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ELF Alternating Magnetic Field Decreases Reproduction by DNA Damage Induction

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In the present experiments, the effect of 50-Hz alternating magnetic field on Drosophila melanogaster reproduction was studied. Newly eclosed insects were separated into identical groups of ten males and ten females and exposed to three different intensities of the ELF magnetic field (1, 11, and 21 G) continuously during the first 5 days of their adult lives. The reproductive capacity was assessed by the number of F1 pupae according to a well-defined protocol of ours. The magnetic field was found to decrease reproduction by up to 4.3 %. The effect increased with increasing field intensities. The decline in reproductive capacity was found to be due to severe DNA damage (DNA fragmentation) and consequent cell death induction in the reproductive cells as determined by the TUNEL assay applied during early and mid-oogenesis (from germarium to stage 10) where physiological apoptosis does not occur. The increase in DNA damage was more significant than the corresponding decrease in reproductive capacity (up to ~7.5 %). The TUNEL-positive signal denoting DNA fragmentation was observed exclusively at the two most sensitive developmental stages of oogenesis: the early and mid-oogenesis checkpoints (i.e. region 2a/2b of the germarium and stages 7–8 just before the onset of vitellogenesis)—in contrast to exposure to microwave radiation of earlier work of ours in which the DNA fragmentation was induced at all developmental stages of early and mid-oogenesis. Moreover, the TUNEL-positive signal was observed in all three types of egg chamber cells, mainly in the nurse and follicle cells and also in the oocyte, in agreement with the microwave exposure of our earlier works. According to previous reports, cell death induction in the oocyte was observed only in the case of microwave exposure and not after exposure to other stress factors as toxic chemicals or food deprivation. Now it is also observed for the first time after ELF magnetic field exposure. Finally, in contrast to microwave exposure of previous experiments of ours in which the germarium checkpoint was found to be more sensitive than stage 7–8, in the magnetic field exposure of the present experiments the mid-oogenesis checkpoint was found to be more sensitive than the germarium.

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References

  1. WHO (1984). Extremely low frequency (ELF) fields, Geneva.

  2. Anderson, L. E., & Kaune, W. T. (1989) Electric and magnetic fields at extremely low frequencies. In M. J. Suess (Ed.), Non-ionizing radiation protection (2nd edn, pp 175–243). WHO.

  3. Lioliousis, C. (1997). Biological effects of electromagnetic radiation. Athens: Diavlos Books.

    Google Scholar 

  4. Wertheimer, N., & Leeper, E. (1979). Electrical wiring configurations and childhood cancer. American Journal of Epidemiology, 109, 273–284.

    PubMed  CAS  Google Scholar 

  5. Savitz, D. A., Wachtel, H., Barnes, F., John, E. M., & Tvrdik, J. G. (1988). Case-control study of childhood cancer and exposure to 60 Hz magnetic fields. American Journal of Epidemiology, 128, 21–38.

    PubMed  CAS  Google Scholar 

  6. Feychting, M., & Ahlbom, A. (1993). Magnetic Fields and Cancer in children residing near Swedish High–Voltage Power Lines. American Journal of Epidemiology, 138, 467–481.

    PubMed  CAS  Google Scholar 

  7. Feychting, M., & Ahlbom, A. (1994). Magnetic fields, Leukemia and Central Nervous System Tumors in Swedish adults residing near High–Voltage Power Lines. Epidemiology, 5, 501–509.

    PubMed  CAS  Google Scholar 

  8. Feychting, M., & Ahlbom, A. (1995). Childhood leukemia and residential exposure to weak extremely low frequency magnetic fields. Environ Health Perspect, suppl, 2, 59–62.

    Google Scholar 

  9. Coleman, M. P., Bell, C. M., Taylor, H. L., & Primic-Zakelj, M. (1989). Leukaemia and residence near electricity transmission equipment: A case-control study. British Journal of Cancer, 60(5), 793–798.

    Article  PubMed  CAS  Google Scholar 

  10. Draper, G., Vincent, T., Kroll, M. E., & Swanson, J. (2005). Childhood cancer in relation to distance from high voltage power lines in England and Wales: A case-control study. BMJ, 330(7503), 1290.

