Can cytogenetics explain the possible association between exposure to extreme low-frequency magnetic fields and Alzheimer's disease?

Journal of Applied Toxicology

Volumn 32, Issue 2, 2012, Pages 81-87

  Maes, Annemarie ^a   Verschaeve, Luc ^a  

^a SCIENTIFIC INSTITUTE OF PUBLIC HEALTH   (Belgium)

Author keywords

Alzheimers disease; Aneuploidy; Electromagnetic fields; ELF; Genomic instability

Indexed keywords

AMYLOID; MELATONIN;

ALZHEIMER DISEASE; ANEUPLOIDY; CHROMOSOMAL INSTABILITY; CHROMOSOME 10; CHROMOSOME 17; CHROMOSOME 9; CYTOGENETICS; ELECTROMAGNETIC FIELD; GENE AMPLIFICATION; GENE MUTATION; GENETIC ASSOCIATION; GENOMIC INSTABILITY; GENOTOXICITY; HORMONE SYNTHESIS; HUMAN; NEUROFIBRILLARY TANGLE; NEUROPATHOLOGY; NONHUMAN; OCCUPATIONAL EXPOSURE; OXIDATIVE STRESS; PRIORITY JOURNAL; REVIEW; RISK ASSESSMENT; RISK FACTOR; SENILE PLAQUE; TELOMERE; TRISOMY; TRISOMY 21; TUMOR;

ALZHEIMER DISEASE; ANEUPLOIDY; CYTOGENETICS; DNA DAMAGE; ELECTROMAGNETIC FIELDS; GENOMIC INSTABILITY; HUMANS; RISK FACTORS;

EID: 84855208271     PISSN: 0260437X     EISSN: 10991263     Source Type: Journal    
DOI: 10.1002/jat.1724     Document Type: Review

References (91)

