Login Register Cart 0
Generic placeholder image

Current Radiopharmaceuticals

Editor-in-Chief

ISSN (Print): 1874-4710
ISSN (Online): 1874-4729

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Research Article

Exposure to Low-Frequency Radiation Changes the Expression of Nestin, VEGF, BCRP and Apoptosis Markers During Glioma Treatment Strategy: An In Vitro Study

Author(s): Maryam Amirinejad, Seyed Hassan Eftekhar-Vaghefi*, Seyed Noureddin Nematollahi Mahani, Moein Salari, Rasoul Yahyapour and Meysam Ahmadi-Zeidabadi*

Volume 17, Issue 1, 2024

Published on: 04 October, 2023

Page: [55 - 67] Pages: 13

DOI: 10.2174/0118744710258350230921065159

Price: $65

Abstract

Background: Exposure to physical contamination during chemotherapy, including non-ionizing electromagnetic fields, raises concerns about the widespread sources of exposure to this type of radiation. Glioblastoma multiforme (GBM) is an aggressive central nervous system tumor that is hard to treat due to resistance to drugs such as temozolomide (TMZ).

Objective: Electromagnetic fields (EMF) and haloperidol (HLP) may have anticancer effects. In this study, we investigated the effects of TMZ, HLP, and EMF on GBM cell lines and analyzed the association between non-ionizing radiation and the risk of change in drug performance.

Methods: Cell viability and reactive oxygen species (ROS) generation were measured by MTT and NBT assay, respectively. Then, the expression levels of breast cancer-resistant protein (BCRP), Bax, Bcl2, Nestin, vascular endothelial growth factor (VEGF) genes, and P53, Bax, and Bcl2 Proteins were evaluated by real-time PCR and western blot.

Results: Co-treatment of GBM cells by HLP and TMZ enhanced apoptosis in T-98G and A172 cells by increasing the expression of P53 and Bax and decreasing Bcl-2. Interestingly, exposure of GBM cells to EMF decreased apoptosis in the TMZ+HLP group.

Conclusion: In conclusion, EMF reduced the synergistic effect of TMZ and HLP. This hypothesis that patients who are treated for brain tumors and suffer from depression should not be exposed to EMF is proposed in the present study. There appears to be an urgent need to reconsider exposure limits for low-frequency magnetic fields, based on experimental and epidemiological research, the relationship between exposure to non-ionizing radiation and adverse human health effects.

