Impact of extremely low-frequency electromagnetic field (100 Hz, 100 G) exposure on human glioblastoma U87 cells during Temozolomide administration

References

• Ahmed, S. I., Javed, G., Laghari, A. A., et al. 2018. CD133 expression in glioblastoma multiforme: A literature review. Cureus 10:10.
   Web of Science ®Google Scholar
• Akbarnejad, Z., H. Eskandary, L. Dini, C. Vergallo, S. N. Nematollahi-Mahani, A. Farsinejad, M. F. S. Abadi, and M. Ahmadi. 2017a. Cytotoxicity of temozolomide on human glioblastoma cells is enhanced by the concomitant exposure to an extremely low-frequency electromagnetic field (100Hz, 100G). Biomed. Pharmacother 92:254–64. doi:10.1016/j.biopha.2017.05.050.
   PubMed Web of Science ®Google Scholar
• Akbarnejad, Z., H. Eskandary, C. Vergallo, S. N. Nematollahi-Mahani, L. Dini, F. Darvishzadeh-Mahani, and M. Ahmadi. 2017b. Effects of extremely low-frequency pulsed electromagnetic fields (ELF-PEMFs) on glioblastoma cells (U87). Electromagn. Biol. Med. 36 (3):238–47. doi:10.1080/15368378.2016.1251452.
   PubMed Web of Science ®Google Scholar
• Akbarnejad, Z., K. Esmaeilpour, M. Shabani, M. Asadi-Shekaari, M. Saeedi Goraghani, and M. Ahmadi-Zeidabadi. 2018. Spatial memory recovery in Alzheimer’s rat model by electromagnetic field exposure. Int. J. Neurosci. 128 (8):691–96. doi:10.1080/00207454.2017.1411353.
   PubMed Web of Science ®Google Scholar
• Amiri, M., M. Basiri, H. Eskandary, Z. Akbarnejad, M. Esmaeeli, Y. Masoumi-Ardakani, and M. Ahmadi-Zeidabadi. 2018. Cytotoxicity of carboplatin on human glioblastoma cells is reduced by the concomitant exposure to an extremely low-frequency electromagnetic field (50 Hz, 70 G). Electromagn. Biol. Med. 1–8. doi:10.1080/15368378.2018.1477052.
   PubMedGoogle Scholar
• Balasubramaniyan, V., Vaillant, B., Wang, S., et al. 2015. Aberrant mesenchymal differentiation of glioma stem-like cells: Implications for therapeutic targeting. Oncotarget 6 (31):31007.
   PubMedGoogle Scholar
• Bao, S., Q. Wu, R. E. McLendon, Y. Hao, Q. Shi, A. B. Hjelmeland, M. W. Dewhirst, D. D. Bigner, and J. N. Rich. 2006. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444 (7120):756–60. doi:10.1038/nature05236.
   PubMed Web of Science ®Google Scholar
• Barbault, A., F. P. Costa, B. Bottger, R. F. Munden, F. Bomholt, N. Kuster, and B. Pasche. 2009. 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. 28:51. doi:10.1186/1756-9966-28-51.
   PubMed Web of Science ®Google Scholar
• Baumgarten, P., Quick-Weller, J., Gessler, F., et al. 2018. Pre-and early postoperative GFAP serum levels in glioma and brain metastases. J. Neurooncol.139 (3):541–546.
   Google Scholar
• Beck, B., and C. Blanpain. 2013. Unravelling cancer stem cell potential. Nat. Rev. Cancer 13 (10):727–38. doi:10.1038/nrc3597.
   PubMed Web of Science ®Google Scholar
• Chen, P.-H., W.-L. Shen, C.-M. Shih, K.-H. Ho, C.-H. Cheng, C.-W. Lin, -C.-C. Lee, A.-J. Liu, and K.-C. Chen. 2017. The CHAC1-inhibited Notch3 pathway is involved in temozolomide-induced glioma cytotoxicity. Neuropharmacol 116:300–14. doi:10.1016/j.neuropharm.2016.12.011.
   PubMed Web of Science ®Google Scholar
• Chomczynski, P., and N. Sacchi. 2006. The single-step method of RNA isolation by acid guanidinium thiocyanate–Phenol–Chloroform extraction: Twenty-something years on. Nat. Protoc. 1 (2):581–85. doi:10.1038/nprot.2006.83.