1. Akdag MZ, Dasdag S, Ulukaya E, Uzunlar AK, Kurt MA, Taşkin A. 2010. Effects of extremely low-frequency magnetic field on caspase activities and oxidative stress values in rat brain. Biol. Trace Elem. Res. 138: 238-249.
2. Bailey KJ, Maslov AY, Pruitt SC. 2004. Accumulation of mutations and somatic selection in aging neural stem/progenitor cells. Aging Cell 3: 391-397.
3. Bergqvist U, Brix J, de Gruijl F, de Seze R, Hietanen M, Jeffereys JGR, Lagroye I, Lotz GW, Owen RD, Repacholi MH, Saunders R, Tenforde TS, Verschaeve L, Veyret B. 2003. Review of experimental investigations of EMF biological effects (0-100kHz) - ICNIRP Standing committee II. In Matthes R, McKinley A, Bernhardt J, Vecchia P, Veyret B, eds, Exposure to Static and Low Frequency Electromagnetic Fields, Biological Effects and Health Consequences. ICNIRP: München, Germany; 121-398.
4. Bertram L, Blacker D, Mullin K, Keeney D, Jones J, Basu S, Yhu S, McInnis MG, Go RC, Vekrellis K, Selkoe DJ, Saunders AJ, Tanzi RE. 2000. Evidence for genetic linkage of Alzheimer's disease to chromosome 10q. Science 290: 2302-2303.
5. Bertram L, Hiltunen M, Parkinson M, Ingelsson M, Lange C, Ramasamy K, Mullin K, Menon R, Sampson AJ, Hsiao MY, Elliott KJ, Velicelebi G, Moscarillo T, Hyman BT, Wagner SL, Becker KD, Blacker D, Tanzi RE. 2005. Family-based association between Alzheimer's disease and variants in UBQLN1. New Engl. J. Med. 352: 884-894.
6. Blacker D, Wilcox MA, Laird NM, Rodes L, Horvath SM, Go RC, Perry R, Watson B Jr, Bassett SS, McInnis MG, Albert MS, Hyman BT, Tanzi RE. 1998. Alpha-2 macroglobulin is genetically associated with Alzheimer disease. Nat. Genet. 19: 357-360.
7. Bullido MJ, Aldudo J, Frank A, Coria F, Avila J, Valdivieso F. 2000. A polymorphism in the tau gene associated with risk for Alzheimer's disease. Neurosci. Lett. 278: 49-52.
8. Cash AD, Aliev G, Siedlak SL, Nunomura A, Fujioka H, Zhu X, Raina AK, Vinters HV, Tabaton M, Johnson AB, Paula-Barbosa M, Avila J, Jones PK, Castellani RJ, Smith MA, Perry G. 2003. Microtubule reduction in Alzheimer's disease and aging is independent of tau filament formation. Am. J. Pathol. 162: 1623-1627.
9. Crawford FC, Freeman MJ, Schinka JA, Morris MD, Abdullah LI, Richards D, Sevush S, Duara R, Mullan MJ. 2001. Association between Alzheimer's disease and a functional polymorphism in the Myeloperoxidase gene. Exp. Neurol. 167: 456-459.
10. Das S, Potter H. 1995. Expression of the Alzheimer amyloid-promoting factor antichymotrypsin is induced in human astrocytes by IL-1. Neuron 14: 447-456.
11. Davanipour Z, Sobel E. 2009. Long-term exposure to magnetic fields and the risks of Alzheimer's disease and breast cancer: further biological research. Pathophysiology 16: 149-156.
12. Del GE, Facchinetti F, Nofrate V, Boccaccio P, Minelli T, Dam M, Leon A, Moschini G. 2007. Fifty Hertz electromagnetic field exposure stimulates secretion of beta-amyloid peptide in cultured human neuroglioma. Neurosci. Lett. 418: 9-12.
13. Ding GR, Yaguchi H, Yoshida M, Miyakoshi J. 2000. Increase in x-ray-induced mutations by exposure to magnetic field (60Hz, 5 mT) in nf-kappa b-inhibited cells. Biochem. Biophys. Res. Commun. 276: 238-243.
14. Dodel RC, Du Y, Bales KR, Gao F, Eastwood B, Glazier B, Zimmer R, Cordell B, Hake A, Evans R, Gallagher-Thompson D, Thompson LW, Tinklenberg JR, Pfefferbaum A, Sullivan EV, Yesavage J, Alstiel L, Gasser T, Farlow MR, Murphy GM Jr, Paul SM. 2000. Alpha2 macroglobulin and the risk of Alzheimer's disease. Neurology 54: 438-442.