    Article  PubMed  Google Scholar 

  11. Ahlbom, A., Day, N., Feychting, M., Roman, E., Skinner, J., Dockerty, J., et al. (2000). A pooled analysis of magnetic fields and childhood leukaemia. British Journal of Cancer, 83(5), 692–698.

    Article  PubMed  CAS  Google Scholar 

  12. Greenland, S., Sheppard, A. R., Kaune, W. T., Poole, C., & Kelsh, M. A. (2000). A pooled analysis of magnetic fields, wire codes, and childhood leukemia. Childhood Leukemia-EMF Study Group. Epidemiology, 11(6), 624–634. Review.

    Article  PubMed  CAS  Google Scholar 

  13. Kheifets, L., Ahlbom, A., Crespi, C. M., Draper, G., Hagihara, J., Lowenthal, R. M., Mezei, G., Oksuzyan, S., Schüz, J., Swanson, J., Tittarelli, A., Vinceti, M., & Wunsch Filho, V. (2010). Pooled analysis of recent studies on magnetic fields and childhood leukaemia. British Journal of Cancer 103(7):1128–1135. Erratum in: British Journal of Cancer 2011, 104(1):228.

    Google Scholar 

  14. Coghill, R. W., Steward, J., & Philips, A. (1996). Extra low frequency electric and magnetic fields in the bed place of children diagnosed with leukaemia: A case-control study. European Journal of Cancer Prevention, 5(3), 153–158.

    Article  PubMed  CAS  Google Scholar 

  15. ICNIRP. (1998). Guidelines for limiting exposure to time-varying electric, magnetic and electromagnetic fields (up to 300 GHz). Health Physics, 74, 494–522.

    Google Scholar 

  16. IRPA. (1990). Interim guidelines on limits of exposure to 50/60 Hz electric and magnetic fields. Health Physics, 58(1), 113–122.

    Google Scholar 

  17. Dubrov, A. P. (1978). The geomagnetic field and life: Geomagnetobiology. New York: Plenum Press.

    Book  Google Scholar 

  18. Presman, A. S. (1977). Electromagnetic fields and life. New York: Plenum Press.

    Google Scholar 

  19. Panagopoulos, D. J. (2013) Electromagnetic interaction between environmental fields and living systems determines Health and Well-Being. In Electromagnetic Fields: Principles, engineering applications and biophysical effects. Nova Science Publishers, New York.

  20. Panagopoulos, D. J. (2011). Analyzing the health impacts of modern telecommunications microwaves. In L. V. Berhardt (Ed.), Advances in medicine and biology (Vol. 17). New York: Nova Science Publishers, Inc.

    Google Scholar 

  21. Ramírez, E., Monteagudo, J. L., García-Gracia, M., & Delgado, J. M. (1983). Oviposition and development of Drosophila modified by magnetic fields. Bioelectromagnetics, 4(4), 315–326.

    Article  PubMed  Google Scholar 

  22. Delgado, J. M. R. (1985). Biological effects of extremely low frequency electromagnetic fields. Journal of Bioelectricity, 4(1), 75–91.

    Google Scholar 

  23. Ma, T. H., & Chu, K. C. (1993). Effect of the extremely low frequency (ELF) electromagnetic field (EMF) on developing embryos of the fruit fly (Drosophila melanogaster L.). Mutation Research, 303(1), 35–39.

    Article  PubMed  CAS  Google Scholar 

  24. Goodman, R., Weisbrot, D., Uluc, A., & Henderson, A. (1992). Transcription in Drosophila melanogaster salivary gland cells is altered following exposure to low-frequency electromagnetic fields: Analysis of chromosome 3R. Bioelectromagnetics, 13(2), 111–118.

    Article  PubMed  CAS  Google Scholar 

  25. Panagopoulos, D. J., & Margaritis, L. H. (2003) Effects of electromagnetic fields on the reproductive capacity of Drosophila melanogaster. In P. Stavroulakis (Ed.), Biological effects of electromagnetic fields. Springer, pp 545–578.

