Radiofrequency radiation at 2.856 GHz does not affect key cellular endpoints in neuron-like PC12 cells

References

• Adey, W. R., Byus, C. V., Cain, C. D., et al. (2000). Spontaneous and nitrosourea-induced primary tumors of the central nervous system in Fischer 344 rats exposed to frequency-modulated microwave fields. Cancer Res. 60:1857–1863.
   PubMed Web of Science ®Google Scholar
• Ammari, M., Lecomte, A., Sakly, M., et al. (2008). Exposure to GSM 900 MHz electromagnetic fields affects cerebral cytochrome c oxidase activity. Toxicology. 250:70–74. doi:10.1016/j.tox.2008.05.019.
   PubMed Web of Science ®Google Scholar
• Ballardin, M., Tusa, I., Fontana, N., et al. (2011). Non-thermal effects of 2.45 GHz microwaves on spindle assembly, mitotic cells and viability of Chinese hamster V-79 cells. Mutat. Res. 716:1–9. doi:10.1016/j.mrfmmm.2011.07.009.
   PubMed Web of Science ®Google Scholar
• Berridge, M. J., Bootman, M. D., Roderick, H. L. (2003). Calcium signalling: Dynamics, homeostasis and remodelling. Nat. Rev. Mol. Cell. Biol. 4:517–529. doi:10.1038/nrm1155.
   PubMed Web of Science ®Google Scholar
• Bhaskara, V. K., Mohanam, I., Rao, J. S., Mohanam, S. (2012). Intermittent hypoxia regulates stem-like characteristics and differentiation of neuroblastoma cells. PLoS One. 7:e30905. doi:10.1371/journal.pone.0030905.
   PubMed Web of Science ®Google Scholar
• Brzozek, C., Benke, K. K., Zeleke, B. M., et al. (2018). Radiofrequency Electromagnetic Radiation and Memory Performance: Sources of Uncertainty in Epidemiological Cohort Studies. Int. J. Environ. Res. Public Health. 15. doi:10.3390/ijerph15061188.
   Web of Science ®Google Scholar
• Celuch, M., Gwarek, W. K. (2007). Properties of the FDTD method relevant to the analysis of microwave power problems. J. Microw. Power Electromagn Energy. 41:62–80.
   PubMed Web of Science ®Google Scholar
• Chen, T. I., Chiu, H. W., Pan, Y. C., et al. (2014). Intermittent hypoxia-induced protein phosphatase 2A activation reduces PC12 cell proliferation and differentiation. J. Biomed. Sci. 21:46. doi:10.1186/1423-0127-21-46.
   PubMed Web of Science ®Google Scholar
• Curcio, G., Ferrara, M., Moroni, F., et al. (2005). Is the brain influenced by a phone call? An EEG study of resting wakefulness. Neurosci. Res. 53:265–270. doi:10.1016/j.neures.2005.07.003.
   PubMed Web of Science ®Google Scholar
• Curcio, G., Nardo, D., Perrucci, M. G., et al. (2012). Effects of mobile phone signals over BOLD response while performing a cognitive task. Clin. Neurophysiol. 123:129–136. doi:10.1016/j.clinph.2011.06.007.
   PubMed Web of Science ®Google Scholar
• D’Andrea, J. A., Chou, C. K., Johnston, S. A., Adair, E. R. (2003). Microwave effects on the nervous system. Bioelectromagnetics. Suppl 6:S107–147.
   PubMed Web of Science ®Google Scholar
• Das, K. P., Freudenrich, T. M., Mundy, W. R. (2004). Assessment of PC12 cell differentiation and neurite growth: A comparison of morphological and neurochemical measures. Neurotoxicol. Teratol. 26:397–406. doi:10.1016/j.ntt.2004.02.006.