15. El-Helaly M, Abu-Hashem E. 2010. Oxidative stress, melatonin level, and sleep insufficiency among electronic equipment repairers. Indian J. Occup. Environ. Med. 14: 66-70.
16. Emre M, Cetiner S, Zencir S, Unlukurt I, Kahraman I, Topcu Z. 2011. Oxidative stress and apoptosis in relation to exposure to magnetic fields. Cell Biochem. Biophys. 59: 71-77.
17. Ertekin-Taner N, Graff-Radford N, Younkin LH, Eckman C, Baker M, Adamson J, Ronald J, Blangero J, Hutton M, Younkin SG. 2000. Linkage of plasma Abeta42 to a quantitative locus on chromosome 10 in late-onset Alzheimer's disease pedigrees. Science 290: 2303-2304.
18. Gabbita SP, Lovell MA, Markesbery WR. 1998. Increased nuclear DNA oxidation in the brain in Alzheimer's disease. J. Neurochem. 71: 2034-2040.
19. Garcia AM, Sisternas A, Hoyos SP. 2008. Occupational exposure to extremely low frequency electric and magnetic fields and Alzheimer disease: a meta-analysis. Int. J. Epidemiol. 37: 329-340.
20. Geller LN, Potter H. 1999. Chromosome missegregation and trisomy 21 mosaicism in Alzheimer's disease. Neurobiol. Dis. 6: 167-179.
21. Goraca A, Ciejka E, Piechota A. 2010. Effects of extremely low frequency magnetic field on the parameters of oxidative stress in heart. J. Physiol. Pharmacol. 61: 333-338.
22. Haimov I, Laudon M, Zisapel N, Souroujon M, Nof D, Shlitner A, Herer P, Tzischinsky O, Lavie P. 1994. Sleep disorders and melatonin rhytms in elderly people. Br. Med. J. 309: 167.
23. Hardy J. 2001. The genetic causes of neurodegenerative diseases. J. Alzheimer's Dis. 3: 109-116.
24. Hintenlang DE. 1993. Synergistic effects of ionising radiation and 60Hz magnetic fields. Bioelectromagnetics 14: 545-551.
25. Huss A, Spoerri A, Egger M, Roosli M. 2009. Residence near power lines and mortality from neurodegenerative diseases: longitudinal study of the Swiss population. Am. J. Epidemiol. 169: 167-175.
26. IARC. 2002. Non-Ionizing Radiation, Part 1: Static and Extremely Low-Frequency (ELF) Electric and Magnetic Fields. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, Volume 80. IARC: Lyon.
27. Ivancsits S, Pilger A, Diem E, Jahn O, Rüdiger HW. 2005. Cell type-specific genotoxic effects of intermittent extremely low-frequency electromagnetic fields. Mutat. Res. 583: 184-188.
28. Kato M, Shigemitsu T. 1997. Effect of 50Hz magentic fields on pineal function in the rat. In The Melatonin Hypothesis, Breast Cancer and Use of Electric Power, Stevens RG, Wilson BW, Anderson LE (eds). Battelle Press: Richland. 337-376.
29. Khalil AM, Qassem W. 1991. Cytogenetic effects of pulsing electromagnetic field on human lymphocytes in vitro: chromosme aberrations, sister-chromatid exchanges and cell kinetics. Mutat. Res. 247: 141-146.
30. Kheifets L, Bowman JD, Checkoway H, Feychting M, Harrington JM, Kavet R, Marsh G, Mezei G, Renew DC, van Wijngaarden E. 2009. Future needs of occupational epidemiology of extremely low frequency electric and magnetic fields: review and recommendations. Occup. Environ. Med. 66: 72-80.
31. Knoepfler PS. 2011. Stem cells on the brain. Arch. Neurol. 65: 311-315.
32. Koo EH. 2002. The beta-amyloid precursor protein (APP) and Alzheimer's disease: does the tail wag the dog? Traffic 3: 763-770.
33. Lai H, Singh NP. 1997a. Acute exposure to a 60-Hz magnetic field increases DNA strand breaks in rat brain cells. Bioelectromagnetics 18: 156-165.
34. Lai H, Singh NP. 1997b. Melatonin and n-ter-butyl-alpha-phenylnitrone block 60-Hz magnetic field-induced DNA single and double strand breaks in rat brain cells. J. Pineal Res. 22: 152-162.