« Previous Next »
Graphical Abstract

[1]
Avcibasi, U.; Dewa, M.T.; Karatay, K.B.; Kilcar, A.Y.; Muftuler, F.Z.B. Investigation of bioactivity of estragole isolated from basil plant on brain cancer cell lines using nuclear method. Curr. Radiopharm., 2023, 16(2), 140-150.
[http://dx.doi.org/10.2174/1874471016666230110144021] [PMID: 36627786]
[2]
Zhong, H.; Liu, S.; Cao, F.; Zhao, Y.; Zhou, J.; Tang, F.; Peng, Z.; Li, Y.; Xu, S.; Wang, C.; Yang, G.; Li, Z.Q. Dissecting tumor antigens and immune subtypes of glioma to develop mrna vaccine. Front. Immunol., 2021, 12, 709986.
[http://dx.doi.org/10.3389/fimmu.2021.709986] [PMID: 34512630]
[3]
Holland, E.C. Progenitor cells and glioma formation. Curr. Opin. Neurol., 2001, 14(6), 683-688.
[http://dx.doi.org/10.1097/00019052-200112000-00002] [PMID: 11723374]
[4]
Parsons, D.W.; Jones, S.; Zhang, X.; Lin, J.C.H.; Leary, R.J.; Angenendt, P.; Mankoo, P.; Carter, H.; Siu, I.M.; Gallia, G.L.; Olivi, A.; McLendon, R.; Rasheed, B.A.; Keir, S.; Nikolskaya, T.; Nikolsky, Y.; Busam, D.A.; Tekleab, H.; Diaz, L.A., Jr; Hartigan, J.; Smith, D.R.; Strausberg, R.L.; Marie, S.K.N.; Shinjo, S.M.O.; Yan, H.; Riggins, G.J.; Bigner, D.D.; Karchin, R.; Papadopoulos, N.; Parmigiani, G.; Vogelstein, B.; Velculescu, V.E.; Kinzler, K.W. An integrated genomic analysis of human glioblastoma multiforme. Science, 2008, 321(5897), 1807-1812.
[http://dx.doi.org/10.1126/science.1164382] [PMID: 18772396]
[5]
Verhaak, R.G.W.; Hoadley, K.A.; Purdom, E.; Wang, V.; Qi, Y.; Wilkerson, M.D.; Miller, C.R.; Ding, L.; Golub, T.; Mesirov, J.P.; Alexe, G.; Lawrence, M.; O’Kelly, M.; Tamayo, P.; Weir, B.A.; Gabriel, S.; Winckler, W.; Gupta, S.; Jakkula, L.; Feiler, H.S.; Hodgson, J.G.; James, C.D.; Sarkaria, J.N.; Brennan, C.; Kahn, A.; Spellman, P.T.; Wilson, R.K.; Speed, T.P.; Gray, J.W.; Meyerson, M.; Getz, G.; Perou, C.M.; Hayes, D.N. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell, 2010, 17(1), 98-110.
[http://dx.doi.org/10.1016/j.ccr.2009.12.020] [PMID: 20129251]
[6]
Shergalis, A.; Bankhead, A., III; Luesakul, U.; Muangsin, N.; Neamati, N. Current challenges and opportunities in treating glioblastoma. Pharmacol. Rev., 2018, 70(3), 412-445.
[http://dx.doi.org/10.1124/pr.117.014944] [PMID: 29669750]
[7]
Bastiancich, C.; Danhier, P.; Préat, V.; Danhier, F. Anticancer drug-loaded hydrogels as drug delivery systems for the local treatment of glioblastoma. J. Control. Release, 2016, 243, 29-42.
[http://dx.doi.org/10.1016/j.jconrel.2016.09.034] [PMID: 27693428]
[8]
Cao, F.; Fan, Y.; Yu, Y.; Yang, G.; Zhong, H. Dissecting prognosis modules and biomarkers in glioblastoma based on weighted gene co-expression network analysis. Cancer Manag. Res., 2021, 13, 5477-5489.
[http://dx.doi.org/10.2147/CMAR.S310346] [PMID: 34267555]
[9]
Goker Bagca, B.; Ozates, N.P.; Asik, A.; Caglar, H.O.; Gunduz, C.; Biray Avci, C. Temozolomide treatment combined with AZD3463 shows synergistic effect in glioblastoma cells. Biochem. Biophys. Res. Commun., 2020, 533(4), 1497-1504.
