Effect of 935-MHz phone-simulating electromagnetic radiation on endometrial glandular cells during mouse embryo implantation

  • Wenhui Liu (刘文惠)
  • Xinmin Zheng (郑新民)Email author
  • Zaiqing Qu (屈在卿)
  • Ming Zhang (张 铭)
  • Chun Zhou (周 春)
  • Ling Ma (马 玲)
  • Yuanzhen Zhang (张元珍)


This study examined the impact of 935MHz phone-simulating electromagnetic radiation on embryo implantation of pregnant mice. Each 7-week-old Kunming (KM) female white mouse was set up with a KM male mouse in a single cage for mating overnight after induction of ovulation. In the first three days of pregnancy, the pregnant mice was exposed to electromagnetic radiation at low-intensity (150 μW/cm2, ranging from 130 to 200 μW/cm2, for 2- or 4-h exposure every day), mid-intensity (570 μW/cm2, ranging from 400 to 700 μW/cm2, for 2- or 4-h exposure every day) or high-intensity (1400 μW/cm2, ranging from 1200 to 1500 μW/cm2, for 2- or 4-h exposure every day), respectively. On the day 4 after gestation (known as the window of murine embryo implantation), the endometrium was collected and the suspension of endometrial glandular cells was made. Laser scanning microscopy was employed to detect the mitochondrial membrane potential and intracellular calcium ion concentration. In high-intensity, 2- and 4-h groups, mitochondrial membrane potential of endometrial glandular cells was significantly lower than that in the normal control group (P<0.05). The calcium ion concentration was increased in low-intensity 2-h group but decreased in high-intensity 4-h group as compared with the normal control group (P<0.05). However, no significant difference was found in mitochondrial membrane potential of endometrial glandular cells between low- or mid-intensity groups and the normal control group, indicating stronger intensity of the electromagnetic radiation and longer length of the radiation are required to inflict a remarkable functional and structural damage to mitochondrial membrane. Our data demonstrated that electromagnetic radiation with a 935-MHz phone for 4 h conspicuously decreased mitochondrial membrane potential and lowered the calcium ion concentration of endometrial glandular cells. It is suggested that high-intensity electromagnetic radiation is very likely to induce the death of embryonic cells and decrease the chance of their implantation, thereby posing a high risk to pregnancy.

Key words

electromagnetic radiation pregnant mouse embryo implantation mitochondrial membrane potential calcium ion concentration 


