Neuronal cellular responses to extremely low frequency electromagnetic field exposure: Implications regarding oxidative stress and neurodegeneration

PLoS ONE

Volumn 9, Issue 8, 2014, Pages

  Reale, Marcella ^a   Kamal, Mohammad A ^b   Patruno, Antonia ^a   Costantini, Erica ^a   D'Angelo, Chiara ^a   Pesce, Miko ^a   Greig, Nigel H ^c  

^a UNIVERSITY OF CHIETI   (Italy)

^b KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

^c NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALASE; CYTOCHROME P450; HYDROGEN PEROXIDE; INTERLEUKIN 18 BINDING PROTEIN; NITRIC OXIDE SYNTHASE; OXYGEN; TRANSFORMING GROWTH FACTOR BETA;

ARTICLE; CELL STRESS; CELL STRUCTURE; CELL VIABILITY; CONTROLLED STUDY; DEGENERATIVE DISEASE; ELECTROMAGNETIC FIELD; ENVIRONMENTAL EXPOSURE; ENZYME ACTIVITY; EXTREMELY LOW FREQUENCY ELECTROMAGNETIC FIELD; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMORTALIZED CELL LINE; NEUROBLASTOMA CELL LINE; OXIDATIVE STRESS; PROTEIN EXPRESSION; CYTOLOGY; METABOLISM; NERVE CELL; NEURODEGENERATIVE DISEASES; PATHOLOGY; TUMOR CELL LINE;

CATALASE; CELL LINE, TUMOR; CYTOCHROME P-450 ENZYME SYSTEM; ELECTROMAGNETIC FIELDS; HUMANS; HYDROGEN PEROXIDE; NEURODEGENERATIVE DISEASES; NEURONS; NITRIC OXIDE SYNTHASE; OXIDATIVE STRESS;

EID: 84910004293     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0104973     Document Type: Article

References (70)

