Comparison of biological effects between continuous and intermittent exposure to GSM-900-MHz mobile phone radiation: Detection of apoptotic cell-death features

Mutation Research - Genetic Toxicology and Environmental Mutagenesis

Volumn 700, Issue 1-2, 2010, Pages 51-61

  Chavdoula, Evangelia D ^a   Panagopoulos, Dimitris J ^a   Margaritis, Lukas H ^a  

^a UNIVERSITY OF ATHENS   (Greece)

Author keywords

Actin disorganization; Apoptosis; DNA fragmentation; Drosophila

Indexed keywords

ACRIDINE ORANGE; ACTIN; DNA; PHALLOIDIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; COMPARATIVE STUDY; CONFOCAL MICROSCOPY; CONTINUOUS EXPOSURE; CONTROLLED STUDY; CYTOSKELETON; DNA FRAGMENTATION; DROSOPHILA MELANOGASTER; EGG; ELECTROMAGNETIC RADIATION; FEMALE; INTERMITTENT EXPOSURE; MALE; MOBILE PHONE; NICK END LABELING; NONHUMAN; OVARY CELL; PRIORITY JOURNAL; RADIATION EXPOSURE; REPRODUCTION;

ANIMALS; APOPTOSIS; CELL DEATH; CELLULAR PHONE; DNA FRAGMENTATION; DROSOPHILA MELANOGASTER; ELECTROMAGNETIC FIELDS; FEMALE; OVUM; RADIATION DOSAGE; REPRODUCTION;

DROSOPHILA MELANOGASTER; HEXAPODA;

EID: 77953915399     PISSN: 13835718     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mrgentox.2010.05.008     Document Type: Article

References (64)

