Electromagnetic fields act via activation of voltage-gated calcium channels to produce beneficial or adverse effects

Journal of Cellular and Molecular Medicine

Volumn 17, Issue 8, 2013, Pages 958-965

  Pall, Martin L ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Calcium channel blockers; Intracellular Ca2+; Low frequency electromagnetic field exposure; Nitric oxide; Oxidative stress; Voltage gated calcium channels

Indexed keywords

ANIMALIA;

CALCIUM CHANNEL; CALCIUM CHANNEL BLOCKING AGENT; NITRIC OXIDE;

ANIMAL; ARTICLE; BONE DEVELOPMENT; CHANNEL GATING; ELECTROMAGNETIC FIELD; HUMAN; INTRACELLULAR CA2+; LOW FREQUENCY ELECTROMAGNETIC FIELD EXPOSURE; METABOLISM; OXIDATIVE STRESS; PHYSIOLOGY; SIGNAL TRANSDUCTION; SINGLE STRANDED DNA BREAK; VOLTAGE-GATED CALCIUM CHANNELS;

CALCIUM CHANNEL BLOCKERS; INTRACELLULAR CA2+; LOW FREQUENCY ELECTROMAGNETIC FIELD EXPOSURE; NITRIC OXIDE; OXIDATIVE STRESS; VOLTAGE-GATED CALCIUM CHANNELS;

ANIMALS; CALCIUM CHANNELS; DNA BREAKS, SINGLE-STRANDED; ELECTROMAGNETIC FIELDS; HUMANS; ION CHANNEL GATING; OSTEOGENESIS; SIGNAL TRANSDUCTION;

EID: 84888201283     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/jcmm.12088     Document Type: Article

References (116)

