Human fibroblasts and 900 MHz radiofrequency radiation: Evaluation of DNA damage after exposure and co-exposure to 3-chloro-4-(dichloromethyl)-5-hydroxy- 2(5h)-furanone (MX)

Radiation Research

Volumn 171, Issue 6, 2009, Pages 743-751

  Sannino, A ^a   Di Costanzo, G ^a   Brescia, F ^a   Sarti, M ^a   Zeni, O ^a   Juutilainen, J ^b   Scarf, M R ^a  

^a CNR   (Italy)

^b UNIVERSITY OF EASTERN FINLAND   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

3 CHLORO 4 DICHLOROMETHYL 5 HYDROXY 2(5H) FURANONE; CHLORINE DERIVATIVE; DRINKING WATER; FURANONE DERIVATIVE; HYDROXYL GROUP; METHYL GROUP; UNCLASSIFIED DRUG; 3-CHLORO-4-(DICHLOROMETHYL)-5-HYDROXY-2(5H)-FURANONE; DNA; FURAN DERIVATIVE; MUTAGENIC AGENT;

ADULT; ARTICLE; CHLORINATION; COMET ASSAY; CONTROLLED STUDY; CYTOKINESIS; CYTOTOXICITY; DNA DAMAGE; DOSIMETRY; EVALUATION; GENOTOXICITY; HUMAN; HUMAN CELL; MICRONUCLEUS TEST; MOBILE PHONE; NORMAL HUMAN; PRIORITY JOURNAL; RADIATION EXPOSURE; RADIOFREQUENCY RADIATION; SKIN FIBROBLAST; TURNER SYNDROME; CELL CULTURE; CELL LINE; CELL PROLIFERATION; CELL SURVIVAL; DRUG EFFECT; FIBROBLAST; GENETICS; PATHOLOGY; TEMPERATURE;

CELL LINE; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; COMET ASSAY; DNA; DNA DAMAGE; FIBROBLASTS; FURANS; HUMANS; MICRONUCLEUS TESTS; MUTAGENS; RADIO WAVES; TEMPERATURE; TURNER SYNDROME;

EID: 67849114330     PISSN: 00337587     EISSN: None     Source Type: Journal    
DOI: 10.1667/RR1642.1     Document Type: Article

References (64)