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  1. 1.
    Baan R, Gross Y, Lauby-Secretan B, et al. Carcinogenicity of radiofrequency electromagnetic fields. Lancet Oncol, 2011,12(7):624–626PubMedCrossRefGoogle Scholar
  2. 2.
    Merhi ZO. Challenging cell phone impact on reproduction: A review. J Assist Reprod Genet, 2012,29(4):293–297PubMedCrossRefGoogle Scholar
  3. 3.
    Batellier F, Couty I, Picard D, et al. Effects of exposing chicken eggs to a cell phone in “call” position over the entire incubation period. Theriogenology, 2008,69(6): 737–745PubMedCrossRefGoogle Scholar
  4. 4.
    Zareen N, Khan MY, Minhas LA. Dose related shifts in the developmental progress of chick embryos exposed to mobile phone induced electromagnetic fields. J Ayub Med Coll Abbottabad, 2009,21(1):130–134PubMedGoogle Scholar
  5. 5.
    Kesari KK, Behari J. Effects of microwave at 2.45 GHz radiations on reproductive system of male rats. Toxicol Environ Chem, 2010,92(6): 1135–1147CrossRefGoogle Scholar
  6. 6.
    Gutschi T, Mohamad Al-Ali B, Shamloul R, et al. Impact of cell phone use on men’s semen parameters. Andrologia, 2011,43(5): 312–316PubMedCrossRefGoogle Scholar
  7. 7.
    Otitoloju AA, Obe IA, Adewale OA, et al. Preliminary study on the induction of sperm head abnormalities in mice, Mus musculus, exposed to radiofrequency radiations from global system for mobile communication base stations. Bull Environ Contam Toxicol, 2010,84(1): 51–54PubMedCrossRefGoogle Scholar
  8. 8.
    Pilger A, Ivancsits S, Diem E, et al. No effects of intermittent 50 Hz EMF on cytoplasmic free calcium and on the mitochondrial membrane potential in human diploid fibroblasts. Radiat Environ Biophys, 2004,43(3): 203–207PubMedCrossRefGoogle Scholar
  9. 9.
    Imai N, Kawabe M, Hikage T, et al. Effects on rat testis of 1.95-GHz W-CDMA for IMT-2000 cellular phones. Syst Biol Reprod Med, 2011,57(4):204–209PubMedCrossRefGoogle Scholar
  10. 10.
    Falzone N, Huyser C, Franken DR, et al. Mobile phone radiation does not induce pro-apoptosis effects in human spermatozoa. Radiat Res, 2010,174(2):169–176PubMedCrossRefGoogle Scholar
  11. 11.
    Kadenbach B, Arnold S, Lee I, et al. The possible role of cytochrome c oxidase in stress-induced apoptosis and degenerative diseases. J Biochim Biophys Acta-Bioenerg, 2004,1655(1–3):400–408CrossRefGoogle Scholar
  12. 12.
    Breckenridge DG, Stojanovic M, Marcellus RC, et al. Caspase cleavage product of BAP31 induces mitochondrial fission through endoplasmic reticulum calcium signals, enhancing cytochrome c release to the cytosol. J Cell Biol, 2003,160(7):1115–1127PubMedCrossRefGoogle Scholar
  13. 13.
    Oral B, Guney M, Ozguner F, et al. Endometrial apoptosis induced by a 900-MHz mobile phone: preventive effects of vitamins E and C. Adv Ther, 2006,23(6):957–973PubMedCrossRefGoogle Scholar
  14. 14.
    Paulraj R, Behari J. The effect of low level continuous 2.45 GHz waves on enzymes of developing rat brain. Electromagn Biol Med, 2002,21(3): 221–231CrossRefGoogle Scholar
  15. 15.
    Paulraj R, Behari J, Rao AR. Effect of amplitude modulated RF radiation on calcium ion efflux and ODC activity in chronically exposed rat brain. Indian J Biochem Biophys, 1999,36(5):337–340PubMedGoogle Scholar
  16. 16.
    Csordas G, Renken C, Varnai P, et al. Structural and functional features and significance of the physical linkage between ER and mitochondria. J Cell Biol, 2006,174(7):915–921PubMedCrossRefGoogle Scholar
  17. 17.
    De Brito OM, Scorrano L. Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature, 2008, 456(7222):605–610PubMedCrossRefGoogle Scholar
  18. 18.
    Hayashi T, Rizzuto R, Hajnoczky G, et al. MAM: more than just a housekeeper. Trends Cell Biol, 2009,19(2): 81–88PubMedCrossRefGoogle Scholar
  19. 19.
    Scorrano L, Oakes SA, Opferman JT, et al. BAX and BAK regulation of endoplasmic reticulum Ca2+: a control point for apoptosis. Science, 2003,300(5616): 135–139PubMedCrossRefGoogle Scholar
  20. 20.
    Walter L, Hajnoczky G. Mitochondria and endoplasmic reticulum: the lethal interorganelle cross-talk. J Bioenerg Biomembr, 2005,37(3):191–206PubMedCrossRefGoogle Scholar
  21. 21.
    Yang J, Zhang YZ, Liu WH. Effect of 935 MHz microwave electromagnetic fields on meiotic maturation of mouse oocytes. Med J Wuhan Univer (Chinese), 2008,29(4):519–523Google Scholar
  22. 22.
    Yang J, Zhang YZ, Liu WH. Effect of 935 MHz microwave electromagnetic fields on the embryo implantation of mouse. Reprod Contracept (Chinese), 2008,28(2):80–83Google Scholar