[http://dx.doi.org/10.1016/j.bbrc.2020.10.058] [PMID: 33109342]
[10]
Xue, Y.Y. Lu, Y.Y.; Sun, G.Q.; Fang, F.; Ji, Y.Q.; Tang, H.F.; Qiu, P.C.; Cheng, G. CN‐3 increases TMZ sensitivity and induces ROS‐dependent apoptosis and autophagy in TMZ‐resistance glioblastoma. J. Biochem. Mol. Toxicol., 2022, 36(3), e22973.
[http://dx.doi.org/10.1002/jbt.22973] [PMID: 34967073]
[11]
Beach, S.R.; Gross, A.F.; Hartney, K.E.; Taylor, J.B.; Rundell, J.R. Intravenous haloperidol: A systematic review of side effects and recommendations for clinical use. Gen. Hosp. Psychiatry, 2020, 67, 42-50.
[http://dx.doi.org/10.1016/j.genhosppsych.2020.08.008] [PMID: 32979582]
[12]
Asha, S.; Vidyavathi, M. Role of human liver microsomes in in vitro metabolism of drugs-a review. Appl. Biochem. Biotechnol., 2010, 160(6), 1699-1722.
[http://dx.doi.org/10.1007/s12010-009-8689-6] [PMID: 19582595]
[13]
Hoertel, N.; Sánchez-Rico, M.; Vernet, R.; Jannot, A.S.; Neuraz, A.; Blanco, C.; Lemogne, C.; Airagnes, G.; Paris, N.; Daniel, C.; Gramfort, A.; Lemaitre, G.; Bernaux, M.; Bellamine, A.; Beeker, N.; Limosin, F. Observational study of haloperidol in hospitalized patients with COVID-19. PLoS One, 2021, 16(2), e0247122.
[http://dx.doi.org/10.1371/journal.pone.0247122] [PMID: 33606790]
[14]
Wei, Z.; Mousseau, D.D.; Dai, Y.; Cao, X.; Li, X-M. Haloperidol induces apoptosis via the σ2 receptor system and Bcl-XS. Pharmacogenomics J., 2006, 6(4), 279-288.
[http://dx.doi.org/10.1038/sj.tpj.6500373] [PMID: 16462815]
[15]
Papadopoulos, F.; Isihou, R.; Alexiou, G.A.; Tsalios, T.; Vartholomatos, E.; Markopoulos, G.S.; Sioka, C.; Tsekeris, P.; Kyritsis, A.P.; Galani, V. Haloperidol induced cell cycle arrest and apoptosis in glioblastoma cells. Biomedicines, 2020, 8(12), 595.
[http://dx.doi.org/10.3390/biomedicines8120595] [PMID: 33322363]
[16]
Urnukhsaikhan, E.; Mishig-Ochir, T.; Kim, S.C.; Park, J.K.; Seo, Y.K. Neuroprotective effect of low frequency-pulsed electromagnetic fields in ischemic stroke. Appl. Biochem. Biotechnol., 2017, 181(4), 1360-1371.
[http://dx.doi.org/10.1007/s12010-016-2289-z] [PMID: 27761795]
[17]
Wu, S.; Yu, Q.; Lai, A.; Tian, J. Pulsed electromagnetic field induces Ca2+-dependent osteoblastogenesis in C3H10T1/2 mesenchymal cells through the Wnt-Ca2+/Wnt-β-catenin signaling pathway. Biochem. Biophys. Res. Commun., 2018, 503(2), 715-721.
[http://dx.doi.org/10.1016/j.bbrc.2018.06.066] [PMID: 29909008]
[18]
Barati, M.; Darvishi, B.; Javidi, M.A.; Mohammadian, A.; Shariatpanahi, S.P.; Eisavand, M.R.; Madjid Ansari, A. Cellular stress response to extremely low‐frequency electromagnetic fields (ELF‐EMF): An explanation for controversial effects of ELF‐EMF on apoptosis. Cell Prolif., 2021, 54(12), e13154.
[http://dx.doi.org/10.1111/cpr.13154] [PMID: 34741480]
[19]
Ivancsits, S.; Diem, E.; Pilger, A.; Rüdiger, H.W.; Jahn, O. Induction of DNA strand breaks by intermittent exposure to extremely-low-frequency electromagnetic fields in human diploid fibroblasts. Mutat. Res. Genet. Toxicol. Environ. Mutagen., 2002, 519(1-2), 1-13.
