Generic placeholder image

Mini-Reviews in Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 1389-5575
ISSN (Online): 1875-5607

Review Article

Targeting Ion Channels for the Treatment of Glioma

Author(s): Saritha Keluth, Srikanth Jitte, Rashmi Bhushan, Om Prakash Ranjan, Krishna Murti, Velayutham Ravichandiran and Nitesh Kumar*

Volume 23, Issue 12, 2023

Published on: 09 March, 2023

Page: [1298 - 1318] Pages: 21

DOI: 10.2174/1389557523666230210150120

conference banner
Abstract

Background: Glioma refers to the most aggressive tumor in the central nervous system that starts from support cells or glial cells. The glial cell is the most common cell type in the CNS, and they insulate, surround, as well as feed, oxygen, and nutrition to the neurons. Seizures, headaches, irritability, vision difficulties, and weakness are some of the symptoms. Targeting ion channels is particularly helpful when it comes to glioma treatment because of their substantial activity in glioma genesis through multiple pathways.

Objective: In this study, we explore how distinct ion channels can be targeted for glioma treatment and summarize the pathogenic ion channels activity in gliomas.

Results: Current research found several side effects such as bone marrow suppression, alopecia, insomnia, and cognitive impairments for presently done chemotherapy. The involvement of research on ion channels in the regulation of cellular biology and towards improvements of glioma have expanded recognition of their innovative roles.

Conclusion: Present review article has expanded knowledge of ion channels as therapeutic targets and detailed cellular mechanisms in the roles of ion channels in gliomas pathogenesis.

Keywords: Gliomas, ion channels, calcium channel, potassium channel, CNS, epigenetic regulation, therapeutic targets, brain tumors.