1. Walleczek J. Electromagnetic field effects on cells of the immune system: the role of calcium signaling. FASEB J. 1992; 6: 3177-85.
2. Cadossi R, Emilia G, Ceccherelli G, et al. 1988 Lymphocytes and pulsing magnetic fields. Marino EE, editor. Modern bioelectricity. New York: Dekker; 1998. pp. 451-96.
3. Papatheofanis FJ. Use of calcium channel antagonists as magnetoprotective agents. Radiat Res. 1990; 122: 24-8.
4. 2+ channels. Annu Rev Cell Dev Biol. 2000; 16: 521-55.
5. 2+ channels in neurite growth of cultured chromaffin cells induced by extremely low frequency (ELF) magnetic field stimulation. Cell Tissue Res. 1998; 291: 217-30.
6. Lorich DG, Brighton CT, Gupta R, et al. Biochemical pathway mediating the response of bone cells to capacitive coupling. Clin Orthop Relat Res. 1998; 246-56.
7. Gobba F, Malagoli D, Ottaviani E. Effects of 50 Hz magnetic fields on fMLP-induced shape changes in invertebrate immunocytes: the role of calcium ion channels. Bioelectromagnetics. 2003; 24: 277-82.
8. Lisi A, Ledda M, Rosola E, et al. Extremely low frequency electromagnetic field exposure promotes differentiation of pituitary corticotrope-derived AtT20 D16V cells. Bioelectromagnetics. 2006; 27: 641-51.
9. Piacentini R, Ripoli C, Mezzogori D, et al. Extremely low-frequency electromagnetic fields promote in vitro neurogenesis via upregulation of Ca(v)1-channel activity. J Cell Physiol. 2008; 215: 129-39.
10. Morris CE, Skalak TC. Acute exposure to a moderate strength static magnetic field reduces edema formation in rats. Am J Physiol Heart Circ Physiol. 2008; 294: H50-7.
11. Ghibelli L, Cerella C, Cordisco S, et al. NMR exposure sensitizes tumor cells to apoptosis. Apoptosis. 2006; 11: 359-65.
12. 2+ influx. FASEB J. 1999; 13: 95-102.
13. Jeong JH, Kum C, Choi HJ, et al. Extremely low frequency magnetic field induces hyperalgesia in mice modulated by nitric oxide synthesis. Life Sci. 2006; 78: 1407-12.
14. Vernier PT, Sun Y, Chen MT, et al. Nanosecond electric pulse-induced calcium entry into chromaffin cells. Bioelectrochemistry. 2008; 73: 1-4.
15. Kim IS, Song JK, Song YM, et al. Novel effect of biphasic electric current on in vitro osteogenesis and cytokine production in human mesenchymal stromal cells. Tissue Eng Part A. 2009; 15: 2411-22.
16. 2+ ion transport through patch-clamped cells exposed to magnetic fields. Bioelectromagnetics. 1995; 16: 33-40.
17. 2+ influx in rat pituitary cells under exposure to a 50 Hz magnetic field. Bioelectromagnetics. 1996; 17: 303-11.
18. 2+ channels and their role in modulation of neuroendocrine cell proliferation and death. Cell Calcium. 2004; 35: 307-15.
19. 2+ channels. Cell Mol Neurobiol. 2010; 30: 1259-65.
20. Marchionni I, Paffi A, Pellegrino M, et al. 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. 2006; 1758: 597-605.
21. Rao VS, Titushkin IA, Moros EG, et al. Nonthermal effects of radiofrequency-field exposure on calcium dynamics in stem cell-derived neuronal cells: elucidation of calcium pathways. Radiat Res. 2008; 169: 319-29.
22. Adair RK, Astumian RD, Weaver JC. Detection of weak electric fields by sharks, rays and skates. Chaos. 1998; 8: 576-87.
23. Constable PA. Nifedipine alters the light-rise of the electro-oculogram in man. Fraefes Arch Clin Exp Ophthalmol. 2011; 249: 677-84.
24. Gmitrov J, Ohkuba C. Verapamil protective effect on natural and artificial magnetic field cardiovascular impact. Bioelectromagnetics. 2002; 23: 531-41.
25. Kindzelskii AL, Petty HR. Ion channel clustering enhances weak electric field detection by neutrophils: apparent role of SKF96365-sensitive cation channels and myeloperoxidase trafficking cellular responses. Eur Biophys J. 2005; 35: 1-26.
26. Xu J, Wang W, Clark CC, et al. Signal transduction in electrically stimulated articular chondrocytes involves translocation of extracellular calcium through voltage-gated channels. Osteoarthritis Cartilage. 2009; 17: 397-405.
