Nonthermal effects of radiofrequency-field exposure on calcium dynamics in stem cell-derived neuronal cells: Elucidation of calcium pathways

Radiation Research

Volumn 169, Issue 3, 2008, Pages 319-329

  Rao, V S ^a   Titushkin, I A ^a   Moros, E G ^b   Pickard, W F ^c   Thatte, H S ^d   Cho, M R ^a,e  

^a University of Illinois at Chicago   (United States)

^b UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^c WASHINGTON UNIVERSITY IN ST LOUIS   (United States)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

^e M/C 063 ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 1H PYRROLE 2,5 DIONE; CALCIUM; CALCIUM CHANNEL N TYPE; CYTOCHALASIN D; NIFEDIPINE; NOCODAZOLE; OMEGA CONOTOXIN GVIA; PHOSPHOLIPASE C; THAPSIGARGIN; CALCIUM CHANNEL L TYPE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOSOL; DNA SYNTHESIS; EMBRYONAL CARCINOMA; EXTRACELLULAR CALCIUM; IMMUNOFLUORESCENCE; LIGAND BINDING; MICROSCOPY; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; RADIATION EXPOSURE; RADIOFREQUENCY; STEM CELL; ANIMAL; CALCIUM SIGNALING; CELL CULTURE; CYTOLOGY; HEAT; METABOLIC CLEARANCE RATE; METABOLISM; PHYSIOLOGY; RADIATION DOSE; RADIATION RESPONSE; RADIOFREQUENCY RADIATION;

ANIMALS; CALCIUM; CALCIUM CHANNELS, L-TYPE; CALCIUM SIGNALING; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, RADIATION; HEAT; METABOLIC CLEARANCE RATE; MICE; NEURONS; RADIATION DOSAGE; RADIO WAVES; STEM CELLS;

EID: 41649114809     PISSN: 00337587     EISSN: None     Source Type: Journal    
DOI: 10.1667/RR1118.1     Document Type: Article

References (62)