[http://dx.doi.org/10.1016/S1383-5718(02)00109-2] [PMID: 12160887]
[20]
Benassi, B.; Filomeni, G.; Montagna, C.; Merla, C.; Lopresto, V.; Pinto, R.; Marino, C.; Consales, C. Extremely low frequency magnetic field (ELF-MF) exposure sensitizes SH-SY5Y cells to the pro-parkinson’s disease toxin MPP+. Mol. Neurobiol., 2016, 53(6), 4247-4260.
[http://dx.doi.org/10.1007/s12035-015-9354-4] [PMID: 26223801]
[21]
Hart, M.G.; Garside, R.; Rogers, G.; Stein, K.; Grant, R. Temozolomide for high grade glioma. Cochrane Database Syst. Rev., 2013, 2013(4), CD007415.
[PMID: 23633341]
[22]
Amiri, M.; Basiri, M.; Eskandary, H.; Akbarnejad, Z.; Esmaeeli, M.; Masoumi-Ardakani, Y.; Ahmadi-Zeidabadi, M. 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., 2018, 37(3), 138-145.
[http://dx.doi.org/10.1080/15368378.2018.1477052] [PMID: 29846098]
[23]
Babaee, A.; Nematollahi-mahani, S.N.; Shojaei, M.; Dehghani-Soltani, S.; Ezzatabadipour, M. Effects of polarized and non-polarized red-light irradiation on proliferation of human Wharton’s jelly-derived mesenchymal cells. Biochem. Biophys. Res. Commun., 2018, 504(4), 871-877.
[http://dx.doi.org/10.1016/j.bbrc.2018.09.010] [PMID: 30219226]
[24]
Akbarnejad, Z.; Eskandary, H.; Dini, L.; Vergallo, C.; Nematollahi-Mahani, S.N.; Farsinejad, A.; Abadi, M.F.S.; Ahmadi, M. Cytotoxicity of temozolomide on human glioblastoma cells is enhanced by the concomitant exposure to an extremely low-frequency electromagnetic field (100 Hz, 100 G). Biomed. Pharmacother., 2017, 92, 254-264.
[http://dx.doi.org/10.1016/j.biopha.2017.05.050] [PMID: 28551545]
[25]
Dehghani Soltani, S.; Babaee, A.; Shojaei, M.; Salehinejad, P.; Seyedi, F. JalalKamali, M.; Nematollahi-Mahani, S.N. Different effects of energy dependent irradiation of red and green lights on proliferation of human umbilical cord matrix-derived mesenchymal cells. Lasers Med. Sci., 2016, 31(2), 255-261.
[http://dx.doi.org/10.1007/s10103-015-1846-y] [PMID: 26714979]
[26]
Babaee, A.; Nematollahi-Mahani, S.N.; Dehghani-Soltani, S.; Shojaei, M.; Ezzatabadipour, M. Photobiomodulation and gametogenic potential of human Wharton’s jelly-derived mesenchymal cells. Biochem. Biophys. Res. Commun., 2019, 514(1), 239-245.
[http://dx.doi.org/10.1016/j.bbrc.2019.04.059] [PMID: 31029424]
[27]
Dehghani-Soltani, S.; Eftekhar-Vaghefi, S.H.; Babaee, A.; Basiri, M.; Mohammadipoor-ghasemabad, L.; Vosough, P.; Ahmadi-Zeidabadi, M. Pulsed and discontinuous electromagnetic field exposure decreases temozolomide resistance in glioblastoma by modulating the expression of O6-methylguanine-DNA methyltransferase, cyclin-D1, and p53. Cancer Biother. Radiopharm., 2021, 36(7), 579-587.
[http://dx.doi.org/10.1089/cbr.2020.3851] [PMID: 32644826]
[28]
Zhang, Y.; Qu, H.; Xue, X. Blood–brain barrier penetrating liposomes with synergistic chemotherapy for glioblastoma treatment. Biomater. Sci., 2022, 10(2), 423-434.
[http://dx.doi.org/10.1039/D1BM01506K] [PMID: 34873606]
