No evidence of DNA damage by co-exposure to extremely low frequency magnetic fields and aluminum on neuroblastoma cell lines

Milena Villarini1, Angela Gambelunghe2, Daniela Giustarini3, Maria Vittoria Ambrosini1, Cristina Fatigoni1, Ranieri Rossi3, Luca Dominici1, Sara Levorato1, Giacomo Muzi2, Danilo Piobbico4, Giuseppina Mariucci1
1Department of Pharmaceutical Sciences, University of Perugia, 06122 Perugia, Italy
2Department of Medicine, University of Perugia, 06132 Perugia, Italy
3Department of Life Sciences, Laboratory of Pharmacology and Toxicology, University of Siena, 53100 Siena, Italy
4Department of Experimental Medicine, University of Perugia, 06132 Perugia, Italy

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Wertheimer, 1979, Electrical wiring configurations and childhood cancer, Am. J. Epidemiol., 109, 273, 10.1093/oxfordjournals.aje.a112681 WHO, 2007 Juutilainen, 1990, Incidence of leukaemia and brain tumours in Finnish workers exposed to ELF magnetic fields, Int. Arch. Occup. Environ. Health, 62, 289, 10.1007/BF00640835 Hardell, 1995, Exposure to extremely low frequency electromagnetic fields and the risk of malignant diseases—an evaluation of epidemiological and experimental findings, Eur. J. Cancer Prev., 4, 3, 10.1097/00008469-199509001-00001 Feychting, 2003, Occupational magnetic field exposure and neurodegenerative disease, Epidemiology, 14, 413, 10.1097/01.EDE.0000071409.23291.7b Roosli, 2007, Leukaemia, brain tumours and exposure to extremely low frequency magnetic fields: cohort study of Swiss railway employees, Occup. Environ. Med., 64, 553, 10.1136/oem.2006.030270 Davanipour, 2009, Long-term exposure to magnetic fields and the risks of Alzheimer's disease and breast cancer: further biological research, Pathophysiology, 16, 149, 10.1016/j.pathophys.2009.01.005 Marcilio, 2011, Adult mortality from leukemia, brain cancer, amyotrophic lateral sclerosis and magnetic fields from power lines: a case-control study in Brazil, Revista brasileira de epidemiologia=Braz. J. Epidemiol., 14, 580, 10.1590/S1415-790X2011000400005 Zhao, 2014, Magnetic fields exposure and childhood leukemia risk: a meta-analysis based on 11,699 cases and 13,194 controls, Leuk. Res., 38, 269, 10.1016/j.leukres.2013.12.008 Feychting, 2006, Electromagnetic fields and female breast cancer, Cancer Causes Control, 17, 553, 10.1007/s10552-005-9008-3 Forssen, 2006, Occupational magnetic field exposure and the risk of acoustic neuroma, Am. J. Ind. Med., 49, 112, 10.1002/ajim.20251 Hug, 2010, Parental occupational exposure to extremely low frequency magnetic fields and childhood cancer: a German case-control study, Am. J. Epidemiol., 171, 27, 10.1093/aje/kwp339 Vijayalaxmi, 2009, Genetic damage in mammalian somatic cells exposed to extremely low frequency electro-magnetic fields: a meta-analysis of data from 87 publications (1990–2007), Int. J. Radiat. Biol., 85, 196, 10.1080/09553000902748575 Ruiz-Gomez, 2009, Electromagnetic fields and the induction of DNA strand breaks, Electromagn. Biol. Med., 28, 201, 10.1080/15368370802608696 Focke, 2010, DNA fragmentation in human fibroblasts under extremely low frequency electromagnetic field exposure, Mutat. Res., 683, 74, 10.1016/j.mrfmmm.2009.10.012 Mariucci, 2010, Brain DNA damage and 70-kDa heat shock protein expression in CD1 mice exposed to extremely low frequency magnetic fields, Int. J. Radiat. Biol., 86, 701, 10.3109/09553001003789588 Kim, 2012, Time-varying magnetic fields of 60Hz at 7mT induce DNA double-strand breaks and activate DNA