1. 2+ oscillations in primary bone marrow stromal cells. J. Cell. Physiol. 206, 664-671 (2006).
2. M. B. Carey and S. G. Matsumoto, Spontaneous calcium transients are required for neuronal differentiation of murine neural crest. Dev. Biol. 215, 298-313 (1999).
3. M. R. Cho, H. S. Thatte, R. C. Lee and D. E. Golan, Reorganization of microfilament structure induced by ac electric fields. FASEB J. 10, 1552-1558 (1996).
4. 2+ signaling in cardiac myocyte excitation- transcription coupling. J. Clin. Invest. 116, 675-682 (2006).
5. D. Brough, M. J. Schell and R. F. Irvine, Agonist-induced regulation of mitochondrial and endoplasmic reticulum motility. Biochem. J. 392, 291-297 (2005).
6. P. Marius, M. T. Guerra, M. H. Nathanson, B. E. Ehrlich and M. F. Leite, Calcium release from ryanodine receptors in the nucleoplasmic reticulum. Cell Calcium 39, 65-73 (2006).
7. 2+ signaling in spike-timing-dependent plasticity. J. Neurosci. 26, 11001-11013 (2006).
8. 2+ liberation in xenopus oocytes. J. Physiol. 476, 17-28 (1994).
9. A. Verkhratsky, The endoplasmic reticulum and neuronal calcium signalling. Cell Calcium 32, 393-404 (2002).
10. B. X. Zhang, X. Ma, Z. J. Shu, R. H. Swerdlow and M. S. Katz, Differential role of mitochondria in intracellular calcium oscillations. Biophys. J. 84, 10A (2003).
11. 2+ from ryanodine receptor-gated stores and lysosome-related acidic organelles in pulmonary arterial smooth muscle cells. J. Biol. Chem. 281, 34312-34323 (2006).
12. R. Bisschops, P. Vanden Berghe, G. Sarnelli, J. Janssens and J. Tack, CRF-induced calcium signaling in guinea pig small intestine myenteric neurons involves CRF-1 receptors and activation of voltage-sensitive calcium channels. Am. J. Physiol. Gastrointest. Liver Physiol. 290, G1252-G1260 (2006).
13. C. G. van der Wees, W. H. Bax, E. J. van der Valk and A. van der Laarse, Integrin stimulation induces calcium signalling in rat cardiomyocytes by a NO-dependent mechanism. Pflugers Arch. 451, 588-595 (2006).
14. A. Verkhratsky and A. Shmigol, Calcium-induced calcium release in neurones. Cell Calcium 19, 1-14 (1996).
15. 2+-oscillations in cultured hippocampal neurons. Acta Anaesthesiol. Scand. 50, 742-748 (2006).
16. H. Ulrich and P. Majumder, Neurotransmitter receptor expression and activity during neuronal differentiation of embryonal carcinoma and stem cells: From basic research towards clinical applications. Cell Prolif. 39, 281-300 (2006).
17. G. Bain, D. Kitchens, M. Yao, J. E. Huettner and D. I. Gottlieb, Embryonic stem cells express neuronal properties in vitro. Dev. Biol. 168, 342-357 (1995).
18. 2+ spikes specify transmitter choice. Trends Neurosci. 27, 415-421 (2004).
19. 2+ channels and regulation of calcium microdomains. Cell Calcium 40, 495-504 (2006).
20. M. E. Spira, R. Oren, A. Dormann, N. Ilouz and S. Lev, Calcium, protease activation, and cytoskeleton remodeling underlie growth cone formation and neuronal regeneration. Cell. Mol. Neurobiol. 21, 591-604 (2001).
21. S. K. Dutta, B. Ghosh and C. F. Blackman, Radiofrequency radiation-induced calcium-ion efflux enhancement from human and other neuroblastoma cells in culture. Bioelectromagnetics 10, 197-202 (1989).
22. A. C. Green, I. R. Scott, R. J. Gwyther, A. Peyman, P. Chadwick, X. Chen, Y. Alfadhl and J. E. H. Tattersall, An investigation of the effects of TETRA RF fields on intracellular calcium in neurones and cardiac myocytes. Int. J. Radiat. Biol. 81, 869-885 (2006).
23. L. J. Anghileri, E. Mayayo, J. L. Domingo and P. Thouvenot, Radiofrequency-induced carcinogenesis: Cellular calcium homeostasis changes as a triggering factor. Int. J. Radiat. Biol. 81, 205-209 (2005).
24. K. R. Maginot, T. S. Klitzner, W. F. Friedman and G. T. Wetzel, The relationship between temperature and calcium in acute cell damage after exposure to radiofrequency or thermal energy in isolated neonatal and adult rabbit cardiac myocytes. Pediatr. Res. 43, 527-531 (1998).
25. M. Simko and M.O. Mattsson, Extremely low frequency electromagnetic fields as effectors of cellular responses in vitro: Possible immune cell activation. J. Cell. Biochem. 93, 83-92 (2004).
26. C. G. Cranfield, A. W. Wood, V. Anderson and K. G. Menezes, Effects of mobile phone type signals on calcium levels within human leukaemic T-cells (Jurkat cells). Int. J. Radiat. Biol. 77, 1207-1217 (2001).
27. Z. Y. Gao, G. Xu, M. M. Stwora-Wojczyk, F. M. Matschinsky, V. M. Lee and B. A. Wolf, Retinoic acid induction of calcium channel expression in human NT2N neurons. Biochem. Biophys. Res. Commun. 247, 407-413 (1998).
28. 2+ channel expression upon differentiation of SN56 cholinergic cells. Brain Res. 916, 199-210 (2001).
29. L. Iacovitti, A. E. Donaldson, C. E. Marshall, S. Suon and M. Yang, A protocol for the differentiation of human embryonic stem cells into dopaminergic neurons using only chemically defined human additives: Studies in vitro and in vivo. Brain Res. 1127, 19-25 (2007).
30. E. M. Jones-Villeneuve, M. A. Rudnicki, J. F. Harris and M. W. McBurney, Retinoic acid-induced neural differentiation of embryonal carcinoma cells. Mol. Cell. Biol. 3, 2271-2279 (1983).
31. E. M. Jones-Villeneuve, M. W. McBurney, K. A. Rogers and V. I. Kalnins, Retinoic acid induces embryonal carcinoma cells to differentiate into neurons and glial cells. J. Cell Biol. 94, 253-262 (1982).
