Shielding of the geomagnetic field reduces hydrogen peroxide production in human neuroblastoma cell and inhibits the activity of CuZn superoxide dismutase

Abstract

Accumulative evidence has shown the adverse effects of a geomagnetic field shielded condition, so called a hypomagnetic field (HMF), on the metabolic processes and oxidative stress in animals and cells. However, the underlying mechanism remains unclear. In this study, we evaluate the role of HMF on the regulation of cellular reactive oxygen species (ROS) in human neuroblastoma SH-SY5Y cells. We found that HMF exposure led to ROS decrease, and that restoring the decrease by additional H₂O₂ rescued the HMF-enhanced cell proliferation. The measurements on ROS related indexes, including total anti-oxidant capacity, H₂O₂ and superoxide anion levels, and superoxide dismutase (SOD) activity and expression, indicated that the HMF reduced H₂O₂ production and inhibited the activity of CuZn-SOD. Moreover, the HMF accelerated the denaturation of CuZn-SOD as well as enhanced aggregation of CuZn-SOD protein, in vitro. Our findings indicate that CuZn-SOD is able to response to the HMF stress and suggest it a mediator of the HMF effect.

Keywords

hypomagnetic field / reactive oxygen species / hydrogen peroxide / superoxide dismutase / oxidative stress

References

[1] BabychVI (1995) The characteristics of tissue lipid peroxidation in the internal organs and the lipid metabolic indices of the blood plasma in a low geomagnetic field. Fiziol Zh41(5–6):44–49

[2] BabychVI (1996) The characteristics of tissue lipid peroxidation of the internal organs in anaphylaxis under the action of a hypo- or hypermagnetic field. Fiziol Zh42(5–6):66–71

[3] BelyavskayaNA (2004) Biological effects due to weak magnetic field on plants. Adv Space Res34(7):1566–1574. doi:10.1016/j.asr.2004.01.021

[4] BinhiVN, SarimovRM (2009) Zero magnetic field effect observed in human cognitive processes. Electromagn Biol Med28(3):310–315. doi:10.1080/15368370903167246

[5] BinhiVN, SarimovRM (2013) Effect of the hypomagnetic field on the size of the eye pupil. Phys Biol Phys. http://arxiv.org/abs/1302.2741

[6] BlissVL, HeppnerFH (1976) Circadian activity rhythm influenced by near zero magnetic field. Nature261(5559):411–412

[7] CalabroE, CondelloS, CurroM, FerlazzoN, CaccamoD, MagazuS (2013) Effects of low intensity static magnetic field on FTIR spectra and ROS production in SH-SY5Y neuronal-like cells. Bioelectromagnetics34(8):618–629. doi:10.1002/bem.21815

[8] ChenL, WeiY, WangX, HeR (2010) Ribosylation rapidly induces alpha-synuclein to form highly cytotoxic molten globules of advanced glycation end products. PLoS ONE5(2):e9052. doi:10.1371/journal.pone.0009052

[9] CiorbaD, MorariuVV (2001) Life in zero magnetic field. III. Activity of aspartate aminotransferasse and alanine aminotransferase during in vitro aging of human blood. Electromagn Biol Med20 (3):313–321

[10] ConleyCC (1970) A review of the biological effects of very low magnetic fields. NASA TN D-5902

[11] DrogeW (2002) Free radicals in the physiological control of cell function. Physiol Rev82(1):47–95. doi:10.1152/physrev.00018.2001

[12] EstacioSG, LealSS, CristovaoJS, FaiscaPF, GomesCM (2015) Calcium binding to gatekeeper residues flanking aggregationprone segments underlies non-fibrillar amyloid traits in superoxide dismutase 1 (SOD1). Biochim Biophys Acta1854(2):118–126. doi:10.1016/j.bbapap.2014.11.005

[13] FesenkoEE, MezhevikinaLM, OsipenkoMA, GordonRY, KhutzianSS (2010) Effect of the “zero” magnetic field on early embryogenesis in mice. Electromagn Biol Med29(1–2):1–8. doi:10.3109/15368371003627290

[14] FormanHJ (2016) Redox signaling: an evolution from free radicals to aging. Free Radic Biol Med97:398–407. doi:10.1016/j.freeradbiomed.2016.07.003

