2.45 GHz microwave irradiation-induced oxidative stress affects implantation or pregnancy in mice, mus musculus

Applied Biochemistry and Biotechnology

Volumn 169, Issue 5, 2013, Pages 1727-1751

  Shahin, Saba ^a   Singh, Vineet Prakash ^a   Shukla, Ritesh K ^b   Dhawan, Alok ^b   Gangwar, Ravi Kumar ^c   Singh, Surya Pal ^c   Chaturvedi, Chandra Mohini ^a  

^a BANARAS HINDU UNIVERSITY   (India)

^b CSIR INDIAN INSTITUTE OF TOXICOLOGY RESEARCH   (India)

^c BANARAS HINDU UNIVERSITY   (India)

Author keywords

Antioxidant enzyme activity; Implantation failure; Microwave radiation; Nitric oxide; Reactive oxygen species (ROS)

Indexed keywords

ANTIOXIDANT ENZYME ACTIVITY; IMPLANTATION SITES; POWER DENSITIES; RADIATION-INDUCED; REACTIVE OXYGEN SPECIES; SPECIFIC ABSORPTION RATE; STRESS PARAMETER; SUPER OXIDE DISMUTASE;

ANTIOXIDANTS; ENZYME ACTIVITY; HEMOGLOBIN; IRRADIATION; MICROWAVE IRRADIATION; MICROWAVES; NITRIC OXIDE; OBSTETRICS; OXIDATIVE STRESS; OXYGEN;

MAMMALS;

ANTIOXIDANT; CATALASE; ESTRADIOL; GLUTATHIONE PEROXIDASE; HEMOGLOBIN; NITRIC OXIDE; PROGESTERONE; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; COMET ASSAY; CONTROLLED STUDY; DNA DAMAGE; DNA STRAND BREAKAGE; ENZYME ACTIVITY; ENZYME IMMUNOASSAY; ERYTHROCYTE COUNT; ESTRADIOL BLOOD LEVEL; FEMALE; KIDNEY; LEUKOCYTE COUNT; LIVER; LYMPHOCYTE COUNT; MICROWAVE IRRADIATION; MOUSE; NATIVE POLYACRYLAMIDE GEL ELECTROPHORESIS; NEUTROPHIL COUNT; NIDATION; NONHUMAN; OVARY; OXIDATIVE STRESS; PREGNANCY; PREGNANCY DISORDER; PROGESTERONE BLOOD LEVEL; RADIATION ABSORPTION; RADIATION EXPOSURE; UTERUS HORN; ANIMAL; BLOOD; BRAIN; BREEDING; ENZYMOLOGY; LIPID PEROXIDATION; METABOLISM; MICROWAVE RADIATION;

MUS; MUS MUSCULUS;

ANIMALS; BRAIN; CATALASE; COMET ASSAY; DNA DAMAGE; EMBRYO IMPLANTATION; ESTRADIOL; FEMALE; GLUTATHIONE PEROXIDASE; KIDNEY; LIPID PEROXIDATION; LIVER; MICE; MICROWAVES; OVARY; OXIDATIVE STRESS; PREGNANCY; PREGNANCY, ANIMAL; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE;

EID: 84882252317     PISSN: 02732289     EISSN: 15590291     Source Type: Journal    
DOI: 10.1007/s12010-012-0079-9     Document Type: Article

References (89)