1. M. L. Meltz, Radiofrequency exposure and mammalian cell toxicity, genotoxicity and transformation. Bioelectromagnetics Suppl. 6, 196-213 (2003).
2. 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).
3. L. Verschaeve, Genetic effects of radiofrequency radiation (RFR). Toxicol. Appl. Pharmacol. 207, 336-341 (2005).
4. Vijayalaxmi and G. Obe, Controversial cytogenetic observations in mammalian somatic cells exposed to radiofrequency radiation. Radiat. Res. 162, 481-496 (2004).
5. J. L. Phillips, O. Ivaschuk, T. Ishida-Jones, R. A. Jones and M. Campbell-Beachler, DNA damage in Molt-4 T-lymphoblastoid cells exposed to cellular telephone radiofrequency fields in vitro. Bioelectrochem. Bioenerg. 45, 103-110 (1998).
6. G. d'Ambrosio, R. Massa, M. R. Scarfí and O. Zeni, Cytogenetic damage in human lymphocytes following GMSK phase modulated microwave exposure. Bioelectromagnetics 23, 7-13 (2002).
7. R. R. Tice, G. G. Hook, M. Donner, D. I. McRee and A. W. Guy, Genotoxicity of Radiofrequency signals. I. Investigation of DNA damage and micronuclei induction in cultured human blood cells. Bioelectromagnetics 23, 113-126 (2002).
8. M. Mashevich, D. Folkman, A. Kesar, A. Barbul, R. Korenstein, E. Jerby and L. Avivi, Exposure of human peripheral blood lymphocytes to electromagnetic fields associated with cellular phones leads to chromosomal instability. Bioelectromagnetics 24, 82-90 (2003).
9. L. Zotti-Martelli, M. Peccatori, V. Maggini, M. Ballardin and R. Barale, Individual responsiveness to induction of micronuclei in human lymphocytes after exposure in vitro to 1800-MHz microwave radiation. Mutat. Res. 582, 42-52 (2005).
10. E. Diem, C. Schwarz, F. Adlkofer, O. Jahn and H. Ruediger, Non-thermal DNA breakage by mobile-phone radiation (1800 MHz) in human fibroblasts and in transformed GFSH-R17 rat granulosa cells in vitro. Mutat. Res. 583, 178-183 (2005).
11. C. Schwarz, E. Kratochvil, A. Pilger, N. Kuster, F. Adlkofer and H. W. Rüdiger, Radiofrequency electromagnetic fields (UMTS, 1,950 MHz) induce genotoxic effects in vitro in human fibroblasts but not in lymphocytes. Int. Arch. Occup. Environ. Health 81, 755-767 (2008).
12. Vijayalaxmi and T. J. Prihoda, Genetic damage in mammalian somatic cells exposed to radiofrequency radiation: A metaanalysis of data from 63 publications (1990-2005). Radiat. Res. 169, 561-574 (2008).
13. W. Burkart and T. Jung, Health risks from combined exposures: mechanistic considerations on deviations from additivity. Mutat. Res. 411, 119-128 (1998).
14. A. Maes, M. Collier, D. Slaets and L. Verschaeve, 954 MHz microwaves enhance the mutagenic properties of mitomycin C. Environ. Mol. Mutagen. 28, 26-30 (1996).
15. A. Maes, M. Collier, U. Van Gorp, S. Vandoninck and L. Verschaeve, Cytogenetic effects of 935.2-MHz (GSM) microwaves alone and in combination with Mitomycin-C. Mutat. Res. 393, 151-156 (1997).
16. W. Baohong, H. Jiliang, J. Lifen, L. Dequiang, Z. Wei, L. Jianlin and D. Hongping, Studying the synergistic damage effects induced by 1.8 GHz radiofrequency field radiation (RFR) with four chemical mutagens on human lymphocyte DNA using comet assay in vitro. Mutat. Res. 578, 149-57 (2005).
17. W. Baohong, J. Lifen, L. Lanjuan, L. Jianlin, L. Dequiang, Z. Wei and H. Jiliang, Evaluating the combinative effects on human lymphocyte DNA damage induced by ultraviolet ray C plus 1.8 GHz microwaves using comet assay in vitro. Toxicology 232, 311-316 (2007).
18. J. Y. Kim, S. Y. Hong, Y. M. Lee, S. A. Yu, W. S. Koh, J. R. Hong, T. Son, S. K. Chang and M. Lee, In vitro assessment of clastogenicity of mobile-phone radiation (835 MHz) using the alkaline comet assay and chromosomal aberration test. Environ. Toxicol. 23, 319-27 (2008).
