Electromagnetic fields at a mobile phone frequency (900 MHz) trigger the onset of general stress response along with DNA modifications in Eisenia fetida earthworms

1. Witthöft M, Rubin GJ. Are media warnings about the adverse health effects of modern life self-fulfilling? An experimental study on idiopathic environmental intolerance attributed to electromagnetic fields (IEI-EMF). J Psychosom Res 2013;74:206-12. doi: 10.1016/j.jpsychores.2012.12.002Search in Google Scholar

2. Hardell L, Carlberg M, Söderqvist F, Mild KH, Morgan LL. Long-term use of cellular phones and brain tumours: increased risk associated with use for ≥10 years. Occup Environ Med 2007;64:626-32. doi: 10.1136/oem.2006.029751Search in Google Scholar

3. Baldi I, Coureau G, Jaffré A, Gruber A, Ducamp S, Provost D, Lebailly P, Vital A, Loiseau H, Salamon R. Occupational and residential exposure to electromagnetic fields and risk of brain tumors in adults: a case-control study in Gironde, France. Int J Cancer 2011;129:1477-84. doi: 10.1002/ijc.25765Search in Google Scholar

4. Coureau G, Bouvier G, Lebailly P, Fabbro-Peray P, Gruber A, Leffondre K, Guillamo JS, Loiseau H, Mathoulin-Pélissier S, Salamon R, Baldi I. Mobile phone use and brain tumours in the CERENAT case-control study. Occup Environ Med 2014;71:514-22. doi: 10.1136/oemed-2013-101754Search in Google Scholar

5. Tkalec M, Malarić K, Pevalek-Kozlina B. Influence of 400, 900, and 1900 MHz electromagnetic fields on Lemna minor growth and peroxidase activity. Bioelectromagnetics 2005;26:185-93. doi: 10.1002/bem.20104Search in Google Scholar

6. Lixia S, Yao K, Kaijun W, Deqiang L, Huajun H, Xiangwei G, Baohong W, Wei Z, Jianling L, Wei W. Effects of 1.8 GHz radiofrequency field on DNA damage and expression of heat shock protein 70 in human lens epithelial cells. Mutat Res 2006;602:135-42. doi: 10.1016/j.mrfmmm.2006.08.010Search in Google Scholar

7. Tkalec M, Štambuk A, Šrut M, Malarić K, Klobučar GI. Oxidative and genotoxic effects of 900 MHz electromagnetic fields in the earthworm Eisenia fetida. Ecotoxicol Environ Saf 2013;90:7-12. doi: 10.1016/j.ecoenv.2012.12.005Search in Google Scholar

8. Cambier S, Gonzalez P, Durrieu G, Bourdineaud JP. Cadmium-induced genotoxicity in zebrafish at environmentally relevant doses. Ecotoxicol Environ Saf 2010;73:312-9. doi: 10.1016/j.ecoenv.2009.10.012Search in Google Scholar

9. Geffroy B, Ladhar C, Cambier S, Treguer-Delapierre M, Brèthes D, Bourdineaud JP. Impact of dietary gold nanoparticles in zebrafish at very low contamination pressure: the role of size, concentration and exposure time. N a n o t o x i c o l o g y 2 0 1 2 ; 6 : 1 4 4 - 6 0 . d o i : 10.3109/17435390.2011.562328Search in Google Scholar

10. Orieux N, Cambier S, Gonzalez P, Morin B, Adam C, Garnier-Laplace J, Bourdineaud JP. Genotoxic damages in zebrafish submitted to a polymetallic gradient displayed by the Lot River (France). Ecotoxicol Environ Saf 2011;74:974-83. doi: 10.1016/j.ecoenv.2011.01.008Search in Google Scholar

11. Ladhar C, Geffroy B, Cambier S, Treguer-Delapierre M, Durand E, Brèthes D, Bourdineaud JP. Impact of dietary cadmium sulfide nanoparticles on Danio rerio zebrafish at very low contamination pressure. Nanotoxicology 2014;8:676-85. doi: 10.3109/17435390.2013.822116Search in Google Scholar

