The ATM kinase inhibitor KU-55933 provides neuroprotection against hydrogen peroxide-induced cell damage via a γH2AX/p-p53/caspase-3-independent mechanism: Inhibition of calpain and cathepsin D

Adams, 2010, Dynamic dependence on ATR and ATM for double-strand break repair in human embryonic stem cells and neural descendants, PLoS One, 5, e10001, 10.1371/journal.pone.0010001 Alvira, 2007, Neuroprotective effects of caffeine against complex I inhibition-induced apoptosis are mediated by inhibition of the Atm/p53/E2F-1 path in cerebellar granule neurons, J. Neurosci. Res., 85, 3079, 10.1002/jnr.21427 Bakkenist, 2003, DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation, Nature, 421, 499, 10.1038/nature01368 Barlow, 1999, Loss of the ataxia-telangiectasia gene product causes oxidative damage in target organs, Proc. Natl. Acad. Sci. U. S. A., 96, 9915, 10.1073/pnas.96.17.9915 Barlow, 2000, ATM is a cytoplasmic protein in mouse brain required to prevent lysosomal accumulation, Proc. Natl. Acad. Sci. U. S. A., 97, 871, 10.1073/pnas.97.2.871 Berkovich, 2007, Roles of ATM and NBS1 in chromatin structure modulation and DNA double-strand break repair, Nat. Cell. Biol., 9, 683, 10.1038/ncb1599 Bernstein, 2011, 6-OHDA generated ROS induces DNA damage and p53- and PUMA-dependent cell death, Mol. Neurodegener., 6, 2, 10.1186/1750-1326-6-2 Boehrs, 2007, Constitutive expression and cytoplasmic compartmentalization of ATM protein in differentiated human neuron-like SH-SY5Y cells, J. Neurochem., 100, 337, 10.1111/j.1471-4159.2006.04254.x Bredesen, 2006, Cell death in the nervous system, Nature, 443, 796, 10.1038/nature05293 Burma, 2001, ATM phosphorylates histone H2AX in response to DNA double-strand breaks, J. Biol. Chem., 276, 42462, 10.1074/jbc.C100466200 Cam, 2010, mTORC1 signaling under hypoxic conditions is controlled by ATM-dependent phosphorylation of HIF-1α, Mol. Cell, 40, 509, 10.1016/j.molcel.2010.10.030 Camins, 2010, Activation of ataxia telangiectasia muted under experimental models and human Parkinson’s disease, Cell. Mol. Life. Sci., 67, 3865, 10.1007/s00018-010-0408-5 Chakrabarti, 2012, ATP depletion triggers acute myeloid leukemia differentiation through an ATR/Chk1 protein-dependent and p53 protein-independent pathway, J. Biol. Chem., 287, 23635, 10.1074/jbc.M111.312801 Cheung, 2009, Effects of all-trans-retinoic acid on human SH-SY5Y neuroblastoma as in vitro model in neurotoxicity research, Neurotoxicology, 30, 127, 10.1016/j.neuro.2008.11.001 Cicenas, 2015, Roscovitine in cancer and other diseases, Ann. Transl. Med., 3, 135 Crighton, 2004, Splicing DNA-damage responses to tumour cell death, BBA-Rev. Cancer, 1705, 3 Di Benedetto, 2012, N-desalkylquetiapine activates ERK1/2 to induce GDNF release in C6 glioma cells: a putative cellular mechanism for quetiapine as antidepressant, Neuropharmacology, 62, 209, 10.1016/j.neuropharm.2011.07.001 Diemert, 2012, Impedance measurement for real time detection of neuronal cell death, J. Neurosci. Methods, 203, 69, 10.1016/j.jneumeth.2011.09.012 Doti, 2014, Inhibition of the AIF/CypA complex protects against intrinsic death pathways induced by oxidative stress, Cell. Death Dis., 5, e993, 10.1038/cddis.2013.518 El-Awady, 2016, Modulation of DNA damage response and induction of apoptosis mediates synergism between doxorubicin and a new imidazopyridine derivative in breast and lung cancer cells, DNA Repair. (Amst.), 37, 1, 10.1016/j.dnarep.2015.10.004 Foster, 2013, Deficiency of ataxia telangiectasia mutated kinase modulates cardiac remodeling following myocardial infarction: involvement in fibrosis and apoptosis, PLoS One, 8, e83513, 10.1371/journal.pone.0083513 Fujimaki, 2012, Blockade of ataxia telangiectasia