19. J. J. Kerbacher, M. L. Meltz and D. N. Erwin, Influence of radiofrequency radiation on chromosome aberrations in CHO cells and its interaction with DNA-damaging agents. Radiat. Res. 123, 311-319 (1990).
20. V. Ciaravino, M. L. Meltz and D. N. Erwin, Absence of a synergistic effect between moderate-power radio-frequency electromagnetic radiation and Adriamycin on cell-cycle progression and sister-chromatid exchange. Bioelectromagnetics 12, 289-298 (1991).
21. A. Maes, M. Collier and L. Verschaeve, Cytogenetic effects of 900 MHz (GSM) microwaves on human lymphocytes. Bioelec-tromagnetics 22, 91-96 (2001).
22. L. Stronati, A. Testa, J. Moquet, A. Edwards, E. Cordelli, P. Villani, C. Marino, A. M. Fresegna, M. Appolloni and D. Lloyd, 935 MHz cellular phone radiation. An in vitro study of genotoxicity in human lymphocytes. Int. J. Radiat. Biol. 82, 339-346 (2006).
23. J. Hemming, B. Holmbom, M. Reunanen and L. Kronberg, Determination of strong mutagen 3-chloro-4-(dichloromethyl)-5-hydroxy-2(5H)-furanone in chlorinated drinking and humic waters. Chemosphere 15, 549-556 (1986).
24. J. R. Meier, R. B. Knohl, W. E. Coleman, H. P. Ringhand, J. W. Munch, W. H. Kaylor, R. P. Streicher and F. C. Kopfler, Studies on the potent bacterial mutagen 3-chloro-4-(dichloromethyl)-5-hydroxy-2(5H)-furanone: aqueous stability, XAD recovery and analytical determination in drinking water and in chlorinated humic acid solutions. Mutat. Res. 189, 363-373 (1987)
25. L. Kronberg and T. Vartiainen, Ames mutagenicity and concentration of the strong mutagen 3-chloro-4-(dichloromethyl)-5-hydroxy-2(5H)-furanone and of its geometric isomer E-2-chloro-3-(dichloromethyl)-4-oxobutenoic acid in tap water. Mutat. Res. 206, 177-182 (1988).
26. J. Maki-Paakkanen and P. Hakulinen, Assessment of the genotoxicity of the rat carcinogen 3-chloro-4-(dichloromethyl)-5-hydroxy-2(5H)-furanone (MX) in rat liver epithelial cells in vitro. Toxicol. In Vitro 22, 535-40 (2008).
27. K. Jansson, J. Maki-Paakkanen, S. L. Vartiainen, T. Vartiainen, H. Kumulainen and J. Tuomisto, Cytogenetic effects of 3-chloro-4-(dichloromethyl)- 5-hydroxy-2(5H)-furanone (MX), in rat peripheral lymphocytes in vitro and in vivo. Mutat. Res. 299, 25-28 (1993).
28. J. Maki-Paakkanen, K. Jansson and T. Vartiainen, Induction of mutation, sister chromatid exchanges and chromosome aberrations by 3-chloro-4- (dichloromethyl)-5-hydroxy-2(5H)-furanone in Chinese hamster ovary cells. Mutat. Res. 310, 117-123 (1994).
29. F. Le Curieux, F. Nesslany, T. Munter, L. Kronberg and D. Marzin, Genotoxic activity of chlorohydroxyfuranones in the microscale micronucleus test on mouse lymphoma cells and the unscheduled DNA synthesis assay in rat hepatocytes. Mutagenesis 14, 457-462 (1999).
30. J. M. Hyttinen, S. Myohanen and K. Jansson, Kinds of mutations induced by 3-chloro-4-(dichloromethyl)-5-hydroxy-2(5H)-furanone (MX) in the hprt gene of Chinese hamster ovary cells. Carcinogenesis 17, 1179-1181 (1996).
31. O. Zeni, R. Di Pietro, F. Salvemini, D. Buonincontri, H. Komulainen, M. Romanó and M. R. Scarfí, Induction of oxidative stress in murine cell lines by 3-chloro-4-(dichloromethyl)-5-hydroxy-2(5H)-furanone (MX). Toxicol. Lett. 147, 79-85 (2004).
32. J. Yuan, H. Liu, L. Zhou, Y. Zou and W. Lu, Oxidative stress and DNA damage induced by a drinking-water chlorination disinfection by-product 3-chloro-4-(dichloromethyl)-5-hydroxy-2(5H)-furanone (MX) in mice. Mutat. Res. 609, 129-136 (2006).
