2,640
Views
20
CrossRef citations to date
0
Altmetric
Reviews

Non-thermal membrane effects of electromagnetic fields and therapeutic applications in oncology

, &
Pages 715-731 | Received 17 Jan 2021, Accepted 01 Apr 2021, Published online: 28 Apr 2021

References

  • Wust P, Hildebrandt B, Sreenivasa G, et al. Hyperthermia in combined treatment of cancer. Lancet Oncol. 2002;3(8):487–497.
  • Issels RD, Lindner LH, Verweij J, et al. Effect of neoadjuvant chemotherapy plus regional hyperthermia on long-term outcomes among patients with localized high-risk soft tissue sarcoma: the EORTC 62961-ESHO 95 randomized clinical trial. JAMA Oncol. 2018;4(4):483–492.
  • Van Der Zee J, Gonzalez Gonzalez D, Van Rhoon GC, et al. Comparison of radiotherapy alone with radiotherapy plus hyperthermia in locally advanced pelvic tumours: a prospective, randomised, multicentre trial. Lancet. 2000;355(9210):1119–1125.
  • Harima Y, Nagata K, Harinma K, et al. A randomized clinical trial of radiation therapy versus thermoradiotherapy in stage III cervical carcinoma. Int J Hyperthermia. 2001;17:97–105.
  • Harima Y, Ohguri T, Imada H, et al. A multicentre randomised clinical trial of chemoradiotherapy plus hyperthermia versus chemoradiotherapy alone in patients with locally advanced cervical cancer. Int J Hyperthermia. 2016;32(7):801–808.
  • Vernon CC, Hand JW, Field SB, et al. Radiotherapy with or without hyperthermia in the treatment of superficial localized breast cancer: results from five randomized controlled trials. International collaborative hyperthermia group. Int J Radiat Oncol Biol Phys. 1996;35(4):731–744.
  • Jones EL, Oleson JR, Prosnitz LR, et al. Randomized trial of hyperthermia and radiation for superficial tumors. J Clin Oncol. 2005;23(13):3079–3085.
  • Van Der Zee J, De Bruijne M, Mens JWM, et al. Reirradiation combined with hyperthermia in breast cancer recurrences: overview of experience in Erasmus MC. Int J Hyperthermia. 2010;26(7):638–648.
  • Overgaard J, Gonzalez Gonzalez D, Hulshof MC, et al. Randomised trial of hyperthermia as adjuvant to radiotherapy for recurrent or metastatic malignant melanoma. Lancet. 1995;345(8949):540–543.
  • Lagendijk JJ, Van Rhoon GC, Hornsleth SN, et al. ESHO quality assurance guidelines for regional hyperthermia. Int J Hyperthermia. 1998;14(2):125–133.
  • Kok HP, Cressman EN, Ceelen W, et al. Heating technology for malignant tumors: a review. Int J Hyperthermia. 2020;37(1):711–741.
  • Dewey WC, Hopwood LE, Sapareto SA, et al. Cellular responses to combinations of hyperthermia and radiation. Radiology. 1977;123(2):463–474.
  • Hahn GM. Potential for therapy of drugs and hyperthermia. Cancer Res. 1979;39(6 Pt 2):2264–2268.
  • Overgaard J. Simultaneous and sequential hyperthermia and radiation treatment of an experimental tumor and its surrounding normal tissue in vivo. Int J Radiat Oncol Biol Phys. 1980;6(11):1507–1517.
  • Urano M, Kahn J, Majima H, et al. The cytotoxic effect of cis-diamminedichloroplatinum(II) on cultured Chinese hamster ovary cells at elevated temperatures: Arrhenius plot analysis . Int J Hyperthermia. 1990;6(3):581–590.
  • Franken NAP, Oei AL, Kok HP, et al. Cell survival and radiosensitisation: modulation of the linear and quadratic parameters of the LQmodel (review). Int J Oncol. 2013;42(5):1501–1515.