1. Lai H., Singh N.P. Acute low-intensity microwave exposure increases DNA single-strand breaks in rat brain cells. Bioelectromagnetics 1995, 16:207-210.
2. Lai H., Singh N.P. Single- and double-strand DNA breaks in rat brain cells after acute exposure to radiofrequency electromagnetic radiation. Int. J. Radiat. Biol. 1996, 69:513-521.
3. Vijayalaxmi B.Z., Leal M., Szilagyi T.J., Prihoda M.L., Meltz Primary DNA damage in human blood lymphocytes exposed in vitro to 2450MHz radiofrequency radiation. Radiat. Res. 2000, 153(4):479-486.
4. Salford L.G., Brun A.E., Eberhardt J.L., Marmgren L., Persson B.R. Nerve cell damage in mammalian brain after exposure to microwaves from GSM mobile phones. Environ. Health Perspect. 2003, 111:881-883.
5. Caraglia M., Marra M., Mancinelli F., D'Ambrosio G., Massa R., Giordano A., Budillon A., Abbruzzese A., Bismuto E. Electromagnetic fields at mobile phone frequency induce apoptosis and inactivation of the multi-chaperone complex in human epidermoid cancer cells. J. Cell. Physiol. 2005, 204:539-548.
6. Diem E., Schwarz C., Adlkofer F., Jahn O., Rudiger H. Non-thermal DNA breakage by mobile-phone radiation (1800MHz) in human fibroblasts and in transformed GFSH-R17 rat granulosa cells in vitro. Mutat. Res. 2005, 583:178-183.
7. Belyaev I.Y., Hillert L., Protopopova M., Tamm C., Malmgren L.O., Persson B.R., Selivanova G., Harms-Ringdahl M. 915MHz microwaves and 50Hz magnetic field affect chromatin conformation and 53BP1 foci in human lymphocytes from hypersensitive and healthy persons. Bioelectromagnetics 2005, 26:173-184.
8. Lixia S., Yao K., Kaijun W., Deqiang L., Huajun H., Xiangwei G., Baohong W., Wei Z., Jianling L., Wei W. Effects of 1.8GHz radiofrequency field on DNA damage and expression of heat shock protein 70 in human lens epithelial cells. Mutat. Res. 2006, 602:135-142.
9. Panagopoulos D.J., Chavdoula E.D., Nezis I.P., Margaritis L.H. Cell death induced by GSM 900MHz and DCS 1800MHz mobile telephony radiation. Mutat. Res. 2007, 626:69-78.
10. Malyapa R.S., Ahern E.W., Straube W.L., Moros E.G., Pickard W.F., Roti Roti J.L. Measurement of DNA damage after exposure to 2450MHz electromagnetic radiation. Radiat. Res. 1997, 148:608-617.
11. Malyapa R.S., Ahern E.W., Straube W.L., Moros E.G., Pickard W.F., Roti Roti J.L. Measurement of DNA damage after exposure to electromagnetic radiation in the cellular phone communication frequency band (835.62 and 847.74MHz). Radiat. Res. 1997, 148:618-627.
12. Malyapa R.S., Ahern E.W., Bi C., Straube W.L., LaRegina M., Pickard W.F., Roti Roti J.L. DNA damage in rat brain cells after in vivo exposure to 2450MHz electromagnetic radiation and various methods of euthanasia. Radiat. Res. 1998, 149:637-645.
13. Capri M., Scarcella E., Bianchi E., Fumelli C., Mesirca P., Agostini C., Remondini D., Schuderer J., Kuster N., Franceschi C., Bersani F. 1800MHz radiofrequency (mobile phones, different Global System for Mobile communication modulations) does not affect apoptosis and heat shock protein 70 level in peripheral blood mononuclear cells from young and old donors. Int. J. Radiat. Biol. 2004, 80:389-397.
14. Capri M., Scarcella E., Fumelli C., Bianchi E., Salvioli S., Mesirca P., Agostini C., Antolini A., Schiavoni A., Castellani G., Bersani F., Franceschi C. In vitro exposure of human lymphocytes to 900MHz CW and GSM modulated radiofrequency: studies of proliferation, apoptosis and mitochondrial membrane potential. Radiat. Res. 2004, 162:211-218.
15. Hook G.J., Zhang P., Lagroye I., Li L., Higashikubo R., Moros E.G., Straube W.L., Pickard W.F., Baty J.D., Roti Roti J.L. Measurement of DNA damage and apoptosis in molt-4 cells after in vitro exposure to radiofrequency radiation. Radiat. Res. 2004, 161:193-200.
16. Zeni O., Romano M., Perrotta A., Lioi M.B., Barbieri R., d'Ambrosio G., Massa R., Scarfi M.R. Evaluation of genotoxic effects in human peripheral blood leukocytes following an acute in vitro exposure to 900MHz radiofrequency fields. Bioelectromagnetics 2005, 26:258-265.
17. Belyaev I.Y., Koch C.B., Terenius O., Roxstrom-Lindquist K., Malmgren L.O., Sommer H., Salford L.G., Persson B.R. Exposure of rat brain to 915MHz GSM microwaves induces changes in gene expression but not double stranded DNA breaks or effects on chromatin conformation. Bioelectromagnetics 2006, 27:295-306.