  26. Gonet, B., Kosik-Bogacka, D. I., & Kuźna-Grygiel, W. (2009). Effects of extremely low-frequency magnetic fields on the oviposition of Drosophila melanogaster over three generations. Bioelectromagnetics, 30(8), 687–689.

    Article  PubMed  Google Scholar 

  27. Kikuchi, T., Ogawa, M., Otaka, Y., & Furuta, M. (1998). Multigeneration exposure test of Drosophila melanogaster to ELF magnetic fields. Bioelectromagnetics, 19(6), 335–340.

    Article  PubMed  CAS  Google Scholar 

  28. Koana, T., Okada, M. O., Takashima, Y., Ikehata, M., & Miyakoshi, J. (2001). Involvement of eddy currents in the mutagenicity of ELF magnetic fields. Mutation Research, 476(1–2), 55–62.

    Article  PubMed  CAS  Google Scholar 

  29. Mirabolghasemi, G., & Azarnia, M. (2002). Developmental changes in Drosophila melanogaster following exposure to alternating electromagnetic fields. Bioelectromagnetics., 23(6), 416–420.

    Article  PubMed  Google Scholar 

  30. Michel, A., & Gutzeit, H. O. (1999). Electromagnetic fields in combination with elevated temperatures affect embryogenesis of Drosophila. Biochemical and Biophysical Research Communications, 265(1), 73–78.

    Article  PubMed  CAS  Google Scholar 

  31. Otaka, Y., Kitamura, S., Furuta, M., & Shinohara, A. (1992). Sex-linked recessive lethal test of Drosophila melanogaster after exposure to 50-Hz magnetic fields. Bioelectromagnetics, 13(1), 67–74.

    Article  PubMed  CAS  Google Scholar 

  32. Mitler, S. (1974) Low frequency electromagnetic radiation and genetic aberrations in Drosophila melanogaster. Genetics, 73–74, Suppl 183.

  33. Walters, E., & Carstensen, E. L. (1987). Test for the effects of 60-Hz magnetic fields on fecundity and development in Drosophila. Bioelectromagnetics, 8(4), 351–354.

    Article  PubMed  CAS  Google Scholar 

  34. Nguyen, P., Bournias-Vardiabasis, N., Haggren, W., Adey, W. R., & Phillips, J. L. (1995). Exposure of Drosophila melanogaster embryonic cell cultures to 60-Hz sinusoidal magnetic fields: Assessment of potential teratogenic effects. Teratology, 51(4), 273–277.

    Article  PubMed  CAS  Google Scholar 

  35. Panagopoulos, D. J. (2012). Gametogenesis, embryonic and post-embryonic development of Drosophila melanogaster, as a model system for the assessment of radiation and environmental genotoxicity. In M. Spindler-Barth (Ed.), Drosophila melanogaster: Life cycle, genetics and development. New York: Nova Science Publishers.

    Google Scholar 

  36. Panagopoulos, D. J., Karabarbounis, A., & Margaritis, L. H. (2004). Effect of GSM 900-MHz mobile phone radiation on the reproductive capacity of Drosophila melanogaster. Electromagnetic Biology and Medicine, 23(1), 29–43.

    Article  Google Scholar 

  37. Panagopoulos, D. J., Chavdoula, E. D., Karabarbounis, A., & Margaritis, L. H. (2007). Comparison of bioactivity between GSM 900 MHz and DCS 1800 MHz mobile telephony radiation. Electromagnetic Biology and Medicine, 26(1), 33–44.

    Article  PubMed  Google Scholar 

  38. Panagopoulos, D. J., & Margaritis, L. H. (2010). The effect of exposure duration on the biological activity of mobile telephony radiation. Mutation Research, 699(1–2), 17–22.

    Article  PubMed  CAS  Google Scholar 

  39. Panagopoulos, D. J., Chavdoula, E. D., Nezis, I. P., & Margaritis, L. H. (2007). Cell death induced by GSM 900 MHz and DCS 1800 MHz mobile telephony radiation. Mutation Research, 626, 69–78.