   PubMed Web of Science ®Google Scholar
• Cui, X., J. Gong, H. Han, L. He, Y. Teng, T. Tetley, R. Sinharay, K. F. Chung, T. Islam, F. Gilliland, et al. 2018. Relationship between free and total malondialdehyde, a well-established marker of oxidative stress, in various types of human biospecimens. J. Thorac. Dis. 10 (5):3088–197. doi:10.21037/jtd.2018.05.92.
   PubMed Web of Science ®Google Scholar
• Dell’Albani, P., M. Rodolico, R. Pellitteri, E. Tricarichi, S. A. Torrisi, S. D’Antoni, M. Zappia, V. Albanese, R. Caltabiano, N. Platania, et al. 2014. Differential patterns of NOTCH1–4 receptor expression are markers of glioma cell differentiation. Neuro-Oncology 16 (2):204–16. doi:10.1093/neuonc/not168.
   PubMed Web of Science ®Google Scholar
• Dotto, G. P. 2009. Crosstalk of Notch with p53 and p63 in cancer growth control. Nat. Rev. Cancer. 9 (8):587–95. doi:10.1038/nrc2675.
   PubMed Web of Science ®Google Scholar
• Efremov, Y. R., A. S. Proskurina, E. A. Potter, E. V. Dolgova, O. V. Efremova, O. S. Taranov, J. Jackson, P. J. Rathouz, M. W. Baker, M. Brilliant, et al. 2018. Cancer Stem Cells: Emergent Nature of Tumor Emergency. Front. Genet. 9: doi: 10.3389/fgene.2018.00173.
   PubMed Web of Science ®Google Scholar
• Ehnert, S., A.-K. Fentz, A. Schreiner, J. Birk, B. Wilbrand, P. Ziegler, M. K. Reumann, H. Wang, K. Falldorf, and A. K. Nussler. 2017. Extremely low frequency pulsed electromagnetic fields cause antioxidative defense mechanisms in human osteoblasts via induction of •O 2 − and H 2 O 2. Sci. Rep. 7 (1):14544. doi:10.1038/s41598-017-14983-9.
   PubMedGoogle Scholar
• Falone, S., M. R. Grossi, B. Cinque, B. D’Angelo, E. Tettamanti, A. Cimini, C. Di Ilio, and F. Amicarelli. 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):2093–106. doi:10.1016/j.biocel.2007.06.001.
   PubMed Web of Science ®Google Scholar
• Golbach, L. A., L. A. Portelli, H. F. J. Savelkoul, S. R. Terwel, N. Kuster, R. B. M. de Vries, and B. M. L. Verburg-van Kemenade. 2016. Calcium homeostasis and low-frequency magnetic and electric field exposure: A systematic review and meta-analysis of in vitro studies. Environ. Int. 92–93:695–706. doi:10.1016/j.envint.2016.01.014.
   PubMed Web of Science ®Google Scholar
• Görlach, A., K. Bertram, S. Hudecova, and O. Krizanova. 2015. Calcium and ROS: A mutual interplay. Redox. Biol. 6:260–71. doi:10.1016/j.redox.2015.08.010.
   PubMed Web of Science ®Google Scholar
• Gorrini, C., I. S. Harris, and T. W. Mak. 2013. Modulation of oxidative stress as an anticancer strategy. Nat. Rev. Drug Discovery 12 (12):931–47. doi:10.1038/nrd4002.
   PubMed Web of Science ®Google Scholar
• Johnson, D. R., and B. P. O’Neill. 2012. Glioblastoma survival in the United States before and during the temozolomide era. J. Neurooncol. 107 (2):359–64. doi:10.1007/s11060-011-0749-4.
   PubMed Web of Science ®Google Scholar
• Kim, H.-J., J. Jung, J.-H. Park, J.-H. Kim, K.-N. Ko, and C.-W. Kim. 2013. Extremely low-frequency electromagnetic fields induce neural differentiation in bone marrow derived mesenchymal stem cells. Exp. Biol. Med. 238 (8):923–31. doi:10.1177/1535370213497173.