33. P. Hakulinen, J. Maki-Paakkanen, J. Naarala, L. Kronberg and H. Komulainen, Potent inhibition of gap junctional intercellular communication by 3-chloro-4-(dichloromethyl)-5-hydroxy-2(5H)-furanone (MX) in BALB/c 3T3 cells. Toxicol. Lett. 151, 439-449 (2004).
34. P. Hakulinen, E. Rintala, J. Maki-Paakkanen and H. Komulainen, Altered expression of connexin43 in the inhibition of gap junctional intercellular communication by chlorohydroxyfuranones in WB-F344 rat liver epithelial cells. Toxicol. Appl. Pharmacol. 212, 146-155 (2006).
35. A. Nishikawa, K. Sai, K. Okazaki, H. Y. Son, K. Kanki, M. Nakajima, N. Kinae, T. Nohmi, J. E. Trosko and M. Hirose, MX, a by-product of water chlorination, lacks in vivo genotoxicity in gpt delta mice but inhibits gap junctional intercellular communication in rat WB cells. Environ. Mol. Mutagen. 47, 48-55 (2006).
36. H. Komulainen, V. M. Kosma, S. L. Vaittinen, T. Vartiainen, E. Kaliste-Korhnonen, S. Lotjonen, R. K. Tuominen and J. Tuomisto, Carcinogenicity of the drinking water mutagen 3-chloro-4-(dichloromethyl)-5-hydroxy-2(5H)- furanone in the rat. J. Natl. Cancer Inst. 89, 848-856 (1997).
37. P. Heikkinen, H. Ernst, H. Huuskonen, H. Komulainen, T. Kumlin, J. Maki-Paakkanen, L. Puranen and J. Juutilainen, No effects of radiofrequency radiation on 3-chloro-4-(dichloromethyl)-5-hydroxy-2(5H)-furanone-induced tumorigenesis in female Wistar rats. Radiat. Res. 166, 397-408 (2006).
38. L. Verschaeve, P. Heikkinen, G. Verheyen, U. Van Gorp, F. Boonen, F. Vander Plaerse, A. Maes, T. Kumlin, J. Maki-Paakkanen and J. Juutilainen, Investigation of co-genotoxic effects of radiofrequency electromagnetic fields in vivo. Radiat. Res. 165, 598-607 (2006).
39. O. Zeni and R. Di Pietro, G. d'Ambrosio, R. Massa, M. Capri, J. Naarala, J. Juutilainen, M. R. Scarfí, Kinetics of reactive oxygen species formation in L929 cell cultures after exposure and coexposure to RF radiation (900 MHz) and 3-chloro-4-(dichloromethyl)-5-hydroxy-2(5H)-furanone (MX). Radiat. Res. 167, 306-311 (2007).
40. E. B. Hook and J. L. Hamertton, The frequency of chromosome abnormalities detected in consecutive newborn studies - results by sex and severity of phenotypic involvement. In Population Cytogenetic Studies in Humans (E. B. Hook and I. H. Porter, Eds.), pp. 63-78. Academic Press, New York, 1977.
41. A. Robinson, Demography and prevalence of Turner syndrome. In Turner Syndrome (R. G. Rosenfeld and M. M. Grumbach, Eds.), pp. 93-105. Marcel Dekker, New York, 1990.
42. M. R. Scarfí, F. Prisco, M. B. Lioi, F. Bersani, G. Franceschetti, O. Zeni, R. Di Pietro, M. Della Noce, C. Franceschi and G. Stoppoloni, Extremely low frequency pulsed magnetic field cytogenetic effects on lymphocytes from Turner's syndrome subjects. Bioelectrochem. Bioenerg. 43, 221-226 (1997).
43. M.R. Scarfí, F. Prisco, M. B. Lioi, O. Zeni, M. Della Noce, R. Di Pietro, C. Franceschi and F. Bersani, 50 Hz, 1 mT sinusoidal magnetic fields do not affect micronucleus frequency and cell proliferation in human lymphocytes from normal and Turner's syndrome subjects. Electro. Magnetobiol. 16, 301-307 (1997).
44. International Commission for Non-Ionising Radiation Protection, Guidelines for limiting exposure to time varying electric, magnetic, and electromagnetic fields (up to 300 GHz). Health Phys. 74, 494-522 (1998).
45. M. R. Scarfí, A. M. Fresegna, P. Villani, R. Pinto, C. Marino, M. Sarti, A. Sannino, P. Altavista and G. A. Lovisolo, Exposure to radiofrequency radiation (900 MHz, GSM signal) does not affect micronucleus frequency and cell proliferation in human peripheral blood lymphocytes. Radiat. Res. 165, 655-663 (2006).
