Anat Cell Biol.  2017 Jun;50(2):115-123. 10.5115/acb.2017.50.2.115.

Effects of radiofrequency exposure emitted from a GSM mobile phone on proliferation, differentiation, and apoptosis of neural stem cells

Affiliations
  • 1Neural Stem Cell and Regenerative Neuroscience Laboratory, Department of Anatomical Sciences, Shiraz School of Medicine, Shiraz Stem Cell Institute, Shiraz University of Medical Sciences, Shiraz, Iran. azarihasan@sums.ac.ir
  • 2Ionizing and Non-ionizing Radiation Protection Research Center (INIRPRC), Shiraz University of Medical Sciences, Shiraz, Iran. mmortazavi@sums.ac.ir
  • 3Department of Medical Physics and Medical Engineering, School of Medicine, Shiraz University of Medical Sciences, Shiraz, Iran.
  • 4Department of Anatomical Sciences, Yasuj University of Medical Sciences, Yasuj, Iran.

Abstract

Due to the importance of neural stem cells (NSCs) in plasticity of the nervous system and treating neurodegenerative diseases, the main goal of this study was to evaluate the effects of radiofrequency radiation emitted from a GSM 900-MHz mobile phone with different exposure duration on proliferation, differentiation and apoptosis of adult murine NSCs in vitro. We used neurosphere assay to evaluate NSCs proliferation, and immunofluorescence assay of neural cell markers to examine NSCs differentiation. We also employed alamarBlue and caspase 3 apoptosis assays to assess harmful effects of mobile phone on NSCs. Our results showed that the number and size of resulting neurospheres and also the percentage of cells differentiated into neurons decreased significantly with increasing exposure duration to GSM 900-MHz radiofrequency (RF)-electromagnetic field (EMF). In contrast, exposure to GSM 900-MHz RF-EMF at different durations did not influence cell viability and apoptosis of NSCs and also their astrocytic differentiation. It is concluded that accumulating dose of GSM 900-MHz RF-EMF might have devastating effects on NSCs proliferation and neurogenesis requiring more causations in terms of using mobile devices.

Keyword

Electromagnetic fields; Cell phones; Neural stem cells; Radiofrequency; Microwaves; Cell proliferation; Cell differentiation; Apoptosis

MeSH Terms

Adult
Apoptosis*
Caspase 3
Cell Differentiation
Cell Phones*
Cell Proliferation
Cell Survival
Electromagnetic Fields
Fluorescent Antibody Technique
Humans
In Vitro Techniques
Microwaves
Nervous System
Neural Stem Cells*
Neurodegenerative Diseases
Neurogenesis
Neurons
Plastics
Caspase 3
Plastics

Figure

  • Fig. 1 Effect of GSM 900 MHz on proliferation of adult neural stem cells in vitro. (A) Mean neurosphere forming frequency. (B) Mean neurosphere diameter. (C) Representative neurospheres formed in different treatment groups. Scale bar=100 µm. **P<.01, ***P<0.001.

  • Fig. 2 Effect of GSM 900 MHz on differentiation of neural stem cell. (A) Mean percentage of astrocytes. (B) Mean percentage of neurons. (C) Representative immunostained pictures from the control and 120-minute treatment groups. GFAP, glial fibrillary acidic protein; IR, immunoreactive. Scale bar=100 µm. *P<0.05, ***P<0.001.

  • Fig. 3 Effect of GSM 900 MHz on cell viability and apoptosis. (A) Cell viability of neural stem cells using alamarBlue assay. (B) Mean percentage of caspase 3 apoptotic cells in different treatment groups. (C) Representative flow cytometry plot analyzing caspase 3 immunoreactive cells.


