Skip to main content

DNMT1 and miRNAs: possible epigenetics footprints in electromagnetic fields utilization in oncology

Abstract

Many studies were performed to unravel the effects of different types of Electromagnetic fields (EMFs) on biological systems. Some studies were conducted to exploit EMFs for medical purposes mainly in cancer therapy. Although many studies suggest that the EMFs exposures can be effective in pre-clinical cancer issues, the treatment outcomes of these exposures on the cancer cells, especially at the molecular level, are challenging and overwhelmingly complicated yet. This article aims to review the epigenetic mechanisms that can be altered by EMFs exposures with the main emphasis on Extremely low frequency electromagnetic field (ELF-EMF). The epigenetic mechanisms are reversible and affected by environmental factors, thus, EMFs exposures can modulate these mechanisms. According to the reports, ELF-EMF exposures affect epigenetic machinery directly or through the molecular signaling pathways. ELF-EMF in association with DNA methylation, histone modification, miRNAs, and nucleosome remodeling could affect the homeostasis of cancer cells and play a role in DNA damage repairing, apoptosis induction, prevention of metastasis, differentiation, and cell cycle regulation. In general, the result of this study shows that ELF-EMF exposure probably can be effective in cancer epigenetic therapy, but more molecular and clinical investigations are needed to clarify the safe and specific dosimetric characteristics of ELF-EMF in practice.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  1. 1.

    García-Minguillán O, et al. CT2A cell viability modulated by electromagnetic fields at extremely low frequency under no thermal effects. Int J Mol Sci. 2020;21(1):152.

    Article  CAS  Google Scholar 

  2. 2.

    Jankowska M, et al. Exposure to 50 Hz electromagnetic field changes the efficiency of the scorpion alpha toxin. J Venom Anim Toxins Inclu Trop Dis. 2015; 21:38

  3. 3.

    Goto T, et al. Noninvasive up-regulation of angiopoietin-2 and fibroblast growth factor-2 in bone marrow by pulsed electromagnetic field therapy. J Orthop Sci. 2010;15(5):661–5.

    CAS  PubMed  Article  Google Scholar 

  4. 4.

    Zhou J, et al. Effects of pulsed electromagnetic fields on bone mass and Wnt/β-catenin signaling pathway in ovariectomized rats. Arch Med Res. 2012;43(4):274–82.

    CAS  PubMed  Article  Google Scholar 

  5. 5.

    Tong J, et al. Pulsed electromagnetic fields promote the proliferation and differentiation of osteoblasts by reinforcing intracellular calcium transients. Bioelectromagnetics. 2017;38(7):541–9.

    CAS  PubMed  Article  Google Scholar 

  6. 6.

    Brighton CT, McCluskey WP. Response of cultured bone cells to a capacitively coupled electric field: inhibition of cAMP response to parathyroid hormone. J Orthop Res. 1988;6(4):567–71.

    CAS  PubMed  Article  Google Scholar 

  7. 7.

    Muehsam D, Pilla A. The sensitivity of cells and tissues to exogenous fields: effects of target system initial state. Bioelectrochem Bioenerg. 1999;48(1):35–42.

    CAS  PubMed  Article  Google Scholar 

  8. 8.

    Lee JH, McLeod KJ. Morphologic responses of osteoblast‐like cells in monolayer culture to ELF electromagnetic fields. Bioelectromagnetics. 2000; 21(2):129–136

  9. 9.

    Bourguignon GJ, Jy W, Bourguignon LY. Electric stimulation of human fibroblasts causes an increase in Ca2+ influx and the exposure of additional insulin receptors. J Cell Physiol. 1989;140(2):379–85.

    CAS  PubMed  Article  Google Scholar 

  10. 10.

    Cossarizza A, et al. Extremely low frequency pulsed electromagnetic fields increase interleukin-2 (IL-2) utilization and IL-2 receptor expression in mitogen-stimulated human lymphocytes from old subjects. FEBS Lett. 1989;248(1–2):141–4.

    CAS  PubMed  Article  Google Scholar 

  11. 11.

    Fitzsimmons RJ, et al. IGF-II receptor number is increased in TE-85 osteosarcoma cells by combined magnetic fields. J Bone Miner Res. 1995;10(5):812–9.

    CAS  PubMed  Article  Google Scholar 

  12. 12.

    Cho MR, et al. Induced redistribution of cell surface receptors by alternating current electric fields. FASEB J. 1994;8(10):771–6.

    CAS  PubMed  Article  Google Scholar 

  13. 13.

