Central European Journal of Biology

, Volume 9, Issue 10, pp 915–921 | Cite as

Hydrogen peroxide induced by modulated electromagnetic radiation protects the cells from DNA damage

  • Andrew B. GapeyevEmail author
  • Nina A. Lukyanova
  • Sergey V. Gudkov
Research Article


It is believed that non-ionizing electromagnetic radiation (EMR) and low-level hydrogen peroxide (H2O2) may change nonspecific resistance and modify DNA damage caused by ionizing radiation. To check this assumption, the combined effects of extremely high-frequency EMR (EHF EMR) and X-rays on induction of DNA damage in mouse whole blood leukocytes were studied. The cells were exposed to X-rays with or without preliminary treatment with EHF EMR or low-level H2O2. With the use of enhanced chemiluminescence, it was shown for the first time that pulse-modulated EHF EMR (42.2 GHz, incident power density of 0.1 mW/cm2, exposure duration of 20 min, modulation frequency of 1 Hz) induced H2O2 at a concentration of 4.6 ± 0.3 nM L−1 in physiological saline. With the use of an alkaline comet assay, it was found that the exposure of cells to the pulse-modulated EHF EMR, 25 min prior to treatment with X-rays at a dose of 4 Gy reduced the level of ionizing radiation-induced DNA damage. Continuous EHF EMR was inefficient. In turn, it was shown that low-level H2O2 (30–500 nM L−1) protected the cells against X-irradiation. Thus, the mechanisms of radiation protective effect of EHF EMR are connected with the induction of the adaptive response by nanomolar concentrations of reactive oxygen species formed by pulse-modulated EHF EMR.