« Previous
Graphical Abstract
[1]
Butowski, N.A. Epidemiology and diagnosis of brain tumors. Continuum (Minneap. Minn.), 2015, 21, 301-313.
[http://dx.doi.org/10.1212/01.CON.0000464171.50638.fa]
[2]
Ostrom, Q.T.; Wright, C.H.; Barnholtz-Sloan, J.S. Brain metastases: epidemiology. Handb. Clin. Neurol., 2018, 149, 27-42.
[http://dx.doi.org/10.1016/B978-0-12-811161-1.00002-5] [PMID: 29307358]
[3]
Razon, N.; Soreq, H.; Roth, E.; Bartal, A.; Silman, I. Characterization of activities and forms of cholinesterases in human primary brain tumors. Exp. Neurol., 1984, 84(3), 681-695.
[http://dx.doi.org/10.1016/0014-4886(84)90215-2] [PMID: 6723888]
[4]
Placone, A.L.; Quiñones-Hinojosa, A.; Searson, P.C. The role of astrocytes in the progression of brain cancer: complicating the picture of the tumor microenvironment. Tumour Biol., 2016, 37(1), 61-69.
[http://dx.doi.org/10.1007/s13277-015-4242-0] [PMID: 26493995]
[5]
Vasconcelos, V.L.d.; Valadares, M.G.C.; Tedeschi, H. Fundamentals of Neurosurgery; Springer: Cham, 2019, pp. 231-240.
[http://dx.doi.org/10.1007/978-3-030-17649-5_17]
[6]
Toh, J.W.T.; Morgan, M. Management approach and surgical strategies for retrorectal tumours: A systematic review. Colorectal Dis., 2016, 18(4), 337-350.
[http://dx.doi.org/10.1111/codi.13232] [PMID: 26663419]
[7]
Vigneswaran, K.; Neill, S.; Hadjipanayis, C.G. Beyond the World Health Organization grading of infiltrating gliomas: Advances in the molecular genetics of glioma classification. Ann. Transl. Med., 2015, 3(7), 95.
[PMID: 26015937]
[8]
Ostrom, Q.T.; Cioffi, G.; Waite, K.; Kruchko, C.; Barnholtz-Sloan, J.S. CBTRUS statistical report: Primary brain and other central nervous system tumors diagnosed in the united states in 2014–2018. Neuro-oncol., 2021, 23(12)(S3), 1-105.
[http://dx.doi.org/10.1093/neuonc/noab200] [PMID: 34608945]
[9]
Barnholtz-Sloan, J.S.; Ostrom, Q.T.; Cote, D. Epidemiology of brain tumors. Neurol. Clin., 2018, 36(3), 395-419.
[http://dx.doi.org/10.1016/j.ncl.2018.04.001] [PMID: 30072062]
[10]
Ostrom, Q. T.; Gittleman, H.; Stetson, L.; Virk, S. M.; Barnholtz-Sloan, J. S. Epidemiology of Gliomas. In Cancer Treatment and Research; Springer International Publishing: Cham, 2015, pp. 1-14.
[11]
Stocker, M.J.N.R.N. Ca2+-activated K+ channels: molecular determinants and function of the SK family. Nat. Rev. Neurosci., 2004, 5(10), 758-770.
[12]
Turner, K.L.; Honasoge, A.; Robert, S.M.; McFerrin, M.M.; Sontheimer, H.J.G. A proinvasive role for the Ca2+‐activated K+ channel KCa3. 1 in malignant glioma. Glia, 2014, 62(6), 971-981.
[13]
Komuro, H.; Kumada, T. Ca2+ transients control CNS neuronal migration. Cell Calcium, 2005, 37(5), 387-393.
[http://dx.doi.org/10.1016/j.ceca.2005.01.006] [PMID: 15820385]
[14]
Talantov, D.; Mazumder, A.; Yu, J.X.; Briggs, T.; Jiang, Y.; Backus, J.; Atkins, D.; Wang, Y.J.C.r. Novel genes associated with malignant melanoma but not benign melanocytic lesions. Clin. Cancer Res., 2005, 11(20), 7234-7242.
[http://dx.doi.org/10.1158/1078-0432.CCR-05-0683]
[15]
Litan, A.; Langhans, S.A.J.F.n. Cancer as a channelopathy: Ion channels and pumps in tumor development and progression. Front. Cell. Neurosci., 2015, 9, 86.
[http://dx.doi.org/10.3389/fncel.2015.00086]
[16]
Liu, J.; Qu, C.; Han, C.; Chen, M-M.; An, L-J.; Zou, W.J.M.b. Potassium channels and their role in glioma: A mini review. Mol. Membr. Biol., 2019, 35(1), 76-85.
[http://dx.doi.org/10.1080/09687688.2020.1729428]
[17]
Ruggieri, P.; Mangino, G.; Fioretti, B.; Catacuzzeno, L.; Puca, R.; Ponti, D.; Miscusi, M.; Franciolini, F.; Ragona, G.; Calogero, A. The inhibition of KCa3. 1 channels activity reduces cell motility in glioblastoma derived cancer stem cells. PLoS One, 2012, 7(10), e47825.
[18]
Catacuzzeno, L.; Franciolini, F. Role of KCa3.1 channels in modulating Ca2+ oscillations during glioblastoma cell migration and invasion. Int. J. Mol. Sci., 2018, 19(10), 2970.
[http://dx.doi.org/10.3390/ijms19102970] [PMID: 30274242]
[19]
Cuddapah, V.A.; Turner, K.L.; Seifert, S.; Sontheimer, H. Bradykinin-induced chemotaxis of human gliomas requires the activation of KCa3.1 and ClC-3. J. Neurosci., 2013, 33(4), 1427-1440.
[http://dx.doi.org/10.1523/JNEUROSCI.3980-12.2013] [PMID: 23345219]
[20]
D’Alessandro, G.; Grimaldi, A.; Chece, G.; Porzia, A.; Esposito, V.; Santoro, A.; Salvati, M.; Mainiero, F.; Ragozzino, D.; Angelantonio, S.D.; Wulff, H.; Catalano, M.; Limatola, C. KCa3.1 channel inhibition sensitizes malignant gliomas to temozolomide treatment. Oncotarget, 2016, 7(21), 30781-30796.
[http://dx.doi.org/10.18632/oncotarget.8761] [PMID: 27096953]
[21]
Simon, O.J.; Müntefering, T.; Grauer, O.M.; Meuth, S.G. The role of ion channels in malignant brain tumors. J. Neurooncol., 2015, 125(2), 225-235.
[http://dx.doi.org/10.1007/s11060-015-1896-9] [PMID: 26334315]
[22]
Caramia, M.; Sforna, L.; Franciolini, F.; Catacuzzeno, L. The volume-regulated anion channel in glioblastoma. Cancers, 2019, 11(3), 307.
[http://dx.doi.org/10.3390/cancers11030307] [PMID: 30841564]
[23]
Liu, M.; Inoue, K.; Leng, T.; Guo, S.; Xiong, Z.G. TRPM7 channels regulate glioma stem cell through STAT3 and Notch signaling pathways. Cell. Signal., 2014, 26(12), 2773-2781.
[24]
Chen, W.L.; Barszczyk, A.; Turlova, E.; Deurloo, M.; Liu, B.; Yang, B.B.; Rutka, J.T.; Feng, Z.P.; Sun, H.S. Inhibition of TRPM7 by carvacrol suppresses glioblastoma cell proliferation, migration and invasion. Oncotarget, 2015, 6(18), 16321-16340.
[http://dx.doi.org/10.18632/oncotarget.3872] [PMID: 25965832]
[25]
Beeler, G., Jr; Reuter, H.J.T.J.o.p. Membrane calcium current in ventricular myocardial fibres. J. Physiol., 1970, 207(1), 191-209.
[http://dx.doi.org/10.1113/jphysiol.1970.sp009056]
[26]
Cuddapah, V.A.; Sontheimer, H. Ion channels and tranporters in cancer. 2. Ion channels and the control of cancer cell migration. Am. J. Physiol. Cell Physiol., 2011, 301(3), C541-C549.
[http://dx.doi.org/10.1152/ajpcell.00102.2011] [PMID: 21543740]
[27]
Bruce, J.I.E.; James, A.D. Targeting the calcium signalling machinery in cancer. Cancers, 2020, 12(9), 2351.
[http://dx.doi.org/10.3390/cancers12092351] [PMID: 32825277]
[28]
Vashisht, A.; Trebak, M.; Motiani, R.K. STIM and Orai proteins as novel targets for cancer therapy, a review in the theme. Am. J. Physiol. Cell Physiol., 2015, 309(7), C457-C469.
[http://dx.doi.org/10.1152/ajpcell.00064.2015] [PMID: 26017146]
[29]
Ahumada-Castro, U.; Bustos, G.; Silva-Pavez, E.; Puebla-Huerta, A.; Lovy, A.; Cárdenas, C.J.F.i.C.; Biology, D. In the right place at the right time: regulation of cell metabolism by IP3R-mediated inter-organelle Ca2+ fluxes. Front. Cell Dev. Biol., 2021, 9, 629522.
[30]
Kang, S.; Hong, J.; Lee, J.M.; Moon, H.E.; Jeon, B.; Choi, J.; Yoon, N.A.; Paek, S.H.; Roh, E.J.; Lee, C.J.; Kang, S.S. Trifluoperazine, a well-known antipsychotic, inhibits glioblastoma invasion by binding to calmodulin and disinhibiting calcium release channel ip3r. Mol. Cancer Ther., 2017, 16(1), 217-227.
[http://dx.doi.org/10.1158/1535-7163.MCT-16-0169-T] [PMID: 28062709]
[31]
Verkhratsky, A.; Toescu, E.J.J.o.c. Endoplasmic reticulum Ca2+ homeostasis and neuronal death. J. Cell. Mol. Med., 2003, 7(4), 351-361.
[32]
Liiv, M.; Cagalinec, M.; Hodurova, Z.; Vaarmann, A.; Mandel, M.; Zeb, A.; Kuum, M.; Hickey, M.A.; Safiulina, D.; Choubey, V.J.S. Wolfram syndrome 1: From ER stress to impaired mitochondrial dynamics and neuronal development. Springerplus, 2015, 4(1), 1-32.
[33]
Richard, S.; Neveu, D.; Carnac, G.; Bodin, P.; Travo, P. Nargeot, Differential expression of voltage-gated Ca2+-currents in cultivated aortic myocytes. Biochimica et Biophysica Acta (BBA), 1992, 1160(1), 95-104.
[34]
Toyota, M.; Ho, C.; Ohe-Toyota, M.; Baylin, S.B.; Issa, J.P. Inactivation of CACNA1G, a T-type calcium channel gene, by aberrant methylation of its 5′ CpG island in human tumors. Cancer Res., 1999, 59(18), 4535-4541.
[PMID: 10493502]
[35]
Lapenna, S.; Giordano, A.J.N.r.D.d. Cell cycle kinases as therapeutic targets for cancer. Nat. Rev. Drug Discov., 2009, 8(7), 547-566.
[http://dx.doi.org/10.1038/nrd2907]
[36]