damage checkpoints without apoptosis, Bioelectromagnetics, 33, 383, 10.1002/bem.21697 Villarini, 2013, Brain hsp70 expression and DNA damage in mice exposed to extremely low frequency magnetic fields: a dose-response study, Int. J. Radiat. Biol., 89, 562, 10.3109/09553002.2013.782449 Korr, 2014, No evidence of persisting unrepaired nuclear DNA single strand breaks in distinct types of cells in the brain, kidney, and liver of adult mice after continuous eight-week 50Hz magnetic field exposure with flux density of 0.1mT or 1.0mT, PLoS One, 9, e109774, 10.1371/journal.pone.0109774 Luukkonen, 2014, Induction of genomic instability, oxidative processes, and mitochondrial activity by 50Hz magnetic fields in human SH-SY5Y neuroblastoma cells, Mutat. Res., 760, 33, 10.1016/j.mrfmmm.2013.12.002 Jin, 2014, Absence of DNA damage after 60-Hz electromagnetic field exposure combined with ionizing radiation hydrogen peroxide, or c-Myc overexpression, Radiat. Environ. Biophys., 53, 93, 10.1007/s00411-013-0506-5 Kesari, 2015, Genomic instability induced by 50Hz magnetic fields is a dynamically evolving process not blocked by antioxidant treatment, Mutation research, Genet. Toxicol. Environ. Mutagen., 794, 46, 10.1016/j.mrgentox.2015.10.004 Maes, 2016, Genetic damage in humans exposed to extremely low-frequency electromagnetic fields, Arch. Toxicol., 90, 2337, 10.1007/s00204-016-1769-9 Brocklehurst, 1996, Free radical mechanism for the effects of environmental electromagnetic fields on biological systems, Int. J. Radiat. Biol., 69, 3, 10.1080/095530096146147 Eveson, 2000, The effects of weak magnetic fields on radical recombination reactions in micelles, Int. J. Radiat. Biol., 76, 1509, 10.1080/09553000050176270 Barnes, 2015, The effects of weak magnetic fields on radical pairs, Bioelectromagnetics, 36, 45, 10.1002/bem.21883 Simko, 2007, Cell type specific redox status is responsible for diverse electromagnetic field effects, Curr. Med. Chem., 14, 1141, 10.2174/092986707780362835 Maes, 2012, Can cytogenetics explain the possible association between exposure to extreme low-frequency magnetic fields and Alzheimer's disease?, J. Appl. Toxicol., 32, 81, 10.1002/jat.1724 Pall, 2013, Electromagnetic fields act via activation of voltage-gated calcium channels to produce beneficial or adverse effects, J. Cell. Mol. Med., 17, 958, 10.1111/jcmm.12088 Loscher, 2001, Do cocarcinogenic effects of ELF electromagnetic fields require repeated long-term interaction with carcinogens? Characteristics of positive studies using the DMBA breast cancer model in rats, Bioelectromagnetics, 22, 603, 10.1002/bem.90 Verheyen, 2003, Effect of coexposure to 50Hz magnetic fields and an aneugen on human lymphocytes, determined by the cytokinesis block micronucleus assay, Bioelectromagnetics, 24, 160, 10.1002/bem.10100 Moretti, 2005, Effects of co-exposure to extremely low frequency (ELF) magnetic fields and benzene or benzene metabolites determined in vitro by the alkaline comet assay, Toxicol. Lett., 157, 119, 10.1016/j.toxlet.2005.01.009 Villarini, 2006, Effects of co-exposure to extremely low frequency (50Hz) magnetic fields and xenobiotics determined in vitro by the alkaline comet assay, Sci. Total Environ., 361, 208, 10.1016/j.scitotenv.2005.05.006 Luukkonen, 2011, Pre-exposure to 50Hz magnetic fields modifies menadione-induced genotoxic effects in human SH-SY5Y neuroblastoma cells, PLoS One, 6, e18021, 10.1371/journal.pone.0018021 IARC, 2002, Non-Ionizing Radiation Static and extremely low frequency (ELF) electric