Radioprotective effects of honeybee venom (Apis mellifera) against 915-MHz microwave radiation-induced DNA damage in wistar rat lymphocytes: In vitro study

International Journal of Toxicology

Volumn 28, Issue 2, 2009, Pages 88-98

  Gajski, Goran ^a   Garaj Vrhovac, Vera ^a  

^a INSTITUTE FOR MEDICAL RESEARCH AND OCCUPATIONAL HEALTH   (Croatia)

Author keywords

Bee venom; Comet assay; Formamidopyrimidine DNA glycosylase (Fpg) modified comet assay; Microwave radiation; Radioprotection

Indexed keywords

BEE VENOM; DNA FORMAMIDOPYRIMIDINE GLYCOSYLASE; REACTIVE OXYGEN METABOLITE;

ABSORPTION; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; COMET ASSAY; CONTROLLED STUDY; DNA DAMAGE; IN VITRO STUDY; IRRADIATION; LYMPHOCYTE; MICROWAVE RADIATION; NONHUMAN; OXIDATIVE STRESS; RADIATION PROTECTION; RAT; SENSITIVITY ANALYSIS;

ANIMALS; BEE VENOMS; CELLULAR PHONE; COMET ASSAY; DNA DAMAGE; LYMPHOCYTES; MALE; MICROWAVES; OXIDATIVE STRESS; RADIATION-PROTECTIVE AGENTS; RATS; RATS, WISTAR;

APIS MELLIFERA; APOIDEA; RATTUS NORVEGICUS;

EID: 68649114545     PISSN: 10915818     EISSN: 1092874X     Source Type: Journal    
DOI: 10.1177/1091581809335051     Document Type: Article

References (72)