  • Mei X, Ten Cate R, Van Leeuwen CM, et al. Radiosensitization by hyperthermia: the effects of temperature, sequence, and time Interval in cervical cell lines. Cancers. 2020;12(3):582.
  • Franckena M, Fatehi D, de Bruijne M, et al. Hyperthermia dose-effect relationship in 420 patients with cervical cancer treated with combined radiotherapy and hyperthermia. Eur J Cancer. 2009;45(11):1969–1978.
  • Dinges S, Harder C, Wurm R, et al. Combined treatment of inoperable carcinomas of the uterine cervix with radiotherapy and regional hyperthermia. Results of a phase II trial. Strahlenther Onkol. 1998;174(10):517–521.
  • Sreenivasa G, Hildebrandt B, Kümmel S, et al. Radiochemotherapy combined with regional pelvic hyperthermia induces high response and resectability rates in patients with nonresectable cervical cancer >/ =FIGO IIB "bulky". Int J Radiat Oncol Biol Phys. 2006;66(4):1159–1167.
  • Tilly W, Wust P, Rau B, et al. Temperature data and specific absorption rates in pelvic tumours: predictive factors and correlations. Int J Hyperthermia. 2001;17(2):172–188.
  • Hildebrandt B, Hegewisch-Becker S, Kerner T, et al. Current status of radiant whole-body hyperthermia at temperatures >41.5 degrees C and practical guidelines for the treatment of adults. The German 'interdisciplinary working group on hyperthermia'. Int J Hyperthermia. 2005;21(2):169–183.
  • Minnaar CA, Kotzen JA, Ayeni OA, et al. The effect of modulated electro-hyperthermia on local disease control in HIV-positive and -negative cervical cancer women in South Africa: early results from a phase III randomised controlled trial. PLOS One. 2019;14(6):e0217894.
  • Minnaar CA, Kotzen JA, Naidoo T, et al. Analysis of the effects of mEHT on the treatment-related toxicity and quality of life of HIV-positive cervical cancer patients. Int J Hyperthermia. 2020;37(1):263–272.
  • Stupp R, Taillibert S, Kanner A, et al. Effect of tumor-treating fields plus maintenance temozolomide vs. maintenance temozolomide alone on survival in patients with glioblastoma: a randomized clinical trial. JAMA. 2017;318(23):2306–2316.
  • Barbault A, Costa FP, Bottger B, et al. Amplitude-modulated electromagnetic fields for the treatment of cancer: discovery of tumor-specific frequencies and assessment of a novel therapeutic approach. J Exp Clin Cancer Res. 2009;28(1):51.
  • Costa FP, De Oliveira AC, Meirelles R, et al. Treatment of advanced hepatocellular carcinoma with very low levels of amplitude-modulated electromagnetic fields. Br J Cancer. 2011;105(5):640–648.
  • Szasz AM, Minnaar CA, Szentmártoni G, et al. Review of the clinical evidences of modulated electro-hyperthermia (mEHT) method: an update for the practicing oncologist. Front Oncol. 2019;9:1012.
  • Lee SY, Lee NR, Cho DH, et al. Treatment outcome analysis of chemotherapy combined with modulated electro-hyperthermia compared with chemotherapy alone for recurrent cervical cancer, following irradiation. Oncol Lett. 2017;14(1):73–78.
  • Lee SY, Kim JH, Han YH, et al. The effect of modulated electro-hyperthermia on temperature and blood flow in human cervical carcinoma. Int J Hyperthermia. 2018;34(7):953–960.
  • Fiorentini G, Sarti D, Milandri C, et al. Modulated electrohyperthermia in integrative cancer treatment for relapsed malignant glioblastoma and astrocytoma: retrospective multicenter controlled study. Integr Cancer Ther. 2019;18:1534735418812691.
  • Stupp R, Hegi ME, Mason WP, et al. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol. 2009;10(5):459–466.