46. R. Palumbo, F. Brescia, D. Capasso, A. Sannino, M. Sarti, M. Capri, E. Grassilli and M. R. Scarfí, Exposure to 900 MHz radiofrequency radiation induces caspase 3 activation in proliferating human lymphocytes. Radiat. Res. 170, 327-334 (2008).
47. L. Laval, P. H. Leveque and B. Jecko, A new in vitro exposure device for the mobile frequency of 900 MHz. Bioelectromagnetics 21, 255-263 (2000).
48. A. Padmapriya, G. Just and N. G. Lewis, Synthesis of 3-chloro-4- (dichloromethyl)-5-hydroxy-2(5H)furanone, a potent mutagen. Can. J. Chem. 63, 828-832 (1985).
49. M. Fenech, The cytokinesis-block micronucleus technique: A detailed description of the method and its application to genotoxicity studies in human population. Mutat. Res. 285, 35-44 (1993).
50. M. Fenech, The cytokinesis-block micronucleus technique and its application to genotoxicity studies in human populations. Environ. Health Perspect. 101 (Suppl. 3), 101-107 (1993).
51. J. Surralles, N. Xamena, A. Creus, J. Catalan, H. Norppa and R. Marcos, Induction of micronuclei by five pyrethroid insecticides in whole-blood and isolated human lymphocyte cultures. Mutat. Res. 341, 169-184 (1995).
52. M. Kirsch-Volders, T. Sofuni, M. Aardema, S. Albertini, D. Eastmond, M. Fenech, M. Ishidate, S. Kirchner, E. Lorge and A. Wakata, Report from the in vitro micronucleus assay working group. Mutat. Res. 540, 153-163 (2003).
53. N. P. Singh, M. T. McCoy, R. R. Tice and E. L. Schneider, A simple technique for quantization of low level of DNA damage in individual cells. Exp. Cell. Res. 175, 184-187 (1988).
54. M. R. Scarfí and F. Bersani, Radiofrequency radiation and replication studies. In Chromosomal Alterations: Importance in Human Health (Vijayalaxmi and G. Obe, Eds.), pp. 471-479. Elsevier, Amsterdam, 2007.
55. S. Ivancsits, A. Pilger, E. Diem, O. Jahn and H. W. Rudiger, Cell type-specific genotoxic effects of intermittent extremely low-frequency electromagnetic fields. Mutat. Res. 583, 184-188 (2005).
56. Vijayalaxmi, J. P. McNamee and M. R. Scarfí, Comments on DNA strand breaks reported by Diem et al. in Mutation Research, 583, 178-183, 2005
57. and Ivancsits et al. in Mutation Research, 583, 184-188, 2005.
58. Mutat. Res. 603, 104-106 (2006).
59. A. Lerchl, Comments on "Radiofrequency electromagnetic fields (UMTS, 1,950 MHz) induce genotoxic effects in vitro in human fibroblasts but not in lymphocytes" by Schwarz et al. (Int. Arch. Occup. Environ. Health 81, 755-67 (2008)).
60. Int. Arch. Occup. Environ. Health 2008. doi: 10.1007/s00420-008- 0305-5.
61. M. R. Scarfí, A. Sannino, A. Perrotta, M. Sarti, P. Mesirca and F. Bersani, Evaluation of genotoxic effects on human fibroblasts following intermittent exposures to 50 Hz electromagnetic fields: a confirmation study. Radiat. Res. 164, 270-276 (2005).
62. G. Speit, P. Schutz and H. Hoffmann, Genotoxic effects of exposure to radiofrequency electromagnetic fields (RF-EMF) in cultured mammalian cells are not independently reproducible. Mutat. Res. 626, 42-47 (2007).
63. O. Zeni, M. Romanó, A. Perrotta, M. B. Lioi, R. Barbieri, G. d'Ambrosio, R. Massa and M. R. Scarfí, Evaluation of genotoxic effects in human peripheral blood leukocytes following an acute in vitro exposure to 900 MHz radiofrequency field. Bioelectromagnetics 26, 258-265 (2005).
64. J. Juutilainen, P. Heikkinen, H. Soikkeli and J. Máki-Paakkanen, Micronucleus frequency in mice after long-term exposure to radiofrequency radiation. Int. J. Radiat. Biol. 83, 213-220 (2007).