    Shankar VS, et al. Effects of electromagnetic stimulation on the functional responsiveness of isolated rat osteoclasts. J Cell Physiol. 1998;176(3):537–44.

    CAS  PubMed  Article  Google Scholar 

  14. 14.

    Varani K, et al. Effect of low frequency electromagnetic fields on A2A adenosine receptors in human neutrophils. Br J Pharmacol. 2002;136(1):57–66.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  15. 15.

    Nagai M, Ota M. Pulsating electromagnetic field stimulates mRNA expression of bone morphogenetic protein-2 and-4. J Dent Res. 1994;73(10):1601–5.

    CAS  PubMed  Article  Google Scholar 

  16. 16.

    Aaron RK, Wang S, Ciombor DM. Upregulation of basal TGFβ1 levels by EMF coincident with chondrogenesis–implications for skeletal repair and tissue engineering. J Orthop Res. 2002;20(2):233–40.

    CAS  PubMed  Article  Google Scholar 

  17. 17.

    Lohmann C, et al. Pulsed electromagnetic fields affect phenotype and connexin 43 protein expression in MLO‐Y4 osteocyte‐like cells and ROS 17/2.8 osteoblast‐like cells. J Orthop Res. 2003;21(2): 326–334

  18. 18.

    Holmes D. Non-union bone fracture: a quicker fix. Nature. 2017;550(7677):S193–S193.

    CAS  PubMed  Article  Google Scholar 

  19. 19.

    Ciombor DM, Aaron RK. The role of electrical stimulation in bone repair. Foot Ankle Clin. 2005;10(4):579–93.

    PubMed  Article  Google Scholar 

  20. 20.

    Ehnert S, et al. Extremely low frequency pulsed electromagnetic fields cause antioxidative defense mechanisms in human osteoblasts via induction of O2 and H2O2. Sci Rep. 2017;7(1):1–11.

    CAS  Article  Google Scholar 

  21. 21.

    Noriega-Luna B, et al. Influence of pulsed magnetic fields on the morphology of bone cells in early stages of growth. Micron. 2011;42(6):600–7.

    CAS  PubMed  Article  Google Scholar 

  22. 22.

    Tsai MT, et al. Pulsed electromagnetic fields affect osteoblast proliferation and differentiation in bone tissue engineering. Bioelectromagnetics. 2007;28(7): 519–528

  23. 23.

    Grassi C, et al. Effects of 50 Hz electromagnetic fields on voltage-gated Ca2+ channels and their role in modulation of neuroendocrine cell proliferation and death. Cell Calcium. 2004;35(4):307–15.

    CAS  PubMed  Article  Google Scholar 

  24. 24.

    Mayer-Wagner S, et al. Effects of low frequency electromagnetic fields on the chondrogenic differentiation of human mesenchymal stem cells. Bioelectromagnetics. 2011;32(4):283–90.

    CAS  PubMed  Article  Google Scholar 

  25. 25.

    Piacentini R, et al. Extremely low-frequency electromagnetic fields promote in vitro neurogenesis via upregulation of Cav1-channel activity. J Cell Physiol. 2008;215(1):129–39.

    CAS  PubMed  Article  Google Scholar 

  26. 26.

    Simkó M, Mattsson MO. Extremely low frequency electromagnetic fields as effectors of cellular responses in vitro: possible immune cell activation. J Cell Biochem. 2004;93(1):83–92.

    PubMed  Article  CAS  Google Scholar 

  27. 27.

    Reale M, et al. Modulation of MCP-1 and iNOS by 50-Hz sinusoidal electromagnetic field. Nitric Oxide. 2006;15(1):50–7.

    CAS  PubMed  Article  Google Scholar 

  28. 28.

    Garip A, Akan Z. Effect of ELF-EMF on number of apoptotic cells; correlation with reactive oxygen species and HSP. Acta Biol Hung. 2010;61(2):158–67.

    CAS  PubMed  Article  Google Scholar 

  29. 29.

    Frahm J, Mattsson M-O, Simkó M. Exposure to ELF magnetic fields modulate redox related protein expression in mouse macrophages. Toxicol Lett. 2010;192(3):330–6.

    CAS  PubMed  Article  Google Scholar 

  30. 30.

    Cichoń N, et al. Increase in blood levels of growth factors involved in the neuroplasticity process by using an extremely low frequency electromagnetic field in post-stroke patients. Front Aging Neurosci. 2018;10:294.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  31. 31.

    Cichoń N, et al. Benign effect of extremely low-frequency electromagnetic field on brain plasticity assessed by nitric oxide metabolism during poststroke rehabilitation. Oxid Med Cell Longev. 2017; 2017.