Extremely high-frequency electromagnetic radiation Pulse modulation X-rays Hydrogen peroxide DNA damage Comet assay Protective effect 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. [1]
    Vijayalaxmi, Cao Y., Scarfi M.R., Adaptive response in mammalian cells exposed to nonionizing radiofrequency fields: A review and gaps in knowledge, Mutat. Res., 2014 (in press), DOI: 10.1016/j.mrrev.2014.02.002Google Scholar
  2. [2]
    Luukkonen J., Liimatainen A., Juutilainen J., Naarala J., Induction of genomic instability, oxidative processes, and mitochondrial activity by 50Hz magnetic fields in human SH-SY5Y neuroblastoma cells, Mutat. Res., 2014, 760, 33–41CrossRefGoogle Scholar
  3. [3]
    Manti L., D’Arco A., Cooperative biological effects between ionizing radiation and other physical and chemical agents, Mutat. Res., 2010, 704, 115–122PubMedCrossRefGoogle Scholar
  4. [4]
    Juutilainen J., Do electromagnetic fields enhance the effects of environmental carcinogens? Radiat. Prot. Dosimetry, 2008, 132, 228–231PubMedCrossRefGoogle Scholar
  5. [5]
    Joiner M.C., Lambin P., Marples B., Adaptive response and induced resistance, C. R. Acad. Sci. III, 1999, 322, 167–175PubMedCrossRefGoogle Scholar
  6. [6]
    Gapeyev A.B., Mikhailik E.N., Chemeris N.K., Antiinflammatory effects of low-intensity extremely highfrequency electromagnetic radiation: frequency and power dependence, Bioelectromagnetics, 2008, 29, 197–206PubMedCrossRefGoogle Scholar
  7. [7]
    Gapeyev A.B., Mikhailik E.N., Chemeris N.K., Features of anti-inflammatory effects of modulated extremely high-frequency electromagnetic radiation, Bioelectromagnetics, 2009, 30, 454–461PubMedCrossRefGoogle Scholar
  8. [8]
    Gapeyev A.B., Romanova N.A., Chemeris N.K., Changes in the chromatin structure of lymphoid cells under the influence of low-intensity extremely high-frequency electromagnetic radiation against the background of inflammatory process, Biophysics, 2011, 56, 672–678CrossRefGoogle Scholar
  9. [9]
    Gapeyev A.B., Chemeris N.K., Dosimetry questions at studying biological effects of extremely highfrequency electromagnetic radiation, Biomed. Radioelectron., 2010, 1, 13–36, (in Russian)Google Scholar
  10. [10]
    Gapeyev A.B., Sokolov P.A., Chemeris N.K., A study of absorption of energy of the extremely high frequency electromagnetic radiation in the rat skin by various dosimetric methods and approaches, Biofizika, 2002, 47, 759–768, (in Russian)Google Scholar
  11. [11]
    Ostling O., Johanson, K.J., Microelectrophoretic study of radiation-induced DNA damages in individual mammalian cells, BBRC, 1984, 123, 291–298PubMedGoogle Scholar
  12. [12]
    Tice R.R., Agurell E., Anderson D., Burlinson B., Hartmann A., Kobayashi H., et al., Single cell gel/ comet assay: guidelines for in vitro and in vivo genetic toxicology testing, Environ. Mol. Mutagen., 2000, 35, 206–221PubMedCrossRefGoogle Scholar
  13. [13]
    Collins A.R., Oscoz A.A., Brunborg G., Gaivão I., Giovannelli L., Kruszewski M., et al., The comet assay: topical issues, Mutagenesis, 2008, 23, 143–151PubMedCrossRefGoogle Scholar
  14. [14]
    Shtarkman I.N., Gudkov S.V., Chernikov A.V., Bruskov V.I., Effect of amino acids on X-ray-induced hydrogen peroxide and hydroxyl radical formation in water and 8-oxoguanine in DNA, Biochemistry (Moscow), 2008, 73, 470–478CrossRefGoogle Scholar
  15. [15]
    Gudkov S.V., Gudkova O.Y., Chernikov A.V., Bruskov V.I., Protection of mice against X-ray injuries by the post-irradiation administration of guanosine and inosine, Int. J. Radiat. Biol., 2009, 85, 116–125PubMedCrossRefGoogle Scholar
  16. [16]
    Potselueva M.M., Pustovidko A.V., Evtodienko Iu.V., Khramov R.N., Chaĭlakhian L.M., Formation of reactive oxygen species in aqueous solutions after exposure to extremely-high frequency electromagnetic fields, Dokl. Akad. Nauk, 1998, 359, 415–418, (in Russian)PubMedGoogle Scholar
  17. [17]
    Gugkova O.Iu., Gudkov S.V., Gapeyev A.B., Bruskov V.I., Rubannik A.V., Chemeris N.K., The study of the mechanisms of formation of reactive oxygen species in aqueous solutions on exposure to high peak-power pulsed electromagnetic radiation of extremely high frequencies, Biofizika, 2005, 50, 773–779, (in Russian)PubMedGoogle Scholar
  18. [18]
    Gudkov S.V., Bruskov V.I., Astashev M.E., Chernikov A.V., Yaguzhinsky L.S., Zakharov S.D., Oxygen-dependent autooscillations of water luminescence triggered by the 1264 nm radiation, J. Phys. Chem. B, 2011, 115, 7693–7698PubMedGoogle Scholar
  19. [19]
    Olivieri G., Bodycote J., Wolff S., Adaptive response of human lymphocytes to low concentrations of radioactive thymidine, Science, 1984, 223, 594–597PubMedCrossRefGoogle Scholar
  20. [20]
    Stecca C., Gerber G.B., Adaptive response to DNA-damaging agents: a review of potential mechanisms, Biochem. Pharmacol., 1998, 55, 941–951PubMedCrossRefGoogle Scholar
  21. [21]
    Lushchak V.I., Adaptive response to oxidative stress: Bacteria, fungi, plants and animals. Comp. Biochem. Physiol. C. Toxicol. Pharmacol., 2011, 153, 175–190PubMedCrossRefGoogle Scholar
  22. [22]
    Wei Q., Huang H., Yang L., Yuan J., Yang X., Liu Y., et al., Hydrogen peroxide induces adaptive response and differential gene expression in human embryo lung fibroblast cells, Environ. Toxicol., 2014, 29, 478–485PubMedCrossRefGoogle Scholar
  23. [23]
    Samson L., Schwartz J.L., Evidence for an adaptive DNA repair pathway in CHO and human skin fibroblast cell lines, Nature, 1980, 287, 861–863PubMedCrossRefGoogle Scholar
  24. [24]
    Nguyen D., Zajac-Kaye M., Rubinstein L., Voeller D., Tomaszewski J.E., Kummar S., et al., Poly(ADP-ribose) polymerase inhibition enhances p53-dependent and -independent DNA damage responses induced by DNA damaging agent, Cell Cycle, 2011, 10, 4074–4082PubMedCrossRefPubMedCentralGoogle Scholar
  25. [25]
    Seong J.K., Kim D.K., Choi K.H., Oh S.H., Kim K.S., Lee S.S., et al., Proteomic analysis of the cellular proteins induced by adaptive concentrations of hydrogen peroxide in human U937 cells, Exp. Mol. Med., 2002, 34, 374–378PubMedCrossRefGoogle Scholar
  26. [26]
    Kim D.K., Cho E.S., Seong J.K., Um H.D., Adaptive concentrations of hydrogen peroxide suppress cell death by blocking the activation of SAPK/JNK pathway, J. Cell Sci., 2001, 114, 4329–4334Google Scholar
  27. [27]
    Yan G., Hua Z., Du G., Chen J., Adaptive response of Bacillus sp. F26 to hydrogen peroxide and menadione, Curr. Microbiol., 2006, 52, 238–242PubMedCrossRefGoogle Scholar

Copyright information

© Versita Warsaw and Springer-Verlag Wien 2014

Authors and Affiliations

  • Andrew B. Gapeyev
    • 1
    • 2
    Email author
  • Nina A. Lukyanova
    • 1
    • 2
  • Sergey V. Gudkov
    • 2
    • 3
  1. 1.Institute of Cell Biophysics of Russian Academy of SciencesPushchino, Moscow RegionRussian Federation
  2. 2.Pushchino State Institute of Natural SciencesPushino, Moscow regionRussian Federation
  3. 3.Institute of Theoretical and Experimental Biophysics of Russian Academy of SciencesPushchino, Moscow RegionRussian Federation

Personalised recommendations