1. Habermann E. Bee and wasp venoms. Science. 1972;177: 314-322.
2. Dotimas EM, Hamid KR, Hider RC, Ragnarsson U. Isolation and structure analysis of bee venom mast cell degra-nulating peptide. Biochim Biophys Acta. 1987;911: 285-293.
3. Lariviere WR, Melzack R. The bee venom test: a new tonic-pain test. Pain. 1996;66:271-277.
4. Neuman W, Habermann E. Characterization of the substances of the bee venom. Naunyn Schmiedebergs Arch Exp Pathol Pharmacol. 1954;222:267-287.
5. Vogel H. Incorporation of melittin into phosphatidylcho-line bilayers: study of binding and conformational changes. FEBS Lett. 1981;134:37-42.
6. Gevod VS, Birdi KS. Melittin and the 8-26 fragment: differences in ionophoric properties as measured by monolayer method. Biophys J. 1984;45:1079-1083.
7. Fletcher JE, Jiang MS. Possible mechanisms of action of cobra snake venom cardiotoxins and bee venom melittin. Toxicon. 1993;31:669-695.
8. Billingham ME, Morley J, Hanson JM, Shipolini RA, Vernon CA. An anti-inflammatory peptide from bee venom [letter]. Nature. 1973;245:163-164.
9. Hider RC. Honeybee venom: a rich source of pharmacologically active peptides. Endeavour. 1988;12:60-65.
10. Varanda EA, Monti R, Tavares DC. Inhibitory effect of propolis and bee venom on the mutagenicity of some direct- and indirect-acting mutagens. Teratog Carcinog Mutagen. 1999;19:403-413.
11. Sumikura H, Andersen OK, Drewes AM, Arendt-Nielsen LA. Comparison of hyperalgesia and neurogenic inflammation induced by melittin and capsaicin in humans. Neurosci Lett. 2003;337:147-150.
12. Nam KW, Je KH, Lee JH, et al. Inhibition of COX-2 activity and proinflammatory cytokines (TNF-alpha and IL-1beta) production by water-soluble sub-fractionated parts from bee (Apis mellifera) venom. Arch Pharm Res. 2003;26:383-388.
13. Kim HW, Kwon YB, Ham TW, et al. Acupoint stimulation using bee venom attenuates formalin-induced pain behavior and spinal cord fos expression in rats. J Vet Med Sci. 2003;65:349-355.
14. Orsolic N, Sver L, Verstovsek S, Terzic S, Basic I. Inhibition of mammary carcinoma cell proliferation in vitro and tumor growth in vivo by bee venom. Toxicon. 2003;41:861-870.
15. Liu X, Chen D, Xie L, Zhang R. Effect of honey bee venom on proliferation of K1735M2 mouse melanoma cells in-vitro and growth of murine B16 melanomas in-vivo. J Pharm Pharmacol. 2002;54:1083-1089.
16. Jang MH, Shin MC, Lim S, et al. Bee venom induces apoptosis and inhibits expression of cyclooxygenase-2 mRNA in human lung cancer cell line NCI-H1299. J Pharmacol Sci. 2003;91:95-104.
17. Yin CS, Lee HJ, Hong SJ, Chung JH, Koh HG. Microarray analysis of gene expression in chondrosarcoma cells treated with bee venom. Toxicon. 2005;45:81-91.
18. HuH, Chen D,LiY,Zhang X. Effect ofpolypeptides inbee venom on growth inhibition and apoptosis induction of the human hepatoma cell line SMMC-7721 in-vitro and Balb/ c nude mice in-vivo. J Pharm Pharmacol. 2006;58:83-89.
19. Moon DO, Park SY, Heo MS, et al. Key regulators in bee venom-induced apoptosis are Bcl-2 and caspase-3 in human leukemic U937 cells through downregulation of ERK and Akt. Int Immunopharmacol. 2006;6:1796-1807.
20. Han S, Lee K, Yeo J, et al. Effect of honey bee venom on microglial cells nitric oxide and tumor necrosis factor-alpha production stimulated by LPS. J Ethnopharmacol. 2007;111:176-181.
21. Lee YJ, Kang SJ, Kim BM, et al. Cytotoxicity of honeybee (Apis mellifera) venom in normal human lymphocytes and HL-60 cells. Chem Biol Interact. 2007;169:189-197.
22. Shipman WH, Cole LJ. Increased resistance of mice to x-irradiation after the injection of bee venom. Nature. 1967;215:311-312.
23. Kanno I, Ito Y, Okuyama S. Radioprotection by bee venom. Nippon Igaku Hoshasen Gakkai Zasshi. 1970;29:1494-1500.
24. Varanda EA, Takahashi CS, Soares AEE, Barreto SAJ. Effect of Apis mellifera bee venom and gamma radiation on bone marrow cells of Wistar rats treated in vivo. Rev Bras Genet. 1992;15:807-819.
25. Varanda EA, Takahashi C. Effect of pretreatment with venom of Apis mellifera bees on the yield of gamma-ray induced chromosome aberrations in human blood lymphocytes. Rev Bras Genet. 1993;16:551-559.