  • Hager ED, Dziambor H, Hohmann D, et al. Deep hyperthermia with radiofrequencies in patients with liver metastases from colorectal cancer. Anticancer Res. 1999;19(4):3403–3408.
  • Lok E, San P, Hua V, et al. Analysis of physical characteristics of tumor treating fields for human glioblastoma. Cancer Med. 2017;6(6):1286–1300.
  • Miranda PC, Mekonnen A, Salvador R, et al. Predicting the electric field distribution in the brain for the treatment of glioblastoma. Phys Med Biol. 2014;59(15):4137–4147.
  • Wenger C, Salvador R, Basser PJ, et al. The electric field distribution in the brain during TTFields therapy and its dependence on tissue dielectric properties and anatomy: a computational study. Phys Med Biol. 2015;60(18):7339–7357.
  • Ballo MT, Urman N, Lavy-Shahaf G, et al. Correlation of tumor treating fields dosimetry to survival outcomes in newly diagnosed glioblastoma: a large-scale numerical simulation-based analysis of data from the phase 3 EF-14 randomized trial. Int J Radiat Oncol Biol Phys. 2019;104(5):1106–1113.
  • Bakitas MA, Tosteson TD, Li Z, et al. Early versus delayed initiation of concurrent palliative oncology care: patient outcomes in the ENABLE III randomized controlled trial. J Clin Oncol. 2015;33(13):1438–1445.
  • Mun EJ, Babiker HM, Weinberg U, et al. Tumor-treating fields: a fourth modality in cancer treatment. Clin Cancer Res. 2018;24(2):266–275.
  • Sharma S, Wu SY, Jimenez H, et al. Ca2+ and CACNA1H mediate targeted suppression of breast cancer brain metastasis by AM RF EMF. EBioMedicine. 2019;44:194–208.
  • Feychting M, Ahlbom A, Kheifets L. EMF and health. Annu Rev Public Health. 2005;26:165–189.
  • Kheifets L, Bowman JD, Checkoway H, et al. Future needs of occupational epidemiology of extremely low frequency electric and magnetic fields: review and recommendations. Occup Environ Med. 2009;66(2):72–80.
  • Foster KR. Thermal and nonthermal mechanisms of interaction of radio-frequency energy with biological systems. IEEE Trans Plasma Sci. 2000;28(1):15–23.
  • Adair RK. Biophysical limits on athermal effects of RF and microwave radiation. Bioelectromagnetics. 2003;24(1):39–48.
  • Ahlbom A, Green A, Kheifets L, et al. Epidemiology of health effects of radiofrequency exposure. Environ Health Perspect. 2004;112(17):1741–1754.
  • Litvak E, Foster KR, Repacholi MH. Health and safety implications of exposure to electromagnetic fields in the frequency range 300 Hz to 10 MHz. Bioelectromagnetics. 2002;23(1):68–82.
  • Schuderer J, Oesch W, Felber N, et al. In vitro exposure apparatus for ELF magnetic fields. Bioelectromagnetics. 2004;25(8):582–591.
  • Schuderer J, Spat D, Samaras T, et al. In vitro exposure systems for RF exposures at 900 MHz. IEEE Trans Microwave Theory Techn. 2004;52(8):2067–2075.
  • Schuderer J, Samaras T, Oesch W, et al. High peak SAR exposure unit with tight exposure and environmental control for in vitro experiments at 1800 MHz. IEEE Trans Microwave Theory Techn. 2004;52(8):2057–2066.
  • Kuster N, Schönborn F. Recommended minimal requirements and development guidelines for exposure setups of bio‐experiments addressing the health risk concern of wireless communications. Bioelectromagnetics. 2000;21(7):508–514.
  • Greenebaum B, Barnes F. Handbook of biological effects of electromagnetic fields. 4th ed. Vol. 1, Biological and medical aspects of electromagnetic fields. Boca Raton: CRC Press;2019.