12. Dedeh A, Ciutat A, Treguer-Delapierre M, Bourdineaud JP. Impact of gold nanoparticles on zebrafish exposed to a spiked sediment. Nanotoxicology 2015;9:71-80. doi: 10.3109/17435390.2014.889238Search in Google Scholar

13. Dedeh A, Ciutat A, Lecroart P, Treguer-Delapierre M, Bourdineaud JP. Cadmium sulfide nanoparticles trigger DNA alterations and modify the bioturbation activity of tubificidae worms exposed through the sediment. Nanotoxicology 2016;10:322-31. doi: 10.3109/17435390.2015.1071444Search in Google Scholar

14. Lerebours A, Cambier S, Hislop L, Adam-Guillermin C, Bourdineaud JP. Genotoxic effects of exposure to waterborne uranium, dietary methylmercury and hyperoxia in zebrafish assessed by the quantitative RAPD-PCR method. Mutation Res 2013;755:55-60. doi: 10.1016/j.mrgentox.2013.05.012Search in Google Scholar

15. Bernard F, Brulle F, Douay F, Lemière S, Demuynck S, Vandenbulcke F. Metallic trace element body burdens and gene expression analysis of biomarker candidates in Eisenia fetida, using an “exposure/depuration” experimental scheme with field soils. Ecotoxicol Environ Saf 2010;73:1034-45. doi: 10.1016/j.ecoenv.2010.01.010Search in Google Scholar

16. Bošnjak I, Bielen A, Babić S, Sver L, Popović NT, Strunjak-Perović I, Což-Rakovac R, Klobučar RS. First evidence of the P-glycoprotein gene expression and multixenobiotic resistance modulation in earthworm. Arh Hig Rada Toksikol 2014;65:67-75. doi: 10.2478/10004-1254-65-2014-2421Search in Google Scholar

17. Hayashi Y, Engelmann P, Foldbjerg R, Szabó M, Somogyi I, Pollák E, Molnár L, Autrup H, Sutherland DS, Scott- Fordsmand J, Heckmann LH. Earthworms and humans in vitro: characterizing evolutionarily conserved stress and immune responses to silver nanoparticles. Environ Sci Technol 2012;46:4166-73. doi: 10.1021/es3000905Search in Google Scholar

18. Brulle F, Mitta G, Cocquerelle C, Vieau D, Lemière S, Leprêtre A, Vandenbulcke F. Cloning and real-time PCR testing of 14 potential biomarkers in Eisenia fetida following cadmium exposure. Environ Sci Technol 2006;40:2844-50. doi: 10.1021/es052299xSearch in Google Scholar

19. Brulle F, Mitta G, Leroux R, Lemière S, Leprêtre A, Vandenbulcke F. The strong induction of metallothionein gene following cadmium exposure transiently affects the expression of many genes in Eisenia fetida: a trade-off mechanism? Comp Biochem Physiol C Toxicol Pharmacol 2007;144:334-41. doi: 10.1016/j.cbpc.2006.10.007Search in Google Scholar

20. Brulle F, Cocquerelle C, Mitta G, Castric V, Douay F, Leprêtre A, Vandenbulcke F. Identification and expression profile of gene transcripts differentially expressed during metallic exposure in Eisenia fetida coelomocytes. Dev Comp Immunol 2008;32:1441-53. doi: 10.1016/j.dci.2008.06.009Search in Google Scholar

21. Brulle F, Lemière S, Waterlot C, Douay F, Vandenbulcke F. Gene expression analysis of 4 biomarker candidates in Eisenia fetida exposed to an environmental metallic trace elements gradient: a microcosm study. Sci Total Environ 2011;409:5470-82. doi: 10.1016/j.scitotenv.2011.08.040Search in Google Scholar