  32. 32.

    Ki G-E, et al. Extremely low-frequency electromagnetic fields increase the expression of Anagen-related molecules in human dermal papilla cells via GSK-3β/ERK/Akt signaling pathway. Int J Mol Sci. 2020;21(3):784.

    CAS  PubMed Central  Article  PubMed  Google Scholar 

  33. 33.

    Ledda M, et al. Non-ionizing radiation for cardiac human amniotic mesenchymal stromal cell commitment: a physical strategy in regenerative medicine. Int J Mol Sci. 2018;19(8):2324.

    PubMed Central  Article  CAS  PubMed  Google Scholar 

  34. 34.

    Costantini E, et al. Human gingival fibroblasts exposed to extremely low-frequency electromagnetic fields: in vitro model of wound-healing improvement. Int J Mol Sci. 2019; 20(9): 2108.

  35. 35.

    Liu Y, et al. Effect of 50 Hz extremely low-frequency electromagnetic fields on the DNA methylation and DNA methyltransferases in mouse spermatocyte-derived cell line GC-2. BioMed Res Int. 2015; 2015.

  36. 36.

    Sharma S, Kelly TK, Jones PA. Epigenetics in cancer. Carcinogenesis. 2010;31(1):27–36.

    CAS  PubMed  Article  Google Scholar 

  37. 37.

    Wolffe AP, Matzke MA. Epigenetics: regulation through repression. Science. 1999; 286(5439): 481–486.

  38. 38.

    Ehnert S, et al. Translational insights into extremely low frequency pulsed electromagnetic fields (ELF-PEMFs) for bone regeneration after trauma and orthopedic surgery. J Clin Med. 2019;8(12):2028.

    CAS  PubMed Central  Article  PubMed  Google Scholar 

  39. 39.

    D’Angelo C, et al. Experimental model for ELF-EMF exposure: concern for human health. Saudi J Biol Sci. 2015;22(1):75–84.

    PubMed  Article  Google Scholar 

  40. 40.

    Lee SK, et al. Extremely low frequency magnetic fields induce spermatogenic germ cell apoptosis: possible mechanism. BioMed Res Int. 2014; 2014.

  41. 41.

    Guerriero F, Ricevuti G. Blog single. Mult Scler. 2010: 0.

  42. 42.

    Friedman J, et al. Mechanism of short-term ERK activation by electromagnetic fields at mobile phone frequencies. Biochem J. 2007;405(3):559–68.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  43. 43.

    Mattsson MO, Simko M. Emerging medical applications based on non-ionizing electromagnetic fields from 0 Hz to 10 THz. Med Devices (Auckl). 2019;12:347–68.

    CAS  Google Scholar 

  44. 44.

    Varani K, et al. Adenosine receptors as a biological pathway for the anti-inflammatory and beneficial effects of low frequency low energy pulsed electromagnetic fields. Mediators Inflamm. 2017;2017:2740963.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  45. 45.

    Kovacic P, Somanathan R. Electromagnetic fields: mechanism, cell signaling, other bioprocesses, toxicity, radicals, antioxidants and beneficial effects. J Recept Signal Transduct Res. 2010;30(4):214–26.

    CAS  PubMed  Article  Google Scholar 

  46. 46.

    Bassett CA. Beneficial effects of electromagnetic fields. J Cell Biochem. 1993;51(4):387–93.

    CAS  PubMed  Article  Google Scholar 

  47. 47.

    Song K, et al. A 60 Hz uniform electromagnetic field promotes human cell proliferation by decreasing intracellular reactive oxygen species levels. PLoS One. 2018; 13(7): e0199753.

  48. 48.

    Glasauer A, Chandel NS. Targeting antioxidants for cancer therapy. Biochem Pharmacol. 2014;92(1):90–101.

    CAS  PubMed  Article  Google Scholar 

  49. 49.

    Wilson D, Jagadeesh P. Experimental regeneration in peripheral nerves and the spinal cord in laboratory animals exposed to a pulsed electromagnetic field. Spinal Cord. 1976;14(1):12–20.

    CAS  Article  Google Scholar 

  50. 50.

    Rusovan A, Kanje M. Stimulation of regeneration of the rat sciatic nerve by 50 Hz sinusoidal magnetic fields. Exp Neurol. 1991;112(3):312–6.

    CAS  PubMed  Article  Google Scholar 

  51. 51.

    Bai W-F, et al. Fifty-Hertz electromagnetic fields facilitate the induction of rat bone mesenchymal stromal cells to differentiate into functional neurons. Cytotherapy. 2013;15(8):961–70.