35. Leach NT, Rehder C, Jensen K, Holt S, Jackson-Cook C. 2004. Human chromosomes with shorter telomeres and large heterochromatin regions have a higher frequency of acquired somatic cell aneuploidy. Mech. Ageing Dev. 125: 563-573.
36. Leitgeb N. 2011. Comparative health risk assessment of electromagnetic fields. Wien. Med. Wochenschr. 161: 251-262.
37. Lo AW, Sabatier L, Fouladi B, Pottier G, Ricoul M, Murnane J P. 2002. DNA amplification by breakage/fusion/bridge cycles initiated by spontaneous telomere loss in a human cancer cell line. Neoplasia 4: 531-538.
38. Mailhes JB, Young D, Marino AA, London SN. 1997. Electromagnetic fields enhance chemically-induced hyperploidy in mammalian oocytes. Mutagenesis 12: 347-351.
39. Markesbery WR, Lovell MA. 2006. DNA oxidation in Alzheimer's disease. Antioxid. Redox Signal. 8: 2039-2045.
40. Markkanen A. 2009. Effects of electromagnetic fields on cellular responses to agents causing oxidative stress and DNA damage. Kuopio Univ. Publ. C Nat. Environ. Sci. 253: 1-59.
41. Martens UM, Zijlmans JM, Poon SS, Dragowska W, Yui J, Chavez EA, Ward RK, Lansdorp PM. 1998. Short telomeres on human chromosome 17p. Nat. Genet. 18: 76-80.
42. Matsubara E, Bryant-Thomas T, Pacheco QJ, Henry TL, Poeggeler B, Herbert D, Cruz-Sanchez F, Chyan YJ, Smith MA, Perry G, Shoji M, Abe K, Leone A, Grundke-Ikbal I, Wilson GL, Ghiso J, Williams C, Refolo LM, Pappolla MA, Chain DG, Neria E. 2003. Melatonin increases survival and inhibits oxidative and amyloid pathology in a transgenic model of Alzheimer's disease. J. Neurochem. 85: 1101-1108.
43. Mecocci P, Polidori MC, Ingegni T, Cherubini A, Chionne F, Cecchetti R, Senin U. 1998. Oxidative damage to DNA in lymphocytes from AD patients. Neurology 51: 1014-1017.
44. Migliore L, Testa A, Scarpato R, Pavese N, Petrozzi L, Bonuccelli U. 1997. Spontaneous and induced aneuploidy in peripheral blood lymphocytes of patients with Alzheimer's disease. Hum. Genet. 101: 299-305.
45. Miller AB, Green LM. 2010. Electric and magnetic fields at power frequencies. Chronic Dis. Can. 29 Suppl 1: 69-83.
46. Mishima K, Tozawa T, Satoh K, Matsumoto Y, Hishikawa Y, Okawa M. 1999. Melatonin secretion rhythm disorders in patients with senile dementia of Alzheimer's type with disturbed sleep-waking. Biol. Psych. 45: 417-421.
47. Miyakoshi J, Yamagishi N, Ohtsu S, Mohri K, Takebe H. 1996. Increase in hypoxantine-guanine phosphoribosyl transferase gene mutations by exposure to high-density 50-Hz magnetic fields. Mutat. Res. 349: 109-114.
48. Miyakoshi J, Kitagawa K, Takebe H. 1997. Mutation induction by high-density, 50-Hz magnetic fields in human MeWo cells exposed in the DNA synthesis phase. Int. J. Radiat. Biol. 71: 75-79.
49. Miyakoshi J, Yoshida M, Shibuya K, Hiraoka M. 2000. Exposure to strong magnetic fields at power frequency potentiates x-ray-induced DNA strand breaks. J. Radiat. Res. 41: 293-302.
50. Neve RL, McPhie DL, Chen Y. 2000. Alzheimer's disease: a dysfunction of the amyloid precursor protein(1). Brain Res. 886: 54-66.
51. Nishimura M, Yu G, St George-Hyslop PH. 1999. Biology of presenilins as causative molecules for Alzheimer disease. Clin. Genet. 55: 219-225.
52. Noonan CW, Reif JS, Burch JB, Ichinose TY, Yost MG, Magnusson K. 2002. Relationship between amyloid beta protein and melatonin metabolite in a study of electric utility workers. J. Occup. Environ. Med. 44: 769-775.
53. Panossian LA, Porter VR, Valenzuela HF, Zhu X, Reback E, Masterman D, Cummings JL, Effros RB. 2003. Telomere shortening in T cells correlates with Alzheimer's disease status. Neurobiol. Aging 24: 77-84.