   Web of Science ®Google Scholar
• Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (5259):680–85.
   PubMed Web of Science ®Google Scholar
• Lee, Y., K. H. Kim, D. G. Kim, H. J. Cho, Y. Kim, J. Rheey, K. Shin, Y. J. Seo, Y.-S. Choi, J.-I. Lee, et al. 2015. FoxM1 promotes stemness and radio-resistance of glioblastoma by regulating the master stem cell regulator Sox2. PLoS ONE 10 (10):e0137703. doi:10.1371/journal.pone.0137703.
   PubMed Web of Science ®Google Scholar
• Luo, X., R. Jin, F. Wang, B. Jia, K. Luan, F.-W. Cheng, L. Li, L.-D. Sun, S. Yang, S.-Q. Zhang, et al. 2016. Interleukin-15 inhibits the expression of differentiation markers induced by Ca(2+) in keratinocytes. Exp. Dermatol. 25 (7):544–47. doi:10.1111/exd.12992.
   PubMed Web of Science ®Google Scholar
• Meijer, D. K., and H. J. Geesink. 2018. Favourable and unfavourable EMF frequency patterns in cancer: Perspectives for improved therapy and prevention. J. Cancer. Ther. 9 (03):188. doi:10.4236/jct.2018.93019.
   Google Scholar
• Monteith, G. R., F. M. Davis, and S. J. Roberts-Thomson. 2012. Calcium channels and pumps in cancer: Changes and consequences. J. Biol. Chem. 287 (38):31666–73. doi:10.1074/jbc.R112.343061.
   PubMed Web of Science ®Google Scholar
• Morabito, C., S. Guarnieri, G. Fanò, and M. A. Mariggiò. 2010. Effects of Acute and Chronic Low Frequency Electromagnetic Field Exposure on PC12 Cells during Neuronal Differentiation. Cell Physiol. Biochem. 26 (6):947–58. doi:10.1159/000324003.
   PubMedGoogle Scholar
• Nikolaos, A. T., K. Young, G. Olga, M. Minesh, and S. Edward. 2016. Socioeconomic status and survival in glioblastoma. Int. J. Clin. Exp. Med. 9 (2):4131–36.
   Web of Science ®Google Scholar
• Obrenovich, M.E, Li, Y., Parvathaneni, K., et al. 2011. Antioxidants in health, disease and aging. CNS Neurol. Disord-Drug Targets (Formerly Current Drug Targets-CNS & Neurological Disorders) 10 (2):192–207.
   PubMed Web of Science ®Google Scholar
• Paolillo, M., C. Boselli, and S. Schinelli. 2018. Glioblastoma under siege: An overview of current therapeutic strategies. Brain Sci. 8 (1):15. doi:10.3390/brainsci8010015.
   PubMed Web of Science ®Google Scholar
• Schmittgen, T. D., and K. J. Livak. 2008. Analyzing real-time PCR data by the comparative CT method. Nat. Protoc. 3 (6):1101–08.
   PubMed Web of Science ®Google Scholar
• Smedler, E., and P. Uhlén. 2014. Frequency decoding of calcium oscillations. Biochim. Biophys Acta, Gen. Subj. 1840 (3):964–69. doi:10.1016/j.bbagen.2013.11.015.
   Web of Science ®Google Scholar
• Stupp, R., Mason, W. P., van Den Bent, M. J., Weller, M., Fisher, B., Taphoorn, M. J. B. et al. 2005. Radiotherapy plus Concomitant and Adjuvant Temozolomide for Glioblastoma. N. Engl. J. Med.. 352(10):987–96. doi:10.1056/NEJMoa043330.
   PubMed Web of Science ®Google Scholar
• Sugimoto, N., S. Miwa, H. Nakamura, H. Tsuchiya, and A. Yachie. 2016. Protein kinase A and Epac activation by cAMP regulates the expression of glial fibrillary acidic protein in glial cells. Arch. Biol. Sci. 68 (4):795–801. doi:10.2298/ABS160112067S.