mutated sensitizes hepatoma cell lines to sorafenib by interfering with Akt signaling, Cancer Lett., 319, 98, 10.1016/j.canlet.2011.12.043 Golding, 2007, Extracellular signal-related kinase positively regulates ataxia telangiectasia mutated, homologous recombination repair, and the DNA damage response, Cancer Res., 67, 1046, 10.1158/0008-5472.CAN-06-2371 Golding, 2009, Improved ATM kinase inhibitor KU-60019 radiosensitizes glioma cells, compromises insulin, AKT and ERK prosurvival signaling, and inhibits migration and invasion, Mol. Cancer Ther., 8, 2894, 10.1158/1535-7163.MCT-09-0519 Guo, 2010, ATM activation by oxidative stress, Science, 330, 517, 10.1126/science.1192912 Harmalkar, 2006, Staurosporine-induced growth inhibition of glioma cells is accompanied by altered expression of cyclins, CDKs and CDK inhibitors, Neurochem. Res., 31, 685, 10.1007/s11064-006-9068-0 Hickson, 2004, Identification and characterization of a novel and specific inhibitor of the ataxia-telangiectasia mutated kinase ATM, Cancer Res., 64, 9152, 10.1158/0008-5472.CAN-04-2727 Hwang, 2008, Zinc and 4-hydroxy-2-nonenal mediate lysosomal membrane permeabilization induced by H2O2 in cultured hippocampal neurons, J. Neurosci., 28, 3114, 10.1523/JNEUROSCI.0199-08.2008 Iijima, 2008, NBS1 regulates a novel apoptotic pathway through Bax activation, DNA Repair. (Amst.), 7, 1705, 10.1016/j.dnarep.2008.06.013 Iijima, 2008, Dancing on damaged chromatin: functions of ATM and the RAD50/MRE11/NBS1 complex in cellular responses to DNA damage, J. Radiat. Res., 49, 451, 10.1269/jrr.08065 Ivanov, 2009, Inhibition of ataxia telangiectasia mutated kinase activity enhances TRAIL-mediated apoptosis in human melanoma cells, Cancer Res., 69, 3510, 10.1158/0008-5472.CAN-08-3883 Jantas, 2009, Protective effect of memantine against Doxorubicin toxicity in primary neuronal cell cultures: influence a development stage, Neurotox. Res., 15, 24, 10.1007/s12640-009-9002-8 Jantas, 2009, Different mechanisms of NMDA-mediated protection against neuronal apoptosis: a stimuli-dependent effect, Neurochem. Res., 34, 2040, 10.1007/s11064-009-9991-y Jantas, 2008, The attenuating effect of memantine on staurosporine-, salsolinol- and doxorubicin-induced apoptosis in human neuroblastoma SH-SY5Y cells, Neurochem. Int., 52, 864, 10.1016/j.neuint.2007.10.003 Jantas, 2009, An involvement of BDNF and PI3-K/Akt in the anti-apoptotic effect of memantine on staurosporine-evoked cell death in primary cortical neurons, Apoptosis, 14, 900, 10.1007/s10495-009-0370-6 Jantas, 2013, The extent of neurodegeneration and neuroprotection in two chemical in vitro models related to Parkinson's disease is critically dependent on cell culture conditions, Neurotox. Res., 24, 41, 10.1007/s12640-012-9374-z Jantas, 2015, An involvement of PI3-K/Akt activation and inhibition of AIF translocation in neuroprotective effects of undecylenic acid (UDA) against pro-apoptotic factors-induced cell death in human neuroblastoma SH-SY5Y cells, J. Cell. Biochem., 116, 2882, 10.1002/jcb.25236 Jantas, 2016, The neuroprotective effects of orthosteric agonists of group II and III mGluRs in primary neuronal cell cultures are dependent on developmental stage, Neuropharmacology, 111, 195, 10.1016/j.neuropharm.2016.09.003 Jaworska-Feil, 2010, Protective effects of TRH and its analogues against various cytotoxic agents in retinoic acid (RA)-differentiated human neuroblastoma SH-SY5Y cells, Neuropeptides, 44, 495, 10.1016/j.npep.2010.08.004 Joza, 2009, AIF: not just an apoptosis-inducing factor, Ann. N.Y. Acad. Sci., 1171, 2, 10.1111/j.1749-6632.2009.04681.x Jung, 2008, Reactive oxygen species stabilize hypoxia-inducible factor-1 alpha protein and stimulate transcriptional activity