27. Pilla AA. Electromagnetic fields instantaneously modulate nitric oxide signaling in challenged biological systems. Biochem Biophys Res Commun. 2012; 426: 330-3.
28. McDonald LJ, Murad F. Nitric oxide and cyclic GMP signaling. Proc Soc Exp Biol Med. 1996; 211: 1-6.
29. Francis SH, Busch JL, Corbin JD, et al. cGMP-dependent protein kinases and cGMP phosphodiesterases in nitric oxide and cGMP action. Pharmacol Rev. 2010; 62: 525-63.
30. Pacher P, Beckman JS, Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol Rev. 2007; 87: 315-424.
31. Pryor WA, Squadrito GL. The chemistry of peroxynitrite: a product from the reaction of nitric oxide with superoxide. Am J Physiol. 1995; 268: L699-722.
32. Lymar SV, Khairutdinov RF, Hurst JK. Hydroxyl radical formation by O-O bond homolysis in peroxynitrous acid. Inorg Chem. 2003; 42: 5259-66.
33. Ryabi JT. Clinical effects of electromagnetic fields on fracture healing. Clin Orthop Relat Res. 1998; 355(Suppl. l): S205-15.
34. Oishi M, Onesti ST. Electrical bone graft stimulation for spinal fusion: a review. Neurosurgery. 2000; 47: 1041-55.
35. Aaron RK, Ciombor DM, Simon BJ. Treatment of nonunions with electric and electromagnetic fields. Clin Orthop Relat Res. 2004; 10: 579-93.
36. Goldstein C, Sprague S, Petrisor BA. Electrical stimulation for fracture healing: current evidence. J Orthop Trauma. 2010; 24(Suppl. 1): S62-5.
37. Demitriou R, Babis GC. Biomaterial osseointegration enhancement with biophysical stimulation. J Musculoskelet Neuronal Interact. 2007; 7: 253-65.
38. Griffin XL, Warner F, Costa M. The role of electromagnetic stimulation in the management of established non-union lf long bone fractures: what is the evidence? Injury. 2008; 39: 419-29.
39. Huang LQ, He HC, He CQ, et al. Clinical update of pulsed electromagnetic fields on osteroporosis. Chin Med J. 2008; 121: 2095-9.
40. Groah SL, Lichy AM, Libin AV, et al. Intensive electrical stimulation attenuates femoral bone loss in acute spinal cord injury. PM R. 2010; 2: 1080-7.
41. Schidt-Rohlfing B, Silny J, Gavenis K, et al. Electromagnetic fields, electric current and bone healing - what is the evidence? Z Orthop Unfall. 2011; 149: 265-70.
42. Griffin XL, Costa ML, Parsons N, et al. Electromagnetic field stimulation for treating delayed union or non-union of long bone fractures in adults. Cochrane Database Syst Rev. 2011; CDO08471. doi: 10.1002/14651858.CD008471.pub2.
43. Chalidis B, Sachinis N, Assiotis A, et al. Stimulation of bone formation and fracture healing with pulsed electromagnetic fields: biologic responses and clinical implications. Int J Immunopathol Pharmacol. 2011; 24(1 Suppl. 2): 17020.
44. Zhong C, Zhao TF, Xu ZJ, et al. Effects of electromagnetic fields on bone regeneration in experimental and clinical studies: a review of the literature. Chin Med J. 2012; 125: 367-72.
45. Diniz P, Soejima K, Ito G. Nitric oxide mediates the effects of pulsed electromagnetic field stimulation on the osteoblast proliferation and differentiation. Nitric Oxide. 2002; 7: 18-23.
46. Fitzsimmons RJ, Gordon SL, Ganey T, et al. A pulsing electric field (PEF) increases human chondrocyte proliferation through a transduction pathway involving nitric oxide signaling. J Orthopaedic Res. 2008; 26: 854-9.
47. Lin H-Y, Lin Y-J. In vitro effects of low frequency electromagnetic fields on osteoblast proliferation and maturation in an inflammatory environment. Bioelectromagnetics. 2011; 32: 552-60.
48. Cheng G, Zhai Y, Chen K, et al. Sinusoidal electromagnetic field stimulates rat osteoblast differentiation and maturation via activation of NO-cGMP-PKG pathway. Nitric Oxide. 2011; 25: 316-25.
49. Pilla A, Fitzsimmons R, Muehsam D, et al. Electromagnetic fields as first messenger in biological signaling: application to calmodulin-dependent signaling in tissue repair. Biochim Biophys Acta. 2011; 1810: 1236-45.
50. Rangaswami H, Schwappacher R, Tran T, et al. Protein kinase G and focal adhesion kinase converge on Src/Akt/β-catenin signaling module in osteoblast mechanotransduction. J Biol Chem. 2012; 287: 21509-19.
