Molecular basis underlying the biological effects elicited by extremely low-frequency magnetic field (ELF-MF) on neuroblastoma cells

Journal of Cellular Biochemistry

Volumn 112, Issue 12, 2011, Pages 3797-3806

  Sulpizio, Marilisa ^a   Falone, Stefano ^a   Amicarelli, Fernanda ^b   Marchisio, Marco ^a   Di Giuseppe, Fabrizio ^a   Eleuterio, Enrica ^a   Di Ilio, Carmine ^a   Angelucci, Stefania ^a  

^a UNIVERSITY OF CHIETI   (Italy)

^b UNIVERSITY OF L'AQUILA   (Italy)

Author keywords

50 Hz magnetic fields; Differentiation; Human health; Neuroblastoma; Proliferation; Proteome

Indexed keywords

3 MERCAPTOPYRUVATE SULFURTRANSFERASE; ACTIN CYTOPLASMATIC 2; PEROXIREDOXIN 2; PEROXIREDOXIN 3; PEROXIREDOXIN 6; PROFILIN II; PROTEIN; PROTEOME; ROPPORIN 1A; SPINDLIN 1; T COMPLEX PROTEIN SUBUNIT BETA; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CELL COUNT; CELL GROWTH; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; CYTOSKELETON; ELECTROMAGNETIC FIELD; EXTREMELY LOW FREQUENCY MAGNETIC FIELD; HUMAN; HUMAN CELL; NEUROBLASTOMA CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RADIATION EXPOSURE;

CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; HUMANS; IMMUNOHISTOCHEMISTRY; MAGNETICS; NEUROBLASTOMA; PROTEOME;

HELIOTHIS ZEA VIRUS 1;

EID: 80054983110     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.23310     Document Type: Article

References (68)