    CAS  PubMed  Article  Google Scholar 

  52. 52.

    Mareschi K, et al. Neural differentiation of human mesenchymal stem cells: evidence for expression of neural markers and eag K+ channel types. Exp Hematol. 2006;34(11):1563–72.

    CAS  PubMed  Article  Google Scholar 

  53. 53.

    Sulpizio M, et al. Molecular basis underlying the biological effects elicited by extremely low-frequency magnetic field (ELF-MF) on neuroblastoma cells. J Cell Biochem. 2011;112(12):3797–806.

    CAS  PubMed  Article  Google Scholar 

  54. 54.

    Rezaie-Tavirani M, et al. Proteomic analysis of the effect of extremely low-frequency electromagnetic fields (ELF-EMF) with different intensities in SH-SY5Y neuroblastoma cell line. J Lasers Med Sci. 2017;8(2):79.

    PubMed  PubMed Central  Article  Google Scholar 

  55. 55.

    Bassett C, Schink-Ascani M, Lewis S. Effects of pulsed electromagnetic fields on Steinberg ratings of femoral head osteonecrosis. Clin Orthop Relat Res. 1989;246:172–85.

    Google Scholar 

  56. 56.

    Ikegami A, et al. Femoral perfusion after pulsed electromagnetic field stimulation in a steroid-induced osteonecrosis model. Bioelectromagnetics. 2015;36(5):349–57.

    CAS  PubMed  Article  Google Scholar 

  57. 57.

    Tepper OM, et al. Electromagnetic fields increase in vitro and in vivo angiogenesis through endothelial release of FGF-2. FASEB J. 2004;18(11):1231–3.

    CAS  PubMed  Article  Google Scholar 

  58. 58.

    Hu H, et al. Promising application of pulsed electromagnetic fields (PEMFs) in musculoskeletal disorders. Biomed Pharmacother. 2020; 131: 110767.

  59. 59.

    Streit A, et al. Effect on clinical outcome and growth factor synthesis with adjunctive use of pulsed electromagnetic fields for fifth metatarsal nonunion fracture: a double-blind randomized study. Foot Ankle Int. 2016;37(9):919–23.

    PubMed  Article  Google Scholar 

  60. 60.

    Fitzsimmons RJ, et al. Low-amplitude, low-frequency electric field-stimulated bone cell proliferation may in part be mediated by increased IGF-II release. J Cell Physiol. 1992;150(1):84–9.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  61. 61.

    Wang T, et al. Pulsed electromagnetic fields: promising treatment for osteoporosis. Osteoporos Int. 2019;30(2):267–76.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  62. 62.

    McCarthy CJ, Callaghan MJ, Oldham JA. Pulsed electromagnetic energy treatment offers no clinical benefit in reducing the pain of knee osteoarthritis: a systematic review. BMC Musculoskelet Disord. 2006;7(1):1–5.

    Article  Google Scholar 

  63. 63.

    Wuschech H, et al. Effects of PEMF on patients with osteoarthritis: results of a prospective, placebo-controlled, double-blind study. Bioelectromagnetics. 2015;36(8):576–85.

    PubMed  Article  Google Scholar 

  64. 64.

    Esposito M, et al. Differentiation of human umbilical cord-derived mesenchymal stem cells, WJ-MSCs, into chondrogenic cells in the presence of pulsed electromagnetic fields. In Vivo. 2013;27(4):495–500.

    CAS  PubMed  Google Scholar 

  65. 65.

    Anbarasan S, et al. Low dose short duration pulsed electromagnetic field effects on cultured human chondrocytes. Indian J Orthop. 2016;50(1):87–93.

    PubMed  PubMed Central  Article  Google Scholar 

  66. 66.

    Ciombor DM, et al. Modification of osteoarthritis by pulsed electromagnetic field—a morphological study. Osteoarthritis Cartilage. 2003;11(6):455–62.

    PubMed  Article  Google Scholar 

  67. 67.

    Spadaro JA, et al. Electromagnetic effects on forearm disuse osteopenia: a randomized, double-blind, sham-controlled study. Bioelectromagnetics. 2011;32(4):273–82.

    PubMed  Article  Google Scholar 

  68. 68.

    Roozbeh N, et al. Influence of radiofrequency electromagnetic fields on the fertility system: protocol for a systematic review and meta-analysis. JMIR Res Protoc. 2018; 7(2): e33.

  69. 69.

    Ishida M, et al. Electromagnetic fields. Clin Orthop Relat Res. 2008;466(5):1068–73.