via AMP-activated protein kinase in DU145 human prostate cancer cells, Carcinogenesis, 29, 713, 10.1093/carcin/bgn032 Jung, 2011, Beta-amyloid increases the expression level of ATBF1 responsible for death in cultured cortical neurons, Mol. Neurodegener., 6, 47, 10.1186/1750-1326-6-47 Katsube, 2014, Most hydrogen peroxide-induced histone H2AX phosphorylation is mediated by ATR and is not dependent on DNA double-strand breaks, J. Biochem., 156, 85, 10.1093/jb/mvu021 Katsuyama, 2012, Clioquinol induces DNA double-strand breaks, activation of ATM, and subsequent activation of p53 signaling, Toxicology, 299, 55, 10.1016/j.tox.2012.05.013 Kim, 2010, The ZFHX3 (ATBF1) transcription factor induces PDGFRB, which activates ATM in the cytoplasm to protect cerebellar neurons from oxidative stress, Dis. Model. Mech., 3, 752, 10.1242/dmm.004689 Kirshner, 2012, Malfunctioning DNA damage response (DDR) leads to the degeneration of nigro-striatal pathway in mouse brain, J. Mol. Neurosci., 46, 554, 10.1007/s12031-011-9643-y Koh, 1995, Staurosporine-induced neuronal apoptosis, Exp. Neurol., 135, 153, 10.1006/exnr.1995.1074 Kowara, 2005, Calpain-mediated truncation of dihydropyrimidinase-like 3 protein (DPYSL3) in response to NMDA and H2O2 toxicity, J. Neurochem., 95, 466, 10.1111/j.1471-4159.2005.03383.x Kruman, 2004, Cell cycle activation linked to neuronal cell death initiated by DNA damage, Neuron, 41, 549, 10.1016/S0896-6273(04)00017-0 Kuang, 2012, Activation of AMP-activated protein kinase in cerebella of Atm-/- mice is attributable to accumulation of reactive oxygen species, Biochem. Biophys. Res. Commun., 418, 267, 10.1016/j.bbrc.2012.01.008 Lee, 2007, Responding to DNA double strand breaks in the nervous system, Neuroscience, 145, 1365, 10.1016/j.neuroscience.2006.07.026 Lee, 2007, Hydrogen peroxide induces lysosomal protease alterations in PC12 cells, Neurochem. Res., 32, 1499, 10.1007/s11064-007-9338-5 Lee, 2013, Effect of conjugated linoleic acid, μ-calpain inhibitor, on pathogenesis of Alzheimer’s disease, Biochim. Biophys. Acta, 1831, 709, 10.1016/j.bbalip.2012.12.003 Lee, 2016, Nitroxide antioxidant as a potential strategy to attenuate the oxidative/nitrosative stress induced by hydrogen peroxide plus nitric oxide in cultured neurons, Nitric Oxide, 54, 38, 10.1016/j.niox.2016.02.001 Li, 2010, The ATM inhibitor KU-55933 suppresses cell proliferation and induces apoptosis by blocking Akt in cancer cells with overactivated Akt, Mol. Cancer Ther., 9, 113, 10.1158/1535-7163.MCT-08-1189 Li, 2012, Nuclear accumulation of HDAC4 in ATM deficiency promotes neurodegeneration in ataxia-telangiectasia, Nat. Med., 18, 783, 10.1038/nm.2709 Lin, 2012, Autophagy and reactive oxygen species modulate cytotoxicity induced by suppression of ATM kinase activity in head and neck cancer cells, Oral Oncol., 48, 1152, 10.1016/j.oraloncology.2012.05.020 Lopes, 2008, Doxorubicin induces biphasic neurotoxicity to rat cortical neurons, Neurotoxicology, 29, 286, 10.1016/j.neuro.2007.12.003 Lopes, 2010, Comparison between proliferative and neuron-like SH-SY5Y cells as an in vitro model for Parkinson disease studies, Brain Res., 1337, 85, 10.1016/j.brainres.2010.03.102 Luchtman, 2010, Why SH-SY5Y cells should be differentiated, Neurotoxicology, 31, 164, 10.1016/j.neuro.2009.10.015 Macleod, 2003, Reduced NMDA-induced apoptosis in neurons lacking ataxia telangiectasia mutated protein, Neuroreport, 14, 215, 10.1097/00001756-200302100-00011 Malagelada, 2010, Rapamycin protects against neuron death in vitro and in vivo models of parkinson’s disease, J. Neurosci., 30, 1166, 10.1523/JNEUROSCI.3944-09.2010 Manchon, 2016, TFEB ameliorates the impairment of the autophagy-lysosome pathway in neurons