1. An JH, Seong JS,. 2006. Proteomics analysis of apoptosis-regulating proteins in tissues with different radiosensitivity. J Radiat Res 47: 147-155. (Pubitemid 44034033)
2. Angelucci S, Marchisio M, Di Giuseppe F, Pierdomenico L, Sulpizio M, Lanuti P, Sabatino G, Miscia S, Di Ilio C,. 2010. Proteome analysis of human Wharton's jelly cells during in vitro expansion. Proteome Sci 8: 1-18.
3. Berg A, Berg H,. 2006. Influence of ELF sinusoidal electromagnetic fields on proliferation and metabolite yield of fungi. Electromagn Biol Med 25 (1): 71-77.
4. Cao Z, Bhella D, Lindsay G,. 2007. Reconstitution of the mitochondrial Prxlll antioxidant defence pathway: General properties and factors affecting Prxlll activity and oligomeric state. J Mol Biol 372: 1022-1033. (Pubitemid 47368351)
5. Chang XZ, Li DQ, Hou YF, Wu J, Lu JS, Di GH, Jin W, Ou ZL, Shen ZZ, Shao ZM,. 2007. Identification of the functional role of peroxiredoxin 6 in the progression of breast cancer. Breast Cancer Res 9 (6): R76.
6. Chemale G, Perally S, LaCourse EJ, Prescott MC, Jones LM, Ward D, Meaney M, Hoey E, Brennan GP, Fairweather I, Trudgett A, Brophy PM,. 2010. Comparative proteomic analysis of triclabendazole response in the liver fluke Fasciola hepatica. J Proteome Res 9 (10): 4940-4951.
7. Cooper GM,. 2000. The cell: Molecular approach, 2nd edn. Sunderland: Sinauer Associates.
8. Crumpton MJ, Collins AR,. 2004. Are environmental electromagnetic fields genotoxic? DNA Repair (Amst) 3 (10): 1385-1387. (Pubitemid 39164601)
9. Davanipour Z, Tseng CC, Lee PJ, Sobel E,. 2007. A case-control study of occupational magnetic field exposure and Alzheimer's disease: Results from the California Alzheimer's Disease Diagnosis and Treatment Centers. BMC Neurol 7: 13.
10. Di Loreto S, Falone S, Caracciolo V, Sebastiani P, D'Alessandro A, Mirabilio A, Zimmitti V, Amicarelli F,. 2009. Fifty hertz extremely low-frequency magnetic field exposure elicits redox and trophic response in rat-cortical neurons. J Cell Physiol 219 (2): 334-343.
11. Draper G, Vincent T, Kroll ME, Swanson J,. 2005. Childhood cancer in relation to distance from high voltage power lines in England and Wales: A case-control study. BMJ 330 (7503): 1290.
12. Falone S, Grossi MR, Cinque B, D'Angelo B, Tettamanti E, Cimini A, Di Ilio C, Amicarelli F,. 2007. Fifty hertz extremely low-frequency electromagnetic field causes changes in redox and differentiative status in neuroblastoma cells. Int J Biochem Cell Biol 39 (11): 2093-2106. (Pubitemid 47369242)
13. Falone S, Mirabilio A, Carbone MC, Zimmitti V, Di Loreto S, Mariggià MA, Mancinelli R, Di Ilio C, Amicarelli F,. 2008. Chronic exposure to 50 Hz magnetic fields causes a significant weakening of antioxidant defence systems in aged rat brain. Int J Biochem Cell Biol 40 (12): 2762-2770.
14. Ferrari-Toninelli G, Bonini SA, Uberti D, Buizza L, Bettinsoli P, Poliani PL, Facchetti F, Memo M,. 2010. Targeting Notch pathway induces growth inhibition and differentiation of neuroblastoma cells. Neuro Oncol 12 (12): 1231-1243.
15. Frahm J, Lantow M, Lupke M, Weiss DG, Simkõ M,. 2006. Alteration in cellular functions in mouse macrophages after exposure to 50 Hz magnetic fields. J Cell Biochem 99 (1): 168-177. (Pubitemid 44297961)
16. Freshney R,. 1987. Culture of animal cells: A manual of basic technique. New York, USA: Alan R. Liss, Inc. 117 p.
17. Fujita A, Nakamura K, Kato T, Watanabe N, Ishizaki T, Kimura K, Mizoguchi A, Narumiya S,. 2000. Ropporin, a sperm-specific binding protein of rhophilin, that is localized in the fibrous sheath of sperm flagella. J Cell Sci 113 (Pt 1): 103-112. (Pubitemid 30066337)