[15] FuJP, MoWC, LiuY, HeRQ (2016a) Decline of cell viability and mitochondrial activity in mouse skeletal muscle cell in a hypomagnetic field. Bioelectromagnetics37(4):212–222. doi:10.1002/bem.21968

[16] FuJP, MoWC, LiuY, BartlettPF, HeRQ (2016b) Elimination of the geomagnetic field stimulates the proliferation of mouse neural progenitor and stem cells. Protein Cell7(9):624–637. doi:10.1007/s13238-016-0300-7

[17] GurfinkelIuI, VasinAL, MatveevaTA, SasonkoML (2014) Evaluation of the hypomagnetic environment effects on capillary blood circulation, blood pressure and heart rate. Aviakosm Ekolog Med48(2):24–30

[18] HeC, HartPC, GermainD, BoniniMG (2016) SOD2 and the Mitochondrial UPR: Partners Regulating Cellular Phenotypic Transitions. Trends Biochem Sci41(7):568–577. doi:10.1016/j.tibs.2016.04.004

[19] JelenkovicA, JanacB, PesicV, JovanovicDM, VasiljevicI, ProlicZ (2006) Effects of extremely low-frequency magnetic field in the brain of rats. Brain Res Bull68(5):355–360. doi:10.1016/j.brainresbull.2005.09.011

[20] KhareSD, CaplowM, DokholyanNV (2004) The rate and equilibrium constants for a multistep reaction sequence for the aggregation of superoxide dismutase in amyotrophic lateral sclerosis. Proc Natl Acad Sci USA101(42):15094–15099. doi:10.1073/pnas.0406650101

[21] KopanevVI, EfimenkoGD, ShakulaAV (1979) Biological effect of a hypogeomagnetic environment on an organism. Biol Bull Acad Sci USSR. 6(3):289–298

[22] LiS, CaseAJ, YangRF, SchultzHD, ZimmermanMC (2013) Overexpressed copper/zinc superoxide dismutase localizes to mitochondria in neurons inhibiting the angiotensin II-mediated increase in mitochondrial superoxide. Redox Biol2:8–14. doi:10.1016/j.redox.2013.11.002

[23] LiuJ, ZhaoW, FanRL, WangWH, TianZQ, PengJ (2009) Investigation of the nonspecific interaction between quantum dots and immunoglobulin G using Rayleigh light scattering. Talanta78 (3):700–704. doi:10.1016/j.talanta.2008.12.033

[24] MartinoCF, CastelloPR (2011) Modulation of hydrogen peroxide production in cellular systems by low level magnetic fields. PLoS ONE6(8):e22753. doi:10.1371/journal.pone.0022753

[25] MoWC, LiuY, HeRQ (2012a) A biological perspective of the hypomagnetic field: from definition towards mechanism. Prog Biochem Biophys39(9):835–842. doi:10.3724/Sp.J.1206.2011.00597

[26] MoWC, LiuY, CooperHM, HeRQ (2012b) Altered development of Xenopus embryos in a hypogeomagnetic field. Bioelectromagnetics33(3):238–246. doi:10.1002/bem.20699

[27] MoWC, ZhangZJ, LiuY, BartlettPF, HeRQ (2013) Magnetic shielding accelerates the proliferation of human neuroblastoma cell by promoting G1-phase progression. PLoS ONE8(1): e54775. doi:10.1371/journal.pone.0054775

[28] MoW, LiuY, HeR (2014a) Hypomagnetic field, an ignorable environmental factor in space? Sci China Life Sci57(7):726–728. doi:10.1007/s11427-014-4662-x

[29] MoW, LiuY, BartlettPF, HeR (2014b) Transcriptome profile of human neuroblastoma cells in the hypomagnetic field. Sci China Life Sci57(4):448–461. doi:10.1007/s11427-014-4644-z

[30] MoWC, FuJP, DingHM, LiuY, HuaQ, HeRQ (2015) Hypomagnetic field alters circadian rhythm and increases algesia in adult male mice. Prog Biochem Biophys. 42(7):639–646

[31] MoWC, ZhangZJ, WangDL, LiuY, BartlettPF, HeRQ (2016) Shielding of the geomagnetic field alters actin assembly and inhibits cell motility in human neuroblastoma cells. Sci Rep6:22624. doi:10.1038/srep22624