    PubMed  PubMed Central  Article  Google Scholar 

  70. 70.

    Marmotti A, et al. Pulsed electromagnetic fields improve tenogenic commitment of umbilical cord-derived mesenchymal stem cells: a potential strategy for tendon repair—an in vitro study. Stem Cells Int. 2018; 2018.

  71. 71.

    De Girolamo L, et al. In vitro functional response of human tendon cells to different dosages of low-frequency pulsed electromagnetic field. Knee Surg Sports Traumatol Arthrosc. 2015;23(11):3443–53.

    PubMed  Article  Google Scholar 

  72. 72.

    Liu M, et al. Role of pulsed electromagnetic fields (PEMF) on tenocytes and myoblasts—potential application for treating rotator cuff tears. J Orthop Res. 2017;35(5):956–64.

    CAS  PubMed  Article  Google Scholar 

  73. 73.

    Wei Y, Xiaolin H, Tao S. Effects of extremely low-frequency-pulsed electromagnetic field on different-derived osteoblast-like cells. Electromagn Biol Med. 2008;27(3):298–311.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  74. 74.

    Canè V, Botti P, Soana S. Pulsed magnetic fields improve osteoblast activity during the repair of an experimental osseous defect. J Orthop Res. 1993;11(5):664–70.

    PubMed  Article  Google Scholar 

  75. 75.

    Ehnert S, et al. Primary human osteoblasts with reduced alkaline phosphatase and matrix mineralization baseline capacity are responsive to extremely low frequency pulsed electromagnetic field exposure—clinical implication possible. Bone Rep. 2015;3:48–56.

    PubMed  PubMed Central  Article  Google Scholar 

  76. 76.

    Yumoto H, et al. Electromagnetic wave irradiation promotes osteoblastic cell proliferation and up-regulates growth factors via activation of the ERK1/2 and p38 MAPK pathways. Cell Physiol Biochem. 2015;35(2):601–15.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  77. 77.

    Nindl G, et al. Experiments showing that electromagnetic fields can be used to treat inflammatory diseases. Biomed Sci Instrum. 2000;36:7–13.

    CAS  PubMed  PubMed Central  Google Scholar 

  78. 78.

    Varani K, et al. Adenosine receptors as a biological pathway for the anti-inflammatory and beneficial effects of low frequency low energy pulsed electromagnetic fields. Mediators Inflamm. 2017; 2017.

  79. 79.

    Vincenzi F, et al. Pulsed electromagnetic fields increased the anti-inflammatory effect of A2A and A3 adenosine receptors in human T/C-28a2 chondrocytes and hFOB 1.19 osteoblasts. PloS One. 2013; 8(5): e65561.

  80. 80.

    Yuan J, Xin F, Jiang W. Underlying signaling pathways and therapeutic applications of pulsed electromagnetic fields in bone repair. Cell Physiol Biochem. 2018;46(4):1581–94.

    CAS  PubMed  Article  Google Scholar 

  81. 81.

    Milgram J, et al. The effect of short, high intensity magnetic field pulses on the healing of skin wounds in rats. Bioelectromagnetics. 2004; 25(4): 271–277.

  82. 82.

    Cheing GLY, et al. Pulsed electromagnetic fields (PEMF) promote early wound healing and myofibroblast proliferation in diabetic rats. Bioelectromagnetics. 2014;35(3):161–9.

    CAS  PubMed  Article  Google Scholar 

  83. 83.

    Athanasiou A, et al. The effect of pulsed electromagnetic fields on secondary skin wound healing: an experimental study. Bioelectromagnetics. 2007; 28(5): 362–368.

  84. 84.

    Matic M, et al. Influence of different types of electromagnetic fields on skin reparatory processes in experimental animals. Lasers Med Sci. 2009;24(3):321–7.

    PubMed  Article  Google Scholar 

  85. 85.

    Henry SL, Concannon MJ, Yee GJ. The effect of magnetic fields on wound healing: experimental study and review of the literature. Eplasty. 2008; 8.

  86. 86.

    Vianale G, et al. Extremely low frequency electromagnetic field enhances human keratinocyte cell growth and decreases proinflammatory chemokine production. Br J Dermatol. 2008;158(6):1189–96.

    CAS  PubMed  Article  Google Scholar 

  87. 87.

    Manni V, et al. Effects of extremely low frequency (50 Hz) magnetic field on morphological and biochemical properties of human keratinocytes. Bioelectromagnetics. 2002; 23(4): 298–305.

  88. 88.