22. Unrine JM, Hunyadi SE, Tsyusko OV, Rao W, Shoults-Wilson WA, Bertsch PM. Evidence for bioavailability of Au nanoparticles from soil and biodistribution within earthworms (Eisenia fetida). Environ Sci Technol 2010;44:8308-13. doi: 10.1021/es101885wSearch in Google Scholar

23. Tsyusko OV, Hardas SS, Shoults-Wilson WA, Starnes CP, Joice G, Butterfield DA, Unrine JM. Short-term molecularlevel effects of silver nanoparticle exposure on the earthworm, Eisenia fetida. Environ Pollut 2012;171:249-55. doi: 10.1016/j.envpol.2012.08.003Search in Google Scholar

24. Chen C, Zhou Q, Liu S, Xiu Z. Acute toxicity, biochemical and gene expression responses of the earthworm Eisenia fetida exposed to polycyclic musks. Chemosphere 2011;83:1147-54. doi: 10.1016/j.chemosphere.2011.01.006Search in Google Scholar

25. Chen C, Xue S, Zhou Q, Xie X. Multilevel ecotoxicity assessment of polycyclic musk in the earthworm Eisenia fetida using traditional and molecular endpoints. Ecotoxicology 2011;20:1949-58. doi: 10.1007/s10646-011-0735-9Search in Google Scholar

26. Wu S, Zhang H, Zhao S, Wang J, Li H, Chen J. Biomarker responses of earthworms (Eisenia fetida) exposured to phenanthrene and pyrene both singly and combined in microcosms. Chemosphere 2012;87:285-93. doi: 10.1016/j.chemosphere.2011.11.055Search in Google Scholar

27. Marjanović AM, Pavičić I, Trošić I. Biological indicators in response to radiofrequency/microwave exposure. Arh Hig Rada Toksikol 2012;63:407-16. doi: 10.2478/10004-1254-63-2012-2215Search in Google Scholar

28. Dasdag S, Akdag MZ. The link between radiofrequencies emitted from wireless technologies and oxidative stress. J Chem Neuroanat 2016;75:85-93. doi: 10.1016/j.jchemneu.2015.09.001Search in Google Scholar

29. Dasdag S, Akdag MZ, Kizil M, Kizil G, Cakir DU, Yokus B. Effect of 900 MHz radiofrequency radiation on beta amyloid protein, protein carbonyl and malondialdehyde in brain. Electromagn Biol Med 2012;31:67-74. doi: 10.3109/15368378.2011.624654Search in Google Scholar

30. Akdag MZ, Dasdag S, Cakir DU, Yokus B, Kizil G, Kizil M. Do 100 and 500 μT ELF magnetic fields alter beta amyloid protein, protein carbonyl and malondialdehyde in brain? E l e c t r o m a g n B i o l M e d 2 0 1 3 ; 3 2 : 3 6 3 - 7 2 . d o i : 10.3109/15368378.2012.721848Search in Google Scholar

31. Kimura T, Takahashi K, Suzuki Y, Konishi Y, Ota Y, Mori C, Ikenaga T, Takanami T, Saito R, Ichiishi E, Awaji S, Watanabe K, Higashitani A. The effect of high strength static magnetic fields and ionizing radiation on gene expression and DNA damage in Caenorhabditis elegans. Bioelectromagnetics 2008;29:605-14. doi: 10.1002/bem.20425Search in Google Scholar

32. Blank M, Goodman R. Electromagnetic fields stress living cells. Pathophysiology 2009;16:71-8. doi: 10.1016/j.pathophys.2009.01.006Search in Google Scholar

33. Rodríguez de la Fuente AO, Alcocer-González JM, Antonio Heredia-Rojas J, Balderas-Candanosa I, Rodríguez-Flores LE, Rodríguez-Padilla C, Taméz-Guerra RS. Effect of 60 Hz electromagnetic fields on the activity of hsp70 promoter: An in vitro study. Cell Biol Int 2009;33:419-23. doi: 10.1042/CBR20110010Search in Google Scholar