   Google Scholar
• Terés, S., Lladó, V., Higuera, M., Barceló-Coblijn, G., Martin, M. L., Noguera-Salvà, M. A. Marcilla-Etxenike, A., García-Verdugo, J.M., Soriano-Navarro, M., and Saus, C. 2012. 2-Hydroxyoleate, a nontoxic membrane binding anticancer drug, induces glioma cell differentiation and autophagy. Proc. Natl. Acad. Sci.. 109(22):8489–94. doi:10.1073/pnas.1118349109.
   PubMed Web of Science ®Google Scholar
• Towbin, H., T. Staehelin, and J. Gordon. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proc. Natl. Acad. Sci. 76 (9):4350–54. doi:10.1073/pnas.76.9.4350.
   PubMed Web of Science ®Google Scholar
• Vadalà, M., C. Morales‐Medina Julio, A. Vallelunga, B. Palmieri, C. Laurino, and T. Iannitti. 2016. Mechanisms and therapeutic effectiveness of pulsed electromagnetic field therapy in oncology. Cancer. Med. 5 (11):3128–39. doi:10.1002/cam4.861.
   PubMed Web of Science ®Google Scholar
• Vergallo, C., M. Ahmadi, H. Mobasheri, and L. Dini. 2014. Impact of inhomogeneous static magnetic field (31.7–232.0 mT) exposure on human neuroblastoma SH-SY5Y cells during cisplatin administration. PLoS ONE 9 (11):e113530. doi:10.1371/journal.pone.0113530.
   PubMed Web of Science ®Google Scholar
• Villalva, C., U. Cortes, M. Wager, J.-M. Tourani, P. Rivet, C. Marquant, S. Martin, A. G. Turhan, and L. Karayan-Tapon. 2012. O6-Methylguanine-Methyltransferase (MGMT) promoter methylation status in glioma stem-like cells is correlated to temozolomide sensitivity under differentiation-promoting conditions. Int. J. Mol. Sci. 13 (6):6983–94. doi:10.3390/ijms13066983.
   PubMed Web of Science ®Google Scholar
• Vincenzo, B., T. Daniele, A. Marcello, A. Francesco, and A. Roberto. 2010. Biomarkers of glial cell proliferation and differentiation in culture. Front. Biosci. (Schol Ed) 2:558–70.
   PubMedGoogle Scholar
• Yoshie, S., Y. Ogasawara, M. Ikehata, K. Ishii, Y. Suzuki, K. Wada, K. Wake, S. Nakasono, M. Taki, and C. Ohkubo. 2016. Evaluation of biological effects of intermediate frequency magnetic field on differentiation of embryonic stem cell. Toxicol. Rep. 3:135–40. doi:10.1016/j.toxrep.2015.12.012.
   PubMed Web of Science ®Google Scholar
• Yuan, Y., X. Xue, R. B. Guo, X. L. Sun, and G. Hu. 2012. Resveratrol Enhances the Antitumor Effects of Temozolomide in Glioblastoma via ROS‐dependent AMPK‐TSC‐mTOR Signaling Pathway. CNS. Neurosci. Ther. 18 (7):536–46. doi:10.1111/j.1755-5949.2012.00319.x.
   PubMed Web of Science ®Google Scholar
• Yun, J., Espinoza, I., Pannuti, A., Romero, D., Martinez, L., Caskey, M. Stanculescu, A., Bocchetta, M., Rizzo, P., and Band, V. 2015. p53 Modulates Notch Signaling in MCF‐7 Breast Cancer Cells by Associating With the Notch Transcriptional Complex Via MAML1. J. Cell. Physiol. 230(12):3115–27. doi:10.1002/jcp.25052.
   PubMed Web of Science ®Google Scholar
• Zhang, M., S. Biswas, X. Qin, W. Gong, W. Deng, and H. Yu. 2016. Does Notch play a tumor suppressor role across diverse squamous cell carcinomas? Cancer Med. 5 (8):2048–60. doi:10.1002/cam4.731.
   PubMed Web of Science ®Google Scholar
• Zündorf, G., and G. Reiser. 2011. Calcium dysregulation and homeostasis of neural calcium in the molecular mechanisms of neurodegenerative diseases provide multiple targets for neuroprotection. Antioxid. Redox Signal. 14 (7):1275–88. doi:10.1089/ars.2010.3359.
   PubMed Web of Science ®Google Scholar