51. Marathe N, Rangaswami H, Zhuang S, et al. Pro-survival effects of 17β-estradiol on osteocytes are mediated by nitric oxide/cGMP via differential actions of cGMP-dependent protein kinases I and II. J Biol Chem. 2012; 287: 978-88.
52. Rangaswami H, Schwappacher R, Marathe N, et al. Cyclic GMP and protein kinase G control a Src-containing mechanosome in osteoblasts. Sci Signal. 2010; 3: ra91.
53. Rangaswami H, Marathe N, Zhuang S, et al. Type II cGMP-dependent protein kinase mediates osteoblast mechanotransduction. J Biol Chem. 2009; 284: 14796-808.
54. Saura M, Tarin C, Zaragoza C. Recent insights into the implication of nitric oxide in osteoblast differentiation and proliferation during bone development. ScientificWorldJournal. 2010; 10: 624-32.
55. Zaragoza C, López-Rivera E, García-Rama C, et al. Cbfa-1 mediates nitric oxide regulation of MMP-13 in osteoblasts. J Cell Sci. 2006; 119: 1896-902.
56. Wang DH, Hu YS, Du JJ, et al. Ghrelin stimulates proliferation of human osteoblastic TE85 cells via NO/cGMP signaling pathway. Endocrine. 2009; 35: 112-7.
57. Simkó M. Cell type specific redox status is responsible for diverse electromagnetic field effects. Curr Med Chem. 2007; 14: 1141-52.
58. Consales C, Merla C, Marino C, et al. Electromagnetic fields, oxidative stress, and neurodegeneration. Int J Cell Biol. 2012; 2012: 683897.
59. Johansson O. Disturbance of the immune system by electromagnetic fields-A potentially underlying cause for cellular damage and tissue repair reduction which could lead to disease and impairment. Pathophysiology. 2009; 16: 157-77.
60. Kovacic P, Somanathan R. Electromagnetic fields: mechanism, cell signaling, other bioprocesses, toxicity, radicals, antioxidants and beneficial effects. J Recept Signal Transduct Res. 2010; 30: 214-26.
61. Wolf FI, Torsello A, Tedesco B, et al. 50-Hz extremely low frequency electromagnetic fields enhance cell proliferation and DNA damage: possible involvement of a redox mechanism. Biochim Biophys Acta. 2005; 1743: 120-9.
62. Iakimenko IL, Sidorik EP, Tsybulin AS. Metabolic changes in cells under electromagnetic radiation of mobile communication systems. Ukr Biokhim Zh. 2011; 83: 20-8.
63. Jing J, Yuhua Z, Xiao-qian Y, et al. The influence of microwave radiation from cellular phone on fetal rat brain. Electromagn Biol Med. 2012; 31: 57-66.
64. Esmekaya MA, Ozer C, Seyhan N. 900 MHz pulse-modulated radiofrequency radiation induces oxidative stress on heart, lung, testis and liver tissues. Gen Physiol Biophys. 2011; 30: 84-9.
65. Aydin B, Akar A. Effects of a 900-MHz electromagnetic field on oxidative stress parameters in rat lymphoid organs, polymorphonuclear leukocytes and plasma. Arch Med Res. 2011; 42: 261-7.
66. Guler G, Turkozer Z, Tomruk A, et al. The protective effects of N-acetyl-L-cysteine and epigallocatechin-3-gallate on electric field-induced hepatic oxidative stress. Int J Radiat Biol. 2008; 84: 669-80.
67. Guney M, Ozguner F, Oral B, et al. 900 MHz radiofrequency-induced histopathologic changes and oxidative stress in rat endometrium: protection by vitamins E and C. Toxicol Ind Health. 2007; 23: 411-20.
68. Sypniewska RK, Millenbaugh NJ, Kiel JL, et al. Protein changes in macrophages induced by plasma from rats exposed to 35 GHz millimeter waves. Bioelectromagnetics. 2010; 31: 656-63.
69. Grigoriev YG, Mikhailov VF, Ivanov AA, et al. Autoimmune processes after long-term low-level exposure to electromagnetic fields part 4. Oxidative intracellular stress response to the long-term rat exposure to nonthermal RF EMF. Biophysics. 2010; 55: 1054-8.
70. Erdal N, Gürgül S, Tamer L, et al. Effects of long-term exposure of extremely low frequency magnetic field on oxidative/nitrosative stress in rat liver. J Radiat Res. 2008; 49: 181-7.
71. Ahuja YR, Vijayashree B, Saran R, et al. In vitro effects of low-level, low-frequency electromagnetic fields on DNA damage in human leucocytes by comet assay. Indian J Biochem Biophys. 1999; 36: 318-22.