induced by doxorubicin, Aging (Milano), 8, 3507, 10.18632/aging.101144 Martin, 2016, Enforced DNA repair enzymes rescue neurons from apoptosis induced by target deprivation and axotomy in mouse models of neurodegeneration, Mech. Ageing Dev. Martin, 2008, DNA damage and repair: relevance to mechanisms of neurodegeneration, J. Neuropath. Exp. Neur., 67, 377, 10.1097/NEN.0b013e31816ff780 Matt, 2016, The DNA damage-induced cell death response: a roadmap to kill cancer cells, Cell. Mol. Life Sci., 73, 2829, 10.1007/s00018-016-2130-4 Mattson, 2006, Neuronal life-and-death signaling, apoptosis, and neurodegenerative disorders, Antioxid. Redox Signal., 8, 1997, 10.1089/ars.2006.8.1997 McKinnon, 2012, ATM and the molecular pathogenesis of ataxia telangiectasia, Annu. Rev. Pathol., 7, 303, 10.1146/annurev-pathol-011811-132509 Moore, 2002, Involvement of caspases and calpains in cerebrocortical neuronal cell death is stimulus-dependent, Br. J. Pharmacol., 135, 1069, 10.1038/sj.bjp.0704538 Mullaart, 1990, Increased levels of DNA breaks in cerebral cortex of Alzheimer's disease patients, Neurobiol. Aging, 11, 169, 10.1016/0197-4580(90)90542-8 Neve, 2006, The cell cycle as a therapeutic target for Alzheimer's disease, Pharmacol. Ther., 111, 99, 10.1016/j.pharmthera.2005.09.005 Pan, 2009, Rapamycin protects against rotenone-induced apoptosis through autophagy induction, Neuroscience, 164, 541, 10.1016/j.neuroscience.2009.08.014 Park, 2015, Neuroprotective effects of Liriope platyphylla extract against hydrogen peroxide-induced cytotoxicity in human neuroblastoma SH-SY5Y cells, BMC Complement. Altern. Med., 15, 171, 10.1186/s12906-015-0679-3 Pelegrí, 2008, Cell cycle activation in striatal neurons from Huntington’s disease patients and rats treated with 3-nitropropionic acid, Int. J. Dev. Neurosci., 26, 665, 10.1016/j.ijdevneu.2008.07.016 Perry, 2011, All stressed out without ATM kinase, Sci. Signal., 4, 1, 10.1126/scisignal.2001961 Piotrowski, 2013, Emulsion-core and polyelectrolyte-shell nanocapsules: biocompatibility and neuroprotection against SH-SY5Y cells, J. Nanopart. Res., 15, 2035, 10.1007/s11051-013-2035-1 Pizarro, 2011, Antiapoptotic effects of roscovitine on camptothecin-induced DNA damage in neuroblastoma cells, Apoptosis, 16, 536, 10.1007/s10495-011-0583-3 Presgraves, 2004, Terminally differentiated SH-SY5Y cells provide a model system for studying neuroprotective effects of dopamine agonists, Neurotox. Res., 5, 579, 10.1007/BF03033178 Raimundo, 2016, Mechanisms of communication between mitochondria and lysosomes, Int. J. Biochem. Cell Biol., 79, 345, 10.1016/j.biocel.2016.08.020 Ranganathan, 2003, Alterations in G(1) to S phase cell-cycle regulators during amyotrophic lateral sclerosis, Am. J. Pathol., 162, 823, 10.1016/S0002-9440(10)63879-5 Richter, 2015, SK channel activation modulates mitochondrial respiration and attenuates neuronal HT-22 cell damage induced by H2O2, Neurochem. Int., 81, 63, 10.1016/j.neuint.2014.12.007 Rocourt, 2013, The catalytic subunit of DNA-dependent protein kinase is downstream of ATM and feeds forward oxidative stress in the selenium-induced senescence response, J. Nutr. Biochem., 24, 781, 10.1016/j.jnutbio.2012.04.011 Sahara, 2010, Calpain-mediated Hsp70.1 cleavage in hippocampal CA1 neuronal death, Biochem. Biophys. Res. Commun., 393, 806, 10.1016/j.bbrc.2010.02.087 Shamseddine, 2015, P53-dependent upregulation of neutral sphingomyelinase-2: role in doxorubicin-induced growth arrest, Cell. Death. Dis., 6, e1947, 10.1038/cddis.2015.268 Shao, 2016, Autophagy induction by SIRT6 is involved in oxidative stress-induced neuronal damage, Protein Cell, 7, 281, 10.1007/s13238-016-0257-6 Shiloh, 2013, The ATM protein kinase: regulating