    Pesce M, et al. Extremely low frequency electromagnetic field and wound healing: implication of cytokines as biological mediators. Eur Cytokine Netw. 2013;24(1):1–10.

    CAS  PubMed  Article  Google Scholar 

  89. 89.

    Patruno A, et al. Extremely low frequency electromagnetic fields modulate expression of inducible nitric oxide synthase, endothelial nitric oxide synthase and cyclooxygenase-2 in the human keratinocyte cell line HaCat: potential therapeutic effects in wound healing. Br J Dermatol. 2010;162(2):258–66.

    CAS  PubMed  Article  Google Scholar 

  90. 90.

    Goodman R, et al. Extremely low frequency electromagnetic fields activate the ERK cascade, increase hsp70 protein levels and promote regeneration in Planaria. Int J Radiat Biol. 2009;85(10):851–9.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  91. 91.

    Kim Y-M, et al. Effects of extremely low frequency electromagnetic fields on melanogenesis through p-ERK and p-SAPK/JNK pathways in human melanocytes. Int J Mol Sci. 2017;18(10):2120.

    PubMed Central  Article  CAS  PubMed  Google Scholar 

  92. 92.

    Klimek A, Rogalska J. Extremely low-frequency magnetic field as a stress factor—really detrimental?—insight into literature from the last decade. Brain Sci. 2021;11(2):174.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  93. 93.

    Paolucci T, et al. Efficacy of extremely low-frequency magnetic field in fibromyalgia pain: a pilot study. J Rehabil Res Dev. 2016;53(6):1023–34.

    PubMed  Article  Google Scholar 

  94. 94.

    Chen G, et al. Effect of electromagnetic field exposure on chemically induced differentiation of friend erythroleukemia cells. Environ Health Perspect. 2000;108(10):967–72.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  95. 95.

    Ding GR, et al. Extremely low frequency magnetic fields and the promotion of H2O2-induced cell death in HL-60 cells. Int J Radiat Biol. 2004;80(4):317–24.

    CAS  PubMed  Article  Google Scholar 

  96. 96.

    Liburdy R, et al. ELF magnetic fields, breast cancer, and melatonin: 60 Hz fields block melatonin’s oncostatic action on ER+ breast cancer cell proliferation. J Pineal Res. 1993;14(2):89–97.

    CAS  PubMed  Article  Google Scholar 

  97. 97.

    Nishimura T, et al. A 1-μT extremely low-frequency electromagnetic field vs. sham control for mild-to-moderate hypertension: a double-blind, randomized study. Hypertens Res. 2011; 34(3): 372–377.

  98. 98.

    Torres-Duran PV, et al. Effects of whole body exposure to extremely low frequency electromagnetic fields (ELF-EMF) on serum and liver lipid levels, in the rat. Lipids Health Dis. 2007;6(1):1–6.

    Article  CAS  Google Scholar 

  99. 99.

    Goldberg AD, Allis CD, Bernstein E. Epigenetics: a landscape takes shape. Cell. 2007;128(4):635–8.

    CAS  PubMed  Article  Google Scholar 

  100. 100.

    Pulliero A, et al. Genetic and epigenetic effects of environmental mutagens and carcinogens. 2015, Hindawi.

  101. 101.

    Jankowska AM, Millward CL, Caldwell CW. The potential of DNA modifications as biomarkers and therapeutic targets in oncology. Expert Rev Mol Diagn. 2015;15(10):1325–37.

    CAS  PubMed  Article  Google Scholar 

  102. 102.

    Alegría-Torres JA, Baccarelli A, Bollati V. Epigenetics and lifestyle. Epigenomics. 2011;3(3):267–77.

    PubMed  Article  CAS  Google Scholar 

  103. 103.

    Manser M, et al. ELF-MF exposure affects the robustness of epigenetic programming during granulopoiesis. Sci Rep. 2017;7(1):1–14.

    Article  Google Scholar 

  104. 104.

    Sigalotti L, et al. Epigenetic drugs as pleiotropic agents in cancer treatment: biomolecular aspects and clinical applications. J Cell Physiol. 2007;212(2):330–44.

    CAS  PubMed  Article  Google Scholar 

  105. 105.

    Abdel-Hafiz HA, Horwitz KB. Role of epigenetic modifications in luminal breast cancer. Epigenomics. 2015;7(5):847–62.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  106. 106.

    Mehta A, et al. Epigenetics in lung cancer diagnosis and therapy. Cancer Metastasis Rev. 2015;34(2):229–41.

    CAS  PubMed  Article  Google Scholar 

  107. 107.