1. Stuchley, M. A. (1988). Biological effects of radiofrequency fields. In: M.H. Repacholi (Ed.) Non-ionizing radiations, physical characterization, biological effects and health hazard assessment. Proceedings for the International Non-Ionizing Radiation workshop, Melbourne, 197-217.
2. Lai, H., Carino, M. A., Horita, A., & Guy, A. W. (1993). Effects of a 60 Hz magnetic field on central cholinergic system of the rat. Bioelectromagnetics, 14, 5-15.
3. Lokhmatova, S. A. (1994). The effect of low-intensity prolonged impulse electromagnetic irradiation in the UHF range on the testis and the appendages of the testis in rats. Radiation Biology and Radioecology, 34, 279-285.
4. Akdag, M. Z., Celik, M. S., Ketani, A., Nergiz, Y., Deniz, M., & Dsadag, S. (1999). Effect of chronic low intensity microwave radiation on sperm count, sperm morphology and testicular and epididymal tissues of rat. Electro- and Magnetobiology, 18, 133-145.
5. Hardell, L., Mild, K. H., & Carlberg, M. (2003). Further aspects on cellular and cordless telephones and brain tumours. International Journal of Oncology, 22, 399-407.
6. Heynick, L. N., Johnston, S. A., Patrick, A., & Mason, P. A. (2003). Radio frequency electromagnetic fields: cancer, mutagenesis, and genotoxicity. Bioelectromagnetics, 24, s74-s100.
7. Paulraj, R., & Behari, J. (2004). Radiofrequency radiation effect on protein kinase C activity in rats' brain. Mutation Research, 545, 127-130.
8. Agarwal, A., Deepinder, F., Sharma, R. K., Ranga, G., & Li, J. (2008). Effect of cell phone usage on semen analysis in men attending infertility clinic: an observational study. Fertility and Sterility, 89, 124-128.
9. Cleveland, R. F., & Ulcek, J. L. (1999). Questions and answers about biological effects and potential hazards of radiofrequency electromagnetic fields. OET Bulletin, 56, 1-36.
10. Fukui, Y., Hoshino, K., Inouye, M., & Kameyama, Y. (1992). Effects of hyperthermia induced by the microwave irradiation on the brain development in mice. Journal of Radiation Research, 33, 1-10.
11. Paulraj, R., & Behari, J. (2006). Single strand DNA breaks in rat brain cells exposed to microwave radiation. Mutation Research/Fundamental and Molecular Mutagenesis, 596, 76-80.
12. Kesari, K. K., Behari, J., & Kumar, S. (2010). Mutagenic response of 2.45 GHz radiation exposure on rat brain. International Journal of Radiation Biology, 86(4), 334-343.
13. Saunders, R. D., & Kowalczuk, C. I. (1981). Effects of 2.45 GHz microwave radiation and heat on mouse spermatogenic epithelium. International Journal of Radiation Biology, 40(6), 623-632.
14. Kim, J. Y., Kim, H. T., Moon, K. H., & Shin, H. J. (2007). Long-term exposure of rats to a 2.45 GHz electromagnetic field: effects on reproductive function. Korean Journal of Urology, 48(12), 1308-1314.
15. Kesari, K. K., & Behari, J. (2010). Effects of microwave at 2.45 GHz radiations on reproductive system of male rats. Toxicological and Environmental Chemistry, 92(6), 1135-1147.
16. Galvin, M. J., MacNichols, G. L., & McRee, D. I. (1984). Effect of 2450 MHz microwave radiation on haematopoiesis of pregnant mice. Radiation Research, 100, 412-417.
17. Trosic, I., & Busljeta, I. (2005). Frequency of micronucleated erythrocytes in rat bone marrow exposed to 2.4 5GHz radiation. Physica Scripta, T118, 168-170.
18. World Health Organization (2011). World Health Organization/International Agency for Research on Cancer classifies radiofrequency electromagnetic fields as possibly carcinogenic to humans. 31 May.ScienceDaily. http://www. sciencedaily.com
19. Luria, R., Eliyahu, I., Hareuveny, R., Margaliot, M., & Meiran, N. (2009). Cognitive effects of radiation emitted by cellular phones: the influence of exposure side and time. Bioelectromagnetics, 3, 198-204.
20. Hardell, L., Carlberg, M., & Hansson, M. K. (2009). Epidemiological evidence for an association between use of wireless phones and tumor diseases. Pathophysiology, 16, 113-122.
21. Hardell, L., Carlberg, M., & Hansson, M. K. (2011). Pooled analysis of case-control studies on malignant brain tumours and the use of mobile and cordless phones including living and deceased subjects. International Journal of Oncology, 38(5), 1465-1474.