  • Greenebaum B, Barnes F. Handbook of biological effects of electromagnetic fields. 4th ed. Vol. 2, Bioengineering and biophysical aspects of electromagnetic fields. Boca Raton: CRC Press; 2019.
  • Verrender A, Loughran SP, Dalecki A, et al. Pulse modulated radiofrequency exposure influences cognitive performance. Int J Radiat Biol. 2016;92(10):603–610.
  • Miyakoshi J. Cellular and molecular responses to radio-frequency electromagnetic fields. Proc IEEE. 2013;101(6):1494–1502.
  • Wust P, Kortüm B, Strauss U, et al. Non-thermal effects of radiofrequency electromagnetic fields. Scientific Rep. 2020;10:13488.
  • Reitz JR, Milford FJ, Christy RW. Foundations of electromagnetic theory. 4th ed. Boston (MA): Addison-Wesley Publishing Company;2008.
  • Szasz A, Szasz O, Iluri N, inventor. Radiofrequency hyperthermia device with targeted feedback signal modulation. United States Patent US 9,320,911 B2. 2016.
  • Wust P, Ghadjar P, Nadobny J, et al. Physical analysis of temperature-dependent effects of amplitude-modulated electromagnetic hyperthermia. Int J Hyperthermia. 2019;36(1):1245–1253.
  • Schaefer H, Schwan H. On the question of selective heating small particles in the ultra-short wave capacitor field (Zur Frage der selektiven Erhitzung kleiner Teilchen im Ultrakurzwellen‐Kondensatorfeld). Ann Phys. 1943;435(1–2):99–135.
  • Rabin Y. Is intracellular hyperthermia superior to extracellular hyperthermia in the thermal sense? Int J Hyperthermia. 2002;18(3):194–202.
  • Yamada K, Oda T, Hashimoto S, et al. Minimally required heat doses for various tumour sizes in induction heating cancer therapy determined by computer simulation using experimental data. Int J Hyperthermia. 2010;26(5):465–474.
  • Hedayati M, Thomas O, Abubaker-Sharif B, et al. The effect of cell cluster size on intracellular nanoparticle-mediated hyperthermia: is it possible to treat microscopic tumors? Nanomedicine). 2013;8(1):29–41.
  • Danics L, Schvarcz CA, Viana P, et al. Exhaustion of protective heat shock response 2 induces significant tumor damage by apoptosis 3 after modulated electro-hyperthermia treatment of 4 triple negative breast cancer isografts in mice. Cancers. 2020;12(9):2581.
  • Krenacs T, Meggyeshazi N, Forika G, et al. Modulated electro-hyperthermia-induced tumor damage mechanisms revealed in cancer models. IJMS. 2020;21(17):6270.
  • Andocs G, Renner H, Balogh L, et al. Strong synergy of heat and modulated electromagnetic field in tumor cell killing. Strahlenther Onkol. 2009;185(2):120–126.
  • Tsang YW, Huang CC, Yang KL, et al. Improving immunological tumor microenvironment using electro-hyperthermia followed by dendritic cell immunotherapy. BMC Cancer. 2015;15:708.
  • Yang KL, Huang CC, Chi MS, et al. In vitro comparison of conventional hyperthermia and modulated electro-hyperthermia. Oncotarget. 2016;7(51):84082–84092.
  • Andocs G, Rehman MU, Zhao QL, et al. Comparison of biological effects of modulated electro-hyperthermia and conventional heat treatment in human lymphoma U937 cells. Cell Death Discov. 2016;2:16039.
  • Andocs G, Rehman MU, Zhao QL, et al. Nanoheating without artificial nanoparticles part II. Experimental support of the nanoheating concept of the modulated electro-hyperthermia method, using U937 cell suspension model. Biol Med. 2015;07(04):1.
  • Meggyesházi N, Andócs G, Spisák S, et al. Early changes in mRNA and protein expression related to cancer treatment by modulated electrohyperthermia Conference Papers in Medicine; 2012 Oct 12–14; Budapest, Hungary; Vol. 2013; Hindawi.