18. Gharahdaghi F, Weinberg CR, Meagher DA, Imai BS, Mische SM,. 1999. Mass spectrometric identification of proteins from silver-stained polyacrylamide gel: A method for the removal of silver ions to enhance sensitivity. Electrophoresis 20: 601-605. (Pubitemid 29183427)
19. Gottwald E, Sontag W, Lahni B, Weibezahn KF,. 2007. Expression of HSP72 after ELF-EMF exposure in three cell lines. Bioelectromagnetics 28 (7): 509-518. (Pubitemid 47556771)
20. Green LM, Reade JL, Ware CF,. 1984. Rapid colorimetric assay for cell viability: Application to the quantitation of cytotoxic and growth inhibitory lymphokines. J Immunol Methods 70 (2): 257-268. (Pubitemid 14111307)
21. Håkansson N, Gustavsson P, Sastre A, Floderus B,. 2003. Occupational exposure to extremely low frequency magnetic fields and mortality from cardiovascular disease. Am J Epidemiol 158 (6): 534-542. (Pubitemid 37093229)
22. Hall A,. 2009. The cytoskeleton and cancer. Cancer Metastasis 28: 5-14.
23. Hashish AH, El-Missiry MA, Abdelkader HI, Abou-Saleh RH,. 2008. Assessment of biological changes of continuous whole body exposure to static magnetic field and extremely low frequency electromagnetic fields in mice. Ecotoxicol Environ Saf 71: 895-902.
24. Ho JN, Lee SB, Lee SS, Yoon SH, Kang GY, Hwang SG, Um HD,. 2010. Phospholipase A2 activity of peroxiredoxin 6 promotes invasion and metastasis of lung cancer cells. Mol Cancer Ther 9 (4): 825-832.
25. IARC. 2002. Non-ionizing radiation, Part 1: Static and extremely low-frequency electric and magnetic fields. IARC Monogr Eval Carcinog Risk Hum 80: 1-395.
26. Immenschuh S, Vogt EB,. 2005. Peroxiredoxins, oxidative stress, and cell proliferation. Antioxid Redox Signal 7 (5-6): 768-777. (Pubitemid 40563217)
27. Jonckheere V, Lambrechts A, Vandekerckhove J, Ampe C,. 1999. Dimerization of profilin II upon binding the (GP5)3 peptide from VASP overcomes the inhibition of actin nucleation by profilin II and thymosin beta4. FEBS Lett 447 (2-3): 257-263. (Pubitemid 29146097)
28. Jurkowska H, Wrobel M,. 2008. N-acetyl- L -cysteine as a source of sulfane sulphur in astrocytoma and astrocyte cultures: Correlations with cell proliferation. Amino Acids 34: 231-237. (Pubitemid 351238261)
29. Jurkowska H, Placha W, Nagahara N, Wrõbel M,. 2011. The expression and activity of cystathionine-γ-lyase and 3-mercaptopyruvate sulfurtransferase in human neoplastic cell lines. Amino Acids 41 (1): 151-158.
30. Kheifets L, Renew D, Sias G, Swanson J,. 2010. Extremely low frequency electric fields and cancer: Assessing the evidence. Bioelectromagnetics 31 (2): 89-101.
31. Kim H, Lee TH, Park ES, Suh JM, Park SJ, Chung HK, Kwon OY, Kim YK, Ro HK, Shong M,. 2000. Role of peroxiredoxins in regulating intracellular hydrogen peroxide and hydrogen peroxide-induced apoptosis in thyroid cells. J Biol Chem 275 (24): 18266-18270. (Pubitemid 30414779)
32. Kinnula VL, Lehtonen S, Sormunen R, Wiik RK, Kang SW, Rhee SG, Soini Y,. 2002. Overexpression of peroxiredoxin I, II, III, V and VI in malignant mesothelioma. J Pathol 196: 316-323. (Pubitemid 34189421)
33. Li Z, Li W, Meklat F, Zhang J, Zhang Y, Lim SH,. 2007. A yeast two-hybrid system using Sp17 identified Ropporin as a novel cancer-testis antigen in hematologic malignancies. Int J Cancer 121: 1507-1511. (Pubitemid 47328709)
34. Lisi A, Ledda M, Rosola E, Pozzi D, D'Emilia E, Giuliani L, Foletti A, Modesti A, Morris SJ, Grimaldi S,. 2006. Extremely low frequency electromagnetic field exposure promotes differentiation of pituitary corticotrope-derived AtT20 D16V cells. Bioelectromagnetics 27 (8): 641-651. (Pubitemid 44863476)