18. Verschaeve L. Genetic effects of radiofrequency radiation (RFR). Toxicol. Appl. Pharmacol. 2005, 207:336-341. Review.
19. Speit G., Schütz P., Hoffmann H. Genotoxic effects of exposure to radiofrequency electromagnetic fields (RF-EMF) in cultured mammalian cells are not independently reproducible. Mutat. Res. 2007, 626:42-47.
20. Scarfi M.R., Sannino A., Perrotta A., Sarti M., Mesirca P., Bersani F. Evaluation of genotoxic effects in human fibroblasts after intermittent exposure to 50Hz electromagnetic fields: a confirmatory study. Radiat. Res. 2005, 164:270-276.
21. 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.
22. Ziemann C., Brockmeyer H., Reddy S.B., Vijayalaxmi T.J., Prihoda N., Kuster T., Tillmann C., Dasenbrock Absence of genotoxic potential of 902MHz (GSM) and 1747MHz (DCS) wireless communication signals: in vivo two-year bioassay in B6C3F1 mice. Int. J. Radiat. Biol. 2009, 85:454-464.
23. Pacini S., Ruggiero M., Sardi I., Aterini S., Gulisano F., Gulisano M. Exposure to global system for mobile communication (GSM) cellular phone radiofrequency alters gene expression, proliferation, and morphology of human skin fibroblasts. Oncol. Res. 2002, 13:19-24.
24. Nylund R., Leszczynski D. Proteomics analysis of human endothelial cell line EA.hy926 after exposure to GSM 900 radiation. Proteomics 2004, 4:1359-1365.
25. Nylund R., Leszczynski D. Mobile phone radiation causes changes in gene and protein expression in human endothelial cell lines and the response seems to be genome- and proteome-dependent. Proteomics 2006, 6:4769-4780.
26. Kwee S., Raskmark P., Velizarov S. Changes in cellular proteins due to environmental non-ionizing radiation. I. Heat-shock proteins. Electro. Magnetobiol. 2001, 20:141-152.
27. Shallom J.M., DiCarlo A.L., Ko D., Penafiel L.M., Nakai A. Microwave exposure induces hsp70 and confers protection against hypoxia in chick embryos. J. Cell. Biochem. 2002, 86:490-496.
28. Lee K.S., Choi J.S., Hong S.Y., Son T.H., Yu K. Mobile phone electromagnetic radiation activates MAPK signaling and regulates viability in Drosophila. Bioelectromagnetics 2008, 29:371-379.
29. Grigor'ev IuG. Biological effects of mobile phone electromagnetic field on chick embryo (risk assessment using the mortality rate). Radiats. Biol. Radioecol. 2003, 43:541-543.
30. Magras I.N., Xenos T.D. RF radiation-induced changes in the prenatal development of mice. Bioelectromagnetics 1997, 18:455-461.
31. Weisbrot D., Lin H., Ye L., Blank M., Goodman R. Effects of mobile phone radiation on reproduction and development in Drosophila melanogaster. J. Cell. Biochem. 2003, 89:48-55.
32. Panagopoulos D.J., Karabarbounis A., Margaritis L.H. Effect of GSM 900-MHz mobile phone radiation on the reproductive capacity of Drosophila melanogaster. Electromagn. Biol. Med. 2004, 23:29-43.
33. Panagopoulos D.J., Chavdoula E.D., Karabarbounis A., Margaritis L.H. Comparison of bioactivity between GSM 900MHz and DCS 1800MHz mobile telephony radiation. Electromagn. Biol. Med. 2007, 26:33-44.
34. Chauhan V., Qutob S.S., Lui S., Mariampillai A., Bellier P.V., Yauk C.L., Douglas G.R., Williams A., McNamee J.P. Analysis of gene expression in two human-derived cell lines exposed in vitro to a 1.9GHz pulse modulated radiofrequency field. Proteomics 2007, 7:3896-3905.
35. Ono T., Saito Y., Komura J., Ikehata H., Yarusawa Y., Nojima T., Goukon K., Ohba Y., Wang J., Fujiwara O., Sato R. Absence of mutagenic effects of 2.45GHz radiofrequency exposure in spleen, liver, brain and testis of lacZ-transgenic mouse exposed in utero. Tohoku J. Exp. Med. 2004, 202:93-103.
36. Kumlin T., Iivonen H., Miettinen P., Juvonen A., Van Groen T., Puranen L., Pitkäaho R., Juutilainen J., Tanila H. Mobile phone radiation and the developing brain: behavioral and morphological effects in juvenile rats. Radiat. Res. 2007, 168:471-479.
37. Ivancsits S., Diem E., Pilger A., Rudiger H.W., Jahn O. Induction of DNA strand breaks by intermittent exposure to extremely-low-frequency electromagnetic fields in human diploid fibroblasts. Mutat. Res. 2002, 519:1-13.
38. Panagopoulos D.J., Margaritis L.H. The effect of exposure duration on the biological activity of mobile telephony radiation. Mut. Res. 2010, 699:17-22.