  • Meggyesházi N, Andocs G, Balogh L, et al. DNA fragmentation and caspase-independent programmed cell death by modulated electrohyperthermia. Strahlenther Onkol. 2014;190(9):815–822.
  • Andocs G, Meggyeshazi N, Balogh L, et al. Upregulation of heat shock proteins and the promotion of damage-associated molecular pattern signals in a colorectal cancer model by modulated electrohyperthermia. Cell Stress Chaperones. 2015;20(1):37–46.
  • Cha J, Jeon TW, Lee CG, et al. Electro-hyperthermia inhibits glioma tumorigenicity through the induction of E2F1-mediated apoptosis. Int J Hyperthermia. 2015;31(7):784–792.
  • Jeon TW, Yang H, Lee CG, et al. Electro-hyperthermia up-regulates tumour suppressor Septin 4 to induce apoptotic cell death in hepatocellular carcinoma. Int J Hyperthermia. 2016;32(6):648–656.
  • Vancsik T, Kovago C, Kiss E, et al. Modulated electro-hyperthermia induced loco-regional and systemic tumor destruction in colorectal cancer allografts. J Cancer. 2018;9(1):41–53.
  • Vancsik T, Forika G, Balogh A, et al. Modulated electro-hyperthermia induced p53 driven apoptosis and cell cycle arrest additively support doxorubicin chemotherapy of colorectal cancer in vitro . Cancer Med. 2019i8(9):4292–4303.
  • Besztercei B, Vancsik T, Benedek A, et al. Stress-induced, p53-mediated tumor growth inhibition of melanoma by modulated electrohyperthermia in mouse models without major immunogenic effects. IJMS. 2019;20(16):4019.
  • Garg AD, Martin S, Golab J, et al. Danger signalling during cancer cell death: origins, plasticity and regulation. Cell Death Differ. 2014;21(1):26–38.
  • Hernandez C, Huebener P, Schwabe RF. Damage-associated molecular patterns in cancer: a double-edged sword. Oncogene. 2016;35(46):5931–5941.
  • Qin W, Akutsu Y, Andocs G, et al. Modulated electro-hyperthermia enhances dendritic cell therapy through an abscopal effect in mice. Oncol Rep. 2014;32(6):2373–2379.
  • Kim W, Kim MS, Kim HJ, et al. Role of HIF-1α in response of tumors to a combination of hyperthermia and radiation in vivo. Int J Hyperthermia. 2018;34(3):276–283.
  • McDonald M, Corde S, Lerch M, et al. First in vitro evidence of modulated electro-hyperthermia treatment performance in combination with megavoltage radiation by clonogenic assay. Sci Rep. 2018;8(1):1–3.
  • Prasad B, Kim S, Cho W, et al. Quantitative estimation of the equivalent radiation dose escalation using radiofrequency hyperthermia in mouse xenograft models of human lung cancer. Sci Rep. 2019;9(1):3942.
  • Forika G, Balogh A, Vancsik T, et al. Modulated electro-hyperthermia resolves radioresistance of Panc1 pancreas adenocarcinoma and promotes DNA damage and apoptosis in vitro. IJMS. 2020;21(14):5100.
  • Tsang YW, Chi KH, Huang CC, et al. Modulated electro-hyperthermia-enhanced liposomal drug uptake by cancer cells. Int J Nanomedicine. 2019;14:1269–1279.
  • Kirson ED, Gurvich Z, Schneiderman R, et al. Disruption of cancer cell replication by alternating electric fields. Cancer Res. 2004;64(9):3288–3295.
  • Kirson ED, Dbalý V, Tovaryš F, et al. Alternating electric fields arrest cell proliferation in animal tumor models and human brain tumors. Proc Natl Acad Sci USA. 2007;104(24):10152–10157.