   PubMed Web of Science ®Google Scholar
• Esmekaya, M. A., Seyhan, N., Omeroglu, S. (2010). Pulse modulated 900 MHz radiation induces hypothyroidism and apoptosis in thyroid cells: A light, electron microscopy and immunohistochemical study. Int. J. Radiat. Biol. 86:1106–1116. doi:10.3109/09553002.2010.502960.
   PubMed Web of Science ®Google Scholar
• Hardell, L. (2017). World Health Organization, radiofrequency radiation and health - a hard nut to crack (Review). Int. J. Oncol. 51:405–413. doi:10.3892/ijo.2017.4046.
   PubMed Web of Science ®Google Scholar
• Hsieh, C. H., Lee, C. H., Liang, J. A., et al. (2010). Cycling hypoxia increases U87 glioma cell radioresistance via ROS induced higher and long-term HIF-1 signal transduction activity. Oncol. Rep. 24:1629–1636.
   PubMed Web of Science ®Google Scholar
• IEEE. (2013). IEEE Std 1528-2013 IEEE Recommended Practice for Determining the Peak Spatial-Average Specific Absorption Rate (SAR) in the Human Head from Wireless Communications Devices: Measurement Techniques. IEEE: The Institute of Electrical and Electronics Engineers, Inc. 3 Park Avenue, NewYork, NY 10016-5997, USA.
   Google Scholar
• Inoue, S., Motoda, H., Koike, Y., et al. (2008). Microwave irradiation induces neurite outgrowth in PC12m3 cells via the p38 mitogen-activated protein kinase pathway. Neurosci. Lett. 432:35–39. doi:10.1016/j.neulet.2007.12.002.
   PubMed Web of Science ®Google Scholar
• Ivaschuk, O. I., Jones, R. A., Ishida-Jones, T., et al. (1997). Exposure of nerve growth factor-treated PC12 rat pheochromocytoma cells to a modulated radiofrequency field at 836.55 MHz: Effects on c-jun and c-fos expression. Bioelectromagnetics. 18:223–229.
   PubMed Web of Science ®Google Scholar
• Joubert, V., Leveque, P., Rametti, A., et al. (2006). Microwave exposure of neuronal cells in vitro: Study of apoptosis. Int. J. Radiat. Biol. 82:267–275. doi:10.1080/09553000600649232.
   PubMed Web of Science ®Google Scholar
• Kang, K. A., Lee, H. C., Lee, J. J., et al. (2014). Effects of combined radiofrequency radiation exposure on levels of reactive oxygen species in neuronal cells. J. Radiat. Res. 55:265–276. doi:10.1093/jrr/rrt116.
   PubMed Web of Science ®Google Scholar
• Kivrak, E. G., Yurt, K. K., Kaplan, A. A., et al. (2017). Effects of electromagnetic fields exposure on the antioxidant defense system. J. Microsc. Ultrastruct. 5:167–176. doi:10.1016/j.jmau.2017.07.003.
   PubMedGoogle Scholar
• Li, H. J., Peng, R. Y., Wang, C. Z., et al. (2015). Alterations of cognitive function and 5-HT system in rats after long term microwave exposure. Physiol. Behav. 140:236–246. doi:10.1016/j.physbeh.2014.12.039.
   PubMed Web of Science ®Google Scholar
• Lindenboim, L., Yuan, J., Stein, R. (2000). Bcl-xS and Bax induce different apoptotic pathways in PC12 cells. Oncogene. 19:1783–1793. doi:10.1038/sj.onc.1203495.
   PubMed Web of Science ®Google Scholar
• Manna, D., Ghosh, R. (2016). Effect of radiofrequency radiation in cultured mammalian cells: A review. Electromagn. Biol. Med. 35:265–301. doi:10.3109/15368378.2015.1092158.
   PubMed Web of Science ®Google Scholar
• Mantiply, E. D., Pohl, K. R., Poppell, S. W., Murphy, J. A. (1997). Summary of measured radiofrequency electric and magnetic fields (10 kHz to 30 GHz) in the general and work environment. Bioelectromagnetics. 18:563–577.