22. Pryor, W. A., Houk, K. N., Foote, C. S., Fukuto, J. M., Ignarro, L. J., Squadrito, G. H., et al. (2006). Free radical biology and medicine: it's a gas, man! American Journal of Physiology - Regulatory, Integrative and Comparative Physiology, 291, R491-R511.
23. Eriksson, U. J. (1999). Oxidative DNA damage and embryo development. Nature Medicine, 5, 715.
24. Baker, M. A., & Aitken, R. J. (2005). Reactive oxygen species in spermatozoa: methods for monitoring and significance for the origins of genetic disease and infertility. Reproductive Biology and Endocrinology, 3, 67.
25. Palacio, J. R., Iborra, A., Ulcova-Gallova, Z., Badia, R., & Martinez, P. (2006). The presence of antibodies to oxidative modified proteins in serum from polycystic ovary syndrome patients. Clinical and Experimental Immunology, 144, 217-222.
26. Liu, H., Zhang, C., & Zeng, W. (2006). Estrogenic and antioxidant effects of a phytoestrogen daidzein on ovarian germ cells in embryonic chickens. Domestic Animal Endocrinology, 31, 258-268.
27. Takahashi, T., Takahashi, E., Igarashi, H., Tezuka, N., & Kurachi, H. (2003). Impact of oxidative stress in aged mouse oocytes on calcium oscillations at fertilization. Molecular Reproduction and Development, 66, 143-152.
28. Kodaman, P. H., & Behrman, H. R. (2001). Endocrine-regulated and protein kinase C-dependent generation of superoxide by rat preovulatory follicles. Endocrinology, 142, 687-693.
29. Dincer, Y., Akcay, T., Erdem, T., Saygili, I. E., & Gundogdu, S. (2005). DNA damage, DNA susceptibility to oxidation and glutathione level in women with polycystic ovary syndrome. Scandinavian Journal of Clinical and Laboratory Investigation, 65, 721-728.
30. Guerin, P. E., Mouatassim, S., & Menezo, Y. (2001). Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Human Reproduction Update, 7, 175-189.
31. Conrad, K. P., Joffe, G. M., Kruszyna, H., et al. (1993). Identification of increased nitric oxide biosynthesis during pregnancy in rats. The FASEB Journal, 7, 566-571.
32. Beckman, J. S., & Crow, J. P. (1993). Pathological implications of nitric oxide, superoxide and peroxynitrite formation. Biochemical Society Transactions, 21, 330-334.
33. Davies, M. G., Fulton, G. J., & Hagen, P. O. (1995). Clinical biology of nitric oxide. British Journal of Surgery, 82, 1598-1610.
34. Akaike, T., Suga, M., & Maeda, H. (1998). Free radicals in viral pathogenesis: molecular mechanisms involving superoxide and NO. Proceedings of the Society for Experimental Biology and Medicine, 217, 64-73.
35. Turko, I. V., & Murad, F. (2002). Protein nitration in cardiovascular diseases. Pharmacological Reviews, 54, 619-634.
36. Kelly, R. A., Balligand, J. L., & Smith, T. N. (1996). Nitric oxide and cardiac function. Circulation Research, 79, 363-380.
37. Cameron, I. T., & Campbell, S. (1998). Nitric oxide in the endometrium. Human Reproduction Update, 4, 565-569.
38. Rollwitz, J., Lupke, M., & Simko, M. (2004). Fifty-hertz magnetic fields induce free radical formation in mouse bone marrow-derived promonocytes and macrophages [J]. Biochimica et Biophysica Acta, 1674(3), 231-238.
39. Ciejka, E., Kleniewska, P., Skibska, B., & Goraca, A. (2011). Effects of extremely low frequency magnetic field on oxidative balance in brain of rats. Journal of Physiology and Pharmacology, 62(6), 657-661.
40. Rugh, R., Ginns, E. I., Ho, H. S., & Leachw, M. (1975). Responses of the mouse to microwave radiation during estrous cycle and pregnancy. Radiation Research, 62, 225-241.
41. Nawrot, P. S., McRee, D. I., & Staples, R. E. (1981). Effects of 2.45 GHz CW microwave radiation on embryofetal development in mice. Teratology, 24(3), 303-314.
42. Nakamura, H., Matsuzaki, I., Hatta, K., Nobukuni, Y., Kambayashi, Y., & Ogino, K. (2003). Nonthermal effects of mobile-phone frequency microwaves on uteroplacental functions in pregnant rats. Reproductive Toxicology, 17, 321-326.
43. Inouye, M., Galvin, M. J., McRee, D. I., & Matsumoto, N. (1982). Lack of effect of 2.45-GHz microwave radiation on the development of preimplantation embryos of mice. Bioelectromagnetics, 3, 275-283.
44. Jensh, R. P., Weinberg, I., & Brent, R. L. (1983). An evaluation of the teratogenic potential of protracted exposure of pregnant rats to 2450-MHz microwave radiation: I. Morphologic analysis at term. Journal of Toxicology and Environmental Health, 11, 23-35.