34. Weisbrot D, Lin H, Ye L, Blank M, Goodman R. Effects of mobile phone radiation on growth and development in Drosophila melanogaster. J Cell Biochem 2003;89:48-55.doi: 10.1002/jcb.10480Search in Google Scholar

35. Osera C, Fassina L, Amadio M, Venturini L, Buoso E, Magenes G, Govoni S, Ricevuti G, Pascale A. Cytoprotective response induced by electromagnetic stimulation on SHSY5Y human neuroblastoma cell line. Tissue Eng Part A 2011;17:2573-82. doi: 10.1089/ten.TEA.2011.0071Search in Google Scholar

36. Campisi A, Gulino M, Acquaviva R, Bellia P, Raciti G, Grasso R, Musumeci F, Vanella A, Triglia A. Reactive oxygen species levels and DNA fragmentation on astrocytes in primary culture after acute exposure to low intensity microwave electromagnetic field. Neurosci Lett 2010;473:52-5. doi: 10.1016/j.neulet.2010.02.018Search in Google Scholar

37. Roux D, Vian A, Girard S, Bonnet P, Paladian F, Davies E, Ledoigt G. Electromagnetic fields (900 MHz) evoke consistent molecular responses in tomato plants. Physiol P l a n t a r u m 2 0 0 6 ; 1 2 8 : 2 8 3 - 8 . d o i : 10.1111/j.1399-3054.2006.00740.xSearch in Google Scholar

38. Roux D, Vian A, Girard S, Bonnet P, Paladian F, Davies E, Ledoigt G. High frequency (900 MHz) low amplitude (5 V m-1) electromagnetic field: a genuine environmental stimulus that affects transcription, translation, calcium and energy charge in tomato. Planta 2008;227:883-91. doi: 10.1007/s00425-007-0664-2Search in Google Scholar

39. Ni S, Yu Y, Zhang Y, Wu W, Lai K, Yao K. Study of oxidative stress in human lens epithelial cells exposed to 1.8 GHz radiofrequency fields. PLoS One 2013;8(8):e72370. doi: 10.1371/journal.pone.0072370Search in Google Scholar

40. Cucurachi S, Tamis WL, Vijver MG, Peijnenburg WJ, Bolte JF, de Snoo GR. A review of the ecological effects of radiofrequency electromagnetic fields (RF-EMF). Environ Int 2013;51:116-40. doi: 10.1016/j.envint.2012.10.009Search in Google Scholar

41. Akdag MZ, Dasdag S, Canturk F, Karabulut D, Caner Y, Adalier N. Does prolonged radiofrequency radiation emitted from Wi-Fi devices induce DNA damage in various tissues of rats? J Chem Neuroanat 2016;75:116-22. doi: 10.1016/j.jchemneu.2016.01.003Search in Google Scholar

42. Hardell L, Sage C. Biological effects from electromagnetic field exposure and public exposure standards. Biomed Pharmacother 2008;62:104-9. doi: 10.1016/j.biopha.2007.12.004Search in Google Scholar

43. Phillips JL, Singh NP, Lai H. Electromagnetic fields and DNA damage. Pathophysiology 2009;16:79-88. doi: 10.1016/j.pathophys.2008.11.005Search in Google Scholar

44. Ruediger HW. Genotoxic effects of radiofrequency electromagnetic fields. Pathophysiology 2009;16:89-102. doi: 10.1016/j.pathophys.2008.11.004Search in Google Scholar

45. Duan W, Liu C, Zhang L, He M, Xu S, Chen C, Pi H, Gao P, Zhang Y, Zhong M, Yu Z, Zhou Z. Comparison of the genotoxic effects induced by 50 Hz extremely low-frequency electromagnetic fields and 1800 MHz radiofrequency electromagnetic fields in GC-2 cells. Radiat Res 2015;183:305-14. doi: 10.1667/RR13851.1Search in Google Scholar