  • Kirson ED, Schneiderman RS, Dbalý V, et al. Chemotherapeutic treatment efficacy and sensitivity are increased by adjuvant alternating electric fields (TTFields). BMC Med Phys. 2009;9(1):1–3.
  • Silginer M, Weller M, Stupp R, et al. Biological activity of tumor-treating fields in preclinical glioma models. Cell Death Dis. 2017;8(4):e2753.
  • Zimmerman JW, Jimenez H, Pennison MJ, et al. Targeted treatment of cancer with radiofrequency electromagnetic fields amplitude-modulated at tumor-specific frequencies. Chin J Cancer. 2013;32(11):573–581.
  • Zimmerman JW, Pennison MJ, Brezovich I, et al. Cancer cell proliferation is inhibited by specific modulation frequencies. Br J Cancer. 2012;106(2):307–313.
  • Jimenez H, Wang M, Zimmerman JW, et al. Tumour-specific amplitude-modulated radiofrequency electromagnetic fields induce differentiation of hepatocellular carcinoma via targeting Cav3.2 T-type voltage-gated calcium channels and Ca2+ influx . EBioMedicine. 2019;44:209–224.
  • Taylor JT, Zeng XB, Pottle JE, et al. Calcium signaling and T-type calcium channels in cancer cell cycling. World J Gastroenterol. 2008;14(32):4984–4991.
  • Buckner CA, Buckner AL, Koren SA, et al. Inhibition of cancer cell growth by exposure to a specific time-varying electromagnetic field involves T-type calcium channels. PLOS One. 2015;10(4):e0124136.
  • Phan NN, Wang CY, Chen CF, et al. Voltage-gated calcium channels: novel targets for cancer therapy. Oncol Lett. 2017;14(2):2059–2074.
  • Pickard WF, Moros EG. Energy deposition processes in biological tissue: nonthermal biohazards seem unlikely in the ultra‐high frequency range. Bioelectromagnetics. 2001;22(2):97–105.
  • Adair RK. Vibrational resonances in biological systems at microwave frequencies. Biophys J. 2002;82(3):1147–1152.
  • Adair RK. Noise and stochastic resonance in voltage-gated ion channels. Proc Natl Acad Sci USA. 2003;100(21):12099–12104.
  • Foster KR, Repacholi MH. Biological effects of radiofrequency fields: does modulation matter? Radiat Res. 2004;162(2):219–225.
  • Prohofsky EW. RF absorption involving biological macromolecules. Bioelectromagnetics. 2004;25(6):441–451.
  • Fröhlich H. Long‐range coherence and energy storage in biological systems. Int J Quantum Chem. 1968;2(5):641–649.
  • Edwards GS, Davis CC, Saffer JD, et al. Resonant microwave absorption of selected DNA molecules. Phys Rev Lett. 1984;53(13):1284–1287.
  • Foster KR, Baish JW. Viscous damping of vibrations in microtubules. J Biol Phys. 2000;26(4):255–260.
  • Wust P, Gneveckow U, Johannsen M, et al. Magnetic nanoparticles for interstitial thermotherapy-feasibility, tolerance and achieved temperatures. Int J Hyperthermia. 2006;22(8):673–685.
  • Wust P. Thermotherapy in oncology. Bremen: UNI-MED Verlag AG; 2016.
  • Dutz S, Hergt R. Magnetic nanoparticle heating and heat transfer on a microscale: basic principles, realities and physical limitations of hyperthermia for tumour therapy. Int J Hyperthermia. 2013;29(8):790–800.
  • Foster KR, Schwan HP. Dielectric properties of tissues and biological materials: a critical review. Crit Rev Biomed Eng. 1989;17(1):25–104.
  • Eibert TF, Alaydrus M, Wilczewski F, et al. Electromagnetic and thermal analysis for lipid bilayer membranes exposed to RF fields. IEEE Trans Biomed Eng. 1999;46(8):1013–1020.
  • Martinsen OG, Grimnes S, Schwan HP. Interface phenomena and dielectric properties of biological tissue. Encyclopedia of Surface and Colloid Science. 2002;20:2643–2653.