45. Sambucci, M., Laudisi, F., Nasta, F., Pinto, R., Lodato, R., Altavista, P., et al. (2010). Prenatal exposure to non-ionizing radiation: effects of WiFi signals on pregnancy outcome, peripheral B-cell compartment and antibody production. Radiation Research, 174, 732-740.
46. Singh, V. P., Singh, P., Shukla, R. K., Dhawan, A., Gangwar, R. K., Singh, S. P., et al. (2009). 2.45 GHz low level CW microwave radiation affects embryo implantation sites and single strand DNA damage in brain cell of mice, Mus musculus. In: Proceedings of 2009 International Conference on Emerging Trends in Electronic and Photonic Devices & Systems (ELECTRO-2009) from IEEE Explore, 22-24 pp 379-382.
47. Chaturvedi, C. M., Singh, V. P., Singh, P., Basu, P., Singaravel, M., Shukla, R. K., et al. (2011). 2.45 GHz (CW) Microwave irradiation alters circadian organization, spatial memory, DNA structure in the brain cells and blood cell counts of male mice, Mus musculus. Progress in Electromagnetics Research B, 29, 23-42.
48. Hartmann, A., Agurell, E., Beevers, C., Brendler-Schwaab, S., Burlinson, B., Clay, P., et al. (2003). Recommendations for conducting the in vivo alkaline Comet assay. Mutagenesis, 18, 45-51.
49. Patel, S., Pandey, A. K., Bajpayee, M., Parmar, D., & Dhawan, A. (2006). Cypermethrin-induced DNA damage in organs and tissues of themouse: evidence fromthe comet assay. Mutation Research, 607, 176-183.
50. Singh, N. P., McCoy, M. T., Tice, R. R., & Schneider, E. L. (1988). A simple technique for quantitation of low levels of DNA damage in individual cells. Experimental Cell Research, 175, 184-191.
51. Sastry, K. V., Moudgal, R. P., Mohan, J., Tyagi, J. S., & Rao, G. S. (2002). Spectrophotometric determination of serum nitrite and nitrate by copper. Analytical Biochemistry, 306, 79-82.
52. Bejma, J., Ramires, P., & Ji, L. L. (2000). Free radical generation and oxidative stress with ageing and exercise: differential effects in the myocardium and liver. Acta Physiologica Scandinavica, 169, 343-351.
53. Das, K., Samanta, L., & Chainy, G. B. N. (2000). A modified spectrophotometric assay of superoxide dismutase using nitrite formation by superoxide radicals. Indian Journal of Biochemistry & Biophysics, 37, 201-204.
54. Aebi, H. (1984). Catalase in vitro. Methods in Enzymology, 105, 121.
55. Mantha, S. V., Prasad, M., Kalra, J., & Prasad, K. (1993). Atherosclerosis, 101, 135-144.
56. Beauchamp, C., & Fridovich, I. (1971). Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Analytical Biochemistry, 44, 276-287.
57. Sun, Y., Elwell, J. H., & Oberley, L. W. (1988). A simultaneous visualization of the antioxidant enzymes glutathione peroxidase and catalase on polyacrylamide gels. Free Radical Research Communications, 5, 67-75.
58. Lin, C. L., Chen, H. J., & Hou, W. C. (2002). Activity staining of glutathione peroxidase after electrophoresis on native and sodium dodecylsulfate polyacrylamide gels. Electrophoresis, 23, 513-516.
59. Lee, G. M., Neutra, R. R., Hristova, L., Yost, M., & Hiatt, R. A. (2002). A nested case-control study of residential and personal magnetic field measures and miscarriages. Epidemiology, 13(1), 21-31.
60. Li, D. K., Odouli, R., Wi, S., Janevic, T., Golditch, I., Bracken, T. D., et al. (2002). A population-based prospective cohort study of personal exposure to magnetic fields during pregnancy and the risk of miscarriage. Epidemiology, 13(1), 9-20.
61. Ouellet-Hellstrom, R., & Stewart, W. F. (1993). Miscarriages among female physical therapists who report using radio- and microwave-frequency electromagnetic radiation. American Journal of Epidemiology, 138(10), 775-786.
62. Frahm, J., Mattsson, M. O., & Simko, M. (2010). Exposure to ELF magnetic fields modulates redox related protein expression in mouse macrophages. Toxicology Letters, 192, 330-336.
63. Lai, H., & Singh, N. P. (1996). Single- and double-strand DNA breaks in rat brain cells after acute exposure to radiofrequency electromagnetic radiation. International Journal of Radiation Biology, 69, 513-521.
64. Regoli, F., Gorbi, S., Machelle, N., Tedesco, S., Benedetti, M., Bocchetti, R., et al. (2005). Prooxidant effects of extremely low frequency electromagnetic fields in the land snail Helix aspersa. Free Radical Biology & Medicine, 39, 1620.
65. Agarwal, A., Gupta, S., & Sharma, R. K. (2005). Role of oxidative stress in female reproduction. Reproductive Biology and Endocrinology, 3, 28.