Kunzelmann, K. Ion channels and cancer. J. Membr. Biol., 2005, 205(3), 159-173.
[http://dx.doi.org/10.1007/s00232-005-0781-4] [PMID: 16362504]
[37]
Panner, A.; Cribbs, L.L.; Zainelli, G.M.; Origitano, T.C.; Singh, S.; Wurster, R.D. Variation of T-type calcium channel protein expression affects cell division of cultured tumor cells. Cell Calcium, 2005, 37(2), 105-119.
[http://dx.doi.org/10.1016/j.ceca.2004.07.002] [PMID: 15589991]
[38]
Zhang, Y.; Zhang, J.; Jiang, D.; Zhang, D.; Qian, Z.; Liu, C.; Tao, J.J.B.j.o.p. Inhibition of T‐type Ca2+ channels by endostatin attenuates human glioblastoma cell proliferation and migration. Br. J. Pharmacol., 2012, 166(4), 1247-1260.
[39]
Yarkoni, Y.; Cambier, J.C. Differential STIM1 expression in T and B cell subsets suggests a role in determining antigen receptor signal amplitude. Mol. Immunol., 2011, 48(15-16), 1851-1858.
[http://dx.doi.org/10.1016/j.molimm.2011.05.006] [PMID: 21663969]
[40]
Prakriya, M.; Lewis, R.S. Store-operated calcium channels. Physiol. Rev., 2015, 95(4), 1383-1436.
[http://dx.doi.org/10.1152/physrev.00020.2014] [PMID: 26400989]
[41]
Mercer, J.C.; DeHaven, W.I.; Smyth, J.T.; Wedel, B.; Boyles, R.R.; Bird, G.S.; Putney, J.W.J.J.o.B.C. Large store-operated calcium selective currents due to co-expression of Orai1 or Orai2 with the intracellular calcium sensor Stim1. J. Biol. Chem., 2006, 281(34), 24979-24990.
[42]
Yen, M.; Lokteva, L.A.; Lewis, R.S. Functional analysis of orai1 concatemers supports a hexameric stoichiometry for the CRAC channel. Biophys. J., 2016, 111(9), 1897-1907.
[http://dx.doi.org/10.1016/j.bpj.2016.09.020] [PMID: 27806271]
[43]
Cai, X.; Zhou, Y.; Nwokonko, R.M.; Loktionova, N.A.; Wang, X.; Xin, P.; Trebak, M.; Wang, Y.; Gill, D.L. The orai1 store-operated calcium channel functions as a hexamer. J. Biol. Chem., 2016, 291(50), 25764-25775.
[http://dx.doi.org/10.1074/jbc.M116.758813]
[44]
Feske, S.; Gwack, Y.; Prakriya, M.; Srikanth, S.; Puppel, S.H.; Tanasa, B.; Hogan, P.G.; Lewis, R.S.; Daly, M.; Rao, A. A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature, 2006, 441(7090), 179-185.
[http://dx.doi.org/10.1038/nature04702] [PMID: 16582901]
[45]
Liou, J.; Kim, M.L.; Do Heo, W.; Jones, J.T.; Myers, J.W.; Ferrell, J.E., Jr; Meyer, T.J.C.b. STIM is a Ca2+ sensor essential for Ca2+-store-depletion-triggered Ca2+ influx. Curr Biol. Physiol. Rev., 2005, 15(13), 1235-1241.
[46]
AB, P.J.P.R.; Putney, J.W. Store-operated calcium channels. 2005, 85(2), 757-810.
[47]
Yuan, F.; Yi, L.; Hai, L.; Wang, Y.; Yang, Y.; Li, T.; Tong, L.; Ma, H.; Liu, P.; Ming, H.; Ren, B.; Yu, S.; Lin, Y.; Yang, X. Identification of key pathways and genes in the Orai2 mediated classical and mesenchymal subtype of glioblastoma by bioinformatic analyses. Dis. Markers, 2019, 2019, 1-13.
[http://dx.doi.org/10.1155/2019/7049294] [PMID: 31772693]
[48]
Liu, H.; Hughes, J.D.; Rollins, S.; Chen, B.; Perkins, E. Calcium entry via ORAI1 regulates glioblastoma cell proliferation and apoptosis. Exp. Mol. Pathol., 2011, 91(3), 753-760.
[http://dx.doi.org/10.1016/j.yexmp.2011.09.005] [PMID: 21945734]
[49]
Bomben, V.C.; Turner, K.L.; Barclay, T.T.C.; Sontheimer, H. Transient receptor potential canonical channels are essential for chemotactic migration of human malignant gliomas. J. Cell. Physiol., 2011, 226(7), 1879-1888.
[http://dx.doi.org/10.1002/jcp.22518] [PMID: 21506118]
[50]
Seeburg, P.H. The TINS/TiPS Lecture the molecular biology of mammalian glutamate receptor channels. Trends Neurosci., 1993, 16(9), 359-365.
[http://dx.doi.org/10.1016/0166-2236(93)90093-2] [PMID: 7694406]
[51]
Hollmann, M.; Heinemann, S. Cloned glutamate receptors. Annu. Rev. Neurosci., 1994, 17(1), 31-108.
[http://dx.doi.org/10.1146/annurev.ne.17.030194.000335] [PMID: 8210177]
[52]
Ozawa, S.; Kamiya, H.; Tsuzuki, K. Glutamate receptors in the mammalian central nervous system. Prog. Neurobiol., 1998, 54(5), 581-618.
[http://dx.doi.org/10.1016/S0301-0082(97)00085-3] [PMID: 9550192]
[53]
Ishiuchi, S.; Tsuzuki, K.; Yoshida, Y.; Yamada, N.; Hagimura, N.; Okado, H.; Miwa, A.; Kurihara, H.; Nakazato, Y.; Tamura, M.J.N.m. Blockage of Ca2+-permeable AMPA receptors suppresses migration and induces apoptosis in human glioblastoma cells. Nat. Med., 2002, 8(9), 971-978.
[54]
Datta, S.R.; Dudek, H.; Tao, X.; Masters, S.; Fu, H.; Gotoh, Y.; Greenberg, M.E. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell, 1997, 91(2), 231-241.
[http://dx.doi.org/10.1016/S0092-8674(00)80405-5] [PMID: 9346240]
[55]
Li, T.; Yi, L.; Hai, L.; Ma, H.; Tao, Z.; Zhang, C.; Abeysekera, I.R.; Zhao, K.; Yang, Y.; Wang, W.; Liu, B.; Yu, S.; Tong, L.; Liu, P.; Zhu, M.; Ren, B.; Lin, Y.; Zhang, K.; Cheng, C.; Huang, Y.; Yang, X. The interactome and spatial redistribution feature of Ca2+ receptor protein calmodulin reveals a novel role in invadopodia-mediated invasion. Cell Death Dis., 2018, 9(3), 292.
[http://dx.doi.org/10.1038/s41419-017-0253-7] [PMID: 29463791]
[56]
Villalobo, A.; Berchtold, M.W. The role of calmodulin in tumor cell migration, invasiveness, and metastasis. Int. J. Mol. Sci., 2020, 21(3), 765.
[http://dx.doi.org/10.3390/ijms21030765] [PMID: 31991573]
[57]
Villalobo, A.; Ishida, H.; Vogel, H.J.; Berchtold, M.W.J.B.E.B.A-M.C.R. Calmodulin as a protein linker and a regulator of adaptor/scaffold proteins. Biochim. Biophys. Acta Mol. Cell Res., 2018, 1865(3), 507-521.
[58]
Chin, D.; Means, A.R. Calmodulin: a prototypical calcium sensor. Trends Cell Biol., 2000, 10(8), 322-328.
[http://dx.doi.org/10.1016/S0962-8924(00)01800-6] [PMID: 10884684]
[59]
Leclerc, C.; Haeich, J.; Aulestia, F.J.; Kilhoffer, M.C.; Miller, A.L.; Néant, I.; Webb, S.E.; Schaeffer, E.; Junier, M.P.; Chneiweiss, H.; Moreau, M. Calcium signaling orchestrates glioblastoma development: Facts and conjunctures. Biochim. Biophys. Acta Mol. Cell Res., 2016, 1863(6)(6 Pt B), 1447-1459.
[http://dx.doi.org/10.1016/j.bbamcr.2016.01.018] [PMID: 26826650]
[60]
Wu, X.; Wu, Y.; Ye, B.; Wu, F.; Wang, P.J.M. High expression of ghrelin and obestatin prepropeptide in tumor tissues predicted adverse overall survival in gastric carcinoma patients. Medicine, 2020, 99(26), e20635.
[http://dx.doi.org/10.1097/MD.0000000000020635]
[61]
Pardo, L.A.; Stühmer, W. The roles of K+ channels in cancer. Nat. Rev. Cancer, 2014, 14(1), 39-48.
[http://dx.doi.org/10.1038/nrc3635] [PMID: 24336491]
[62]
Niday, Z.; Tzingounis, A.V. Potassium channel gain of function in epilepsy: An unresolved paradox. Neuroscientist, 2018, 24(4), 368-380.
[http://dx.doi.org/10.1177/1073858418763752] [PMID: 29542386]
[63]
Zhang, Y.; Zhang, P.; Chen, L.; Zhao, L.; Zhu, J.; Zhu, T. The long non-coding RNA-14327.1 promotes migration and invasion potential of endometrial carcinoma cells by stabilizing the potassium channel Kca3.1. OncoTargets Ther., 2019, 12, 10287-10297.
[http://dx.doi.org/10.2147/OTT.S226737] [PMID: 31819513]
[64]
Cázares-Ordoñez, V.; Pardo, L.A. Kv10.1 potassium channel: from the brain to the tumors. Biochem. Cell Biol., 2017, 95(5), 531-536.
[http://dx.doi.org/10.1139/bcb-2017-0062] [PMID: 28708947]
[65]
Ryland, K.E.; Svoboda, L.K.; Vesely, E.D.; McIntyre, J.C.; Zhang, L.; Martens, J.R.; Lawlor, E.R. Polycomb-dependent repression of the potassium channel-encoding gene KCNA5 promotes cancer cell survival under conditions of stress. Oncogene, 2015, 34(35), 4591-4600.
[http://dx.doi.org/10.1038/onc.2014.384] [PMID: 25435365]
[66]
Abdullaev, I.F.; Rudkouskaya, A.; Mongin, A.A.; Kuo, Y-H.J.P.o. Calcium-activated potassium channels BK and IK1 are functionally expressed in human gliomas but do not regulate cell proliferation. PLoS One, 2010, 5(8), e12304.
[http://dx.doi.org/10.1371/journal.pone.0012304]
[67]
Zúñiga, L.; Zúñiga, R. Understanding the Cap Structure in K2P Channels. Front. Physiol., 2016, 7, 228.
[http://dx.doi.org/10.3389/fphys.2016.00228] [PMID: 27378938]
[68]
Huang, L.; Li, B.; Li, W.; Guo, H.; Zou, F.J.C. ATP-sensitive potassium channels control glioma cells proliferation by regulating ERK activity. Carcinogenesis, 2009, 30(5), 737-744.
[http://dx.doi.org/10.1093/carcin/bgp034]
[69]