54. Pappolla MA, Sos M, Omar RA, Bick RJ, Hickson-Bick DL, Reiter RJ, Efthimiopoulos S, Robakis NK. 1997. Melatonin prevents death of neuroblastoma cells exposed to the Alzheimer amyloid peptide. J. Neurosci. 17: 1683-1690.
55. Pennaneach V, Kolodner RD. 2004. Recombination and the Tel1 and Mec1 checkpoints differentially effect genome rearrangements driven by telomere dysfunction in yeast. Nat. Genet. 36: 612-617.
56. Perry ME, Rolfe M, McIntyre P, Commane M, Stark GR. 1992. Induction of gene amplification by 5-aza-2'-deoxycytidine. Mutat. Res. 276: 189-197.
57. Petrozzi L, Lucetti C, Scarpato R, Gambaccini G, Trippi F, Bernardini S, Del DP, Migliore L, Bonuccelli U. 2002. Cytogenetic alterations in lymphocytes of Alzheimer's disease and Parkinson's disease patients. Neurol. Sci. 23(suppl. 2): S97-S98.
58. Portier CJ, Wolfe MS (eds). 1998. Assessment of Health Effects from Exposure to Power-line Frequency Electric and Magnetic Fields. Working group report. NIH publication no. 98-3981.
59. Potter H. 1991. Review and hypothesis: Alzheimer disease and Down syndrome - chromosome 21 nondisjunction may underlie both disorders. Am. J. Hum. Genet. 48: 1192-1200.
60. Ramirez MJ, Puerto S, Galofre P, Parry EM, Parry JM, Creus A, Marcos R, Surralles J. 2000. Multicolour FISH detection of radioactive iodine-induced 17cen-p53 chromosomal breakage in buccal cells from therapeutically exposed patients. Carcinogenesis 21: 1581-1586.
61. Roosli M. 2008. Commentary: epidemiological research on extremely low frequency magnetic fields and Alzheimer's disease - biased or informative? Int. J. Epidemiol. 37: 341-343.
62. Roses AD. 1997. A model for susceptibility polymorphisms for complex diseases: apolipoprotein E and Alzheimer disease. Neurogenetics 1: 3-11.
63. Ruiz-Gómez MJ, Martinez-Morillo A. 2009. Electromagnetic fields and the induction of DNA strand breaks. Electromagn. Biol. Med. 28: 201-214.
64. Scarfi M-R, Prisco F, Lioi MB, Zeni O, Della Noce M, Di Pietro R, Prisco MB, Franceschi C, Iafusco D, Motta M, Bersani F. 1997. Cytogenetic effects induced by extremely low frequency pulsed magnetic fields in lymphocytes from Turner's syndrome subjects. Bioelectrochem. Bioenerg. 43: 221-226.
65. Scheel C, Schaefer KL, Jauch A, Keller M, Wai D, Brinkschmidt C, van VF, Boecker W, Dockhorn-Dworniczak B, Poremba C. 2001. Alternative lengthening of telomeres is associated with chromosomal instability in osteosarcomas. Oncogene 20: 3835-3844.
66. Schellenberg GD. 1995. Genetic dissection of Alzheimer disease, a heterogeneous disorder. Proc. Natl. Acad. Sci. U.S.A. 92: 8552-8559.
67. Senechal Y, Larmet Y, Dev KK. 2006. Unraveling in vivo functions of amyloid precursor protein: insights from knockout and knockdown studies. Neurodegener Dis 3: 134-147.
68. Simko M, Kriehuber R, Lange S. 1998a. Micronucleus formation in human amniotic cells after exposure to 50Hz MF applied horizontally and vertically. Muation Res. 418: 101-111.
69. Simko M, Kriehuber R, Weiss DG, Luben RA. 1998b. Effects of 50Hz EMF exposure on micronucleus formation and apoptosis in transformed an non transformed human cell lines. Bioelectromagnetics 19: 85-91.
70. Simko M, Richard D, Kriehuber R, Weiss DG. 2001. Micronucleus induction in syrian hamster embryo cells following exposure to 50Hz magnetic fields, benzo(α)pyrene, and TPA in vitro. Mutat. Res. 495: 43-50.
71. Singh NP, Lai H. 1998. 60Hz magnetic field exposure induces DNA crosslinks in rat brain cells. Mutat. Res. 400: 313-320.
72. SSM 2011. Recent Research on EMF and Health Risk: Seventh Annual Report from SSM's Independent Expert Group on Electromagnetic Fields. Swedish Radiation Safety Authority (Strålsäkerhetsmyndigheten), 2010. Available from.