66. Mouatassim, S. E., Guerin, P., & Menezo, Y. (1999). Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Molecular Human Reproduction, 5, 720-725.
67. Carbone, M. C., Tatone, C., DelleMonache, S., Marci, R., Caserta, D., Colonna, R., et al. (2003). Antioxidant enzymatic defences in human follicular fluid: characterization and age-dependent changes. Molecular Human Reproduction, 9, 639-643.
68. Stone, J. R., & Yang, S. (2006). Hydrogen peroxide: a signaling messenger. Antioxidants & Redox Signaling, 8, 243-270.
69. Passos, J. F., Saretzki, G., Ahmed, S., Nelson, G., Richter, T., Peters, H., et al. (2007). Mitochondrial dysfunction accounts for the stochastic heterogeneity in telomere-dependent senescence. PLoS Biology, 5, 110.
70. Yang, H. W., Hwang, K. J., Kwon, H. C., Kim, H. S., Choi, K. W., & Oh, K. S. (1998). Detection of reactive oxygen species (ROS) and apoptosis in human fragmented embryos. Human Reproduction, 13, 998-1002.
71. Cook, J. P., & Tsao, P. S. (1993). Cytoprotective effects of nitric oxide. Circulation, 88, 2451-2454.
72. Gardner, D. K., & Lane, M. (1996). Alleviation of the '2-cell block' and development to the blastocyst of CF1 mouse embryos: role of amino acids, EDTA and physical parameters. Human Reproduction, 11, 2703-2712.
73. Van Soom, A., Yuan, Y. Q., Peelman, L. J., de Matos, D. G., Dewulf, J., Laevens, H., et al. (2002). Prevalence of apoptosis and inner cell allocation in bovine embryos cultured under different oxygen tensions with or without cysteine addition. Theriogenology, 57, 1453-1465.
74. Khurana, N. K., & Wales, R. G. (1989). Effects of oxygen concentration on the metabolism of [U-14C] glucose by mouse morulae and early blastocysts in vitro. Reproduction, Fertility, and Development, 1, 99-106.
75. Du, Z. F., & Wales, R. G. (1993). Glycolysis and glucose oxidation by the sheep conceptus at different oxygen concentrations. Reproduction, Fertility, and Development, 5, 383-393.
76. Choi, J. W., Im, M. W., Pai, S. H. (2002). Nitric oxide production increases during normal pregnancy and decreases in preeclampsia. Annals of Clinical & Laboratory Science, 32(3).
77. Yang, D., Lang, U., Greenberg, S. G., Myatt, L., & Clark, K. E. (1996). Elevation of nitrate levels in pregnant ewes and their fetuses. American Journal of Obstetrics and Gynecology, 174, 573-577.
78. Gray, R. H., & Becker, S. (2000). Selected topics in the epidemiology of reproductive outcomes. Epidemiologic Reviews, 22, 71-75.
79. Tarin, J. J. (1995). Aetiology of age-associated aneuploidy: a mechanism based on the 'free radical theory of ageing'. Molecular Human Reproduction, 10, 1563-1565.
80. Porter, T. F., & Scott, J. R. (2005). Evidence-based care of recurrent miscarriage. Best Practice & Research. Clinical Obstetrics & Gynaecology, 19, 85-101.
81. Diskin, M. G., & Morris, D. G. (2008). Embryonic and early foetal losses in cattle and other ruminants. Reproduction in Domestic Animals, 43(Suppl. 2), 260-267.
82. Harman, D. (1988). Free radical theory of aging: an update: increasing the functional life span. Annals of the New York Academy of Sciences, 1067, 10-21.
83. Jenkins, C.,Wilson, R., Roberts, J., Miller, H., McKillop, J. H., &Walker, J. J. (2000). Antioxidants: their role in pregnancy and miscarriage. Antioxidants & Redox Signaling, 2, 623ox.
84. Alikani, M., Dale, B. (1995). Should fragmenting blastomeres stay together? Alpha, September 1-2.
85. Nasr-Esfahani, M. H., Aitken, J. R., & Johnson, M. H. (1990). Hydrogen peroxide levels in mouse oocytes and early cleavage stage embryos developed in vitro or in vivo. Development, 109, 501-507.
86. Nasr-Esfahani, M. H., & Johnson, M. H. (1992). Quantitative analysis of cellular glutathione in early preimplantation mouse embryos developing in vivo and in vitro. Human Reproduction, 7, 1281-1290.
87. Orsi, N. M., & Leese, H. J. (2001). Protection against reactive oxygen species during mouse preimplantation embryo development: role of EDTA, oxygen tension, catalase, superoxide dismutase and pyruvate. Molecular Reproduction and Development, 59, 44-53.
88. Fröhlich, H. (1981). The biological effects of microwaves and related questions. Advances in Electronics and Electron Physics, 53, 85-152.
89. Lerner, E. J. (Contributing Editor) (1984). Biological effects of electromagnetic fields. IEEE spectrum, 57-69.