Lang, F.; Föller, M.; Lang, K.S.; Lang, P.A.; Ritter, M.; Gulbins, E.; Vereninov, A.; Huber, S.M. Ion channels in cell proliferation and apoptotic cell death. J. Membr. Biol., 2005, 205(3), 147-157.
[http://dx.doi.org/10.1007/s00232-005-0780-5] [PMID: 16362503]
[70]
Chin, L.S.; Park, C.C.; Zitnay, K.M.; Sinha, M.; DiPatri, A.J., Jr; Perillán, P.; Simard, J.M. 4-Aminopyridine causes apoptosis and blocks an outward rectifier K+ channel in malignant astrocytoma cell lines. J. Neurosci. Res., 1997, 48(2), 122-127.
[http://dx.doi.org/10.1002/(SICI)1097-4547(19970415)48:2<122:AID-JNR4>3.0.CO;2-E] [PMID: 9130140]
[71]
Yang, K.B.; Zhao, S.G.; Liu, Y.H.; Hu, E.X.; Liu, B.X. Tetraethylammonium inhibits glioma cells via increasing production of intracellular reactive oxygen species. Chemotherapy, 2009, 55(5), 372-380.
[http://dx.doi.org/10.1159/000235730] [PMID: 19707016]
[72]
Lang, F.; Ritter, M.; Gamper, N.; Huber, S.; Fillon, S.; Tanneur, V.; Lepple-Wienhues, A.; Szabo, I.; Bulbins, E. Cell volume in the regulation of cell proliferation and apoptotic cell death. Cell. Physiol. Biochem., 2000, 10(5-6), 417-428.
[http://dx.doi.org/10.1159/000016367] [PMID: 11125224]
[73]
Meuth, S.G.; Herrmann, A.M.; Ip, C.W.; Kanyshkova, T.; Bittner, S.; Weishaupt, A.; Budde, T.; Wiendl, H. The two-pore domain potassium channel TASK3 functionally impacts glioma cell death. J. Neurooncol., 2008, 87(3), 263-270.
[http://dx.doi.org/10.1007/s11060-008-9517-5] [PMID: 18217213]
[74]
McFerrin, M.B.; Turner, K.L.; Cuddapah, V.A.; Sontheimer, H.J.A.J.o.P-C.P. Differential role of IK and BK potassium channels as mediators of intrinsic and extrinsic apoptotic cell death. Am. J. Physiol. Cell Physiol., 2012, 303(10), C1070-C1078.
[http://dx.doi.org/10.1152/ajpcell.00040.2012]
[75]
Weaver, A.K.; Liu, X.; Sontheimer, H. Role for calcium-activated potassium channels (BK) in growth control of human malignant glioma cells. J. Neurosci. Res., 2004, 78(2), 224-234.
[http://dx.doi.org/10.1002/jnr.20240] [PMID: 15378515]
[76]
Chang, K.H.; Chen, M.L.; Chen, H.C.; Huang, Y.W.; Wu, T.Y.; Chen, Y.J. Enhancement of radiosensitivity in human glioblastoma U138MG cells by tetrandrine. Neoplasma, 1999, 46(3), 196-200.
[PMID: 10613597]
[77]
Khalid, M.H.; Shibata, S.; Hiura, T. Effects of clotrimazole on the growth, morphological characteristics, and cisplatin sensitivity of human glioblastoma cells in vitro. J. Neurosurg., 1999, 90(5), 918-927.
[http://dx.doi.org/10.3171/jns.1999.90.5.0918] [PMID: 10223459]
[78]
Hu, L.; Li, L.L.; Lin, Z.G.; Jiang, Z.C.; Li, H.X.; Zhao, S.G.; Yang, K.B. Blockage of potassium channel inhibits proliferation of glioma cells via increasing reactive oxygen species. Oncol. Res., 2014, 22(1), 57-65.
[http://dx.doi.org/10.3727/096504014X14098532393518] [PMID: 25700359]
[79]
Blackiston, D.J.; McLaughlin, K.A.; Levin, M. Bioelectric controls of cell proliferation: Ion channels, membrane voltage and the cell cycle. Cell Cycle, 2009, 8(21), 3527-3536.
[http://dx.doi.org/10.4161/cc.8.21.9888] [PMID: 19823012]
[80]
Bordey, A.; Lyons, S.A.; Hablitz, J.J.; Sontheimer, H. Electrophysiological characteristics of reactive astrocytes in experimental cortical dysplasia. J. Neurophysiol., 2001, 85(4), 1719-1731.
[http://dx.doi.org/10.1152/jn.2001.85.4.1719] [PMID: 11287494]
[81]
Sontheimer, H. An unexpected role for ion channels in brain tumor metastasis. Exp. Biol. Med. (Maywood), 2008, 233(7), 779-791.
[http://dx.doi.org/10.3181/0711-MR-308] [PMID: 18445774]
[82]
Higashimori, H.; Sontheimer, H. Role of Kir4.1 channels in growth control of glia. Glia, 2007, 55(16), 1668-1679.
[http://dx.doi.org/10.1002/glia.20574] [PMID: 17876807]
[83]
Sciaccaluga, M.; Fioretti, B.; Catacuzzeno, L.; Pagani, F.; Bertollini, C.; Rosito, M.; Catalano, M.; D’Alessandro, G.; Santoro, A.; Cantore, G.; Ragozzino, D.; Castigli, E.; Franciolini, F.; Limatola, C. CXCL12-induced Glioblastoma cell migration requires intermediate conductance Ca 2+ -activated K + channel activity. Am. J. Physiol. Cell Physiol., 2010, 299(1), C175-C184.
[http://dx.doi.org/10.1152/ajpcell.00344.2009] [PMID: 20392929]
[84]
Turner, K.L.; Sontheimer, H. KCa3.1 modulates neuroblast migration along the Rostral Migratory Stream (RMS) in vivo. Cereb. Cortex, 2014, 24(9), 2388-2400.
[http://dx.doi.org/10.1093/cercor/bht090] [PMID: 23585521]
[85]
Schwab, A.; Fabian, A.; Hanley, P.J.; Stock, C. Role of ion channels and transporters in cell migration. Physiol. Rev., 2012, 92(4), 1865-1913.
[http://dx.doi.org/10.1152/physrev.00018.2011] [PMID: 23073633]
[86]
Furnari, F.B.; Fenton, T.; Bachoo, R.M.; Mukasa, A.; Stommel, J.M.; Stegh, A.; Hahn, W.C.; Ligon, K.L.; Louis, D.N.; Brennan, C.; Chin, L.; DePinho, R.A.; Cavenee, W.K. Malignant astrocytic glioma: genetics, biology, and paths to treatment. Genes Dev., 2007, 21(21), 2683-2710.
[http://dx.doi.org/10.1101/gad.1596707] [PMID: 17974913]
[87]
Chi, A.S.; Wen, P.Y. Inhibiting kinases in malignant gliomas. Expert Opin. Ther. Targets, 2007, 11(4), 473-496.
[http://dx.doi.org/10.1517/14728222.11.4.473] [PMID: 17373878]
[88]
Sathornsumetee, S.; Reardon, D.A.; Desjardins, A.; Quinn, J.A.; Vredenburgh, J.J.; Rich, J.N. Molecularly targeted therapy for malignant glioma. Cancer, 2007, 110(1), 13-24.
[http://dx.doi.org/10.1002/cncr.22741] [PMID: 17520692]
[89]
Stommel, J.M.; Kimmelman, A.C.; Ying, H.; Nabioullin, R.; Ponugoti, A.H.; Wiedemeyer, R.; Stegh, A.H.; Bradner, J.E.; Ligon, K.L.; Brennan, C.; Chin, L.; DePinho, R.A. Coactivation of receptor tyrosine kinases affects the response of tumor cells to targeted therapies. Science, 2007, 318(5848), 287-290.
[http://dx.doi.org/10.1126/science.1142946] [PMID: 17872411]
[90]
Wen, P.Y.; Yung, W.K.A.; Lamborn, K.R.; Dahia, P.L.; Wang, Y.; Peng, B.; Abrey, L.E.; Raizer, J.; Cloughesy, T.F.; Fink, K.; Gilbert, M.; Chang, S.; Junck, L.; Schiff, D.; Lieberman, F.; Fine, H.A.; Mehta, M.; Robins, H.I.; DeAngelis, L.M.; Groves, M.D.; Puduvalli, V.K.; Levin, V.; Conrad, C.; Maher, E.A.; Aldape, K.; Hayes, M.; Letvak, L.; Egorin, M.J.; Capdeville, R.; Kaplan, R.; Murgo, A.J.; Stiles, C.; Prados, M.D. Phase I/II study of imatinib mesylate for recurrent malignant gliomas: North American Brain Tumor Consortium Study 99-08. Clin. Cancer Res., 2006, 12(16), 4899-4907.
[http://dx.doi.org/10.1158/1078-0432.CCR-06-0773] [PMID: 16914578]
[91]
Viana-Pereira, M.; Lopes, J.M.; Little, S.; Milanezi, F.; Basto, D.; Pardal, F.; Jones, C.; Reis, R.M. Analysis of EGFR overexpression, EGFR gene amplification and the EGFRvIII mutation in Portuguese high-grade gliomas. Anticancer Res., 2008, 28(2A), 913-920.
[PMID: 18507036]
[92]
Liang, Z.; Yang, Y.; Jia, F.; Sai, K.; Ullah, S.; Fidelis, C.; Lin, Z.; Li, F. Intrathecal delivery of folate conjugated near-infrared quantum dots for targeted in vivo imaging of gliomas in mice brains. ACS Appl. Bio Mater., 2019, 2(4), 1432-1439.
[http://dx.doi.org/10.1021/acsabm.8b00629] [PMID: 35026918]
[93]
Galanis, E.; Buckner, J.C.; Maurer, M.J.; Kreisberg, J.I.; Ballman, K.; Boni, J.; Peralba, J.M.; Jenkins, R.B.; Dakhil, S.R.; Morton, R.F.; Jaeckle, K.A.; Scheithauer, B.W.; Dancey, J.; Hidalgo, M.; Walsh, D.J. Phase II trial of temsirolimus (CCI-779) in recurrent glioblastoma multiforme: A North Central Cancer Treatment Group Study. J. Clin. Oncol., 2005, 23(23), 5294-5304.
[http://dx.doi.org/10.1200/JCO.2005.23.622] [PMID: 15998902]
[94]
Chang, S.M.; Wen, P.; Cloughesy, T.; Greenberg, H.; Schiff, D.; Conrad, C.; Fink, K.; Robins, H.I.; De Angelis, L.; Raizer, J.; Hess, K.; Aldape, K.; Lamborn, K.R.; Kuhn, J.; Dancey, J.; Prados, M.D. Phase II study of CCI-779 in patients with recurrent glioblastoma multiforme. Invest. New Drugs, 2005, 23(4), 357-361.
[http://dx.doi.org/10.1007/s10637-005-1444-0] [PMID: 16012795]
[95]
Cloughesy, T.F.; Wen, P.Y.; Robins, H.I.; Chang, S.M.; Groves, M.D.; Fink, K.L.; Junck, L.; Schiff, D.; Abrey, L.; Gilbert, M.R.J.J.o.C.O. Phase II trial of tipifarnib in patients with recurrent malignant glioma either receiving or not receiving enzyme-inducing antiepileptic drugs: A North American Brain Tumor Consortium Study. J. Clin. Oncol., 2006, 24(22), 3651-3656.
[http://dx.doi.org/10.1200/JCO.2006.06.2323]
[96]