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Reference

1. Feychting M, Ahlbom A, Kheifets L. EMF and health. Annu Rev Public Health. 2005; 26:165–189.
2. Wu S, Razavi B. A 900-MHz/1.8-GHz CMOS receiver for dual-band applications. IEEE J Solid-State Circuits. 1998; 33:2178–2185.
3. Bas O, Odaci E, Kaplan S, Acer N, Ucok K, Colakoglu S. 900 MHz electromagnetic field exposure affects qualitative and quantitative features of hippocampal pyramidal cells in the adult female rat. Brain Res. 2009; 1265:178–185.
4. Moulder JE, Erdreich LS, Malyapa RS, Merritt J, Pickard WF, Vijayalaxmi . Cell phones and cancer: what is the evidence for a connection? Radiat Res. 1999; 151:513–531.
5. Odaci E, Bas O, Kaplan S. Effects of prenatal exposure to a 900 MHz electromagnetic field on the dentate gyrus of rats: a stereological and histopathological study. Brain Res. 2008; 1238:224–229.
6. Bas O, Odaci E, Mollaoglu H, Ucok K, Kaplan S. Chronic prenatal exposure to the 900 megahertz electromagnetic field induces pyramidal cell loss in the hippocampus of newborn rats. Toxicol Ind Health. 2009; 25:377–384.
7. Mausset-Bonnefont AL, Hirbec H, Bonnefont X, Privat A, Vignon J, de Sèze R. Acute exposure to GSM 900-MHz electromagnetic fields induces glial reactivity and biochemical modifications in the rat brain. Neurobiol Dis. 2004; 17:445–454.
8. Reynolds BA, Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science. 1992; 255:1707–1710.
9. Abrous DN, Koehl M, Le Moal M. Adult neurogenesis: from precursors to network and physiology. Physiol Rev. 2005; 85:523–569.
10. Azari H, Reynolds BA. In vitro models for neurogenesis. Cold Spring Harb Perspect Biol. 2016; 8:a021279.
11. Lee TH, Lee CH, Kim IH, Yan BC, Park JH, Kwon SH, Park OK, Ahn JH, Cho JH, Won MH, Kim SK. Effects of ADHD therapeutic agents, methylphenidate and atomoxetine, on hippocampal neurogenesis in the adolescent mouse dentate gyrus. Neurosci Lett. 2012; 524:84–88.
12. Utsugi C, Miyazono S, Osada K, Sasajima H, Noguchi T, Matsuda M, Kashiwayanagi M. Hard-diet feeding recovers neurogenesis in the subventricular zone and olfactory functions of mice impaired by soft-diet feeding. PLoS One. 2014; 9:e97309.
13. Yagita Y, Kitagawa K, Sasaki T, Terasaki Y, Todo K, Omura-Matsuoka E, Matsumoto M, Hori M. Postischemic exercise decreases neurogenesis in the adult rat dentate gyrus. Neurosci Lett. 2006; 409:24–29.
14. Bergami M, Masserdotti G, Temprana SG, Motori E, Eriksson TM, Göbel J, Yang SM, Conzelmann KK, Schinder AF, Götz M, Berninger B. A critical period for experience-dependent remodeling of adult-born neuron connectivity. Neuron. 2015; 85:710–717.
15. Abbasnia K, Ghanbari A, Abedian M, Ghanbari A, Sharififar S, Azari H. The effects of repetitive transcranial magnetic stimulation on proliferation and differentiation of neural stem cells. Anat Cell Biol. 2015; 48:104–113.
16. Sherafat MA, Heibatollahi M, Mongabadi S, Moradi F, Javan M, Ahmadiani A. Electromagnetic field stimulation potentiates endogenous myelin repair by recruiting subventricular neural stem cells in an experimental model of white matter demyelination. J Mol Neurosci. 2012; 48:144–153.
17. Joubert V, Leveque P, Cueille M, Bourthoumieu S, Yardin C. No apoptosis is induced in rat cortical neurons exposed to GSM phone fields. Bioelectromagnetics. 2007; 28:115–121.
18. Sonmez OF, Odaci E, Bas O, Kaplan S. Purkinje cell number decreases in the adult female rat cerebellum following exposure to 900 MHz electromagnetic field. Brain Res. 2010; 1356:95–101.
19. Nikolova T, Czyz J, Rolletschek A, Blyszczuk P, Fuchs J, Jovtchev G, Schuderer J, Kuster N, Wobus AM. Electromagnetic fields affect transcript levels of apoptosis-related genes in embryonic stem cell-derived neural progenitor cells. FASEB J. 2005; 19:1686–1688.