35. Nevo I, Sagi-Assif O, Edry Botzer L, Amar D, Maman S, Kariv N, Leider-Trejo LE, Savelyeva L, Schwab M, Yron I, Witz IP,. 2008. Generation and characterization of novel local and metastatic human neuroblastoma variants. Neoplasia 10 (8): 816-827.
36. Nicolini G, Miloso M, Zoia C, Di Silvestro A, Cavaletti G, Tredici G,. 1998. Retinoic acid differentiated SH-SY5Y human neuroblastoma cells: An in vitro model to assess drug neurotoxicity. Anticancer Res 18 (4A): 2477-2481. (Pubitemid 28386536)
37. Pak JH, Choi WH, Lee HM, Joo WD, Kim JH, Kim YT, Kim YM, Nam JH,. 2011. Peroxiredoxin 6 overexpression attenuates cisplatin-induced apoptosis in human ovaris cancer cells. Cancer Invest 29 (1): 21-28.
38. Palumbo R, Capasso D, Brescia F, Mita P, Sarti M, Bersani F, Scarfi MR,. 2006. Effects on apoptosis and reactive oxygen species formation by Jurkat cells exposed to 50 Hz electromagnetic fields. Bioelectromagnetics 27 (2): 159-162.
39. Park CK, Kim JH, Moon MJ, Jung JH, Lim SY, Park SH, Kim JH, Kim DG, Jung HW, Cho BK, Paek SH,. 2008. Investigation of molecular factors associated with malignant transformation of oligodendroglioma by proteomic study of a single case of rapid tumor progression. J Cancer Res Clin Oncol 134 (2): 255-262. (Pubitemid 350234071)
40. Pirozzoli MC, Marino C, Lovisolo GA, Laconi C, Mosiello L, Negroni A,. 2003. Effects of 50 Hz electromagnetic field exposure on apoptosis and differentiation in a neuroblastoma cell line. Bioelectromagnetics 24 (7): 510-516. (Pubitemid 38622787)
41. Porstmann T, Ternynck T, Avrameas S,. 1985. Quantitation of 5-bromo-2-deoxyuridine incorporation into DNA: An enzyme immunoassay for the assessment of the lymphoid cell proliferative response. J Immunol Methods 82 (1): 169-179. (Pubitemid 16253231)
42. Quan C, Cha EJ, Lee HL, Han KH, Lee MK, Kim WJ,. 2006. Enhanced expression of peroxiredoxin I and VI correlates with development, recurrence and progression of human bladder cancer. J Urol 175: 1512-1516.
43. Regoli F, Gorbi S, Machella N, Tedesco S, Benedetti M, Bocchetti R, Notti A, Fattorini D, Piva F, Principato G,. 2005. Pro-oxidant effects of extremely low frequency electromagnetic fields in the land snail Helix aspersa. Free Radic Biol Med 39 (12): 1620-1628. (Pubitemid 41642593)
44. Roobol A, Holmes FE, Hayes NVL, Baines AJ, Carden MJ,. 1995. Cytoplasmic chaperonin complexes enter neurites developing in vitro and differ in subunit composition within single cells. J Cell Sci 108: 1477-1488.
45. Santini MT, Ferrante A, Rainaldi G, Indovina P, Indovina PL,. 2005. Extremely low frequency (ELF) magnetic fields and apoptosis: A review. Int J Radiat Biol 81 (1): 1-11. (Pubitemid 40674529)
46. Santini MT, Rainaldi G, Ferrante A, Indovina P, Donelli G, Indovina PL,. 2006. A 50 Hz sinusoidal magnetic field does not damage MG-63 three-dimensional tumour spheroids but induces changes in their invasive properties. Bioelectromagnetics 27 (2): 132141.
47. Seyyedi SS, Dadras MS, Tavirani MR, Mozdarani H, Toossi P, Zali AR,. 2007. Proteomic analysis in human fibroblasts by continuous exposure to extremely low-frequency electromagnetic fields. Pak J Biol Sci 10 (22): 4108-4112. (Pubitemid 350158625)
48. Simkõ M,. 2004. Induction of cell activation processes by low frequency electromagnetic fields. Sci World J 4 (Suppl 2): 4-22.
49. Simkõ M,. 2007. Cell type specific redox status is responsible for diverse electromagnetic field effects. Curr Med Chem 14 (10): 1141-1152. (Pubitemid 46672632)
50. Simkõ M, Mattsson MO,. 2004. Extremely low frequency electromagnetic fields as effectors of cellular responses in vitro: Possible immune cell activation. J Cell Biochem 93 (1): 83-92.