Kale, V.P.; Amin, S.G.; Pandey, M.K. Targeting ion channels for cancer therapy by repurposing the approved drugs. Biochim. Biophys. Acta Biomembr., 2015, 1848(10)(10 Pt B), 2747-2755.
[http://dx.doi.org/10.1016/j.bbamem.2015.03.034] [PMID: 25843679]
[97]
Bagal, S.K.; Brown, A.D.; Cox, P.J.; Omoto, K.; Owen, R.M.; Pryde, D.C.; Sidders, B.; Skerratt, S.E.; Stevens, E.B.; Storer, R.I.J.J.o.m.c. Ion channels as therapeutic targets: a drug discovery perspective. J. Med. Chem., 2013, 56(3), 593-624.
[http://dx.doi.org/10.1021/jm3011433]
[98]
Arvanitis, C.D.; Ferraro, G.B.; Jain, R.K. The blood–brain barrier and blood-tumour barrier in brain tumours and metastases. Nat. Rev. Cancer, 2020, 20(1), 26-41.
[http://dx.doi.org/10.1038/s41568-019-0205-x] [PMID: 31601988]
[99]
Alphandéry, E. Nano-Therapies for Glioblastoma Treatment. Cancers (Basel), 2020, 12(1), 242.
[http://dx.doi.org/10.3390/cancers12010242] [PMID: 31963825]
[100]
Smith, S.J.; Tyler, B.M.; Gould, T.; Veal, G.J.; Gorelick, N.; Rowlinson, J.; Serra, R.; Ritchie, A.; Berry, P.; Otto, A.J.C.C.R. Overall survival in malignant glioma is significantly prolonged by neurosurgical delivery of etoposide and temozolomide from a thermo-responsive biodegradable paste long-term survival from intracavity biodegradable paste. 2019, 25(16), 5094-5106.
[101]
Lundbæk, J.A.; Koeppe, R.E., II; Andersen, O.S. Amphiphile regulation of ion channel function by changes in the bilayer spring constant. Proc. Natl. Acad. Sci., 2010, 107(35), 15427-15430.
[http://dx.doi.org/10.1073/pnas.1007455107] [PMID: 20713738]
[102]
Santi, C.M.; Cayabyab, F.S.; Sutton, K.G.; McRory, J.E.; Mezeyova, J.; Hamming, K.S.; Parker, D.; Stea, A.; Snutch, T.P. Differential inhibition of T-type calcium channels by neuroleptics. J. Neurosci., 2002, 22(2), 396-403.
[http://dx.doi.org/10.1523/JNEUROSCI.22-02-00396.2002] [PMID: 11784784]
[103]
Shaw, V. Repurposing antipsychotics of the diphenylbutylpiperidine class for cancer therapy.Semi. Cancer Biol; Elsevier, 2021, 68, p. 75-83.
[104]
Zhang, Y.; Cruickshanks, N.; Yuan, F.; Wang, B.; Pahuski, M.; Wulfkuhle, J.; Gallagher, I.; Koeppel, A.F.; Hatef, S.; Papanicolas, C.; Lee, J.; Bar, E.E.; Schiff, D.; Turnerr, S.D.; Petricoin, E.F.; Gray, L.S.; Abounader, R. Targetable T-type Calcium Channels Drive Glioblastoma-Role and Targeting of Calcium Channels in Glioblastoma. Cancer Res., 2017, 77(13), 3479-3490.
[105]
Lee, C.Y.; Lai, H.Y.; Chiu, A.; Chan, S.H.; Hsiao, L.P.; Lee, S.T. The effects of antiepileptic drugs on the growth of glioblastoma cell lines. J. Neurooncol., 2016, 127(3), 445-453.
[http://dx.doi.org/10.1007/s11060-016-2056-6] [PMID: 26758059]
[106]
Dong, Y.; Furuta, T.; Sabit, H.; Kitabayashi, T.; Jiapaer, S.; Kobayashi, M.; Ino, Y.; Todo, T.; Teng, L.; Hirao, A.J.O. Identification of antipsychotic drug fluspirilene as a potential anti-glioma stem cell drug. Oncotarget, 2017, 8(67), 111728-111741.
[http://dx.doi.org/10.18632/oncotarget.22904]
[107]
Munson, J.M.; Fried, L.; Rowson, S.A.; Bonner, M.Y.; Karumbaiah, L.; Diaz, B.; Courtneidge, S.A.; Knaus, U.G.; Brat, D.J.; Arbiser, J.L.; Bellamkonda, R.V. Anti-invasive adjuvant therapy with imipramine blue enhances chemotherapeutic efficacy against glioma. Sci. Transl. Med., 2012, 4(127), 127ra36.
[http://dx.doi.org/10.1126/scitranslmed.3003016] [PMID: 22461640]
[108]
Shchors, K.; Massaras, A.; Hanahan, D. Dual targeting of the autophagic regulatory circuitry in gliomas with repurposed drugs elicits cell-lethal autophagy and therapeutic benefit. Cancer Cell, 2015, 28(4), 456-471.
[http://dx.doi.org/10.1016/j.ccell.2015.08.012] [PMID: 26412325]
[109]
Rao, V.; Perez-Neut, M.; Kaja, S.; Gentile, S. Voltage-gated ion channels in cancer cell proliferation. Cancers, 2015, 7(2), 849-875.
[http://dx.doi.org/10.3390/cancers7020813] [PMID: 26010603]
[110]
Liu, H.; Li, Y.; Raisch, K.P. Clotrimazole induces a late G1 cell cycle arrest and sensitizes glioblastoma cells to radiation in vitro. Anticancer Drugs, 2010, 21(9), 841-849.
[http://dx.doi.org/10.1097/CAD.0b013e32833e8022] [PMID: 20724915]
[111]
Khalid, M.H.; Tokunaga, Y.; Caputy, A.J.; Walters, E. Inhibition of tumor growth and prolonged survival of rats with intracranial gliomas following administration of clotrimazole. J. Neurosurg., 2005, 103(1), 79-86.
[http://dx.doi.org/10.3171/jns.2005.103.1.0079] [PMID: 16121977]
[112]
Lu, V.M.; Texakalidis, P.; McDonald, K.L.; Mekary, R.A.; Smith, T.R. The survival effect of valproic acid in glioblastoma and its current trend: a systematic review and meta-analysis. Clin. Neurol. Neurosurg., 2018, 174, 149-155.
[http://dx.doi.org/10.1016/j.clineuro.2018.09.019] [PMID: 30243186]
[113]
Valiyaveetti, D.; Malik, M.; Joseph, D.M.; Ahmed, S.F.; Kothwal, S.A.; Vijayasaradhi, M.J.S.A.J.o.C. Effect of valproic acid on survival in glioblastoma: A prospective single-arm study. South Asian J. Cancer, 2018, 7(3), 159-162.
[http://dx.doi.org/10.4103/sajc.sajc_188_17]
[114]
Ryu, J.Y.; Min, K.L.; Chang, M.J. Effect of anti-epileptic drugs on the survival of patients with glioblastoma multiforme: A retrospective, single-center study. PLoS One, 2019, 14(12), e0225599.
[http://dx.doi.org/10.1371/journal.pone.0225599] [PMID: 31790459]
[115]
Sperling, S.; Aung, T.; Martin, S.; Rohde, V.; Ninkovic, M. Riluzole: a potential therapeutic intervention in human brain tumor stem-like cells. Oncotarget, 2017, 8(57), 96697-96709.
[http://dx.doi.org/10.18632/oncotarget.18043] [PMID: 29228563]
[116]
Yamada, T.; Tsuji, S.; Nakamura, S.; Egashira, Y.; Shimazawa, M.; Nakayama, N.; Yano, H.; Iwama, T.; Hara, H. Riluzole enhances the antitumor effects of temozolomide via suppression of MGMT expression in glioblastoma. J. Neurosurg., 2020, 134(3), 1-10.
[http://dx.doi.org/10.3171/2019.12.JNS192682] [PMID: 32168477]
[117]
Yu, Z.; Zhao, G.; Li, P.; Li, Y.; Zhou, G.; Chen, Y.; Xie, G. Temozolomide in combination with metformin act synergistically to inhibit proliferation and expansion of glioma stem-like cells. Oncol. Lett., 2016, 11(4), 2792-2800.
[http://dx.doi.org/10.3892/ol.2016.4315] [PMID: 27073554]
[118]
Valtorta, S.; Dico, A.L.; Raccagni, I.; Gaglio, D.; Belloli, S.; Politi, L.S.; Martelli, C.; Diceglie, C.; Bonanomi, M.; Ercoli, G.; Vaira, V.; Ottobrini, L.; Moresco, R.M. Metformin and temozolomide, a synergic option to overcome resistance in glioblastoma multiforme models. Oncotarget, 2017, 8(68), 113090-113104.
[http://dx.doi.org/10.18632/oncotarget.23028] [PMID: 29348889]
[119]
Mouhieddine, T.H.; Nokkari, A.; Itani, M.M.; Chamaa, F.; Bahmad, H.; Monzer, A.; El-Merahbi, R.; Daoud, G.; Eid, A.; Kobeissy, F.H.; Abou-Kheir, W. Metformin and Ara-a Effectively Suppress Brain Cancer by Targeting Cancer Stem/Progenitor Cells. Front. Neurosci., 2015, 9, 442.
[http://dx.doi.org/10.3389/fnins.2015.00442] [PMID: 26635517]
[120]
Cohen-Inbar, O.; Zaaroor, M.J.J.o.C.N. Glioblastoma multiforme targeted therapy: The Chlorotoxin story. J. Clin. Neurosci., 2016, 33, 52-58.
[121]
Cheng, Y.; Zhao, J.; Qiao, W.; Chen, K.J.A.j.o.n.m. Recent advances in diagnosis and treatment of gliomas using chlorotoxin-based bioconjugates. Am. J. Nucl. Med. Mol. Imaging, 2014, 4(5), 385.
[122]
Wang, X.; Guo, Z.J.O.L. Chlorotoxin-conjugated onconase as a potential anti-glioma drug. Oncol. Lett., 2015, 9(3), 1337-1342.
[http://dx.doi.org/10.3892/ol.2014.2835]
[123]
Agarwal, S.; Mohamed, M.S.; Mizuki, T.; Maekawa, T.; Sakthi Kumar, D. Chlorotoxin modified morusin–PLGA nanoparticles for targeted glioblastoma therapy. J. Mater. Chem. B Mater. Biol. Med., 2019, 7(39), 5896-5919.
[http://dx.doi.org/10.1039/C9TB01131E] [PMID: 31423502]
[124]
Venkatesh, H.S.; Morishita, W.; Geraghty, A.C.; Silverbush, D.; Gillespie, S.M.; Arzt, M.; Tam, L.T.; Espenel, C.; Ponnuswami, A.; Ni, L.J.N. Electrical and synaptic integration of glioma into neural circuits. Nature, 2019, 573(7775), 539-545.
[http://dx.doi.org/10.1038/s41586-019-1563-y]
[125]
Pollak, J.; Rai, K.G.; Funk, C.C.; Arora, S.; Lee, E.; Zhu, J.; Price, N.D.; Paddison, P.J.; Ramirez, J.M.; Rostomily, R.C. Ion channel expression patterns in glioblastoma stem cells with functional and therapeutic implications for malignancy. PLoS One, 2017, 12(3), e0172884.