[29]
Yahyapour, R.; Khoei, S.; Kordestani, Z.; Larizadeh, M.H.; Jomehzadeh, A.; Amirinejad, M. Comparative study of extremely low-frequency electromagnetic field, radiation, and temozolomide administration in spheroid and monolayer forms of the glioblastoma cell line (T98). Curr. Radiopharm., 2022, 16(2), 123-132.
[PMID: 36503396]
[30]
Kanzawa, T.; Germano, I.M.; Komata, T.; Ito, H.; Kondo, Y.; Kondo, S. Role of autophagy in temozolomide-induced cytotoxicity for malignant glioma cells. Cell Death Differ., 2004, 11(4), 448-457.
[http://dx.doi.org/10.1038/sj.cdd.4401359] [PMID: 14713959]
[31]
Resende, F.; Titze-de-Almeida, S.; Titze-de-Almeida, R. Function of neuronal nitric oxide synthase enzyme in temozolomide-induced damage of astrocytic tumor cells. Oncol. Lett., 2018, 15(4), 4891-4899.
[http://dx.doi.org/10.3892/ol.2018.7917] [PMID: 29552127]
[32]
Liu, Z.; Jiang, X.; Gao, L.; Liu, X.; Li, J.; Huang, X.; Zeng, T. Synergistic suppression of glioblastoma cell growth by combined application of temozolomide and dopamine D2 receptor antagonists. World Neurosurg., 2019, 128, e468-e477.
[http://dx.doi.org/10.1016/j.wneu.2019.04.180] [PMID: 31048057]
[33]
Hendouei, N.; Saghafi, F.; Shadfar, F.; Hosseinimehr, S.J. Molecular mechanisms of anti-psychotic drugs for improvement of cancer treatment. Eur. J. Pharmacol., 2019, 856, 172402.
[http://dx.doi.org/10.1016/j.ejphar.2019.05.031] [PMID: 31108054]
[34]
Fond, G.; Macgregor, A.; Attal, J.; Larue, A.; Brittner, M.; Ducasse, D.; Capdevielle, D. Antipsychotic drugs: Pro-cancer or anti-cancer? A systematic review. Med. Hypotheses, 2012, 79(1), 38-42.
[http://dx.doi.org/10.1016/j.mehy.2012.03.026] [PMID: 22543071]
[35]
Duty, S.; Jenner, P. Animal models of Parkinson’s disease: A source of novel treatments and clues to the cause of the disease. Br. J. Pharmacol., 2011, 164(4), 1357-1391.
[http://dx.doi.org/10.1111/j.1476-5381.2011.01426.x] [PMID: 21486284]
[36]
Bertagna, F.; Lewis, R.; Silva, S.R.P.; McFadden, J.; Jeevaratnam, K. Thapsigargin blocks electromagnetic field‐elicited intracellular Ca2+ increase in HEK 293 cells. Physiol. Rep., 2022, 10(9), e15189.
[http://dx.doi.org/10.14814/phy2.15189] [PMID: 35510320]
[37]
Matsubara, T.; Satoh, K.; Homma, T.; Nakagaki, T.; Yamaguchi, N.; Atarashi, R.; Sudo, Y.; Uezono, Y.; Ishibashi, D.; Nishida, N. Prion protein interacts with the metabotropic glutamate receptor 1 and regulates the organization of Ca2+ signaling. Biochem. Biophys. Res. Commun., 2020, 525(2), 447-454.
[http://dx.doi.org/10.1016/j.bbrc.2020.02.102] [PMID: 32107004]
[38]
Ehnert, S.; Fentz, A.K.; Schreiner, A.; Birk, J.; Wilbrand, B.; Ziegler, P.; Reumann, M.K.; Wang, H.; Falldorf, K.; Nussler, A.K. Extremely low frequency pulsed electromagnetic fields cause antioxidative defense mechanisms in human osteoblasts via induction of •O2 − and H2O2. Sci. Rep., 2017, 7(1), 14544.
[http://dx.doi.org/10.1038/s41598-017-14983-9] [PMID: 29109418]
[39]