    Mayes K, et al. ATP-dependent chromatin remodeling complexes as novel targets for cancer therapy, in Advances in cancer research. 2014, Elsevier. pp. 183-233

  108. 108.

    Becker PB, Workman JL. Nucleosome remodeling and epigenetics. Cold Spring Harb Perspect Biol. 2013; 5(9): a017905.

  109. 109.

    Iacobucci I, et al. Genomic subtyping and therapeutic targeting of acute erythroleukemia. Nat Genet. 2019;51(4):694–704.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  110. 110.

    Yi J, Wu J. Epigenetic regulation in medulloblastoma. Mol Cell Neurosci. 2018;87:65–76.

    CAS  PubMed  Article  Google Scholar 

  111. 111.

    Geller JI, Roth JJ, Biegel JA. Biology and treatment of rhabdoid tumor. Crit Rev Oncog. 2015; 20(3–4).

  112. 112.

    Bottani M, Banfi G, Lombardi G. Circulating miRNAs as diagnostic and prognostic biomarkers in common solid tumors: focus on lung, breast, prostate cancers, and osteosarcoma. J Clin Med. 2019;8(10):1661.

    CAS  PubMed Central  Article  Google Scholar 

  113. 113.

    Chen Z, et al. High-resolution and high-accuracy topographic and transcriptional maps of the nucleosome barrier. Elife. 2019; 8: e48281.

  114. 114.

    Mazina MY, Vorobyeva N. The role of ATP-dependent chromatin remodeling complexes in regulation of genetic processes. Russ J Genet. 2016;52(5):463–72.

    CAS  Article  Google Scholar 

  115. 115.

    Hamam R, et al. Circulating microRNAs in breast cancer: novel diagnostic and prognostic biomarkers. Cell Death Dis. 2017;8(9):e3045–e3045.

    PubMed  PubMed Central  Article  Google Scholar 

  116. 116.

    Filipów S, Łaczmański Ł. Blood circulating miRNAs as cancer biomarkers for diagnosis and surgical treatment response. Front Genet. 2019;10:169.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  117. 117.

    Kawaguchi T, et al. Circulating microRNAs: a next-generation clinical biomarker for digestive system cancers. Int J Mol Sci. 2016;17(9):1459.

    PubMed Central  Article  CAS  PubMed  Google Scholar 

  118. 118.

    Audia JE, Campbell RM. Histone modifications and cancer. Cold Spring Harb Perspect Biol. 2016; 8(4): a019521.

  119. 119.

    Liu Y, et al. Overexpression of miR-26b-5p regulates the cell cycle by targeting CCND2 in GC-2 cells under exposure to extremely low frequency electromagnetic fields. Cell Cycle. 2016;15(3):357–67.

    CAS  PubMed  Article  Google Scholar 

  120. 120.

    Kheifets L, et al. Extremely low frequency electric fields and cancer: assessing the evidence. Bioelectromagnetics. 2010; 31(2): 89–101.

  121. 121.

    Azadian E, et al. A comprehensive overview on utilizing electromagnetic fields in bone regenerative medicine. Electromagn Biol Med. 2019;38(1):1–20.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  122. 122.

    Koziorowska A, et al. Extremely low frequency variable electromagnetic fields affect cancer and noncancerous cells in vitro differently: preliminary study. Electromagn Biol Med. 2018;37(1):35–42.

    PubMed  Article  Google Scholar 

  123. 123.

    Provenzano AE, et al. Effects of fifty-hertz electromagnetic fields on granulocytic differentiation of ATRA-treated acute promyelocytic leukemia NB4 cells. Cell Physiol Biochem. 2018;46(1):389–400.

    CAS  Article  Google Scholar 

  124. 124.

    Blankenburg M, et al. High-throughput omics technologies: potential tools for the investigation of influences of EMF on biological systems. Curr Genomics. 2009;10(2):86–92.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  125. 125.

    Sage C, Burgio E. Electromagnetic fields, pulsed radiofrequency radiation, and epigenetics: how wireless technologies may affect childhood development. Child Dev. 2018;89(1):129–36.

    PubMed  Article  Google Scholar 

  126. 126.

    Zimmerman JW, et al. Targeted treatment of cancer with radiofrequency electromagnetic fields amplitude-modulated at tumor-specific frequencies. Chin J Cancer. 2013;32(11):573.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  127. 127.

    Vadalà M, et al. Mechanisms and therapeutic effectiveness of pulsed electromagnetic field therapy in oncology. Cancer Med. 2016;5(11):3128–39.

