10.1080/09553000310001632903 · Cited by 34 · see citing works
“In a cell culture model, it has been found that ataxia telangiectasia mutated (ATM) plays a role in sustained activation of NF-kB after DNA damage (Piret et al. 1999).”
BackgroundCellular Monitoring of the Nuclear Factor κB Pathway for Assessment of Space Environmental Radiation
Baumstark‐Khan, C., Hellweg, C. E., Arenz, A., & Meier, M. M. (2005) · Radiation Research · doi:10.1667/rr3397.1 · Cited by 35 · see citing works
“In a cell culture model, it has been found that ataxia telangiectasia mutated protein (ATM) plays a role in sustained activation of NF-kB in response to DNA double-strand breaks (12, 13), probably by its PI3 kinase-like activity (3).”
BackgroundATM-dependent activation of the gene encoding MAP kinase phosphatase 5 by radiomimetic DNA damage
Bar‐Shira, A., Rashi‐Elkeles, S., Zlochover, L., Moyal, L., Smorodinsky, N. I., Seger, R., & Shiloh, Y. (2002) · Oncogene · doi:10.1038/sj.onc.1205127 · Cited by 34 · see citing works
“It appears that when the damage involves DSBs, this response is ATM-dependent with regard to both the NF-kB pathway (Lee et al., 1998; Li et al., 2000; Piret et al., 1999) and the MAP kinase system (Shafman et al., 1995; Wang et al., 2000).”
BackgroundLiu, K., Song, J., Yan, Y., Zou, K., Che, Y., Wang, B., Li, Z., Yu, W., Guo, W., Zou, L., et al. (2020) · Translational Oncology · doi:10.1016/j.tranon.2020.100876 · Cited by 31 · see citing works
Nuclear factor-κB as a predictor of treatment response in breast cancer
Garg, A. K., Hortobágyi, G. N., Aggarwal, B. B., Şahin, A. A., & Buchholz, T. A. (2003) · Current Opinion in Oncology · doi:10.1097/00001622-200311000-00001 · Cited by 30 · see citing works
Calcium-Dependent Regulation of NEMO Nuclear Export in Response to Genotoxic Stimuli
Berchtold, C. M., Wu, Z., Huang, T. T., & Miyamoto, S. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.01772-06 · Cited by 31 · see citing works
“Similarly, a picture is also emerging in which certain genotoxic stress inducers mediate NF- B signaling by triggering IKK activation (31, 42, 52, 61, 65, 69).”
Backgroundc‐IAP2 is induced by ionizing radiation through NF‐κB binding sites
Ueda, T., Akiyama, N., Sai, H., Oya, N., Noda, M., Hiraoka, M., & Kizaka‐Kondoh, S. (2001) · FEBS Letters · doi:10.1016/s0014-5793(01)02145-7 · Cited by 30 · see citing works
Ariumi, Y., & Trono, D. (2006) · Journal of Virology · doi:10.1128/jvi.80.5.2445-2452.2006 · Cited by 28 · see citing works
“Interestingly, the activation of NF- B following DNA damage is abrogated in ATM-deficient cells (29), indicating a link between NF- B and the ATM signaling pathway.”
BackgroundHabraken, Y., Jolois, O., & Piette, J. G. (2003) · Oncogene · doi:10.1038/sj.onc.1206893 · Cited by 28 · see citing works
“ATM is the only nuclear protein shown to be an intermediate in NF-kB activation by DSB, since NF-kB activation by CPT or IR is reduced in intensity and duration in AT-deficient cell lines (Piret et al., 1999; Li et al., 2001).”
BackgroundSelf-citationRodríguez-Vargas, J. M., Martin-Hernandez, K., Wang, W., Kunath, N., Suganthan, R., Amé, J., Oliver, F. J., Ye, J., Bjørås, M., & Dantzer, F. (2020) · Cell Death and Disease · doi:10.1038/s41419-020-03167-5 · Cited by 27 · see citing works
Zhao, Q., Ma, Y., Li, Z., Zhang, K., Zheng, M., & Zhang, S. (2020) · Stem Cells International · doi:10.1155/2020/8835714 · Cited by 27 · see citing works
“PTM of NF-κB essential modulator (NEMO) is indispensable to link the cellular genotoxic response to NF-κB via the ATM kinase [69, 70].”
BackgroundCrosstalk between cGAS-STING pathway and autophagy in cancer immunity
Lu, Q., Chen, Y., Li, J., Zhu, F., & Zheng, Z. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1139595 · Cited by 27 · see citing works
Quantitative Proteomics Reveal ATM Kinase-dependent Exchange in DNA Damage Response Complexes
Choi, S., Srivas, R., Fu, K. Y., Hood, B. L., Dost, B., Gibson, G. A., Watkins, S. C., Houten, B. V., Bandeira, N., Conrads, T. P., et al. (2012) · Journal of Proteome Research · doi:10.1021/pr3005524 · Cited by 27 · see citing works
- Authors
- Piret, B., Schoonbroodt, S., & Piette, J.
- Affiliations
- University of Liège (BE)
- Venue
- Oncogene
- Published
- 1999-04-01
- Volume
- 18
- Issue
- 13
- Pages
- 2261-2271
- ISSN
- 0950-9232 (ISSN-L)
- 1476-5594
- OpenAlex
- W2316716290
- Cited by
- 176
- References
- 96
- Citations by year
- 2025: 4 · 2024: 5 · 2023: 2 · 2022: 6 · 2021: 4 · 2020: 5 · 2019: 2 · 2018: 4 · 2017: 4 · 2016: 10 · 2015: 11 · 2014: 2 · 2013: 5 · 2012: 9
- FWCI
- 3.21
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Oncogene (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › NF-κB Signaling Pathways
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Effects of Radiation Exposure
- Keywords
- ATM protein, NF-κB activation, DNA damage response, camptothecin, topoisomerase I poisons, ataxia telangiectasia, p53, cell cycle checkpoints, radiosensitivity, DNA-dependent protein kinase, transcription factors
- MeSH terms
- NF-KappaB Inhibitor alpha, Adolescent, Age Factors, Antineoplastic Agents, Phytogenic, Ataxia Telangiectasia, Brain Neoplasms, Camptothecin, Cells, Cultured, Child, Child, Preschool, DNA Damage, DNA-Binding Proteins, Enzyme Inhibitors, Fibroblasts, Gene Expression Regulation, Glioblastoma, Humans, Leupeptins, Nuclear Proteins, Phosphoric Monoester Hydrolases, Protease Inhibitors, Proteins, Radiation Tolerance, Recombinant Fusion Proteins, Transcription, Genetic, Tumor Cells, Cultured, Tumor Necrosis Factor-alpha, Tumor Suppressor Protein p53, NF-kappa B, Protein Serine-Threonine Kinases, Cell Cycle Proteins, I-kappa B Proteins, Tumor Suppressor Proteins, DNA-Activated Protein Kinase, Topoisomerase I Inhibitors, Ataxia Telangiectasia Mutated Proteins
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