and magnetic fields, vol. 80, 1 Tomljenovic, 2011, Aluminum and Alzheimer's disease: after a century of controversy, is there a plausible link?, J. Alzheimer Dis., 23, 567, 10.3233/JAD-2010-101494 Zhang, 2013, Extremely low-frequency magnetic exposure appears to have no effect on pathogenesis of Alzheimer's disease in aluminum-overloaded rat, PLoS One, 8, e71087, 10.1371/journal.pone.0071087 Deng, 2013, Effects of aluminum and extremely low frequency electromagnetic radiation on oxidative stress and memory in brain of mice, Biol. Trace Elem. Res., 156, 243, 10.1007/s12011-013-9847-9 EFSA, Safety of aluminium from dietary intake, The EFSA Journal, European Food Safety Authority 2008, pp. 1–34. Roskams, 1990, Aluminum access to the brain: a role for transferrin and its receptor, Proc. Natl. Acad. Sci. U. S. A., 87, 9024, 10.1073/pnas.87.22.9024 Yokel, 2006, Blood-brain barrier flux of aluminum, manganese, iron and other metals suspected to contribute to metal-induced neurodegeneration, J. Alzheimer Dis., 10, 223, 10.3233/JAD-2006-102-309 Kumar, 2008, Impairment of mitochondrial energy metabolism in different regions of rat brain following chronic exposure to aluminium, Brain Res., 1232, 94, 10.1016/j.brainres.2008.07.028 Bondy, 2014, Prolonged exposure to low levels of aluminum leads to changes associated with brain aging and neurodegeneration, Toxicology, 315, 1, 10.1016/j.tox.2013.10.008 Kumar, 2014, Oxidative stress and mitochondrial dysfunction in aluminium neurotoxicity and its amelioration: a review, Neurotoxicology, 41, 154, 10.1016/j.neuro.2014.02.004 Willhite, 2014, Systematic review of potential health risks posed by pharmaceutical, occupational and consumer exposures to metallic and nanoscale aluminum, aluminum oxides, aluminum hydroxide and its soluble salts, Crit. Rev. Toxicol., 44, 1, 10.3109/10408444.2014.934439 Exley, 2004, The pro-oxidant activity of aluminum, Free Rad. Biol. Med., 36, 380, 10.1016/j.freeradbiomed.2003.11.017 Yousef, 2004, Aluminium-induced changes in hemato-biochemical parameters, lipid peroxidation and enzyme activities of male rabbits: protective role of ascorbic acid, Toxicology, 199, 47, 10.1016/j.tox.2004.02.014 Campbell, 2004, Chronic exposure to aluminum in drinking water increases inflammatory parameters selectively in the brain, J. Neurosci. Res., 75, 565, 10.1002/jnr.10877 Lukiw, 2005, Nanomolar aluminum induces pro-inflammatory and pro-apoptotic gene expression in human brain cells in primary culture, J. Inorg. Biochem., 99, 1895, 10.1016/j.jinorgbio.2005.04.021 Lankoff, 2006, A comet assay study reveals that aluminium induces DNA damage and inhibits the repair of radiation-induced lesions in human peripheral blood lymphocytes, Toxicol. Lett., 161, 27, 10.1016/j.toxlet.2005.07.012 Lima, 2007, Genotoxic effects of aluminum chloride in cultured human lymphocytes treated in different phases of cell cycle, Food Chem. Toxicol., 45, 1154, 10.1016/j.fct.2006.12.022 Veas-Perez de Tudela, 2010, Human neuroblastoma cells with MYCN amplification are selectively resistant to oxidative stress by transcriptionally up-regulating glutamate cysteine ligase, J. Neurochem., 113, 819, 10.1111/j.1471-4159.2010.06648.x Ivancsits, 2002, Induction of DNA strand breaks by intermittent exposure to extremely-low-frequency electromagnetic fields in human diploid fibroblasts, Mutat. Res., 519, 1, 10.1016/S1383-5718(02)00109-2 Tice, 2000, Single cell gel/comet assay: guidelines for in vitro and in vivo genetic toxicology testing, Environ. Mol. Mutagen., 35, 206, 