[http://dx.doi.org/10.1371/journal.pone.0172884] [PMID: 28264064]
[126]
Reiser, G.; Hamprecht, B.J.P.A.E.J.o.P. Sodium-channels in non-excitable glioma cells, shown by the influence of veratridine, scorpion toxin, and tetrodotoxin on membrane potential and on ion transport. Pflugers Arch., 1983, 397(4), 260-264.
[http://dx.doi.org/10.1007/BF00580258]
[127]
Rooj, A.K.; McNicholas, C.M.; Bartoszewski, R.; Bebok, Z.; Benos, D.J.; Fuller, C.M. Glioma-specific cation conductance regulates migration and cell cycle progression. J. Biol. Chem., 2012, 287(6), 4053-4065.
[http://dx.doi.org/10.1074/jbc.M111.311688] [PMID: 22130665]
[128]
Bubien, J.K.; Ji, H.L.; Gillespie, G.Y.; Fuller, C.M.; Markert, J.M.; Mapstone, T.B.; Benos, D.J. Cation selectivity and inhibition of malignant glioma Na+ channels by Psalmotoxin 1. Am. J. Physiol. Cell Physiol., 2004, 287(5), C1282-C1291.
[http://dx.doi.org/10.1152/ajpcell.00077.2004] [PMID: 15253892]
[129]
Sliwa, M.; Markovic, D.; Gabrusiewicz, K.; Synowitz, M.; Glass, R.; Zawadzka, M.; Wesolowska, A.; Kettenmann, H.; Kaminska, B.J.B. The invasion promoting effect of microglia on glioblastoma cells is inhibited by cyclosporin A. Brain, 2007, 130(Pt 2), 476-489.
[http://dx.doi.org/10.1093/brain/awl263]
[130]
Bi, D.; Toyama, K.; Lemaître, V.; Takai, J.; Fan, F.; Jenkins, D.P.; Wulff, H.; Gutterman, D.D.; Park, F.; Miura, H. The intermediate conductance calcium-activated potassium channel KCa3.1 regulates vascular smooth muscle cell proliferation via controlling calcium-dependent signaling. J. Biol. Chem., 2013, 288(22), 15843-15853.
[http://dx.doi.org/10.1074/jbc.M112.427187] [PMID: 23609438]
[131]
Ru, Q.; Tian, X.; Pi, M.S.; Chen, L.; Yue, K.; Xiong, Q.; Ma, B.M.; Li, C.Y.; Voltage-gated, K. Voltage-gated K+ channel blocker quinidine inhibits proliferation and induces apoptosis by regulating expression of microRNAs in human glioma U87-MG cells. Int. J. Oncol., 2015, 46(2), 833-840.
[http://dx.doi.org/10.3892/ijo.2014.2777] [PMID: 25420507]
[132]
Szabó, I.; Bock, J.; Grassmé, H.; Soddemann, M.; Wilker, B.; Lang, F.; Zoratti, M.; Gulbins, E. Mitochondrial potassium channel Kv1.3 mediates Bax-induced apoptosis in lymphocytes. Proc. Natl. Acad. Sci., 2008, 105(39), 14861-14866.
[http://dx.doi.org/10.1073/pnas.0804236105] [PMID: 18818304]
[133]
MacFarlane, S.N.; Sontheimer, H. Changes in ion channel expression accompany cell cycle progression of spinal cord astrocytes. Glia, 2000, 30(1), 39-48.
[http://dx.doi.org/10.1002/(SICI)1098-1136(200003)30:1<39:AID-GLIA5>3.0.CO;2-S] [PMID: 10696143]
[134]
Taglialatela, M.; Secondo, A.; Fresi, A.; Rosati, B.; Pannaccione, A.; Castaldo, P.; Giorgio, G.; Wanke, E.; Annunziato, L.J.B.p. Inhibition of depolarization-induced [3H] noradrenaline release from SH-SY5Y human neuroblastoma cells by some second-generation H1 receptor antagonists through blockade of store-operated Ca2+ channels (SOCs). Biochem. Pharmacol., 2001, 62(9), 1229-1238.
[135]
Ahmad, I.J.E.j.o.m.c. Tamoxifen a pioneering drug: An update on the therapeutic potential of tamoxifen derivatives. 2018, 143, 515-531.
[136]
Chae, Y.J.; Lee, K.J.; Lee, H.J.; Sung, K.W.; Choi, J.S.; Lee, E.H.; Hahn, S.J. Endoxifen, the active metabolite of tamoxifen, inhibits cloned hERG potassium channels. Eur. J. Pharmacol., 2015, 752, 1-7.
[http://dx.doi.org/10.1016/j.ejphar.2015.01.048] [PMID: 25680947]
[137]
Ferrer, T.; Figueroa, I.A.A.; Shapiro, M.S.; Tristani-Firouzi, M.; Sánchez-Chapula, J.A.J.B.J. Tamoxifen inhibition of Kv7. 2/Kv7. 3 Channels. 2014, 106(2), 142a.
[138]
Stoneking, C.J.; Shivakumar, O.; Thomas, D.N.; Colledge, W.H.; Mason, M.J.J.A.J.o.P-C.P. Voltage dependence of the Ca2+-activated K+ channel KCa3. 1 in human erythroleukemia cells. Am. J. Physiol. Cell Physiol., 2013, 304(9), C858-C872.
[139]
Keir, S.T.; Friedman, H.S.; Reardon, D.A.; Bigner, D.D.; Gray, L.A. Mibefradil, a novel therapy for glioblastoma multiforme: cell cycle synchronization and interlaced therapy in a murine model. J. Neurooncol., 2013, 111(2), 97-102.
[http://dx.doi.org/10.1007/s11060-012-0995-0] [PMID: 23086436]
[140]
Holdhoff, M.; Ye, X.; Supko, J.G.; Nabors, L.B.; Desai, A.S.; Walbert, T.; Lesser, G.J.; Read, W.L.; Lieberman, F.S.; Lodge, M.A.; Leal, J.; Fisher, J.D.; Desideri, S.; Grossman, S.A.; Wahl, R.L.; Schiff, D. Timed sequential therapy of the selective T-type calcium channel blocker mibefradil and temozolomide in patients with recurrent high-grade gliomas. Neuro-oncol., 2017, 19(6), 845-852.
[http://dx.doi.org/10.1093/neuonc/nox020] [PMID: 28371832]
[141]
Sheehan, J.P.; Xu, Z.; Popp, B.; Kowalski, L.; Schlesinger, D.J.J.o.n. Inhibition of glioblastoma and enhancement of survival via the use of mibefradil in conjunction with radiosurgery. J. Neurosurg., 2013, 118(4), 830-837.
[http://dx.doi.org/10.3171/2012.11.JNS121087]
[142]
Lee, G.L.; Hait, W.N. Inhibition of growth of C6 astrocytoma cells by inhibitors of calmodulin. Life Sci., 1985, 36(4), 347-354.
[http://dx.doi.org/10.1016/0024-3205(85)90120-1] [PMID: 2981390]
[143]
Shin, H.J.; Lee, S.; Jung, H.J.J.J.o.c.b. A curcumin derivative hydrazinobenzoylcurcumin suppresses stem‐like features of glioblastoma cells by targeting Ca2+/calmodulin‐dependent protein kinase II. J. Cell. Biochem., 2019, 120(4), 6741-6752.
[144]
Bomben, V.C.; Sontheimer, H.W. Inhibition of transient receptor potential canonical channels impairs cytokinesis in human malignant gliomas. Cell Prolif., 2008, 41(1), 98-121.
[http://dx.doi.org/10.1111/j.1365-2184.2007.00504.x] [PMID: 18211288]
[145]
Curran, J.; Mohler, P.J. Alternative paradigms for ion channelopathies: disorders of ion channel membrane trafficking and posttranslational modification. Annu. Rev. Physiol., 2015, 77(1), 505-524.
[http://dx.doi.org/10.1146/annurev-physiol-021014-071838] [PMID: 25293528]
[146]
Bomben, V.C.; Sontheimer, H. Disruption of transient receptor potential canonical channel 1 causes incomplete cytokinesis and slows the growth of human malignant gliomas. Glia, 2010, 58(10), 1145-1156.
[http://dx.doi.org/10.1002/glia.20994] [PMID: 20544850]
[147]
Ding, X.; He, Z.; Zhou, K.; Cheng, J.; Yao, H.; Lu, D.; Cai, R.; Jin, Y.; Dong, B.; Xu, Y.; Wang, Y. Essential role of TRPC6 channels in G2/M phase transition and development of human glioma. J. Natl. Cancer Inst., 2010, 102(14), 1052-1068.
[http://dx.doi.org/10.1093/jnci/djq217] [PMID: 20554944]
[148]
Chigurupati, S.; Venkataraman, R.; Barrera, D.; Naganathan, A.; Madan, M.; Paul, L.; Pattisapu, J.V.; Kyriazis, G.A.; Sugaya, K.; Bushnev, S.J.C.r. Receptor channel TRPC6 is a key mediator of notch-driven glioblastoma growth and invasivenessexpression and function of trpc6 in glioblastomas. Cancer Res., 2010, 70(1), 418-427.
[149]
Li, S.; Wang, J.; Wei, Y.; Liu, Y.; Ding, X.; Dong, B.; Xu, Y.; Wang, Y. Crucial role of TRPC6 in maintaining the stability of HIF-1α in glioma cells under hypoxia. J. Cell Sci., 2015, 128(17), 3317-3329.
[150]
Amantini, C.; Mosca, M.; Nabissi, M.; Lucciarini, R.; Caprodossi, S.; Arcella, A.; Giangaspero, F.; Santoni, G.J.J.o.n. Capsaicin‐induced apoptosis of glioma cells is mediated by TRPV1 vanilloid receptor and requires p38 MAPK activation. J. Neurochem., 2007, 102(3), 977-990.
[http://dx.doi.org/10.1111/j.1471-4159.2007.04582.x]
[151]
Nabissi, M.; Morelli, M.B.; Santoni, M.; Santoni, G. Triggering of the TRPV2 channel by cannabidiol sensitizes glioblastoma cells to cytotoxic chemotherapeutic agents. Carcinogenesis, 2013, 34(1), 48-57.
[http://dx.doi.org/10.1093/carcin/bgs328] [PMID: 23079154]
[152]
Morelli, M.B.; Nabissi, M.; Amantini, C.; Farfariello, V.; Ricci-Vitiani, L.; di Martino, S.; Pallini, R.; Larocca, L.M.; Caprodossi, S.; Santoni, M.; De Maria, R.; Santoni, G. The transient receptor potential vanilloid-2 cation channel impairs glioblastoma stem-like cell proliferation and promotes differentiation. Int. J. Cancer, 2012, 131(7), E1067-E1077.
[http://dx.doi.org/10.1002/ijc.27588] [PMID: 22492283]
[153]