32. W. F. Pickard, E. G. Moros, B. A. Cha and P. Novak, Electromagnetic and thermal characterization of an UHF-applicator for concurrent irradiation and high resolution non-perturbing optical microscopy of cells. Bioelectromagnetics 27, 593-601 (2006).
33. L. Khatib, D. E. Golan and M. Cho, Physiologic electrical stimulation provokes intracellular calcium increase mediated by phospholipase C activation in human osteoblasts. FASEB J. 18, 1903-1905 (2004).
34. A. Hamed, P. Kim and M. Cho, Synthesis of nitric oxide in human osteoblasts in response to physiologic stimulation of electrotherapy. Ann. Biomed. Eng. 34, 1908-1916 (2006).
35. S. Miyazaki, Inositol trisphosphate receptor mediated spatiotemporal calcium signalling. Curr. Opin. Cell Biol. 7, 190-196 (1995).
36. J. Sneyd, J. Keizer and M. J. Sanderson, Mechanisms of calcium oscillations and waves: A quantitative analysis. FASEB J. 9, 1463-1472 (1995).
37. K. Takei, R. M. Shin, T. Inoue, K. Kato and K. Mikoshiba, Regulation of nerve growth mediated by inositol 1,4,5-trisphosphate receptors in growth cones. Science 282, 1705-1708 (1998).
38. 2+ released from internal stores via PLC/IP3 pathway. Neuroreport 12, 2203-2207 (2001).
39. A. Ahlbom, A. Green, L. Kheifets, D. Savitz, A. Swerdlow and ICNIRP (International Commission for Non-Ionizing Radiation Protection) Standing Committee on Epidemiology, Epidemiology of health effects of radiofrequency exposure. Environ. Health Perspect. 112, 1741-1754 (2004).
40. Pavicic, Impact of radiofrequency/microwave radiation on cell and cytoskeleton structure. Arh. Hig. Rada. Toksikol. 55, 321-328 (2004).
41. 2+ signalling pathways mediated by type 1 metabotropic glutamate receptors in rat Purkinje neurones. J. Physiol. 573, 65-82 (2006).
42. 2+ channels. Mol. Pharmacol. 68, 1387-1396 (2005).
43. M. R. Pagani, R. C. Reisin and O. D. Uchitel, Calcium signaling pathways mediating synaptic potentiation triggered by amyotrophic lateral sclerosis IgG in motor nerve terminals. J. Neurosci. 26, 2661-2672 (2006).
44. 2+ channels. J. Neurosci. 24, 10980-10992 (2004).
45. S. Sun and M. Cho, Human fibroblast migration in three-dimensional collagen gel in response to noninvasive electrical stimulus. II. identification of electrocoupling molecular mechanisms. Tissue Eng. 10, 1558-1565 (2004).
46. S. Sun, Y. Liu, S. Lipsky and M. Cho, Physical manipulation of calcium oscillations facilitates osteodifferentiation of human mesenchymal stem cells. FASEB J. 21, 1472-1480 (2007).
47. T. Schubert, R. Weiler and A. Feigenspan, Intracellular calcium is regulated by different pathways in horizontal cells of the mouse retina. J. Neurophysiol. 96, 1278-1292 (2006).
48. 2+ channels. Proc. Natl. Acad. Sci. USA 99, 14458-14463 (2002).
49. I. Brunig, S. Kaech, H. Brinkhaus, T. G. Oertner and A. Matus, Influx of extracellular calcium regulates actin-dependent morphological plasticity in dendritic spines. Neuropharmacology 47, 669-676 (2004).
50. 2+ current that is dependent on F-actin cytoskeleton. FASEB J. 17, 1907-1909 (2003).
51. M. D. Neely and M. Gesemann, Disruption of microfilaments in growth cones following depolarization and calcium influx. J. Neurosci. 14, 7511-7520 (1994).
52. C. E. Schmidt, J. W. Dai, D. A. Lauffenburger, M. P. Sheetz and A. F. Horwitz, Integrin-cytoskeletal interactions in neuronal growth cones. J. Neurosci. 15, 3400-3407 (1995).
53. W. R. Adey, S. M. Bawin and A. F. Lawrence, Effects of weak amplitude-modulated microwave fields on calcium efflux from awake cat cerebral cortex. Bioelectromagnetics 3, 295-307 (1982).
54. R. Huber, V. Treyer, J. Schuderer, T. Berthold, A. Buck, N. Kuster, H. P. Landolt and P. Achermann, Exposure to pulse-modulated radio frequency electromagnetic fields affects regional cerebral blood flow. Eur. J. Neurosci. 21, 1000-1006 (2005).
55. J. E. Moulder, K. R. Foster, L. S. Erdreich and J. P. McNamee, Mobile phones, mobile phone base stations and cancer: A review. Int. J. Radiat. Biol. 81, 189-203 (2005).
56. K. R. Foster, Thermal and nonthermal mechanisms of interaction of radio-frequency energy with biological systems. IEEE Trans. Plasma Sci. 28, 15-23 (2000).
57. W. F. Pickard and E. G. Moros, Energy deposition processes in biological tissue: Nonthermal biohazards seem unlikely in the ultrahigh frequency range. Bioelectromagnetics 22, 97-105 (2001).
58. R. K. Adair, Biophysical limits on the athermal effects of RF and microwave radiation. Bioelectromagnetics 24, 39-48 (2003).
59. L. J. Challis, Mechanisms for interaction between RF fields and biological tissue. Bioelectromagnetics Suppl., S98-S106 (2005).
60. Y. H. Barsoum and W. F. Pickard, The vacuolar potential of Characean cells subjected to electromagnetic radiation in the range 200-8,200 MHz. Bioelectromagnetics 3, 393-400 (1982).
61. K. Tawada, P. Wahl and J. C. Auchet, Study of actin and its interactions with heavy meromyosin and the regulatory proteins by the pulse fluorimetry in polarized light of a fluorescent probe attached to an actin cysteine. Eur. J. Biochem. 88, 411-419 (1978).
62. M. W. Clarkson, S. A. Gilmore, M. H. Edgell and A. L. Lee, Dynamic coupling and allosteric behavior in a nonallosteric protein. Biochemistry 45, 7693-7699 (2006).