46. Lai H, Singh NP. Magnetic-field-induced DNA strand breaks in brain cells of the rat. Environ Health Perspect 2004;112:687-94. PMCID: PMC124196310.1289/ehp.6355124196315121512Search in Google Scholar

47. Yao K, Wu W, Wang K, Ni S, Ye P, Yu Y, Ye J, Sun L. Electromagnetic noise inhibits radiofrequency radiationinduced DNA damage and reactive oxygen species increase in human lens epithelial cells. Mol Vis 2008;14:964-9. PMCID: PMC2391079Search in Google Scholar

48. Khaki AA, Tubbs RS, Shoja MM, Rad JS, Khaki A, Farahani RM, Zarrintan S, Nag TC. The effects of an electromagnetic field on the boundary tissue of the seminiferous tubules of the rat: a light and transmission electron microscope study. Folia Morphol 2006;65:188-94. PMID: 16988914Search in Google Scholar

49. Tenorio BM, Jimenez GC, de Morais RN, Peixoto CA, de Albuquerque Nogueira R, da Silva VA Jr. Evaluation of testicular degeneration induced by low-frequency electromagnetic fields. J Appl Toxicol 2012;32:210-8. doi: 10.1002/jat.1680Search in Google Scholar

50. Shams Lahijani M, Tehrani DM, Sabouri E. Histopathological and ultrastructural studies on the effects of electromagnetic fields on the liver of preincubated white leghorn chicken embryo. Electromagnetic Biol Med 2009;28:391-413. doi: 10.3109/15368370903287689Search in Google Scholar

51. De Iuliis GN, Newey RJ, King BV, Aitken RJ. Mobile phone radiation induces reactive oxygen species production and DNA damage in human spermatozoa in vitro. PLoS One 2009;4:e6446. doi: 10.1371/journal.pone.0006446Search in Google Scholar

52. Xu S, Zhou Z, Zhang L, Yu Z, Zhang W, Wang Y, Wang X, Li M, Chen Y, Chen C, He M, Zhang G, Zhong M. Exposure to 1800 MHz radiofrequency radiation induces oxidative damage to mitochondrial DNA in primary cultured neurons. Brain Res 2010;1311:189-96. doi: 10.1016/j.brainres.2009.10.062Search in Google Scholar

53. Ikehara T, Nishisako H, Minami Y, Ichinose Sasaki H, Shiraishi T, Kitamura M, Shono M, Houchi H, Kawazoe K, Minakuchi K, Yoshizaki K, Kinouchi Y, Miyamoto H. Effects of exposure to a time-varying 1.5 T magnetic field on the neurotransmitter-activated increase in intracellular Ca(2+) in relation to actin fiber and mitochondrial functions in bovine adrenal chromaffin cells. Biochim Biophys Acta 2010;1800:1221-30. doi: 10.1016/j.bbagen.2010.09.001Search in Google Scholar

54. Ford WE, Ren W, Blackmore PF, Schoenbach KH, Beebe SJ. Nanosecond pulsed electric fields stimulate apoptosis without release of pro-apoptotic factors from mitochondria in B16f10 melanoma. Arch Biochem Biophys 2010;497:82-9. doi: 10.1016/j.abb.2010.03.008Search in Google Scholar

55. Morabito C, Rovetta F, Bizzarri M, Mazzoleni G, Fanò G, Mariggiò MA. Modulation of redox status and calcium handling by extremely low frequency electromagnetic fields in C2C12 muscle cells: A real-time, single-cell approach. Free Radical Biol Med 2010;48:579-89. doi: 10.1016/j.freeradbiomed.2009Search in Google Scholar

56. Beaubois E, Girard S, Lallechere S, Davies E, Paladian F, Bonnet P, Ledoigt G, Vian A. Intercellular communication in plants: evidence for two rapidly transmitted systemic signals generated in response to electromagnetic field stimulation in tomato. Plant Cell Environ 2007;30:834-44. doi: 10.1111/j.1365-3040.2007.01669.xSearch in Google Scholar