  23. 23.
    Perry SW, Norman JP, Barbieri J, et al. Mitochondrial membrane potential probes and the proton gradient: a practical usage guide. Biotechniques, 2011,50(2):98–102PubMedCrossRefGoogle Scholar
  24. 24.
    Susa M, Pavicic’ I. Effects of radiofrequency electromagnetic fields on mammalian spermatogenesis. Arh Hig Rada Toksikol, 2007,58(4):449–459PubMedCrossRefGoogle Scholar
  25. 25.
    Aitken RJ, Bennetts LE, Sawyer D, et al. Impact of radio frequency electromagnetic radiation on DNA integrity in the male germline. Int J Androl, 2005,28(3):171–179PubMedCrossRefGoogle Scholar
  26. 26.
    Falzone N, Huyser C, Fourie F, et al. In vitro effect of pulsed 900MHz GSM radiation on mitochondrial membrane potential and motility of human spermatozoa. Bioelectromagnetics, 2008,29(4):268–276PubMedCrossRefGoogle Scholar
  27. 27.
    Zhao TY, Zou SP, Knapp PE. Exposure to cell phone radiation up-regulates apoptosis genes in primary cultures of neurons and astrocytes. J Neurosci lett, 2007,412(1): 34–38CrossRefGoogle Scholar
  28. 28.
    Zhang H, Zhang J, Chen Y, et al. Influence of intracellular Ca2+, mitochondria membrane potential, reactive oxygen species, and intracellular ATP on the mechanism of microcystin-LR induced apoptosis in Carassius auratus lymphocytes in vitro. Environ Toxicol, 2007,22(6): 559–564PubMedCrossRefGoogle Scholar
  29. 29.
    Carafoli E. Calcium-a universal carrier of biological signals. FEBS J, 2005,272(5):1073–1089PubMedCrossRefGoogle Scholar
  30. 30.
    Amat A, Rigau J, Waynant RW, et al. The electric field induced by light can explain cellular responses to electromagnetic energy: A hypothesis of mechanism. J Photochem Photobiol B, 2006,82(2):152–160PubMedCrossRefGoogle Scholar
  31. 31.
    Xia HJ, Yang G. Inositol 1, 4, 5-trisphosphate 3-kinases: functions and regulations. Cell Res, 2005,15(2):83–91PubMedCrossRefGoogle Scholar
  32. 32.
    Qin YH, Li TD, Sheng H. Protective effect of naloxone on mitochondrial membranal potential of hypoxic myocardial cells and apoptosis. J Clin Rehabil Tissue Engineering Res (Chinese), 2007,11(8):1573–1576Google Scholar
  33. 33.
    Shi JH, Ju Q, Yin XP, et al. The effect of Hydrochloride small fold on intracellular free calcium and mitochondrial membrane potential of the base HaCaT. Chin J Dermatol (Chinese), 2005,38(2):105–107Google Scholar
  34. 34.
    Apáti A, Jánossy J, Brózik A, et al. Effects of Intracellular Calcium on Cell Survival and the MAPK Pathway in a Human Hormone-Dependent Leukemia Cell Line (TF-1). JAnn N Y Acad Sci, 2003,1010(1):70–73CrossRefGoogle Scholar
  35. 35.
    Rao VS, Titushkin IA, Moros EG, et al. Non-thermal effects of radiofrequency-field exposure on calcium dynamics in stem cell-derived neuronal cells: elucidation of calcium pathways. Radiat Res, 2008,169(3):319–329PubMedCrossRefGoogle Scholar
  36. 36.
    Zhao YL, Song JP, Yang YH, et al. Effect of microwave irradiation of different densities on Ca2+, Mg2+-ATPase activity of mouse brain. Chin J Aerospace Med, 2000,11(2): 101–104Google Scholar
  37. 37.
    Philippova TM, Novoselov VI, Alekseev SI. Influence of microwaves on different types of receptors and the role of peroxidation of lipids on receptor-protein shedding. Bioelectromagnetics, 1994,15(3):183–192PubMedCrossRefGoogle Scholar
  38. 38.
    Hossmann KA, Hermann DM. Effects of electromagnetic radiation of mobile phones on the central nervous system. Bioelectromagnetics, 2003,24(1):49–62PubMedCrossRefGoogle Scholar
  39. 39.
    Paulraj R, Behari J. Radio frequency radiation effects on protein kinase C activity in rats’ brain. Mutat Res, 2004,545(1–2):127–130PubMedGoogle Scholar
  40. 40.
    Bauréus KCL, Sommarin M, Persson BRR, et al. Interaction between weak low frequency magnetic fields and cell membranes. Bioelectromagnetics, 2003,24(6): 395–402CrossRefGoogle Scholar

Copyright information

© Huazhong University of Science and Technology and Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Wenhui Liu (刘文惠)
    • 1
  • Xinmin Zheng (郑新民)
    • 2
    Email author
  • Zaiqing Qu (屈在卿)
    • 3
  • Ming Zhang (张 铭)
    • 1
  • Chun Zhou (周 春)
    • 1
  • Ling Ma (马 玲)
    • 1
  • Yuanzhen Zhang (张元珍)
    • 1
  1. 1.Reproductive Medicine CenterWuhan UniversityWuhanChina
  2. 2.Department of Urological Medicine, Zhongnan HospitalWuhan UniversityWuhanChina
  3. 3.Department of Obstetrics and Gynecologythe First Hospital of Kunming University of Medical ScienceKunmingChina

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