51. Sinclair J, Weeks M, Butt A, Worthington JL, Akpan A, Jones N, Waterfield M, Allanand D, Timms JF,. 2006. Proteomic response of Schizosaccharomyces pombe to static and oscillating extremely low-frequency electromagnetic fields. Proteomics 6 (17): 4755-4764. (Pubitemid 44369054)
52. Thompson DK, Chourey K, Wickham GS, Thieman SB, VerBerkmoes NC, Zhang B, McCarthy AT, Rudisill MA, Shah M, Hettich RL,. 2010. Proteomics reveals a core molecular response of Pseudomonas putida F1 to acute chromate challenge. BMC Genomics 11: 311.
53. Timeus F, Crescenzio N, Fandi A, Doria A, Foglia L, Cordero di Montezemolo L,. 2008. In vitro antiproliferative and antimigratory activity of dasatinib in neuroblastoma and Ewing sarcoma cell lines. Oncol Rep 19 (2): 353-359. (Pubitemid 351176094)
54. Toohey JI,. 1989. Sulphane sulphur in biological systems: A possible regulatory role. Biochem J 264: 625-632. (Pubitemid 20023429)
55. Voigt A, Zintl F,. 2003. Effects of retinoic acid on proliferation, apoptosis, cytotoxicity, migration, and invasion of neuroblastoma cells. Med Pediatr Oncol 40 (4): 205-213. (Pubitemid 36222824)
56. Wertheimer N, Leeper E,. 1979. Electrical wiring configurations and childhood cancer. Am J Epidemiol 109 (3): 273-284. (Pubitemid 10209603)
57. Witke W,. 2004. The role of profiling complexes in cell motility and other cellular processes. Trends Cell Biol 14 (8): 461-469. (Pubitemid 39092704)
58. Wolf FI, Torsello A, Tedesco B, Fasanella S, Boninsegna A, D'Ascenzo M, Grassi C, Azzena GB, Cittadini A,. 2005. 50-Hz extremely low frequency electromagnetic fields enhance cell proliferation and DNA damage: Possible involvement of a redox mechanism. Biochim Biophys Acta 1743 (1-2): 120-129. (Pubitemid 40380612)
59. Wonsey DR, Zeller KI, Dang CV,. 2002. The c-Myc target gene PRDX3 is required for mitochondrial homeostasis and neoplastic transformation. Proc Natl Acad Sci USA 99 (10): 6649-6654. (Pubitemid 34526187)
60. Wood ZA, Poole LB, Karplus PA,. 2003. Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science 300 (5619): 650-653. (Pubitemid 36520591)
61. Xie HR, Hu LS, Li GY,. 2010. SH-SY5Y human neuroblastoma cell line: In vitro cell model of dopaminergic neurons in Parkinson's disease. Chin Med J (Engl) 123 (8): 1086-1092.
62. Yokus B, Cakir DU, Akdag MZ, Sert C, Mete N,. 2005. Oxidative DNA damage in rats exposed to extremely low frequency electro magnetic fields. Free Radic Res 39 (3): 317-323. (Pubitemid 40439394)
63. Yuan H, Zhang P, Qin L, Yan F, Bai C, Nan X, Liu D, Li Y, Yue W, Pei X,. 2008. Overexpression of SPINDLIN1 induces cellular senescence, multinucleation and apoptosis. Gene 410 (1): 67-74.
64. Zhang P, Cong B, Yuan H, Chen L, Lv Y, Bai C, Nan X, Shi S, Yue W, Pei X,. 2008. Overexpression of spindlin1 induces metaphase arrest and chromosomal instability. J Cell Physiol 217: 400-408.
65. Zhang B, Wang Y, Su Y,. 2009. Peroxiredoxins, a novel target in cancer radiotherapy. Cancer Lett 286: 154-160.
66. Zhao Q, Qin L, Jiang F, Wu B, Yue W, Xu F, Rong Z, Yuan H, Xie X, Gao Y, Bai C, Bartlam M, Pei X, Rao Z,. 2007. Structure ok human spindlin 1. Tandem tumor-like domains for cycle regulation. J Biol Chem 282 (1): 647-656. (Pubitemid 47076605)
67. Zhao J, Wei XL, Jia YS, Zheng JQ,. 2008. Silencing of herg gene by shRNA inhibits SH-SY5Y cell growth in vitro and in vivo. Eur J Pharmacol 579 (1-3): 50-57.
68. Zwirska-Korczala K, Jochem J, Adamczyk-Sowa M, Sowa P, Polaniak R, Birkner E,. 2005. Effect of extremely low frequency of electromagnetic fields on cell proliferation, antioxidative enzyme activities and lipid peroxidation in 3T3-L1 preadipocytes-an in vitro study. J Physiol Pharmacol 56 (Suppl 6): 101-108. (Pubitemid 43120947)