   PubMed Web of Science ®Google Scholar
• Marchionni, I., Paffi, A., Pellegrino, M., et al. (2006). Comparison between low-level 50 Hz and 900 MHz electromagnetic stimulation on single channel ionic currents and on firing frequency in dorsal root ganglion isolated neurons. Biochim. Biophys. Acta. 1758:597–605. doi:10.1016/j.bbamem.2006.03.014.
   PubMed Web of Science ®Google Scholar
• Maskey, D., Kim, M., Aryal, B., et al. (2010). Effect of 835 MHz radiofrequency radiation exposure on calcium binding proteins in the hippocampus of the mouse brain. Brain. Res. 1313:232–241. doi:10.1016/j.brainres.2009.11.079.
   PubMed Web of Science ®Google Scholar
• Morgan, L. L., Miller, A. B., Sasco, A., Davis, D. L. (2015). Mobile phone radiation causes brain tumors and should be classified as a probable human carcinogen (2A) (review). Int. J. Oncol. 46:1865–1871. doi:10.3892/ijo.2015.2908.
   PubMed Web of Science ®Google Scholar
• O’Connor, R. P., Madison, S. D., Leveque, P., et al. (2010). Exposure to GSM RF fields does not affect calcium homeostasis in human endothelial cells, rat pheocromocytoma cells or rat hippocampal neurons. PLoS One. 5:e11828. doi:10.1371/journal.pone.0011828.
   PubMed Web of Science ®Google Scholar
• Orendacova, J., Orendac, M., Racekova, E., Marsala, J. (2007). Neurobiological effects of microwave exposure: A review focused on morphological findings in experimental animals. Arch. Ital. Biol. 145:1–12.
   PubMed Web of Science ®Google Scholar
• Palumbo, R., Capasso, D. F., Mita, P., et al. (2010). Effects on apoptosis and reactive oxygen species formation by Jurkat cells exposed to 50 Hz electromagnetic fields. Bioelectromagnetics. 27:159–162. doi:10.1002/bem.20199.
   Google Scholar
• Qiao, S., Peng, R., Yan, H., et al. (2014). Reduction of phosphorylated synapsin I (ser-553) leads to spatial memory impairment by attenuating GABA release after microwave exposure in Wistar rats. PLoS One. 9:e95503. doi:10.1371/journal.pone.0095503.
   PubMed Web of Science ®Google Scholar
• Sastry, P. S., Rao, K. S. (2000). Apoptosis and the nervous system. J. Neurochem. 74:1–20.
   PubMed Web of Science ®Google Scholar
• Schuz, J., Waldemar, G., Olsen, J. H., Johansen, C. (2009). Risks for central nervous system diseases among mobile phone subscribers: A Danish retrospective cohort study. PLoS One. 4:e4389. doi:10.1371/journal.pone.0004389.
   PubMed Web of Science ®Google Scholar
• Shahin, S., Mishra, V., Singh, S. P., Chaturvedi, C. M. (2014). 2.45-GHz microwave irradiation adversely affects reproductive function in male mouse, Mus musculus by inducing oxidative and nitrosative stress. Free Radic. Res. 48:511–525. doi:10.3109/10715762.2014.888717.
   PubMed Web of Science ®Google Scholar
• Shirai, T., Kawabe, M., Ichihara, T., et al. (2005). Chronic exposure to a 1.439 GHz electromagnetic field used for cellular phones does not promote N-ethylnitrosourea induced central nervous system tumors in F344 rats. Bioelectromagnetics. 26:59–68. doi:10.1002/bem.20079.
   PubMed Web of Science ®Google Scholar
• Simko, M., Hartwig, C., Lantow, M., et al. (2006). Hsp70 expression and free radical release after exposure to non-thermal radio-frequency electromagnetic fields and ultrafine particles in human Mono Mac 6 cells. Toxicol. Lett. 161:73–82. doi:10.1016/j.toxlet.2005.08.005.