10.1002/(SICI)1098-2280(2000)35:3<206::AID-EM8>3.0.CO;2-J Giustarini, 2011, Detection of glutathione in whole blood after stabilization with N-ethylmaleimide, Anal. Biochem., 415, 81, 10.1016/j.ab.2011.04.013 Giustarini, 2015, Glutathione, glutathione disulfide, and S-glutathionylated proteins in cell cultures, Free Rad. Biol. Med., 89, 972, 10.1016/j.freeradbiomed.2015.10.410 Sasaki, 2007, What is better experimental design for in vitro comet assay to detect chemical genotoxicity?, Altern. Anim. Test. Exp., 14, 499 Sies, 1999, Glutathione and its role in cellular functions, Free Rad. Biol. Med., 27, 916, 10.1016/S0891-5849(99)00177-X Biedler, 1978, Multiple neurotransmitter synthesis by human neuroblastoma cell lines and clones, Cancer Res., 38, 3751 ICNIRP, 2010, ICNIRP guidelines for limiting exposure to time varying electric and magnetic fields (1Hz–100kHz), Health Phys. Int. Comm. Non Ioniz. Radiat. Prot., 818 Bondy, 2010, The neurotoxicity of environmental aluminum is still an issue, Neurotoxicology, 31, 575, 10.1016/j.neuro.2010.05.009 Keshelava, 2001, Loss of p53 function confers high-level multidrug resistance in neuroblastoma cell lines, Cancer Res., 61, 6185 Davidoff, 1992, Expression of p53 in human neuroblastoma- and neuroepithelioma-derived cell lines, Oncogene, 7, 127 Zmyslony, 2000, DNA damage in rat lymphocytes treated in vitro with iron cations and exposed to 7mT magnetic fields (static or 50Hz), Mutat. Res., 453, 89, 10.1016/S0027-5107(00)00094-4 Toimela, 2004, Mitochondrial viability and apoptosis induced by aluminum, mercuric mercury and methylmercury in cell lines of neural origin, Arch. Toxicol., 78, 565, 10.1007/s00204-004-0575-y Di Loreto, 2009, Fifty hertz extremely low-frequency magnetic field exposure elicits redox and trophic response in rat-cortical neurons, J. Cell. Physiol., 219, 334, 10.1002/jcp.21674 Falone, 2007, Fifty hertz extremely low-frequency electromagnetic field causes changes in redox and differentiative status in neuroblastoma cells, Int. J. Biochem. Cell Biol., 39, 2093, 10.1016/j.biocel.2007.06.001 Campbell, 1999, Aluminum-induced oxidative events in cell lines: glioma are more responsive than neuroblastoma, Free Rad. Biol. Med., 26, 1166, 10.1016/S0891-5849(98)00308-6 Turkez, 2011, The efficiacy of bismuth subnitrate against genotoxicity and oxidative stress induced by aluminum sulphate, Toxicol. Ind. Health, 27, 133, 10.1177/0748233710381894 Nagasawa, 2006, Transport and toxic mechanism for aluminum citrate in human neuroblastoma SH-SY5Y cells, Life Sci., 79, 89, 10.1016/j.lfs.2005.12.048 Bondy, 1996, The promotion of iron-induced generation of reactive oxygen species in nerve tissue by aluminum, Mol. Chem. Neuropathol., 27, 185, 10.1007/BF02815093 Khalil, 2011, Heat shock proteins in oncology: diagnostic biomarkers or therapeutic targets?, Biochim. Biophys. Acta, 1816, 89 Wang, 2011, Targeting heat shock proteins 70/90 and proteasome for cancer therapy, Curr. Med. Chem., 18, 4250, 10.2174/092986711797189574 Sargazi, 2006, Aluminium-induced injury to kidney proximal tubular cells: effects on markers of oxidative damage, J. Trace Elements Med. Biol.: Organ Soc. Miner. Trace Elements, 19, 267, 10.1016/j.jtemb.2005.11.002 Stacchiotti, 2006, Stress proteins expression in rat kidney and liver chronically exposed to aluminium sulphate, Histol. Histopathol., 21, 131 Sood, 2012, Stress proteins and glial cell functions during chronic aluminium exposures: protective role of curcumin, Neurochem. Res., 37, 639, 10.1007/s11064-011-0655-3