Huang, L.; Dong, L.; Chen, Y.; Qi, H.; Xiao, D. Effects of sinusoidal magnetic field observed on cell proliferation, ion concentration, and osmolarity in two human cancer cell lines. Electromagn. Biol. Med., 2006, 25(2), 113-126.
[http://dx.doi.org/10.1080/15368370600719067] [PMID: 16771300]
[40]
Jandaghi, P.; Najafabadi, H.S.; Bauer, A.S.; Papadakis, A.I.; Fassan, M.; Hall, A.; Monast, A.; von Knebel Doeberitz, M.; Neoptolemos, J.P.; Costello, E.; Greenhalf, W.; Scarpa, A.; Sipos, B.; Auld, D.; Lathrop, M.; Park, M.; Büchler, M.W.; Strobel, O.; Hackert, T.; Giese, N.A.; Zogopoulos, G.; Sangwan, V.; Huang, S.; Riazalhosseini, Y.; Hoheisel, J.D. Expression of DRD2 is increased in human pancreatic ductal adenocarcinoma and inhibitors slow tumor growth in mice. Gastroenterology, 2016, 151(6), 1218-1231.
[http://dx.doi.org/10.1053/j.gastro.2016.08.040] [PMID: 27578530]
[41]
Wei, Z.; Qi, J.; Dai, Y.; Bowen, W.; Mousseau, D. Haloperidol disrupts Akt signalling to reveal a phosphorylation-dependent regulation of pro-apoptotic Bcl-XS function. Cell. Signal., 2009, 21(1), 161-168.
[http://dx.doi.org/10.1016/j.cellsig.2008.10.005] [PMID: 18951975]
[42]
Romeo, S.; Zeni, O.; Scarfì, M.; Poeta, L.; Lioi, M.; Sannino, A. Radiofrequency electromagnetic field exposure and apoptosis: A scoping review of In vitro studies on mammalian cells. Int. J. Mol. Sci., 2022, 23(4), 2322.
[http://dx.doi.org/10.3390/ijms23042322] [PMID: 35216437]
[43]
Reale, M.; Kamal, M.A.; Patruno, A.; Costantini, E.; D’Angelo, C.; Pesce, M.; Greig, N.H. Neuronal cellular responses to extremely low frequency electromagnetic field exposure: Implications regarding oxidative stress and neurodegeneration. PLoS One, 2014, 9(8), e104973.
[http://dx.doi.org/10.1371/journal.pone.0104973] [PMID: 25127118]
[44]
Kenny, T.C.; Hart, P.; Ragazzi, M.; Sersinghe, M.; Chipuk, J.; Sagar, M A K.; Eliceiri, K.W.; LaFramboise, T.; Grandhi, S.; Santos, J.; Riar, A.K.; Papa, L.; D’Aurello, M.; Manfredi, G.; Bonini, M.G.; Germain, D. Selected mitochondrial DNA landscapes activate the SIRT3 axis of the UPRmt to promote metastasis. Oncogene, 2017, 36(31), 4393-4404.
[http://dx.doi.org/10.1038/onc.2017.52] [PMID: 28368421]
[45]
Janać B.; Tovilović G.; Tomić M.; Prolić Z.; Radenović L. Effect of continuous exposure to alternating magnetic field (50 Hz, 0.5 mT) on serotonin and dopamine receptors activity in rat brain. Gen. Physiol. Biophys., 2009, 28(Spec No), 41-46.
[PMID: 19893078]
[46]
Sieroń A.; Labus, Ł.; Nowak, P.; Cieślar, G.; Brus, H.; Durczok, A.; Zagził T.; Kostrzewa, R.M.; Brus, R. Alternating extremely low frequency magnetic field increases turnover of dopamine and serotonin in rat frontal cortex. Bioelectromagnetics, 2004, 25(6), 426-430.
[http://dx.doi.org/10.1002/bem.20011] [PMID: 15300728]
[47]
Hayashi, S.; Kakikawa, M. Exposure to 60 Hz magnetic field can affect membrane proteins and membrane potential in human cancer cells. Electromagn. Biol. Med., 2021, 40(4), 459-466.
[http://dx.doi.org/10.1080/15368378.2021.1958340] [PMID: 34396886]