    Article  PubMed  CAS  Google Scholar 

  40. Panagopoulos, D. J., Chavdoula, E. D., & Margaritis, L. H. (2010). Bioeffects of mobile telephony radiation in relation to its intensity or distance from the antenna. International Journal of Radiation Biology, 86(5), 345–357.

    Article  PubMed  CAS  Google Scholar 

  41. Panagopoulos, D. J. (2012). Effect of microwave exposure on the ovarian development of Drosophila melanogaster. Cell Biochemistry and Biophysics, 63, 121–132.

    Article  PubMed  CAS  Google Scholar 

  42. King, R. C. (1970). Ovarian development in Drosophila Melanogaster. New York: Academic Press.

    Google Scholar 

  43. McCall, K. (2004). Eggs over easy: Cell death in the Drosophila ovary. Developmental Biology, 274(1), 3–14.

    Article  PubMed  CAS  Google Scholar 

  44. Nezis, I. P., Stravopodis, D. J., Papassideri, I., Robert-Nicoud, M., & Margaritis, L. H. (2000). Stage-specific apoptotic patterns during Drosophila oogenesis. European Journal of Cell Biology, 79, 610–620.

    Article  PubMed  CAS  Google Scholar 

  45. Nezis, I. P., Stravopodis, D. J., Papassideri, I., Robert-Nicoud, M., & Margaritis, L. H. (2002). Dynamics of apoptosis in the ovarian follicle cells during the late stages of Drosophila oogenesis. Cell and Tissue Research, 307, 401–409.

    Article  PubMed  Google Scholar 

  46. Weiss, N. A. (1995) Introductory statistics. Addison-Wesley Publ. Co. Inc.

  47. Maber, J. (1999). Data analysis for biomolecular sciences. England: Longman.

    Google Scholar 

  48. Drummond-Barbosa, D., & Spradling, A. C. (2001). Stem cells and their progeny respond to nutritional changes during Drosophila oogenesis. Dev. Biol., 231, 265–278.

    Article  PubMed  CAS  Google Scholar 

  49. Srivastava, T., & Singh, B. N. (1998). Effect of temperature on oviposition in four species of the melanogaster group of Drosophila. Revista Brasileira de Biologia, 58(3), 491–495.

    Article  PubMed  CAS  Google Scholar 

  50. Liburdy, R. P. (1992). Calcium signalling in lymphocytes and ELF fields: Evidence for an electric field metric and a site of interaction involving the calcium ion channel. FEBS Letters, 301, 53–59.

    Article  PubMed  CAS  Google Scholar 

  51. Greene, J. J., Skowronski, W. J., Mullins, J. J., Nardone, R. M., Penafiel, M., & Meister, R. (1991). Delineation of electric and magnetic field effects of extremely low frequency electromagnetic radiation on transcription. Biochemical and Biophysical Research Communications, 174, 742–749.

    Article  PubMed  CAS  Google Scholar 

  52. Panagopoulos, D. J., Messini, N., Karabarbounis, A., Filippetis, A. L., & Margaritis, L. H. (2000). A mechanism for action of oscillating electric fields on cells. Biochemical and Biophysical Research Communications, 272(3), 634–640.

    Article  PubMed  CAS  Google Scholar 

  53. Panagopoulos, D. J., Karabarbounis, A., & Margaritis, L. H. (2002). Mechanism for action of electromagnetic fields on cells. Biochemical and Biophysical Research Communications, 298(1), 95–102.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The study was supported by the Special Account for Research Grants of the University of Athens. We wish to thank Evangelia D. Chavdoula and Evangelia Pasiou for laboratory assistance.

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Correspondence to Dimitris J. Panagopoulos.

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Panagopoulos, D.J., Karabarbounis, A. & Lioliousis, C. ELF Alternating Magnetic Field Decreases Reproduction by DNA Damage Induction. Cell Biochem Biophys 67, 703–716 (2013). https://doi.org/10.1007/s12013-013-9560-5

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