72. Amara S, Douki T, Ravanat JL, et al. Influence of a static magnetic field (250 mT) on the antioxidant response and DNA integrity in THP1 cells. Phys Med Biol. 2007; 52: 889-98.
73. Focke F, Schuermann D, Kuster N, et al. DNA fragmentation in human fibroblasts under extremely low frequency electromagnetic field exposure. Mutat Res. 2010; 683: 74-83.
74. Franzellitti S, Valbonesi P, Ciancaglini N, et al. Transient DNA damage induced by high-frequency electromagnetic fields (GSM 1.8 GHz) in the human trophoblast HTR-8/SVneo cell line evaluated with the alkaline comet assay. Mutat Res. 2010; 683: 35-42.
75. Garaj-Vrhovac V, Gajski G, Pažanin S, et al. Assessment of cytogenetic damage and oxidative stress in personnel occupationally exposed to the pulsed microwave radiation of marine radar equipment. Int J Hyg Environ Health. 2011; 214: 59-65.
76. Hong R, Zhang Y, Liu Y, et al. Effects of extremely low frequency electromagnetic fields on DNA of testicular cells and sperm chromatin structure in mice. Zhonghua Lao Dong Wei Sheng Zhi Ye Bing Za Zhi. 2005; 23: 414-7. [Article in Chinese].
77. Ivancsits S, Diem E, Pilger A, et al. Induction of DNA strand breaks by intermittent exposure to extremely-low-frequency electromagnetic fields in human diploid fibroblasts. Mutat Res. 2002; 519: 1-13.
78. Ivancsits S, Diem E, Jahn O, et al. Intermittent extremely low frequency electromagnetic fields cause DNA damage in a dose-dependent way. Int Arch Occup Environ Health. 2003; 76: 431-6.
79. Ivancsits S, Pilger A, Diem E, et al. Cell type-specific genotoxic effects of intermittent extremely low-frequency electromagnetic fields. Mutat Res. 2005; 583: 184-8.
80. Kesari KK, Behari J, Kumar S. Mutagenic response of 2.45 GHz radiation exposure on rat brain. Int J Radiat Biol. 2010; 86: 334-43.
81. Lai H, Singh NP. Melatonin and a spin-trap compound block radiofrequency electromagnetic radiation-induced DNA strand breaks in rat brain cells. Bioelectromagnetics. 1997; 18: 446-54.
82. Lai H, Singh NP. Magnetic-field-induced DNA strand breaks in brain cells of the rat. Environ Health Perspect. 2004; 112: 687-94.
83. Lee JW, Kim MS, Kim YJ, et al. Genotoxic effects of 3 T magnetic resonance imaging in cultured human lymphocytes. Bioelectromagnetics. 2011; 32: 535-42.
84. Paulraj R, Behari J. Single strand DNA breaks in rat brain cells exposed to microwave radiation. Mutat Res. 2006; 596: 76-80.
85. Romeo S, Zeni L, Sarti M, et al. DNA electrophoretic migration patterns change after exposure of Jurkat cells to a single intense nanosecond electric pulse. PLoS ONE. 2011; 6: e28419.
86. Schwarz C, Kratochvil E, Pilger A, et al. Radiofrequency electromagnetic fields (UMTS, 1, 950 MHz) induce genotoxic effects in vitro in human fibroblasts but not in lymphocytes. Int Arch Occup Environ Health. 2008; 81: 755-67.
87. Svedenstål BM, Johanson KJ, Mattsson MO, et al. DNA damage, cell kinetics and ODC activities studied in CBA mice exposed to electromagnetic fields generated by transmission lines. In Vivo. 1999; 13: 507-13.
88. Svedenstål BM, Johanson KJ, Mild KH. DNA damage induced in brain cells of CBA mice exposed to magnetic fields. In Vivo. 1999; 13: 551-2.
89. Trosić I, Pavicić I, Milković-Kraus S, et al. Effect of electromagnetic radiofrequency radiation on the rats' brain, liver and kidney cells measured by comet assay. Coll Antropol. 2011; 35: 1259-64.
90. Burdak-Rothkamm S, Rothkamm K, Folkard M, et al. DNA and chromosomal damage in response to intermittent extremely low-frequency magnetic fields. Mutat Res. 2009; 672: 82-9.
91. Fairbairn DW, O'Neill KL. The effect of electromagnetic field exposure on the formation of DNA single strand breaks in human cells. Cell Mol Biol (Noisy-le-grand). 1994; 40: 561-7.
92. Fiorani M, Cantoni O, Sestili P, et al. Electric and/or magnetic field effects on DNA structure and function in cultured human cells. Mutat Res. 1992; 282: 25-9.
93. Malyapa RS, Ahern EW, Straube WL, et al. Measurement of DNA damage after exposure to 2450 MHz electromagnetic radiation. Radiat Res. 1997; 148: 608-17.