   PubMed Web of Science ®Google Scholar
• Simko, M., Remondini, D., Zeni, O., Scarfi, M. R. (2016). Quality Matters: Systematic Analysis of Endpoints Related to “Cellular Life” in Vitro Data of Radiofrequency Electromagnetic Field Exposure. Int. J. Environ. Res. Public Health. 13:7. doi:10.3390/ijerph13121252.
   Web of Science ®Google Scholar
• Song, X. L., Wang, C. H., Hu, H. Y., et al. (2011). Microwave induces apoptosis in A549 human lung carcinoma cell line. Chin. Med. J. (Engl). 124:1193–1198.
   PubMed Web of Science ®Google Scholar
• Tan, S., Wang, H., Xu, X., et al. (2017). Study on dose-dependent, frequency-dependent, and accumulative effects of 1.5 GHz and 2.856 GHz microwave on cognitive functions in Wistar rats. Sci. Rep. 7:10781. doi:10.1038/s41598-017-11420-9.
   PubMed Web of Science ®Google Scholar
• Valbonesi, P., Franzellitti, S., Bersani, F., et al. (2014). Effects of the exposure to intermittent 1.8 GHz radio frequency electromagnetic fields on HSP70 expression and MAPK signaling pathways in PC12 cells. Int. J. Radiat. Biol. 90:382–391. doi:10.3109/09553002.2014.892225.
   PubMed Web of Science ®Google Scholar
• Valbonesi, P., Franzellitti, S., Bersani, F., et al. (2016). Activity and expression of acetylcholinesterase in PC12 cells exposed to intermittent 1.8 GHz 217-GSM mobile phone signal. Int. J. Radiat. Biol. 92:1–10. doi:10.3109/09553002.2016.1114188.
   PubMed Web of Science ®Google Scholar
• Wang, C., Wang, X., Zhou, H., et al. (2015a). Effects of pulsed 2.856 GHz microwave exposure on BM-MSCs isolated from C57BL/6 mice. PLoS One. 10:e0117550. doi:10.1371/journal.pone.0117550.
   PubMed Web of Science ®Google Scholar
• Wang, C., Zhou, H., Peng, R., et al. (2013a). Electromagnetic pulse reduces free radical generation in rat liver mitochondria in vitro. Free Radic. Res. 47:276–282. doi:10.3109/10715762.2013.768342.
   PubMed Web of Science ®Google Scholar
• Wang, C., Zhou, H., Wang, L., et al. (2015b). Pulsed microwave exposure real time and dynamically reduces reactive oxygen species in rat pheochromocytoma cells in vivo. Microw. Opt. Techn. Let. 57:2395–2400. doi:10.1002/mop.29342.
   Web of Science ®Google Scholar
• Wang, H., Peng, R., Zhao, L., et al. (2015c). The relationship between NMDA receptors and microwave-induced learning and memory impairment: A long-term observation on Wistar rats. Int. J. Radiat. Biol. 91:262–269. doi:10.3109/09553002.2014.988893.
   PubMed Web of Science ®Google Scholar
• Wang, H., Peng, R., Zhou, H., et al. (2013b). Impairment of long-term potentiation induction is essential for the disruption of spatial memory after microwave exposure. Int. J. Radiat. Biol. 89:1100–1107. doi:10.3109/09553002.2013.817701.
   PubMed Web of Science ®Google Scholar
• Wang, L. F., Li, X., Gao, Y. B., et al. (2015d). Activation of VEGF/Flk-1-ERK Pathway Induced Blood-Brain Barrier Injury After Microwave Exposure. Mol. Neurobiol. 52:478–491. doi:10.1007/s12035-014-8848-9.