    PubMed  PubMed Central  Article  Google Scholar 

  128. 128.

    Pasi F, et al. Pulsed electromagnetic field with temozolomide can elicit an epigenetic pro-apoptotic effect on glioblastoma T98G cells. Anticancer Res. 2016;36(11):5821–6.

    CAS  PubMed  Article  Google Scholar 

  129. 129.

    Giorgi G, et al. Assessing the combined effect of extremely low-frequency magnetic field exposure and oxidative stress on LINE-1 promoter methylation in human neural cells. Radiat Environ Biophys. 2017;56(2):193–200.

    CAS  PubMed  Article  Google Scholar 

  130. 130.

    Calcabrini C, et al. Effect of extremely low-frequency electromagnetic fields on antioxidant activity in the human keratinocyte cell line NCTC 2544. Biotechnol Appl Biochem. 2017;64(3):415–22.

    CAS  PubMed  Article  Google Scholar 

  131. 131.

    Kivrak EG, et al. Effects of electromagnetic fields exposure on the antioxidant defense system. J Microsc Ultrastruct. 2017;5(4):167–76.

    PubMed  PubMed Central  Article  Google Scholar 

  132. 132.

    Santini SJ, et al. Corrigendum to “Role of mitochondria in the oxidative stress induced by electromagnetic fields: focus on reproductive systems.” Oxid Med Cell Longev. 2020;2020:5203105.

    PubMed  PubMed Central  Article  Google Scholar 

  133. 133.

    Santini SJ, et al. Role of mitochondria in the oxidative stress induced by electromagnetic fields: focus on reproductive systems. Oxid Med Cell Longev. 2018;2018:5076271.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  134. 134.

    Lim SO, et al. Epigenetic changes induced by reactive oxygen species in hepatocellular carcinoma: methylation of the E-cadherin promoter. Gastroenterology. 2008; 135(6): 2128–40, 2140 e1–8.

  135. 135.

    Koturbash I. 2017 Michael fry award lecture when DNA is actually not a target: radiation epigenetics as a tool to understand and control cellular response to ionizing radiation. Radiat Res. 2018;190(1):5–11.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  136. 136.

    Miousse IR, et al. One-carbon metabolism and ionizing radiation: a multifaceted interaction. Biomol Concepts. 2017;8(2):83–92.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  137. 137.

    Kim J-G, et al. Epigenetics meets radiation biology as a new approach in cancer treatment. Int J Mol Sci. 2013;14(7):15059–73.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  138. 138.

    Dasdag S, et al. Effects of 2.4 GHz radiofrequency radiation emitted from Wi-Fi equipment on microRNA expression in brain tissue. Int J Radiat Biol. 2015; 91(7): 555–561.

  139. 139.

    Varghese E, et al. Anti-cancer agents in proliferation and cell death: the calcium connection. Int J Mol Sci. 2019; 20(12).

  140. 140.

    Brzozowski JS, Skelding KA. The multi-functional calcium/calmodulin stimulated protein kinase (CaMK) family: emerging targets for anti-cancer therapeutic intervention. Pharmaceuticals (Basel). 2019; 12(1).

  141. 141.

    Bissonnette SL, et al. The role of CaMKII in calcium-activated death pathways in bone marrow B cells. Toxicol Sci. 2010;118(1):108–18.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  142. 142.

    Chuang HC, Wang X, Tan TH. MAP4K family kinases in immunity and inflammation. Adv Immunol. 2016;129:277–314.

    CAS  PubMed  Article  Google Scholar 

  143. 143.

    Lee S, Rauch J, Kolch W. Targeting MAPK signaling in cancer: mechanisms of drug resistance and sensitivity. Int J Mol Sci. 2020; 21(3).

  144. 144.

    Jaquenod De Giusti C, Roman B, Das S. The influence of micrornas on mitochondrial calcium. Front Physiol. 2018; 9: 1291.

Download references

Author information

Affiliations

Authors

Corresponding authors

Correspondence to Alireza Madjid Ansari or Mohammad Amin Javidi.

Ethics declarations

Conflict of interest

The authors state that there is no conflict of interest regarding the publication of this article.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Shayeghan, M., Forouzesh, F., Madjid Ansari, A. et al. DNMT1 and miRNAs: possible epigenetics footprints in electromagnetic fields utilization in oncology. Med Oncol 38, 125 (2021). https://doi.org/10.1007/s12032-021-01574-y

Download citation

Keywords

  • Epigenetics
  • Anti-cancer
  • Electromagnetic fields
  • Non-ionizing EMF
  • Oncology