39. Panagopoulos D.J., Margaritis L.H. Mobile telephony radiation effects on living organisms. Mobile Telephones, Network Applications and Performance 2008, 107-149. Nova Science Publishers Inc., Review. A.C. Harper, R.V. Burees (Eds.).
40. Panagopoulos D.J., Chavdoula E.D., Margaritis L.H. Bioeffects of mobile telephony radiation in relation to its intensity or distance from the antenna. Int. J. Radiat. Biol. 2010, 86(5):345-357.
41. Panagopoulos D.J., Margaritis L.H. The identification of an intensity " Window" on the bioeffects of mobile telephony radiation. Int. J. Radiat. Biol. 2010, 86(5):358-366.
42. Nikolova T., Czyz J., Rolletschek A., Blyszczuk P., Fuchs J., Jovtchev G., Schuderer J., Kuster N., Wobus A.M. Electromagnetic fields affect transcript levels of apoptosis-related genes in embryonic stem cell-derived neural progenitor cells. ASEB J. 2005, 19:1686-1688.
43. King R.C. Origin and development of the egg chamber within the adult ovarioles. Ovarian Development in Drosophila melanogaster 1970, 38-54. Academic Press, New York London. R.C. King (Ed.).
44. Margaritis L.H. Structure and physiology of the eggshell. Comprehensive Insect Biochemistry, Physiology and Pharmacology 1985, vol. 1:151-230. Pergammon, Oxford New York.
45. Margaritis L.H. The eggshell of Drosophila melanogaster. New staging characteristics and fine structural analysis of choriogenesis. Can. J. Zool. 1986, 64:2152-2175.
46. Spradling A.C. Developmental genetics of oogenesis. The Development of Drosophila melanogaster 1993, vol. I:1-70. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
47. Robinson D.N., Kant K., Cooley L. Morphogenesis of Drosophila ovarian ring canals. Development 1994, 120:2015-2025.
48. Cavaliere V., Taddei C., Gargiulo G. Apoptosis of nurse cells at the late stages of oogenesis of Drosophila melanogaster. Dev. Genes Evol. 1998, 208:106-112.
49. Foley K., Cooley L. Apoptosis in late stage Drosophila nurse cells does not require genes within the H99 deficiency. Development 1998, 125:1075-1082.
50. McCall K., Steller H. Requirement for DCP-1 caspase during Drosophila oogenesis. Science 1998, 279:230-234.
51. Nezis I.P., Stravopodis D.J., Papassideri I., Robert-Nicoud M., Margaritis L.H. Stage-specific apoptotic patterns during Drosophila oogenesis. Eur. J. Cell. Biol. 2000, 79:610-620.
52. Nezis I.P., Stravopodis D.J., Papassideri I., Margaritis L.H. Actin cytoskeleton reorganization of the apoptotic nurse cells during the late developmental stages of oogenesis in Dacus oleae. Cell. Motil. Cytoskeleton 2001, 48:224-233.
53. Nezis I.P., Stravopodis D.J., Papassideri I., Robert-Nicoud M., Margaritis L.H. The dynamics of apoptosis in the ovarian follicle cells during the late stages of Drosophila oogenesis. Cell Tissue Res. 2002, 307:401-409.
54. McCall K. Eggs over easy: cell death in the Drosophila ovary. Dev. Biol. 2004, 274:3-14.
55. ICNIRP Guide lines for limiting exposure to time-varying electric, magnetic and electromagnetic fi{ligature}elds (up to 300GHz). Health Phys. 1998, 74:494-522.
56. Nias A.H.W. An Introduction to Radiobiology 1998, J. Wiley & sons. 2nd ed.
57. Hall E.J., Giaccia A.J. Radiobiology for the Radiologist 2006, Lippincott Williams & Wilkins, Philadelphia.
58. Drummond-Barbosa D., Spradling A.C. Stem cells and their progeny respond to nutritional changes during Drosophila oogenesis. Dev. Biol. 2001, 23:265-278.
59. Panagopoulos D.J., Messini N., Karabarbounis A., Filippetis A.L., Margaritis L.H. A mechanism for action of oscillating electric fi{ligature}elds on cells. Biochem. Biophys. Res. Commun. 2000, 272:634-640.
60. Panagopoulos D.J., Karabarbounis A., Margaritis L.H. Mechanism for action of electromagnetic fields on cells. Biochem. Biophys. Res. Commun. 2002, 298:95-102.
61. Panagopoulos D.J., Margaritis L.H. Theoretical considerations for the biological effects of electromagnetic fields. Biological Effects of Electromagnetic Fields 2003, 5-33. Springer. P. Stavroulakis (Ed.).
62. Joubert V., Bourthoumieu S., Leveque P., Yardin C. Apoptosis is induced by radiofrequency fields through the caspase-independent mitochondrial pathway in cortical neurons. Radiat. Res. 2008, 169:38-45.
63. Kerr J.F.R., Wyllie A.H., Currie A.R. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 1972, 26:239-257.
64. Mills J.C., Stone N.L., Pittman R.N. Extranuclear apoptosis. The role of the cytoplasm in the execution phase. J. Cell. Biol. 1999, 146:703-708.