94. McNamee JP, Bellier PV, Chauhan V, et al. Evaluating DNA damage in rodent brain after acute 60 Hz magnetic-field exposure. Radiat Res. 2005; 164: 791-7.
95. Scarfí MR, Sannino A, Perrotta A, et al. Evaluation of genotoxic effects in human fibroblasts after intermittent exposure to 50 Hz electromagnetic fields: a confirmatory study. Radiat Res. 2005; 164: 270-6.
96. Stronati L, Testa A, Villani P, et al. Absence of genotoxicity in human blood cells exposed to 50 Hz magnetic fields as assessed by comet assay, chromosome aberration, micronucleus, and sister chromatid exchange analyses. Bioelectromagnetics. 2004; 25: 41-8.
97. Testa A, Cordelli E, Stronati L, et al. Evaluation of genotoxic effect of low level 50 Hz magnetic fields on human blood cells using different cytogenetic assays. Bioelectromagnetics. 2004; 25: 613-9.
98. Szabó G, Bährle S. Role of nitrosative stress and poly(ADP-ribose) polymerase activation in myocardial reperfusion injury. Curr Vasc Pharmacol. 2005; 3: 215-20.
99. Moon HK, Yang ES, Park JW. Protection of peroxynitrite-induced DNA damage by dietary antioxidants. Arch Pharm Res. 2006; 29: 213-7.
100. Sakihama Y, Maeda M, Hashimoto M, et al. Beetroot betalain inhibits peroxynitrite-mediated tyrosine nitration and DNA strand damage. Free Radic Res. 2012; 46: 93-9.
101. Hybertson BM, Gao B, Bose SK, et al. Oxidative stress in health and disease: the therapeutic potential of Nrf2 activation. Mol Aspects Med. 2011; 32: 234-46.
102. Ridley AJ, Paterson HF, Johnston CL, et al. The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell. 1992; 70: 401-10.
103. Wennström S, Hawkins P, Cooke F, et al. Activation of phosphoinositide 3-kinase is required for PDGF-stimulated membrane ruffling. Curr Biol. 1994; 4: 385-93.
104. Joucla S, Yvert B. Modeling of extracellular neural stimulation: from basic understanding to MEA-based applications. J Physiol Paris. 2012; 106: 146-58.
105. Pashut T, Wolfus S, Friedman A, et al. Mechanisms of magnetic stimulation of central nervous system neurons. PLoS Comput Biol. 2011; 7: e1002022.
106. Fatemi-Ardekani A. Transcranial magnetic stimulation: physics, electrophysiology, and applications. Crit Rev Biomed Eng. 2008; 36: 375-412.
107. Silva S, Basser PJ, Miranda PC. Elucidating the mechanisms and loci of neuronal excitation by transcranial magnetic stimulation using a finite element model of a cortical sulcus. Clin Neurophysiol. 2008; 119: 2405-13.
108. Radman T, Ramos RL, Brumberg JC, et al. Role of cortical cell type and morphology in subthreshold and suprathreshold uniform electric field stimulation in vitro. Brain Stimul. 2009; 2: 215-28.
109. Minelli TA, Balduzzo M, Milone FF, et al. Modeling cell dynamics under mobile phone radiation. Nonlinear cell dynamics under mobile phone radiation. Nonlinear Dynamics Psychol Life Sci. 2007; 11: 197-218.
110. Saunders RD, Jefferys JGR. A neurobiological basis for ELF guidelines. Health Phys. 2007; 92: 596-603.
111. Havas M. Dirty electricity elevates blood sugar among electrically sensitive diabetics and may explain brittle diabetes. Electromagn Biol Med. 2008; 27: 135-46.
112. Havas M. Electromagnetic hypersensitivity: biological effects of dirty electricity with emphasis on diabetes and multiple sclerosis. Electromagn Biol Med. 2006; 25: 259-68.
113. de Vochta F. "Dirty electricity": what, where, and should we care? J Expo Sci Environ Epidemiol. 2010; 20: 399-405.
114. Friedman J, Kraus S, Hauptman Y, et al. Mechanism of short-term ERK activation by electromagnetic fields at mobile phone frequencies. Biochem J. 2007; 405: 559-68.
115. Desai NR, Kesari KK, Agarwal A. Pathophysiology of cell phone radiation: oxidative stress and carcinogenesis with focus on the male reproductive system. Reproduct Biol Endocrinol. 2009; 7: 114. doi:10.1186/1477-7827-7-114.
116. 2+ currents in type I cells isolated from the rat carotid body. Neurosci Lett. 1994; 172: 63-6.