Abstract
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
WHO (1984). Extremely low frequency (ELF) fields, Geneva.
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.
Lioliousis, C. (1997). Biological effects of electromagnetic radiation. Athens: Diavlos Books.
Wertheimer, N., & Leeper, E. (1979). Electrical wiring configurations and childhood cancer. American Journal of Epidemiology, 109, 273–284.
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.
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.
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.
Feychting, M., & Ahlbom, A. (1995). Childhood leukemia and residential exposure to weak extremely low frequency magnetic fields. Environ Health Perspect, suppl, 2, 59–62.
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.
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.
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.
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.
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.
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.
ICNIRP. (1998). Guidelines for limiting exposure to time-varying electric, magnetic and electromagnetic fields (up to 300 GHz). Health Physics, 74, 494–522.
IRPA. (1990). Interim guidelines on limits of exposure to 50/60 Hz electric and magnetic fields. Health Physics, 58(1), 113–122.
Dubrov, A. P. (1978). The geomagnetic field and life: Geomagnetobiology. New York: Plenum Press.
Presman, A. S. (1977). Electromagnetic fields and life. New York: Plenum Press.
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.
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.
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.
Delgado, J. M. R. (1985). Biological effects of extremely low frequency electromagnetic fields. Journal of Bioelectricity, 4(1), 75–91.
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.
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.
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.
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.
Kikuchi, T., Ogawa, M., Otaka, Y., & Furuta, M. (1998). Multigeneration exposure test of Drosophila melanogaster to ELF magnetic fields. Bioelectromagnetics, 19(6), 335–340.
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.
Mirabolghasemi, G., & Azarnia, M. (2002). Developmental changes in Drosophila melanogaster following exposure to alternating electromagnetic fields. Bioelectromagnetics., 23(6), 416–420.
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.
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.
Mitler, S. (1974) Low frequency electromagnetic radiation and genetic aberrations in Drosophila melanogaster. Genetics, 73–74, Suppl 183.
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.
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.
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.
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.
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.
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.
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.
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.
Panagopoulos, D. J. (2012). Effect of microwave exposure on the ovarian development of Drosophila melanogaster. Cell Biochemistry and Biophysics, 63, 121–132.
King, R. C. (1970). Ovarian development in Drosophila Melanogaster. New York: Academic Press.
McCall, K. (2004). Eggs over easy: Cell death in the Drosophila ovary. Developmental Biology, 274(1), 3–14.
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.
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.
Weiss, N. A. (1995) Introductory statistics. Addison-Wesley Publ. Co. Inc.
Maber, J. (1999). Data analysis for biomolecular sciences. England: Longman.
Drummond-Barbosa, D., & Spradling, A. C. (2001). Stem cells and their progeny respond to nutritional changes during Drosophila oogenesis. Dev. Biol., 231, 265–278.
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.
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.
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.
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.
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.
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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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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DOI: https://doi.org/10.1007/s12013-013-9560-5