[32] NepomnyashchikhLM, LushnikovaEL, KlinnikovaMG, MolodykhOP, AshcheulovaNV (1997) Effect of hypogeomagnetic field on tissue and intracellular reorganization of mouse myocardium. Bull Exp Biol Med124(10):1021–1024. doi:10.1007/Bf02446851

[33] OsipenkoMA, MezhevikinaLM, KrastsIV, IashinVA, NovikovVV, FesenkoEE (2008) Influence of “zero” magnetic field on the growth of embryonic cells and primary embryos of mouse in vitro. Biofizika53(4):705–712

[34] PratoFS, RobertsonJA, DesjardinsD, HenselJ, ThomasAW (2005) Daily repeated magnetic field shielding induces analgesia in CD-1 mice. Bioelectromagnetics26(2):109–117. doi:10.1002/bem.20056

[35] RheeSG, ChangTS, BaeYS, LeeSR, KangSW (2003) Cellular regulation by hydrogen peroxide. J Am Soc Nephrol14:S211–S215. doi:10.1097/01.Asn.0000077404.45564.7e

[36] ShustIV, KostinikIM (1975) Effect of a strong constant magnetic field and a hypomagnetic surrounding medium on histochemical indices of albino rat liver. Kosm Biol Aviakosm Med9(6):19–25

[37] ShustIV, KostinikIM (1976) Reaction of the animal adrenal cortex to the action of a strong, constant magnetic field and to a hypomagnetic environment. Probl Endokrinol (Mosk). 22(2):86–92

[38] SongX, LiuBC, LuXY, YangLL, ZhaiYJ, EatonAF (2014) Lovastatin inhibits human B lymphoma cell proliferation by reducing intracellular ROS and TRPC6 expression. Biochim Biophys Acta1843(5):894–901. doi:10.1016/j.bbamcr.2014.02.002

[39] TauletN, Delorme-WalkerVD, DerMardirossianC (2012) Reactive oxygen species regulate protrusion efficiency by controlling actin dynamics. PLoS ONE7(8):e41342. doi:10.1371/journal.pone.0041342

[40] TrachoothamD, LuW, OgasawaraMA, NilsaRD, HuangP (2008) Redox regulation of cell survival. Antioxid Redox Signal10 (8):1343–1374. doi:10.1089/ars.2007.1957

[41] WanGJ, JiangSL, ZhaoZC, XuJJ, TaoXR, SwordGA (2014) Bio-effects of near-zero magnetic fields on the growth, development and reproduction of small brown planthopper, Laodelphax striatellusand brown planthopper, Nilaparvata lugens. J Insect Physiol68:7–15. doi:10.1016/j.jinsphys.2014.06.016

[42] XiaoY, WangQ, XuML, JiangJC, LiB (2009) Chicks incubated in hypomagnetic field need more exogenous noradrenaline for memory consolidation. Adv Space Res44(2):226–232. doi:10.1016/j.asr.2009.04.013

[43] ZamoshchinaTA, KrivovaNA, KhodanovichM, TrukhanovKA, TukhvatulinRT, ZaevaOB (2012) Influence of simulated hypomagnetic environment in a far space flight on the rhythmic structure of rat’s behavior. Aviakosm Ekolog Med46(1):17–23

[44] ZellerKS, RiazA, SarveH, LiJ, TengholmA, JohanssonS (2013) The role of mechanical force and ROS in integrin-dependent signals. PLoS ONE8(5):e64897. doi:10.1371/journal.pone.0064897

[45] ZhangB, LuH, XiW, ZhouX, XuS, ZhangK (2004) Exposure to hypomagnetic field space for multiple generations causes amnesia in Drosophila melanogaster. Neurosci Lett371(2–3):190–195. doi:10.1016/j.neulet.2004.08.072

[46] ZhangY, BermanGP, KaisS (2014) Sensitivity and entanglement in the avian chemical compass. Phys Rev E90(4):042707. doi:10.1103/PhysRevE.90.042707

[47] ZhaoXB, QianH, CourtneyJM (1998) Artificial cell containing superoxide dismutase—selection of folding aids for stabilisation of SOD. Artif Cells Blood Substit Immobil Biotechnol26(4):341–358

[48] ZhuD, ScandaliosJG (1995) The maize mitochondrial MnSODS encoded by multiple genes are localized in the mitochondrial matrix of transformed yeast cells. Free Radic Biol Med18 (2):179–183

RIGHTS & PERMISSIONS

2017 The Author(s) 2017. This article is an open access publication