20. Azari H, Rahman M, Sharififar S, Reynolds BA. Isolation and expansion of the adult mouse neural stem cells using the neurosphere assay. J Vis Exp. 2010; (45):pii: 2393.
21. Mortazavi S, Mosleh-Shirazi M, Tavassoli A, Taheri M, Mehdizadeh A, Namazi S, Jamali A, Ghalandari R, Bonyadi S, Haghani M, Shafie M. Increased radioresistance to lethal doses of gamma rays in mice and rats after exposure to microwave radiation emitted by a GSM mobile phone simulator. Dose Response. 2013; 11:281–292.
22. Mortazavi SM, Erfani N, Mozdarani H, Azmoonfar R, Shokrpour N. Induction of apoptosis by 900 MHz radiofrequency radiation emitted from a GSM mobile phone simulator in bystander Jurkat cells. Int J Radiat Res. 2015; 13:181–186.
23. Kazemi E, Mortazavi SM, Ali-Ghanbari A, Sharifzadeh S, Ranjbaran R, Mostafavi-Pour Z, Zal F, Haghani M. Effect of 900 MHz electromagnetic radiation on the induction of ROS in human peripheral blood mononuclear Cells. J Biomed Phys Eng. 2015; 5:105–114.
24. Hamedi A, Ghanbari A, Razavipour R, Saeidi V, Zarshenas MM, Sohrabpour M, Azari H. Alyssum homolocarpum seeds: phytochemical analysis and effects of the seed oil on neural stem cell proliferation and differentiation. J Nat Med. 2015; 69:387–396.
25. Azari H, Sharififar S, Darioosh RP, Fortin JM, Rahman M, Reynolds BA. Purifying immature neurons from differentiating neural stem cell progeny using a simple shaking method. J Stem Cell Res Ther. 2014; 4:178.
26. Cuccurazzu B, Leone L, Podda MV, Piacentini R, Riccardi E, Ripoli C, Azzena GB, Grassi C. Exposure to extremely low-frequency (50 Hz) electromagnetic fields enhances adult hippocampal neurogenesis in C57BL/6 mice. Exp Neurol. 2010; 226:173–182.
27. Piacentini R, Ripoli C, Mezzogori D, Azzena GB, Grassi C. Extremely low-frequency electromagnetic fields promote in vitro neurogenesis via upregulation of Ca(v)1-channel activity. J Cell Physiol. 2008; 215:129–139.
28. Leone L, Fusco S, Mastrodonato A, Piacentini R, Barbati SA, Zaffina S, Pani G, Podda MV, Grassi C. Epigenetic modulation of adult hippocampal neurogenesis by extremely low-frequency electromagnetic fields. Mol Neurobiol. 2014; 49:1472–1486.
29. Mori H, Ninomiya K, Kino-oka M, Shofuda T, Islam MO, Yamasaki M, Okano H, Taya M, Kanemura Y. Effect of neurosphere size on the growth rate of human neural stem/progenitor cells. J Neurosci Res. 2006; 84:1682–1691.
30. Salford LG, Brun AE, Eberhardt JL, Malmgren L, Persson BR. Nerve cell damage in mammalian brain after exposure to microwaves from GSM mobile phones. Environ Health Perspect. 2003; 111:881–883.
31. Masuda H, Ushiyama A, Takahashi M, Wang J, Fujiwara O, Hikage T, Nojima T, Fujita K, Kudo M, Ohkubo C. Effects of 915 MHz electromagnetic-field radiation in TEM cell on the blood-brain barrier and neurons in the rat brain. Radiat Res. 2009; 172:66–73.
32. Wickman G, Julian L, Olson MF. How apoptotic cells aid in the removal of their own cold dead bodies. Cell Death Differ. 2012; 19:735–742.
33. Abdanipour A, Tiraihi T, Noori-Zadeh A, Majdi A, Gosaili R. Evaluation of lovastatin effects on expression of anti-apoptotic Nrf2 and PGC-1alpha genes in neural stem cells treated with hydrogen peroxide. Mol Neurobiol. 2014; 49:1364–1372.
34. Zhang S, Chen X, Yang Y, Zhou X, Liu J, Ding F. Neuroprotection against cobalt chloride-induced cell apoptosis of primary cultured cortical neurons by salidroside. Mol Cell Biochem. 2011; 354:161–170.
35. Chen C, Ma Q, Liu C, Deng P, Zhu G, Zhang L, He M, Lu Y, Duan W, Pei L, Li M, Yu Z, Zhou Z. Exposure to 1800 MHz radiofrequency radiation impairs neurite outgrowth of embryonic neural stem cells. Sci Rep. 2014; 4:5103.
36. Liu YX, Tai JL, Li GQ, Zhang ZW, Xue JH, Liu HS, Zhu H, Cheng JD, Liu YL, Li AM, Zhang Y. Exposure to 1950-MHz TD-SCDMA electromagnetic fields affects the apoptosis of astrocytes via caspase-3-dependent pathway. PLoS One. 2012; 7:e42332.
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