   PubMed Web of Science ®Google Scholar
• Watilliaux, A., Edeline, J. M., Leveque, P., et al. (2011). Effect of exposure to 1,800 MHz electromagnetic fields on heat shock proteins and glial cells in the brain of developing rats. Neurotox. Res. 20:109–119. doi:10.1007/s12640-010-9225-8.
   PubMed Web of Science ®Google Scholar
• Xu, S., Zhou, Z., Zhang, L., et al. (2010). Exposure to 1800 MHz radiofrequency radiation induces oxidative damage to mitochondrial DNA in primary cultured neurons. Brain. Res. 1311:189–196. doi:10.1016/j.brainres.2009.10.062.
   PubMed Web of Science ®Google Scholar
• Yakymenko, I., Tsybulin, O., Sidorik, E., et al. (2016). Oxidative mechanisms of biological activity of low-intensity radiofrequency radiation. Electromagn. Biol. Med. 35:186–202. doi:10.3109/15368378.2015.1043557.
   PubMed Web of Science ®Google Scholar
• Yoshizumi, M., Kogame, T., Suzaki, Y., et al. (2002). Ebselen attenuates oxidative stress-induced apoptosis via the inhibition of the c-Jun N-terminal kinase and activator protein-1 signalling pathway in PC12 cells. Br. J. Pharmacol. 136:1023–1032. doi:10.1038/sj.bjp.0704808.
   PubMed Web of Science ®Google Scholar
• Zeni, O., Di Pietro, R., d’Ambrosio, G., et al. (2007). Formation of reactive oxygen species in L929 cells after exposure to 900 MHz RF radiation with and without co-exposure to 3-chloro-4-(dichloromethyl)-5-hydroxy-2(5H)-furanone. Radiat. Res. 167:306–311. doi:10.1667/RR0595.1.
   PubMed Web of Science ®Google Scholar
• Zeni, O., Sannino, A., Sarti, M., et al. (2012). Radiofrequency radiation at 1950 MHz (UMTS) does not affect key cellular endpoints in neuron-like PC12 cells. Bioelectromagnetics. 33:497–507. doi:10.1002/bem.21712.
   PubMed Web of Science ®Google Scholar
• Zhang, J., Sumich, A., Wang, G. Y. (2017). Acute effects of radiofrequency electromagnetic field emitted by mobile phone on brain function. Bioelectromagnetics. 38:329–338. doi:10.1002/bem.22052.
   PubMed Web of Science ®Google Scholar
• Zhao, L., Peng, R. Y., Wang, S. M., et al. (2012). Relationship between cognition function and hippocampus structure after long-term microwave exposure. Biomed. Environ. Sci. 25:182–188. doi:10.3967/0895-3988.2012.02.009.
   PubMed Web of Science ®Google Scholar
• Zhao, R., Zhang, S., Xu, Z., et al. (2007). Studying gene expression profile of rat neuron exposed to 1800MHz radiofrequency electromagnetic fields with cDNA microassay. Toxicology. 235:167–175. doi:10.1016/j.tox.2007.03.015.
   PubMed Web of Science ®Google Scholar
• Zook, B. C., Simmens, S. J. (2006). The effects of pulsed 860 MHz radiofrequency radiation on the promotion of neurogenic tumors in rats. Radiat. Res. 165:608–615. doi:10.1667/RR3551.1.
   PubMed Web of Science ®Google Scholar
• Zuo, H., Lin, T., Wang, D., et al. (2014). Neural cell apoptosis induced by microwave exposure through mitochondria-dependent caspase-3 pathway. Int. J. Med. Sci. 11:426–435. doi:10.7150/ijms.6540.
   PubMed Web of Science ®Google Scholar
• Zuo, H., Lin, T., Wang, D., et al. (2015). RKIP Regulates Neural Cell Apoptosis Induced by Exposure to Microwave Radiation Partly Through the MEK/ERK/CREB Pathway. Mol. Neurobiol. 51:1520–1529. doi:10.1007/s12035-014-8831-5.
   PubMed Web of Science ®Google Scholar