[48]
Yuan, L.Q.; Wang, C.; Lu, D.F.; Zhao, X.D.; Tan, L.H.; Chen, X. Induction of apoptosis and ferroptosis by a tumor suppressing magnetic field through ROS-mediated DNA damage. Aging, 2020, 12(4), 3662-3681.
[http://dx.doi.org/10.18632/aging.102836] [PMID: 32074079]
[49]
Akbarnejad, Z.; Eskandary, H.; Vergallo, C.; Nematollahi-Mahani, S.N.; Dini, L.; Darvishzadeh-Mahani, F.; Ahmadi, M. Effects of extremely low-frequency pulsed electromagnetic fields (ELF-PEMFs) on glioblastoma cells (U87). Electromagn. Biol. Med., 2017, 36(3), 238-247.
[http://dx.doi.org/10.1080/15368378.2016.1251452] [PMID: 27874284]
[50]
Maksoud, S. The DNA double-strand break repair in glioma: Molecular players and therapeutic strategies. Mol. Neurobiol., 2022, 59(9), 5326-5365.
[http://dx.doi.org/10.1007/s12035-022-02915-2] [PMID: 35696013]
[51]
Manjua, A.C.; Cabral, J.M.S.; Ferreira, F.C.; Portugal, C.A.M. Magnetic field dynamic strategies for the improved control of the angiogenic effect of mesenchymal stromal cells. Polymers, 2021, 13(11), 1883.
[http://dx.doi.org/10.3390/polym13111883] [PMID: 34204049]
[52]
Ahmed, M.R.; Gurevich, V.V.; Dalby, K.N.; Benovic, J.L.; Gurevich, E.V. Haloperidol and clozapine differentially affect the expression of arrestins, receptor kinases, and extracellular signal-regulated kinase activation. J. Pharmacol. Exp. Ther., 2008, 325(1), 276-283.
[http://dx.doi.org/10.1124/jpet.107.131987] [PMID: 18178904]
[53]
Wang, J.S.; Zhu, H.J.; Markowitz, J.S.; Donovan, J.L.; Yuan, H.J.; DeVane, C.L. Antipsychotic drugs inhibit the function of breast cancer resistance protein. Basic Clin. Pharmacol. Toxicol., 2008, 103(4), 336-341.
[http://dx.doi.org/10.1111/j.1742-7843.2008.00298.x] [PMID: 18834354]
[54]
Baharara, J.; Hosseini, N.; Farzin, T.R. Extremely low frequency electromagnetic field sensitizes cisplatin-resistant human ovarian adenocarcinoma cells via P53 activation. Cytotechnology, 2016, 68(4), 1403-1413.
[http://dx.doi.org/10.1007/s10616-015-9900-y] [PMID: 26370097]
[55]
Jin, X.; Jin, X.; Jung, J.E.; Beck, S.; Kim, H. Cell surface Nestin is a biomarker for glioma stem cells. Biochem. Biophys. Res. Commun., 2013, 433(4), 496-501.
[http://dx.doi.org/10.1016/j.bbrc.2013.03.021] [PMID: 23524267]
[56]
Ahmadi-Zeidabadi, M.; Akbarnejad, Z.; Esmaeeli, M.; Masoumi-Ardakani, Y.; Mohammadipoor-Ghasemabad, L.; Eskandary, H. Impact of extremely low-frequency electromagnetic field (100 Hz, 100 G) exposure on human glioblastoma U87 cells during Temozolomide administration. Electromagn. Biol. Med., 2019, 38(3), 198-209.
[http://dx.doi.org/10.1080/15368378.2019.1625784] [PMID: 31179753]
[57]
Nakod, P.S.; Kondapaneni, R.V.; Edney, B.; Kim, Y.; Rao, S.S. The impact of temozolomide and lonafarnib on the stemness marker expression of glioblastoma cells in multicellular spheroids. Biotechnol. Prog., 2022, 38(5), e3284.
[http://dx.doi.org/10.1002/btpr.3284]

Rights & Permissions Print Cite
Article Metrics
1
© 2024 Bentham Science Publishers | Privacy Policy