Nabissi, M.; Morelli, M.B.; Amantini, C.; Farfariello, V.; Ricci-Vitiani, L.; Caprodossi, S.; Arcella, A.; Santoni, M.; Giangaspero, F.; De Maria, R.; Santoni, G. TRPV2 channel negatively controls glioma cell proliferation and resistance to Fas-induced apoptosis in ERK-dependent manner. Carcinogenesis, 2010, 31(5), 794-803.
[http://dx.doi.org/10.1093/carcin/bgq019] [PMID: 20093382]
[154]
Ishii, M.; Oyama, A.; Hagiwara, T.; Miyazaki, A.; Mori, Y.; Kiuchi, Y.; Shimizu, S. Facilitation of H2O2-induced A172 human glioblastoma cell death by insertion of oxidative stress-sensitive TRPM2 channels. Anticancer Res., 2007, 27(6B), 3987-3992.
[PMID: 18225560]
[155]
Wondergem, R.; Ecay, T.W.; Mahieu, F.; Owsianik, G.; Nilius, B. HGF/SF and menthol increase human glioblastoma cell calcium and migration. Biochem. Biophys. Res. Commun., 2008, 372(1), 210-215.
[http://dx.doi.org/10.1016/j.bbrc.2008.05.032] [PMID: 18485891]
[156]
Wondergem, R.; Bartley, J.W. Menthol increases human glioblastoma intracellular Ca2+, BK channel activity and cell migration. J. Biomed. Sci., 2009, 16(1), 90.
[http://dx.doi.org/10.1186/1423-0127-16-90] [PMID: 19778436]
[157]
Motiani, R.K.; Hyzinski-García, M.C.; Zhang, X.; Henkel, M.M.; Abdullaev, I.F.; Kuo, Y.H.; Matrougui, K.; Mongin, A.A.; Trebak, M. STIM1 and Orai1 mediate CRAC channel activity and are essential for human glioblastoma invasion. Pflugers Arch., 2013, 465(9), 1249-1260.
[http://dx.doi.org/10.1007/s00424-013-1254-8] [PMID: 23515871]
[158]
Valerie, N.C.K.; Dziegielewska, B.; Hosing, A.S.; Augustin, E.; Gray, L.S.; Brautigan, D.L.; Larner, J.M.; Dziegielewski, J. Inhibition of T-type calcium channels disrupts Akt signaling and promotes apoptosis in glioblastoma cells. Biochem. Pharmacol., 2013, 85(7), 888-897.
[http://dx.doi.org/10.1016/j.bcp.2012.12.017] [PMID: 23287412]
[159]
Gehring, M.P.; Pereira, T.C.B.; Zanin, R.F.; Borges, M.C.; Filho, A.B.; Battastini, A.M.O.; Bogo, M.R.; Lenz, G.; Campos, M.M.; Morrone, F.B. P2X7 receptor activation leads to increased cell death in a radiosensitive human glioma cell line. Purinergic Signal., 2012, 8(4), 729-739.
[http://dx.doi.org/10.1007/s11302-012-9319-2] [PMID: 22644907]
[160]
Gehring, M.P.; Kipper, F.; Nicoletti, N.F.; Sperotto, N.D.; Zanin, R.; Tamajusuku, A.S.; Flores, D.G.; Meurer, L.; Roesler, R. Aroldo Filho, Len Z.G.; Campos, M.M.; Morrone, F.B. P2X7 receptor as predictor gene for glioma radiosensitivity and median survival. 2015, 68, 92-100.
[161]
Fang, J.; Chen, X.; Zhang, L.; Chen, J.; Liang, Y.; Li, X.; Xiang, J.; Wang, L.; Guo, G.; Zhang, B.; Zhang, W.C. P2X7R suppression promotes glioma growth through epidermal growth factor receptor signal pathway. Int. J. Biochem. Cell Biol., 2013, 45(6), 1109-1120.
[162]
Wei, W.; Ryu, J.K.; Choi, H.B.; McLarnon, J.G.J.C.l. Expression and function of the P2X7 receptor in rat C6 glioma cells. Cancer Letters, 2008, 260(1-2), 79-87.
[http://dx.doi.org/10.1016/j.canlet.2007.10.025]
[163]
Gendron, F.P.; Neary, J.T.; Theiss, P.M.; Sun, G.Y.; Gonzalez, F.A.; Weisman, G.A. Mechanisms of P2X 7 receptor-mediated ERK1/2 phosphorylation in human astrocytoma cells. Am. J. Physiol. Cell Physiol., 2003, 284(2), C571-C581.
[http://dx.doi.org/10.1152/ajpcell.00286.2002] [PMID: 12529254]
[164]
Kang, S.S.; Han, K.S.; Ku, B.M.; Lee, Y.K.; Hong, J.; Shin, H.Y.; Almonte, A.G.; Woo, D.H.; Brat, D.J.; Hwang, E.M.; Yoo, S.H.; Chung, C.K.; Park, S.H.; Paek, S.H.; Roh, E.J.; Lee, S.; Park, J.Y.; Traynelis, S.F.; Lee, C.J. Caffeine-mediated inhibition of calcium release channel inositol 1,4,5-trisphosphate receptor subtype 3 blocks glioblastoma invasion and extends survival. Cancer Res., 2010, 70(3), 1173-1183.
[http://dx.doi.org/10.1158/0008-5472.CAN-09-2886] [PMID: 20103623]
[165]
Cosens, D.J.; Manning, A. Abnormal electroretinogram from a Drosophila mutant. Nature, 1969, 224(5216), 285-287.
[http://dx.doi.org/10.1038/224285a0] [PMID: 5344615]
[166]
Nilius, B.; Szallasi, A.J.P.r. Transient receptor potential channels as drug targets: from the science of basic research to the art of medicine. Pharmacol. Rev., 2014, 66(3), 676-814.
[http://dx.doi.org/10.1124/pr.113.008268]
[167]
Smani, T.; Shapovalov, G.; Skryma, R.; Prevarskaya, N.; Rosado, J.A. Functional and physiopathological implications of TRP channels. Biochim. Biophys. Acta Mol. Cell Res., 2015, 1853(8), 1772-1782.
[http://dx.doi.org/10.1016/j.bbamcr.2015.04.016] [PMID: 25937071]
[168]
Adachi, T.; Weisbrod, R.M.; Pimentel, D.R.; Ying, J.; Sharov, V.S.; Schöneich, C.; Cohen, R.A. S-Glutathiolation by peroxynitrite activates SERCA during arterial relaxation by nitric oxide. Nat. Med., 2004, 10(11), 1200-1207.
[http://dx.doi.org/10.1038/nm1119] [PMID: 15489859]
[169]
Bian, X.; Hughes, F.M., Jr; Huang, Y.; Cidlowski, J.A.; Putney, J.W. Jr Roles of cytoplasmic Ca2+ and intracellular Ca2+ stores in induction and suppression of apoptosis in S49 cells. Am. J. Physiol. Cell Physiol., 1997, 272(4), C1241-C1249.
[http://dx.doi.org/10.1152/ajpcell.1997.272.4.C1241] [PMID: 9142849]
[170]
Mahalingam, D.; Wilding, G.; Denmeade, S.; Sarantopoulas, J.; Cosgrove, D.; Cetnar, J.; Azad, N.; Bruce, J.; Kurman, M.; Allgood, V.E.; Carducci, M. Mipsagargin, a novel thapsigargin-based PSMA-activated prodrug: results of a first-in-man phase I clinical trial in patients with refractory, advanced or metastatic solid tumours. Br. J. Cancer, 2016, 114(9), 986-994.
[http://dx.doi.org/10.1038/bjc.2016.72] [PMID: 27115568]
[171]
Lester-Coll, N.; Kluytenaar, J.; Pavlik, K.; Yu, J.; Contessa, J.; Moliterno, J.; Piepmeier, J.; Becker, K.; Baehring, J.; Huttner, A.J.; Vortmeyer, A.O.; Ramani, R.; Lampert, R.J.; Yao, X.; Bindra, R.S. Mibefradil dihydrochloride with hypofractionated radiation for recurrent glioblastoma: Preliminary results of a phase 1 dose expansion trial. Int. J. Radiat. Oncol. Biol. Phys., 2016, 96(2), S93.
[172]
Omuro, A.; Beal, K.; McNeill, K.; Young, R.J.; Thomas, A.; Lin, X.; Terziev, R.; Kaley, T.J.; DeAngelis, L.M.; Daras, M.; Gavrilovic, I.T.; Mellinghoff, I.; Diamond, E.L.; McKeown, A.; Manne, M.; Caterfino, A.; Patel, K.; Bavisotto, L.; Gorman, G.; Lamson, M.; Gutin, P.; Tabar, V.; Chakravarty, D.; Chan, T.A.; Brennan, C.W.; Garrett-Mayer, E.; Karmali, R.A.; Pentsova, E. Multicenter phase IB trial of carboxyamidotriazole orotate and temozolomide for recurrent and newly diagnosed glioblastoma and other anaplastic gliomas. J. Clin. Oncol., 2018, 36(17), 1702-1709.
[http://dx.doi.org/10.1200/JCO.2017.76.9992] [PMID: 29683790]
[173]
Das, M. Carboxyamidotriazole orotate in glioblastoma. Lancet Oncol., 2018, 19(6), e292.
[http://dx.doi.org/10.1016/S1470-2045(18)30347-4] [PMID: 29731337]
[174]
Karsy, M.; Hoang, N.; Barth, T.; Burt, L.; Dunson, W.; Gillespie, D.L.; Jensen, R.L. Combined hydroxyurea and verapamil in the clinical treatment of refractory meningioma: Human and orthotopic xenograft studies. World Neurosurg., 2016, 86, 210-219.
[http://dx.doi.org/10.1016/j.wneu.2015.09.060] [PMID: 26428319]
[175]
Niklasson, M.; Maddalo, G.; Sramkova, Z.; Mutlu, E.; Wee, S.; Sekyrova, P.; Schmidt, L.; Fritz, N.; Dehnisch, I.; Kyriatzis, G.; Krafcikova, M.; Carson, B.B.; Feenstra, J.M.; Marinescu, V.D.; Segerman, A.; Haraldsson, M.; Gustavsson, A.L.; Hammarström, L.G.J.; Jenmalm Jensen, A.; Uhrbom, L.; Altelaar, A.F.M.; Linnarsson, S.; Uhlén, P.; Trantirek, L.; Vincent, C.T.; Nelander, S.; Enger, P.Ø.; Andäng, M. Membrane-depolarizing channel blockers induce selective glioma cell death by impairing nutrient transport and unfolded protein/amino acid responses. Cancer Res., 2017, 77(7), 1741-1752.
[http://dx.doi.org/10.1158/0008-5472.CAN-16-2274] [PMID: 28087597]
[176]
Peters, A.A.; Jamaludin, S.Y.N.; Yapa, K.T.D.S.; Chalmers, S.; Wiegmans, A.P.; Lim, H.F.; Milevskiy, M.J.G.; Azimi, I.; Davis, F.M.; Northwood, K.S.; Pera, E.; Marcial, D.L.; Dray, E.; Waterhouse, N.J.; Cabot, P.J.; Gonda, T.J.; Kenny, P.A.; Brown, M.A.; Khanna, K.K.; Roberts-Thomson, S.J.; Monteith, G.R. Oncosis and apoptosis induction by activation of an overexpressed ion channel in breast cancer cells. Oncogene, 2017, 36(46), 6490-6500.
[http://dx.doi.org/10.1038/onc.2017.234] [PMID: 28759041]
[177]