the cellular response to genotoxic stress, and more, Nat. Rev. Mol. Cell Bio., 14, 197, 10.1038/nrm3546 Silva, 2014, Repair of oxidative DNA damage, cell-cycle regulation and neuronal death may influence the clinical manifestation of Alzheimer’s disease, PLoS One, 9, e99897, 10.1371/journal.pone.0099897 Smith, 2004, CDKs: taking on a role as mediators of dopaminergic loss in Parkinson’s disease, Trends Mol. Med., 10, 445, 10.1016/j.molmed.2004.07.003 Son, 2009, Apoptosis inducing factor plays a critical role in caspase-independent, pyknotic cell death in hydrogen peroxide-exposed cells, Apoptosis, 14, 796, 10.1007/s10495-009-0353-7 Stracker, 2013, The ATM signaling network in development and disease, Front. Genet., 4, 37, 10.3389/fgene.2013.00037 Tan, 1998, Oxidative stress induces a form of programmed cell death with characteristics of both apoptosis and necrosis in neuronal cells, J. Neurochem., 71, 95, 10.1046/j.1471-4159.1998.71010095.x Trippier, 2013, Target- and mechanism-based therapeutics for neurodegenerative diseases: strength in numbers, J. Med. Chem., 56, 3121, 10.1021/jm3015926 Unnithan, 2014, N-acetyl cysteine prevents synergistic, severe toxicity from two hits of oxidative stress, Neurosci. Lett., 560, 71, 10.1016/j.neulet.2013.12.023 Valerie, 2003, Regulation and mechanisms of mammalian doublestrand break repair, Oncogene, 22, 5792, 10.1038/sj.onc.1206679 Wang, 2014, Effects of DSP4 on the noradrenergic phenotypes and its potential molecular mechanisms in SH-SY5Y cells, Neurotox. Res., 25, 193, 10.1007/s12640-013-9421-4 Wang, 2015, Effects of Antidepressants on DSP4/CPT-Induced DNA Damage Response in Neuroblastoma SH-SY5Y Cells, Neurotox. Res., 28, 154, 10.1007/s12640-015-9534-z Wang, 2015, Neurotoxin-induced DNA damage is persistent in SH-SY5Y cells and LC neurons, Neurotox. Res., 27, 368, 10.1007/s12640-015-9521-4 Ward, 2001, Histone H2AX Is Phosphorylated in an ATR dependent Manner in Response to Replicational Stress, J. Biol. Chem., 276, 47759, 10.1074/jbc.C100569200 Wenker, 2010, Differential antiapoptotic effect of erythropoietin on undifferentiated and retinoic acid-differentiated SH-SY5Y cells, J. Cell. Biochem., 110, 151 Wu, 2016, Nuclear Accumulation of Histone Deacetylase 4 (HDAC4) Exerts Neurotoxicity in Models of Parkinson’s Disease, Molecular Neurobiology, 2016 Oct 26. Yang, 2011, Peroxisome proliferator-activated receptor (is inhibited by histone deacetylase 4 in cortical neurons under oxidative stress, Journal of Neurochemistry, 118, 429, 10.1111/j.1471-4159.2011.07316.x Ye, 2011, Chk1 has an essential role in the survival of differentiated cortical neurons in the absence of DNA damage, Apoptosis, 16, 4449, 10.1007/s10495-011-0579-z Ye, 2014, L-carnitine attenuates H2O2-induced neuron apoptosis via inhibition of endoplasmic reticulum stress, Neurochem. Int., 78, 86, 10.1016/j.neuint.2014.08.009 Yong-Kee, 2011, Development and validation of a screening assay for the evaluation of putative neuroprotective agents in the treatment of Parkinson’s disease, Neurotox. Res., 19, 519, 10.1007/s12640-010-9174-2 Yu, 2015, Ataxia telangiectasia mutated inhibits oxidative stress-induced apoptosis by regulating heme oxygenase-1 expression, Int. J. Biochem. Cell B., 60, 147, 10.1016/j.biocel.2015.01.002 Yuan, 2016, Roles of Caspases in Necrotic Cell Death, Cell, 167, 1693, 10.1016/j.cell.2016.11.047 Zhang, 2014, Hydrogen peroxide/ATR-Chk2 activation mediates p53 protein stabilization and anti-cancer activity of cheliensisin A in human cancer cells, Oncotarget, 5, 841, 10.18632/oncotarget.1780 Zhao, 2006, Preclinical evaluation of a potent novel DNA-dependent protein kinase inhibitor NU7441, Cancer Res., 66, 5354, 10.1158/0008-5472.CAN-05-4275