26. Varanda EA, Tavares DC. Radioprotection: mechanism and radioprotective agents including honey bee venom. Venom Anim Toxins. 1998;4:5-21.
27. Roberts NJ Jr, Michaelson SM, Lu ST. The biological effects of radiofrequency radiation: a critical review and recommendations. Int J Radiat Biol Relat Stud Phys Chem Med. 1986;50:379-420.
28. Breckenkamp J, Berg G, Blettner M. Biological effects on human health due to radiofrequency/microwave exposure: a synopsis of cohort studies. Radiat Environ Biophys. 2003;42:141-154.
29. ICNIRP Report. Epidemiology of health effects of radio-frequency. Environ Health Perspect. 2004;112:1741-1754.
30. Jauchem JR. Effects of low-level radio-frequency (3kHz to 300GHz) energy on human cardiovascular, reproductive, immune, and other systems: a review of the recent literature. Int J Hyg Environ Health. 2008;211:1-29.
31. Brusick D, Albertini R, McRee D, et al. Genotoxicity of radiofrequency radiation. Environ Mol Mutagen. 1998;32:1-16.
32. Verschaeve L, Maes A. Genetic, carcinogenic and teratogenic effects of radiofrequency fields. Mutat Res. 1998;410:141-165.
33. Vijayalaxmi, Obe G. Controversial cytogenetic observations in mammalian somatic cells exposed to radiofrequency radiation. Radiat Res. 2004;162:481-496.
34. Verschaeve L. Genetic effects of radiofrequency radiation (RFR). Toxicol Appl Pharmacol. 2005;207:336-341.
35. Maes A, Collier M, Slaets D, Verschaeve L. Cytogenetic effects of microwaves from mobile communication frequencies (954 MHz). Electro- Magnetobiol. 2005;14:91-98.
36. Maes A, Collier M, Van Gorp U, Vandoninck S, Verschaeve L. Cytogenetic effects of 935.2-MHz GSM microwaves alone and in combination with mitomycin C. Mutat Res. 1997;393:151-156.
37. Malyapa RS, Ahern EW, Straube WL, et al. Measurement of DNA damage after exposure to 2450 MHz electromagnetic radiation. Radiat Res. 1997a;148:608-617.
38. Malyapa RS, Ahern EW, Straube WL, et al. Measurement of DNA damage after exposure to electromagnetic radiation in the cellular phone communication frequency band (835.62 and 847.74 MHz). Radiat Res. 1997b;148:618-627.
39. Scarfì MR, Fresegna AM, Villani P, et al. Exposure to radiofrequency radiation (900 MHz, GSM signal) does not affect micronucleus frequency and cell proliferation in human peripheral blood lymphocytes: an interlaboratory study. Radiat Res. 2006;165:655-663.
40. Vijayalaxmi, Leal BZ, Szilagyi M, Prihoda TJ, Meltz ML. Primary DNA damage in human blood lymphocytes exposed in vitro to 2450 MHz radiofrequency radiation. Radiat Res. 2000;153:479-486.
41. Li L, Bisht KS, Lagroye I, et al. Measurement of DNA damage in mammalian cells exposed in vitro to radiofre-quency fields at SARs of 3-5 W/kg. Radiat Res. 2001;156: 328-332.
42. McNamee JP, Bellier PV, Gajda GB, et al. No evidence for genotoxic effects from 24 h exposure of human leukocytes to 1.9 GHz radiofrequency fields. Radiat Res. 2003;159:693-697.
43. Garaj-Vrhovac V, Horvat D, Koren Z. The effect of microwave radiation on the cell genome. Mutat Res. 1990a;243:87-93.
44. Garaj-Vrhovac V, Fucic A, Horvat D. Comparison of chromosome aberration and micronucleus induction in human lymphocytes after occupational exposure to vinyl chloride monomer and microwave radiation. Period Biol. 1990b;92:411-416.
45. Garaj-Vrhovac V, Horvat D, Koren Z. The relationship between colony-forming ability, chromosome aberrations and incidence of micronuclei in V79 Chinese hamster cells exposed to microwave radiation. Mutat Res. 1991;263:143-149.
46. Garaj-Vrhovac V, Fucic A, Horvat D. The correlation between the frequency of micronuclei and specific chromosome aberrations in human lymphocytes exposed to microwave radiation in vitro. Mutat Res. 1992;281:181-186.
47. Fucic A, Garaj-Vrhovac V, Skara M, Dimitrovic B. X-rays, microwaves and vinyl chloride monomer: their clastogenic and aneugenic activity, using the micronucleus assay on human lymphocytes. Mutat Res. 1992;282:265-271.
48. Maes A, Verschaeve L, Arroyo A, De Wagter C, Vercruyssen L. In vitro cytogenetic effects of 2450 MHz waves on human peripheral blood lymphocytes. Bioelectromagnetics. 1993;14:495-501.