73. St George-Hyslop PH. 2000. Piecing together Alzheimer's. Sci. Am. 283: 76-83.
74. Svendestål BM, Johansson KJ, Mild KH. 1999a. DNA damage induced in rat brain cells of CBA mice exposed to magnetic fields. In vivo 13: 551-552.
75. Svendestål BM, Johansson KJ, Mattson MO, Paulsson LE. 1999b. DNA damage, cell kinetics and ODC activities studies in CBA mice exposed to electromagnetic fields generated by transmission lines. In vivo 13: 507-513.
76. Teller JK, Russo C, DeBusk LM, Angelini G, Zaccheo D, Dagna-Bricarelli F, Scartezzini P, Bertolini S, Mann DM, Tabaton M, Gambetti P. 1996. The presence of soluble amyloid beta-peptide precedes amyloid plaque formation in Down's syndrome. Nat. Med. 2: 93-95.
77. Thomas P, Fenech M. 2007. A review of genome mutation and Alzheimer's disease. Mutagenesis 22: 15-33.
78. Thomas P, Fenech M. 2008. Chromosome 17 and 21 aneuploidy in buccal cells is increased with ageing and in Alzheimer's disease. Mutagenesis 23: 57-65.
79. Trippi F, Botto N, Scarpato R, Petrozzi L, Bonuccelli U, Latorraca S, Sorbi S, Migliore L. 2001. Spontaneous and induced chromosome damage in somatic cells of sporadic and familial Alzheimer's disease patients. Mutagenesis 16: 323-327.
80. Udroiu I, Cristaldi M, Ieradi LA, Bedini A, Giuliani L, Tanzarella C. 2006. Clastogenicity and aneuploidy in newborn and adult mice exposed to 50Hz magnetic fields. Int. J. Radiat. Biol. 82: 561-567.
81. Verheyen G, Pauwels G, Verschaeve L, Schoeters G. 2003. Effect of coexposure to 50Hz magnetic fields and an aneugen on human lymphocytes, determined by the cytokinesis Block micronucleus assay. Bioelectromagnetics 24: 160-164.
82. Vijayalaxmi, Obe G 2005. Controversial cytogenetic observations in mammalian somatic cells exposed to extremely low frequency electromagnetic radiation: a review and future research recommendations. Bioelectromagnetics 26: 412-430.
83. Vijayalaxmi, Prihoda TJ. 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: 196-213.
84. Von Zglinicki T, Serra V, Lorenz M, Saretzki G, Lenzen-Groβimlighaus R, Geβner R, Risch A, Steinhagen-Thiessen E. 2000. Short telomeres in parients with vascular dementia: an indicator of low antioxidative capacity and a possible risk factor? Lab. Invest. 80: 1739-1747.
85. Von Zglinicki T. 2002. Oxidative stress shortens telomeres. Trends Biochem. Sci. 27: 339-344.
86. Wang XC, Zhang J, Yu X, Han L, Zhou ZT, Zhang Y, Wang JZ. 2005. Prevention of isoproterenol-induced tau hyperphosphorylation by melatonin in the rat. Sheng Li Xue Bao 57: 7-12.
87. Wisniewski T, Ghiso J, Frangione B. 1997. Biology of A beta amyloid in Alzheimer's disease. Neurobiol. Dis. 4: 313-328.
88. Wolf FI, Torsello A, Tedesco B, Fasanella S, Boninsegna A, S'Ascenzo M, Grassi C, Azzena GB, Cittadini A. 2005. 50-Hz extremely low frequency electromagnetic fields enhance cell proloferation and DNA damage: possible involvement of redox mechanism. Biochim. Biophys. Acta 1743: 120-129.
89. Wu RY, Yang H, Chiang H, Shao BJ, Bao JL. 1998. The effects of low-frequency magnetic fields on DNA unscheduled synthesis induced by methylnitro-nitroguanidine in vitro. Electro-Magnetobiol. 17: 57-65.
90. Yagushi H, Yoshida M, Ejima Y, Miyakoshi J. 1999. Effect of high-density extremely low frequency magnetic fiel don sister chromatid exchanges in mouse m5S cells. Mutat. Res. 440: 189-194.
91. Zmyslony M, Palus J, Jajte J, Dziubaltowska E, Rajkowska E. 2000. DNA damage in rat lymphoctyes treated in vitro with iron cations and exposed to 7-mT magnetic fields (static or 50Hz). Mutat. Res. 453: 89-96.