1. Bossy-Wetzel E, Schwarzenbacher R, Lipton SA (2004) Molecular pathways to neurodegeneration. Nat Med. 10 Suppl:S2-9. (Pubitemid 38901861)
2. Bertram L, Tanzi RE (2005) The genetic epidemiology of neurodegenerative disease. J Clin Invest. 115(6):1449-57. (Pubitemid 40814649)
3. Moreno-Gonzalez I, Soto C (2012) Natural animal models of neurodegenerative protein misfolding diseases. Curr Pharm Des. 18(8):1148-58.
4. Mullard A (2012) Sting of Alzheimer's failures offset by upcoming prevention trials. Nature Rev. Drug Discov. 11: 657-60.
5. Becker RE, Greig NH, Giacobini E, Schneider LS, Ferrucci L (2014) A new roadmap for drug development for Alzheimer's disease. Nat Rev Drug Discov. 13(2):156.
6. Brown RC, Lockwood AH, Sonawane BR (2005) Neurodegenerative diseases: An overview of environmental risk factors. Environmental Health Perspectives 113: 1250-6. (Pubitemid 41387669)
7. Cannon JR, Greenamyre JT (2011) The Role of environmental exposures in neurodegeneration and neurodegenerative diseases. Toxicological Sciences 124: 225-50.
8. Kraft AD, Harry GJ (2011) Features of microglia and neuroinflammation relevant to environmental exposure and neurotoxicity. Int. J. Environ. Res. Public Health 8: 2980-18.
9. Lahiri DK, Maloney B, Basha MR, Ge YW, Zawia NH (2007) How and when environmental agents and dietary factors affect the course of Alzheimer's disease: the "LEARn" model (latent early-life associated regulation) may explain the triggering of AD. Curr Alzheimer Res. 4(2):219-28. (Pubitemid 46557511)
10. Lahiri DK, Maloney B, Zawia NH (2009) The LEARn model: an epigenetic explanation for idiopathic neurobiological diseases. Mol Psychiatry. 14(11):992-1003
11. Luukkonen J, Liimatainen A, Hoyto A, Juutilainen J, Naarala J (2011) Preexposure to 50 Hz magnetic fields modifies menadione-induced genotoxic effects in human SH-SY5Y neuroblastoma cells. PLoS One 6: e18021.
12. Piacentini R, Ripoli C, Mezzogori D, Azzena GB, Grassi C (2008) Extremely low-frequency electromagnetic fields promote in vitro neurogenesis via upregulation of Ca(v)1-channel activity. J Cell Physiol 215: 129-39. (Pubitemid 351363198)
13. Arendash GW, Mori T, Dorsey M, Gonzalez R, Tajiri N, et al. (2012) Electromagnetic treatment to old Alzheimer's mice reverses beta-amyloid deposition, modifies cerebral blood flow, and provides selected cognitive benefit. PLoS One 7: e35751
14. Sonnier H, Kolomytkin O, Marino A (2003) Action potentials from human neuroblastoma cells in magnetic fields. Neuroscience Letters 337: 163-6. (Pubitemid 36106582)
15. Del Vecchio G, Giuliani A, Fernandez M, Mesirca P, Bersani F, et al. (2009) Effect of Radiofrequency Electromagnetic Field Exposure on In Vitro Models of Neurodegenerative Disease. Bioelectromagnetics 30: 564-72.
16. Tweedie D, Sambamurti K, Greig NH (2007) TNF-alpha inhibition as a treatment strategy for neurodegenerative disorders: new drug candidates and targets. Curr Alzheimer Res. 4(4):378-85. (Pubitemid 47421968)
17. Reale M, Iarlori C, Feliciani C, Gambi D (2008) Peripheral chemokine receptors, their ligands, cytokines and Alzheimer's disease. J Alzheimer's Dis. 14 (2): 147-59. (Pubitemid 352040032)
18. Reale M, De Angelis F, Di Nicola M, Capello E, Di Ioia M, et al. (2012) Relation between Pro-inflammatory Cytokines and Acetylcholine Levels in Relapsing-Remitting Multiple Sclerosis Patients. Int J Mol Sci. 13(10):12656-64.
19. Reale M, Iarlori C, Thomas A, Gambi D, Perfetti B, et al. (2009) Peripheral cytokines profile in Parkinson's Disease. Brain, Behavior Immunity 23(1):55-63.
20. Reale M, Kamal MA, Velluto L, Gambi D, Di Nicola M, et al. (2012) Relationship between Inflammatory Mediators, Ab Levels and APOE Genotype in Alzheimer's Disease. Curr Alzheimer Res. 9(4):447-57.
21. Moreau C, Devos D, Brunaud-Danel V, Defebvre L, Perez T, et al. (2005) Elevated IL-6 and TNF-alpha levels in patients with ALS: inflammation or hypoxia? Neurology 65: 1958-60. (Pubitemid 43970118)
22. Poloni M, Facchetti D, Mai R, Micheli A, Agnoletti L, et al. (2000) Circulating levels of tumour necrosis factor-alpha and its soluble receptors are increased in the blood of patients with amyotrophic lateral sclerosis. Neurosci Lett 287: 211-4. (Pubitemid 30339386)
23. Bonda DJ, Wang X, Perry G, Nunomura A, Tabaton M, et al. (2010) Oxidative stress in Alzheimer disease: A possibility for prevention. Neuropharmacology 59: 290-4.
24. Stefani IC, Wright D, Polizzi KM, Kontoravdi C (2012) The role of ER stress-induced apoptosis in neurodegeneration. Curr Alzheimer Res. 9(3):373-87.