  • Stoy RD, Foster KR, Schwan HP. Dielectric properties of mammalian tissues from 0.1 to 100 MHz: a summary of recent data. Phys Med Biol. 1982;27(4):501–513.
  • Papp E, Vancsik T, Kiss E, et al. Energy absorption by the membrane rafts in the modulated electro-hyperthermia (mEHT). OJBIPHY. 2017;07(04):216–229.
  • Doyle DA, Cabral JM, Pfuetzner RA, et al. The structure of the potassium channel: molecular basis of K + conduction and selectivity. Science. 1998;280(5360):69–77.
  • Hille B. Ion channels of excitable membranes. 3rd ed. Sunderland: Sinauer Associates Inc.;2001.
  • Friedman MH. Principles and models of biological transport. 2nd ed. New York: Springer Science + Media;2010.
  • Berg JM, Tymoczko J, Gatto GJ, et al. Biochemistry. 9th ed. New York: W.H. Freeman;2019.
  • Neuhaus E, Zirjacks L, Ganser K, et al. Alternating electric fields (TTFields) activate Cav1.2 channels in human glioblastoma cells. Cancers. 2019;11(1):110.
  • Pall ML. Electromagnetic fields act via activation of voltage-gated calcium channels to produce beneficial or adverse effects . J Cell Mol Med. 2013;17(8):958–965.
  • Yamakage M, Namiki A. Calcium channels-basic aspects of their structure, function and gene encoding; anesthetic action on the channels-a review. Can J Anaesth. 2002;49(2):151–164.
  • Huber SM. Oncochannels. Cell Calcium. 2013;53(4):241–255.
  • Fraser SP, Pardo LA. Ion channels: functional expression and therapeutic potential in cancer. Colloquium on ion channels and cancer. EMBO Rep. 2008;9(6):512–515.
  • Stühmer W, Pardo LA. K(+) channels as therapeutic targets in oncology. Future Med Chem. 2010;2(5):745–755.
  • Becchetti A. Ion channels and transporters in cancer. 1. Ion channels and cell proliferation in cancer. Am J Physiol Cell Physiol. 2011;301(2):C255–65.
  • Santoni G, Farfariello V. TRP channels and cancer: new targets for diagnosis and chemotherapy. Endocr Metab Immune Disord Drug Targets. 2011;11(1):54–67.
  • Pardo LA, Stühmer W. The roles of K(+) channels in cancer. Nat Rev Cancer. 2014;14(1):39–48.
  • Lang F, Stournaras C. Ion channels in cancer: future perspectives and clinical potential. Philos Trans R Soc Lond B Biol Sci. 2014;369(1638):20130108.
  • Santoni G, Maggi F, Morelli MB, et al. Transient receptor potential cation channels in cancer therapy. Medical Sciences. 2019;7(12):108.
  • Ashrafuzzaman M. Nanoscale biophysics of the cell. New York: Springer International Publishing AG;2018.
  • Bawin SM, Kaczmarek LK, Adey WR. Effects of modulated VHF fields on the central nervous system. Ann N Y Acad Sci. 1975;247(1):74–81.
  • Blackman CF, Benane SG, Elder JA, et al. Induction of calcium-ion efflux from brain tissue by radiofrequency radiation: effect of sample number and modulation frequency on the power-density window . Bioelectromagnetics. 1980;1(1):35–43.
  • Blackman CF, Benane SG, Kinney LS, et al. Effects of ELF fields on calcium-ion efflux from brain tissue in vitro. Rad Res. 1982;92(3):510–520.
  • Blackman CF, Benane SG, House DE. The influence of temperature during electric- and magnetic-field-induced alteration of calcium-ion release from in vitro brain tissue. Bioelectromagnetics. 1991;12(3):173–182.
  • Merritt JH, Chamness AF, Shelton WW. Attempts to alter 45Ca2+ binding to brain tissue with pulse-modulated microwave energy. Bioelectromagnetics. 1982;3(4):475–478.