49. Maes A, Collier M, Verschaeve L. Cytogenetic investigations on microwaves emitted by a 455.7 MHz car phone. Folia Biol. 2000;46:175-180.
50. Zotti-Martelli L, Peccatori M, Scarpato R, Migliore L. Induction of micronuclei in human lymphocytes exposed in vitro to microwave radiation. Mutat Res. 2000;472: 51-58.
51. Tice RR, Hook GG, Donner M, McRee DI, Guy AW. Genotoxicity of radiofrequency signals, I: investigation of DNA damage and micronuclei induction in cultured human blood cells. Bioelectromagnetics. 2002;23: 113-126.
52. Paulraj R, Behari J. Single strand DNA breaks in rat brain cells exposed to microwave radiation. Mutat Res. 2006;596:76-80.
53. Singh NP, McCoy MT, Tice RR, Schneider LL. A simple technique for quantitation of low levels of DNA damage in individual cells. Exp Cell Res. 1988;175: 184-191.
54. Collins AR, Dusinská M, Franklin M, et al. Comet Assay in human biomonitoring studies: reliability, validation, and applications. Environ Mol Mutagen. 1997;30: 139-146.
55. European Standards Committee on Oxidative DNA Damage (ESCODD). Measurement of DNA oxidation in human cells by chromatographic and enzymic methods. Free Radic Biol Med. 2003;34:1089-1099.
56. Kumaravel TS, Vilhar B, Faux SP, Jha AN. Comet assay measurements: a perspective. Cell Biol Toxicol. 2009;25: 53-64.
57. Collins AR, Duthie SJ, Dobson VL. Direct enzymic detection of endogenous oxidative base damage in human lymphocyte DNA. Carcinogenesis. 1993;14: 1733-1735.
58. Collins AR, Dusinská M, Horská A. Detection of alkylation damage in human lymphocyte DNA with the comet assay. Acta Biochim Pol. 2001a;48:611-614.
59. Collins AR, Dusinská M, Horváthová E, et al. Inter-individual differences in repair of DNA base oxidation, measured in vitro with the comet assay. Mutagenesis. 2001b;16:297-301.
60. Kruman II, Kumaravel TS, Lohani A, et al. Folic acid deficiency and homocysteine impair DNA repair in hip-pocampal neurons and sensitize them to amyloid toxicity in experimental models of Alzheimer's disease. J Neurosci. 2002;22:1752-1762.
61. Gajski G, Garaj-Vrhovac V, Orescanin V. Cytogenetic status and oxidative DNA-damage induced by atorvasta-tin in human peripheral blood lymphocytes: standard and Fpg-modified comet assay. Toxicol Appl Pharmacol. 2008;231:85-93.
62. Law on the Welfare of Animals in Republic of Croatia, N.N. 19; 1999.
63. Guide for the Care and Use of Laboratory Animals. DHHS Publ (NIH) 86-23. Washington DC: National Institutes of Health, Department of Health and Human Services; 1986.
64. Durney CH, Massoudi H, Iskander MF. Radiofrequency Radiation Handbook. 4th ed. Report SAM-TR-85-73. Brooks Air Force Base, Tex: USAF School of Aerospace Medicine; 1986.
65. Yuhas JM, Spellman JM, Cuto F. The role of WR-2721 in the radiotherapy and for chemotherapy. Cancer Clin Trials. 1980;3:211-216.
66. Grdina DJ, Sigdestad CP. Radiation protectors: the unexpected benefits. Drug Metab Rev. 1989;20:13-42.
67. Khalikov SK, Turakulov IaKh, Rakhimov MM. Radioprotective properties of Central Asian snake venoms. Radiobiologiia. 1975;15:910-913.
68. Kazaryan SA, Grigoryan KP, Airapetyan SN, Mndzhoyan OL. Derivatives of natural amino acids as radioprotectors. Pharma Chem J. 1995;29:454-458.
69. Stopczyk D, Gnitecki W, Buczyń ski A, Markuszewski L, Buczyński J. Effect of electromagnetic field produced by mobile phones on the activity of superoxide dismutase (SOD-1) and the level of malonyldialdehyde (MDA) - in vitro study. Med Pr. 2002;53:311-314.
70. Stopczyk D, Gnitecki W, Buczyń ski A. Effect of electromagnetic field produced by mobile phones on the activity of superoxide dismutase (SOD-1)-in vitro researches. Ann Acad Med Stetin. 2005;51:125-128.
71. Köylü H, Mollaoglu H, Ozguner F, Naziroglu M, Delibas N. Melatonin modulates 900 Mhz microwave-induced lipid peroxidation changes in rat brain. Toxicol Ind Health. 2006;22:211-216.
72. Yurekli AI, Ozkan M, Kalkan T, et al. GSM base station electromagnetic radiation and oxidative stress in rats. Electromagn Biol Med. 2006;25:177-188.