25. Ortiz GG, Macias-Islas MA, Pacheco-Moises FP, Cruz-Ramos JA, Sustersik S, et al. (2009) Oxidative stress is increased in serum from Mexican patients with relapsing-remitting multiple sclerosis. Dis. Markers 26: 35-9.
26. Taskiran D, Sagduyu A, Yüceyar N, Kutay FZ, Pögün S (2000) Increased cerebrospinal fluid and serum nitrite and nitrate levels in amyotrophic lateral sclerosis. Int J Neurosci 101: 65-72 (Pubitemid 30199419)
27. Blandini F (2013) Neural and immune mechanisms in the pathogenesis of Parkinson's disease. J Neuroimmune Pharmacol. 8(1):189-201.
28. Korhonen R, Lahti A, Kankaanranta H, Moilanen E (2005) Nitric oxide production and signaling in inflammation. Curr. Drug Targets Inflamm. Allergy 4: 471-9. (Pubitemid 41052412)
29. Vaz AR, Silva SL, Barateiro A, Fernandes A, Falcão AS, et al. (2011) Proinflammatory cytokines intensify the activation of NO/NOS, JNK1/2 and caspase cascades in immature neurons exposed to elevated levels of unconjugated bilirubin. Exp Neurol. 229(2):381-90.
30. Tesseur I, Zou K, Esposito L, Bard F, Berber E, et al. (2006) Deficiency in neuronal TGF-beta signaling promotes neurodegeneration and Alzheimer's pathology. J Clin Invest. 116: 3060-9. (Pubitemid 44684491)
31. Battista D, Ferrari CC, Gage FH, Pitossi FJ (2006) Neurogenic niche modulation by activated microglia: transforming growth factor beta increases neurogenesis in the adult dentate gyrus. Eur J Neurosci. 23(1): 83-93.
32. Ren RF, Hawver DB, Kim RS, Flanders KC (1997) Transforming growth factor-β protects human hNT cells from degeneration induced by β-amyloid peptide: involvement of the TGF-β type II receptor. Mol Brain Res. 48: 315-22. (Pubitemid 27390068)
33. Dinarello CA, Novick D, Kim S, Kaplanski G (2013) Interleukin-18 and IL-18 Binding Protein. Front Immunol. 4: 289.
34. Sutinen EM, Pirttilä T, Anderson G, Salminen A, Ojala JO (2012) Proinflammatory interleukin-18 increases Alzheimer's disease-associated amyloid-β production in human neuron-like cells. J Neuroinflammation. 9: 199.
35. Reale M, Greig NH, Kamal MA (2009) Peripheral chemo-cytokine profiles in Alzheimer's and Parkinson's diseases. Mini Rev Med Chem. 9(10):1229-41.
36. Bose S, Cho J (2013) Role of chemokine CCL2 and its receptor CCR2 in neurodegenerative diseases. Arch Pharm Res. 36(9):1039-50.
37. Vianale G, Reale M, Amerio P, Stefanachi M, Di Luzio S, et al. (2008) Extremely Low Frequency Electromagnetic Field (ELF-EMF) enhances human keratinocyte cell growth and decreases pro-inflammatory chemokines production. Brit J Dermatol 158(6):1189-96. (Pubitemid 351692868)
38. Pritchard KA Jr, Groszek L, Smalley DM, Sessar WC, Wu M, et al. (1995) Native low-density lipoprotein increases endothelial cell nitric oxide synthase generation of superoxide anion. Circ Res 77: 510-518.
39. Aebi HE (1974) Methods of Enzymatic Analysis. In: Bergmayer HU, editor. Chemie. 2nd Edition, Vol. 2. Weinheim: F.R.G. 673-84.
40. Su B, Wang X, Nunomura A, Moreira PI, Lee HG, et al. (2008) Oxidative stress signaling in Alzheimer's disease. Curr Alzheimer Res. 5(6):525-32.
41. Falone S, Grossi MR, Cinque B, D'Angelo B, Tettamanti E, et al. (2007) Fifty hertz extremely low-frequency electromagnetic field causes changes in redox and differentiative status in neuroblastoma cells. Int J Biochem Cell Biol. 39(11):2093-106. (Pubitemid 47369242)
42. Lacy-Hulbert A, Metcalfe JC, Hesketh R (1998) Biological responses to electromagnetic fields. FASEB J 12(6): 395-420. (Pubitemid 28146520)
43. Feychting M, Ahlbom A, Kheifets L (2005) EMF and health. Ann Rev Public Health 26: 165-189. (Pubitemid 40547380)
44. Consales C, Merla C, Marino C, Benassi B (2012) Electromagnetic fields, oxidative stress, and neurodegeneration. Int J Cell Biol. 2012: 683897.
45. WHO (2007) "Electromagnetic fields and public health. Exposure to extremely low frequency fields," Fact Sheet no. 322, WHO, Geneva, Switzerland. 〈http://www.who.int/peh-emf/publications/facts/fs322/en/〉 viewed May 16, 2014〉
46. WHO (2007) (Environmental Health Criteria 238), Extremely Low Frequency Fields, vol. 35, WHO, Geneva, Switzerland. 〈http://www.who.int/peh-emf/ publications/Complet-DEC-2007.pdf〉 viewed May 16, 2014.
47. International Programme On Chemical Safety (1984) Environmental Health Criteria 35. Extremely Low Frequency (ELF) Fields 〈http://www.inchem.org/ documents/ehc/ehc/ehc35.htm-PartNumber:9〉 viewed May 16, 2014.
48. Jack CR Jr, Knopman DS, Jagust WJ, Petersen RC, Weiner MW, et al. (2013) Tracking pathophysiological processes in Alzheimer's disease: an updated hypothetical model of dynamic biomarkers. Lancet Neurol. 12(2):207-16.