  • Cranfield CG, Wood AW, Anderson V, et al. Effects of mobile phone type signals on calcium levels within human leukaemic T-cells (Jurkat cells). Int J Radiat Biol. 2001;77(12):1207–1217.
  • Blackman CF. Treating cancer with amplitude-modulated electromagnetic fields: a potential paradigm shift, again? Br J Cancer. 2012;106(2):241–242.
  • Boal D. Mechanics of the cell. 2nd ed. New York: Cambridge University Press;2012.
  • Landau LD, Lifshitz EM. Theory of elasticity. Oxford: Pergamon Press;1986.
  • Suresh S. Biomechanics and biophysics of cancer cells. Acta Biomater. 2007; 3(4):413–438.
  • Katira P, Bonnecaze RT, Zaman MH. Modeling the mechanics of cancer: effect of changes in cellular and extra-cellular mechanical properties. Frontiers Oncol. 2013;3:145.
  • Cross SE, Jin YS, Rao J, et al. Nanomechanical analysis of cells from cancer patients. Nat Nanotechnol. 2007;2(12):780–783.
  • Jonas O, Mierke CT, Käs JA. Invasive cancer cell lines exhibit biomechanical properties that are distinct from their noninvasive counterparts. Soft Matter. 2011;7(24):11488–11495.
  • Smolyakov G, Thiebot B, Campillo C, et al. Elasticity, adhesion, and tether extrusion on breast cancer cells provide a signature of their invasive potential. ACS Appl Mater Interfaces. 2016;8(41):27426–27431.
  • Xu W, Mezencev R, Kim B, et al. Cell stiffness is a biomarker of the metastatic potential of ovarian cancer cells. PLOS One. 2012;7(10):e46609.
  • Diem E, Schwarz C, Adlkofer F, et al. 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. 2005;583(2):178–183.
  • Panagopoulos DJ, Chavdoula ED, Karabarbounis A, et al. Comparison of bioactivity between GSM 900 MHz and DCS 1800 MHz mobile telephony radiation. Electromagn Biol Med. 2007;26(1):33–44.
  • Zhijian C, Xiaoxue L, Yezhen L, et al. Impact of 1.8-GHz radiofrequency radiation (RFR) on DNA damage and repair induced by doxorubicin in human B-cell lymphoblastoid cells. Mutat Res. 2010;695(1–2):16–21.
  • Franzellitti S, Valbonesi P, Ciancaglini N, et al. Transient DNA damage induced by high-frequency electromagnetic fields (GSM 1.8 GHz) in the human trophoblast HTR-8/SVneo cell line evaluated with the alkaline comet assay. Mutat Res. 2010;683(1–2):35–42.
  • Al-Serori H, Ferk F, Kundi M, et al. Mobile phone specific electromagnetic fields induce transient DNA damage and nucleotide excision repair in serum-deprived human glioblastoma cells. PLOS One. 2018;13(4):e0193677.
  • Blank M, Goodman R. DNA is a fractal antenna in electromagnetic fields. Int J Radiat Biol. 2011;87(4):409–415.
  • Yakymenko I, Sidorik E. Risks of carcinogenesis from electromagnetic radiation of mobile telephony devices. Exp Oncol. 2010;32(2):54–60.
  • Yakymenko I, Tsybulin O, Sidorik E, et al. Oxidative mechanisms of biological activity of low-intensity radiofrequency radiation. Electromagn Biol Med. 2016;35(2):186–202.
  • Panagopoulos DJ, Messini N, Karabarbounis A, et al. A mechanism for action of oscillating electric fields on cells. Biochem Biophys Res Commun. 2000;272(3):634–640.
  • Wust P, Cho CH, Hildebrandt B, et al. Thermal monitoring: invasive, minimal-invasive and non-invasive approaches. Int J Hyperthermia. 2006;22(3):255–262.