Yuan, P.; Leonetti, M.D.; Pico, A.R.; Hsiung, Y.; MacKinnon, R.J.S. Structure of the human BK channel Ca2+-activation apparatus at 3.0 Å resolution. Science, 2010, 329(5988), 182-186.
[178]
Miller, C. An overview of the potassium channel family. Genome Biol., 2000, 1(4), reviews0004.1.
[http://dx.doi.org/10.1186/gb-2000-1-4-reviews0004] [PMID: 11178249]
[179]
Singh, H.; Stefani, E.; Toro, L.J.T.J.p. Intracellular BKCa (iBKCa) channels. J. Physicol., 2012, 590(23), 5937-5947.
[180]
Catacuzzeno, L.; Fioretti, B.; Franciolini, F. Expression and role of the intermediate-conductance calcium-activated potassium channel kca3.1 in glioblastoma. J. Signal Transduct., 2012, 2012, 1-11.
[http://dx.doi.org/10.1155/2012/421564] [PMID: 22675627]
[181]
Salkoff, L.; Butler, A.; Ferreira, G.; Santi, C.; Wei, A. High-conductance potassium channels of the SLO family. Nat. Rev. Neurosci., 2006, 7(12), 921-931.
[http://dx.doi.org/10.1038/nrn1992] [PMID: 17115074]
[182]
Meera, P.; Wallner, M.; Song, M.; Toro, L. Large conductance voltage- and calcium-dependent K+ channel, a distinct member of voltage-dependent ion channels with seven N-terminal transmembrane segments (S0-S6), an extracellular N terminus, and an intracellular (S9-S10) C terminus. Proc. Natl. Acad. Sci. USA, 1997, 94(25), 14066-14071.
[http://dx.doi.org/10.1073/pnas.94.25.14066] [PMID: 9391153]
[183]
Ransom, C.B.; Liu, X.; Sontheimer, H.J.G. BK channels in human glioma cells have enhanced calcium sensitivity. Glia, 2002, 38, 281-291.
[http://dx.doi.org/10.1002/glia.10064]
[184]
Liu, X.; Chang, Y.; Reinhart, P.H.; Sontheimer, H.; Chang, Y. Cloning and characterization of glioma BK, a novel BK channel isoform highly expressed in human glioma cells. J. Neurosci., 2002, 22(5), 1840-1849.
[http://dx.doi.org/10.1523/JNEUROSCI.22-05-01840.2002] [PMID: 11880513]
[185]
Yellen, G. Ionic permeation and blockade in Ca2+-activated K+ channels of bovine chromaffin cells. J. Gen. Physiol., 1984, 84(2), 157-186.
[http://dx.doi.org/10.1085/jgp.84.2.157] [PMID: 6092514]
[186]
Sanchez, M.; Mc Manus, O.B. Paxilline inhibition of the alpha-subunit of the high-conductance calcium-activated potassium channel. Neuropharmacology, 1996, 35(7), 963-968.
[http://dx.doi.org/10.1016/0028-3908(96)00137-2] [PMID: 8938726]
[187]
Zhou, Y.; Lingle, C.J. Paxilline inhibits BK channels by an almost exclusively closed-channel block mechanism. J. General Physiol., 2014, 144(5), 415.
[http://dx.doi.org/10.1085/jgp.201411259]
[188]
Bilmen, J.G.; Wootton, L.L.; Michelangeli, F. The mechanism of inhibition of the sarco/endoplasmic reticulum Ca2+ ATPase by paxilline. Arch. Biochem. Biophys., 2002, 406(1), 55-64.
[http://dx.doi.org/10.1016/S0003-9861(02)00240-0] [PMID: 12234490]
[189]
Olesen, S-P.; Munch, E.; Moldt, P.; Drejer, J.J.E.j.o.p. Selective activation of Ca2+-dependent K+ channels by novel benzimidazolone. Arch. Biochem. Biophys., 1994, 406(1), 53-59.
[190]
Wrzosek, A. The potassium channel opener NS1619 modulates calcium homeostasis in muscle cells by inhibiting SERCA. Cell Calcium, 2014, 56(1), 14-24.
[http://dx.doi.org/10.1016/j.ceca.2014.03.005] [PMID: 24813114]
[191]
Warth, R.; Hamm, K.; Bleich, M.; Kunzelmann, K.; von Hahn, T.; Schreiber, R.; Ullrich, E.; Mengel, M.; Trautmann, N.; Kindle, P.J.P.A. Molecular and functional characterization of the small Ca2+-regulated K+ channel (rSK4) of colonic crypts. 1999, 438(4), 437-444.
[192]
Strange, K.; Yamada, T.; Denton, J.S. A 30-year journey from volume-regulated anion currents to molecular structure of the LRRC8 channel. J. Gen. Physiol., 2019, 151(2), 100-117.
[http://dx.doi.org/10.1085/jgp.201812138] [PMID: 30651298]
[193]
Ernest, N.J.; Weaver, A.K.; Van Duyn, L.B.; Sontheimer, H.W. Relative contribution of chloride channels and transporters to regulatory volume decrease in human glioma cells. Am. J. Physiol. Cell Physiol., 2005, 288(6), C1451-C1460.
[http://dx.doi.org/10.1152/ajpcell.00503.2004] [PMID: 15659714]
[194]
Akita, T.; Okada, Y. Characteristics and roles of the volume-sensitive outwardly rectifying (VSOR) anion channel in the central nervous system. Neuroscience, 2014, 275, 211-231.
[http://dx.doi.org/10.1016/j.neuroscience.2014.06.015] [PMID: 24937753]
[195]
Catacuzzeno, L.; Aiello, F.; Fioretti, B.; Sforna, L.; Castigli, E.; Ruggieri, P.; Tata, A.M.; Calogero, A.; Franciolini, F. Serum-activated K and Cl currents underlay U87-MG glioblastoma cell migration. J. Cell. Physiol., 2011, 226(7), 1926-1933.
[http://dx.doi.org/10.1002/jcp.22523] [PMID: 21506123]
[196]
Catacuzzeno, L.; Michelucci, A.; Sforna, L.; Aiello, F.; Sciaccaluga, M.; Fioretti, B.; Castigli, E.; Franciolini, F. Identification of key signaling molecules involved in the activation of the swelling-activated chloride current in human glioblastoma cells. J. Membr. Biol., 2014, 247(1), 45-55.
[http://dx.doi.org/10.1007/s00232-013-9609-9] [PMID: 24240542]
[197]
Joseph, J.V.; Roosmalen, I.A.V.; Busschers, E.; Tomar, T.; Conroy, S.; Eggens-Meijer, E.; Peñaranda Fajardo, N.; Pore, M.M.; Balasubramanyian, V.; Wagemakers, M.; Copray, S.; den Dunhen, W.F.A.; Kruyt, F.A.E. Serum-induced differentiation of glioblastoma neurospheres leads to enhanced migration/invasion capacity that is associated with increased MMP9. PLoS One, 2015, 10(12), e0145393.
[198]
Rondé, P.; Giannone, G.; Gerasymova, I.; Stoeckel, H.; Takeda, K.; Haiech, J. Mechanism of calcium oscillations in migrating human astrocytoma cells. Biochim. Biophys. Acta Mol. Cell Res., 2000, 1498(2-3), 273-280.
[http://dx.doi.org/10.1016/S0167-4889(00)00102-6] [PMID: 11108969]
[199]
Bordey, A.; Sontheimer, H.; Trouslard, J. Muscarinic activation of BK channels induces membrane oscillations in glioma cells and leads to inhibition of cell migration. J. Membr. Biol., 2000, 176(1), 31-40.
[http://dx.doi.org/10.1007/s002320001073] [PMID: 10882426]
[200]
Manning, T.J., Jr; Parker, J.C.; Sontheimer, H.J.C.m. Role of lysophosphatidic acid and rho in glioma cell motility. 2000, 45(3), 185-199.
[201]
C, M.; G, D.; R, V.; B, N. Block of volume-regulated anion channels by selective serotonin reuptake inhibitors. Naunyn Schmiedebergs Arch. Pharmacol., 2002, 366(2), 158-165.
[http://dx.doi.org/10.1007/s00210-002-0567-5] [PMID: 12122503]
[202]
Nilius, B.; Eggermont, J.; Voets, T.; Buyse, G.; Manolopoulos, V.; Droogmans, G. Properties of volume-regulated anion channels in mammalian cells. Prog. Biophys. Mol. Biol., 1997, 68(1), 69-119.
[http://dx.doi.org/10.1016/S0079-6107(97)00021-7] [PMID: 9481145]
[203]
Wang, G.X.; Hatton, W.J.; Wang, G.L.; Zhong, J.; Yamboliev, I.; Duan, D.; Hume, J.R. Functional effects of novel anti-ClC-3 antibodies on native volume-sensitive osmolyte and anion channels in cardiac and smooth muscle cells. Am. J. Physiol. Heart Circ. Physiol., 2003, 285(4), H1453-H1463.
[http://dx.doi.org/10.1152/ajpheart.00244.2003] [PMID: 12816749]
[204]
Olsen, M.L.; Schade, S.; Lyons, S.A.; Amaral, M.D.; Sontheimer, H. Expression of voltage-gated chloride channels in human glioma cells. J. Neurosci., 2003, 23(13), 5572-5582.
[http://dx.doi.org/10.1523/JNEUROSCI.23-13-05572.2003] [PMID: 12843258]
[205]
DeBin, J.A.; Maggio, J.E.; Strichartz, G.R. Purification and characterization of chlorotoxin, a chloride channel ligand from the venom of the scorpion. Am. J. Physiol. Cell Physiol., 1993, 264(2), C361-C369.
[http://dx.doi.org/10.1152/ajpcell.1993.264.2.C361] [PMID: 8383429]
[206]
Mao, J.; Chen, L.; Xu, B.; Wang, L.; Li, H.; Guo, J.; Li, W.; Nie, S.; Jacob, T.J.C.; Wang, L. Suppression of ClC-3 channel expression reduces migration of nasopharyngeal carcinoma cells. Biochem. Pharmacol., 2008, 75(9), 1706-1716.
[http://dx.doi.org/10.1016/j.bcp.2008.01.008] [PMID: 18359479]
[207]
Cuddapah, V.A. Regulation of ClC-3 in human malignant glioma; The University of Alabama at Birmingham, 2012.
[208]
Cuddapah, V.A.; Sontheimer, H. Molecular interaction and functional regulation of ClC-3 by Ca2+/calmodulin-dependent protein kinase II (CaMKII) in human malignant glioma. J. Biol. Chem., 2010, 285(15), 11188-11196.
[http://dx.doi.org/10.1074/jbc.M109.097675] [PMID: 20139089]

© 2024 Bentham Science Publishers | Privacy Policy