49. Saracchi E, Fermi S, Brighina L (2013) Emerging candidate biomarkers for Parkinson's disease: a review. Aging Dis. 5(1):27-34.
50. Moreno-Gonzalez I, Soto C (2011) Misfolded protein aggregates: mechanisms, structures and potential for disease transmission. Semin Cell Dev Biol. 22(5):482-7.
51. von Bernhardi R, Eugenín J (2012) Alzheimer's disease: redox dysregulation as a common denominator for diverse pathogenic mechanisms. Antioxid Redox Signal. 16(9):974-1031.
52. Bonda DJ, Castellani RJ, Zhu X, Nunomura A, Lee HG, et al. (2011) A novel perspective on tau in Alzheimer's disease. Curr Alzheimer Res. 8(6):639-42.
53. Barja G (1998) Mitochondrial free radical production and aging in mammals and birds. Ann N Y Acad Sci 854: 224-238.
54. Eleuteri AM, Amici M, Bonfili L, Cecarini V, Cuccioloni M, et al. (2009) 50 Hz extremely low frequency electromagnetic fields enhance protein carbonyl groups content in cancer cells: effects on proteasomal systems. J Biomed Biotechnol. 2009: 834239.
55. Simkó M, Mattsson MO (2004) Extremely low frequency electromagnetic fields as effectors of cellular responses in vitro: possible immune cell activation. J Cell Biochem. 93(1):83-92.
56. Reale M, De Lutiis MA, Patruno A, Speranza L, Felaco M, et al. (2006) Modulation of MCP-1 and iNOS by 50-Hz sinusoidal electromagnetic field. Nitric Oxide. 15(1):50-7. (Pubitemid 43963424)
57. Patruno A, Amerio P, Pesce M, Vianale G, Di Luzio S (2010) Extremely low frequency electromagnetic field (elf-emf) modulate iNOS, eNOS and Cox-2 expressions in the human keratinocyte cell line hacat: potential therapeutical effects in wound healing. Brit J Dermatol 162: 258-66.
58. Patruno A, Tabrez S, Amerio P, Pesce M, Vianale G, et al. (2011) Kinetic Study on the Effects of Extremely Low Frequency Electromagnetic Field on Catalase, Cytochrome P450, Inducible Nitric Oxide Synthase in Human HaCaT and THP-1 Cell Lines. CNS Neurol Disord Drug Targets. 10(8):936-44.
59. Sunkari VG, Aranovitch B, Portwood N, Nikoshkov A (2011) Effects of a low-ntensity electromagnetic field on fibroblast migration and proliferation. Electromagnet Biol Med 30(2): 80-5.
60. Antonini RA, Benfante R, Gotti C, Moretti M, Kuster N, et al. (2006) Extremely low-frequency electromagnetic field (ELF-EMF) does not affect the expression of alpha3, alpha5 and alpha7 nicotinic receptor subunit genes in SH-SY5Y neuroblastoma cell line. Toxicol Lett. 164(3):268-77 (Pubitemid 43766793)
61. Martínez-Sámano J, Torres-Durán PV, Juárez-Oropeza MA, Verdugo-Díaz L (2012) Effect of acute extremely low frequency electromagnetic field exposure on the antioxidant status and lipid levels in rat brain. Arch Med Res. 43(3):183-9.
62. Gerard C, Rollins BJ (2001) Chemokines and disease. Nature Immunology 2 (2): 108-115. (Pubitemid 33707927)
63. Azizi G, Khannazer N, Mirshafiey A (2014) The potential role of chemokines in Alzheimer's disease pathogenesis. Am J Alzheimers Dis Other Demen. [Epub ahead of print]
64. Bossù P, Ciaramella A, Salani F, Vanni D, Palladino I, et al. (2010) Interleukin-18, from neuroinflammation to Alzheimer's disease. Curr Pharm Des. 16(38):4213
65. Lisi A, Ledda M, Rosola E, Pozzi D, D'Emilia E, et al. (2006) Extremely low frequency electromagnetic field exposure promotes differentiation of pituitary corticotrope-derived AtT20 D16V cells. Bioelectromagnetics 27: 641-51. (Pubitemid 44863476)
66. Tasset I, Medina FJ, Jimena I, Agüera E, Gascón F, et al. (2010) Neuroprotective effects of extremely low-frequency electromagnetic fields on a Huntington's disease rat model: effects on neurotrophic factors and neuronal density. Neuroscience 209: 54-63.
67. Tasset I, Pérez-Herrera A, Medina FJ, Arias-Carrión O, Drucker-Colín R, et al. (2013) Extremely low-frequency electromagnetic fields activate the antioxidant pathway Nrf2 in a Huntington's disease-like rat model. Brain Stimul. 6: 84-6.
68. Túnez I, Drucker-Colín R, Jimena I, Medina FJ, Muñoz Mdel C, et al. (2006) Transcranial magnetic stimulation attenuates cell loss and oxidative damage in the striatum induced in the 3-nitropropionic model of Huntington's disease. J Neurochem. 97: 619-30.
69. Túnez I, Santamaría A (2009) Model of Huntington's disease induced with 3-nitropropionic acid. Rev Neurol, 48: 430-434.
70. Arias-Carrión O, Verdugo-Díaz L, Feria-Velasco A, Millán-Aldaco D, Gutiérrez AA, et al. (2004) Neurogenesis in the subventricular zone following transcranial magnetic field stimulation and nigrostriatal lesions. J Neurosci Res. 78: 16-28. (Pubitemid 39305150)