Skip to main content
SpringerLink
Log in

Ion Channels in Glioma Malignancy

  • Chapter
  • First Online:
Transportome Malfunction in the Cancer Spectrum

Part of the book series: Reviews of Physiology, Biochemistry and Pharmacology ((REVIEWS,volume 181))

Abstract

Brain tumors come in many types and differ greatly in outcome. They are classified by the cell of origin (astrocytoma, ependymoma, meningioma, medulloblastoma, glioma), although more recently molecular markers are used in addition to histology. Brain tumors are graded (from I to IV) to measure their malignancy. Glioblastoma, one of the most common adult primary brain tumors, displays the highest malignancy (grade IV), and median survival of about 15 months. Main reasons for poor outcome are incomplete surgical resection, due to the highly invasive potential of glioblastoma cells, and chemoresistance that commonly develops during drug treatment. An important role in brain tumor malignancy is played by ion channels. The Ca2+-activated K+ channels of large and intermediate conductance, KCa3.1 and KCa1.1, and the volume-regulated anion channel, whose combined activity results in the extrusion of KCl and osmotic water, control cell volume, and in turn migration, invasion, and apoptotic cell death. The transient receptor potential (TRP) channels and low threshold-activated Ca (T-type) channels have equally critical role in brain tumor malignancy, as dysregulated Ca2+ signals heavily impact on glioma cell proliferation, migration, invasion. The review provides an overview of the current evidence involving these channels in brain tumor malignancy, and the application of these insights in the light of future prospects for experimental and clinical practice.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 119.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 159.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 159.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Notes

  1. 1.

    IDH1 catalyzes the conversion of isocitrate to α-ketoglutarate as part of normal function of brain metabolism. IDH1 mutation results in gain of function to catalyze the production of α-ketoglutarate and hydroxyglutarate (2-HG), an oncometabolite that is thought to influence a range of cellular programs involved in epigenetic control and various processes leading to tumor development.

  2. 2.

    DIDS (4,4′–diisothiocyano-2,2′-stilbenedisulfonic acid); NPPB (5-nitro-2-(3-phenylpropylamino)benzoic acid); DCPIB (4-(2-butyl-6,7-dichloro-2-cyclopentylindan-1-on-5-yl)oxybutyric acid).

  3. 3.

    Notice that glutamate is also released by the cystine/glutamate antiporter xCT expressed in many malignant tumors, including GBM (Chairoungdua et al. 2001).

  4. 4.

    DAG, diacylglycerol; DGK, diacylglycerol kinase; PA, phosphatidic acid.

References

  • Abascal F, Zardoya R (2012) LRRC8 proteins share a common ancestor with pannexins, and may form hexameric channels involved in cell-cell communication. BioEssays 34, 551–560 (2012). RC8 proteins share a common ancestor with pannexins, and may form hexam. BioEssays 34(7):551–560

    CAS  PubMed  Google Scholar 

  • Abdullaev IF, Rudkouskaya A, Schools GP, Kimelberg HK, Mongin AA (2006) Pharmacological comparison of swelling-activated excitatory amino acid release and Cl- currents in cultured rat astrocytes. J Physiol 572(Pt 3):677–689

    CAS  PubMed  PubMed Central  Google Scholar 

  • Abdullaev IF, Rudkouskaya A, Mongin AA, Kuo Y-H (2010) Calcium-activated potassium channels BK and IK1 are functionally expressed in human gliomas but do not regulate cell proliferatiosn. PLoS One 5(8):e12304

    PubMed  PubMed Central  Google Scholar 

  • Abramovici H, Mojtabaie P, Parks RJ, Zhong XP, Koretzky GA, Topham MK, Gee SH (2009) Diacylglycerol kinase ζ regulates actin cytoskeleton reorganization through dissociation of Rac1 from RhoGDI. Mol Biol Cell 20(7):2049–2059

    CAS  PubMed  PubMed Central  Google Scholar 

  • Akita T, Okada Y (2014) Characteristics and roles of the volume-sensitive outwardly rectifying (VSOR) anion channel in the central nervous system. Neuroscience 275:211–231

    CAS  PubMed  Google Scholar 

  • Alptekin M, Eroglu S, Tutar E, Sencan S, Geyik MA, Ulasli M, Demiryurek AT, Camci C (2015) Gene expressions of TRP channels in glioblastoma multiforme and relation with survival. Tumour Biol 36(12):9209–9213

    CAS  PubMed  Google Scholar 

  • Amantini C, Mosca M, Nabissi M, Lucciarini R, Caprodossi S, Arcella A, Giangaspero F, Santoni G (2007) Capsaicin-induced apoptosis of glioma cells is mediated by TRPV1 vanilloid receptor and requires P38 MAPK activation. J Neurochem 102(3):977–990

    CAS  PubMed  Google Scholar 

  • Arias-Darraz L, Cabezas D, Colenso CK, Alegría-Arcos M, Bravo-Moraga F, Varas-Concha I, Almonacid DE, Madrid R, Brauchi S (2015) A transient receptor potential ion channel in chlamydomonas shares key features with sensory transduction-associated Trp channels in mammals. Plant Cell 27(1):177–188

    CAS  PubMed  PubMed Central  Google Scholar 

  • Arnoult D, Parone P, Martinou J-C, Antonsson B, Estaquier J, Ameisen JC (2002) Mitochondrial release of apoptosis-inducing factor occurs downstream of cytochrome c release in response to several proapoptotic stimuli. J Cell Biol 159(6):923–929

    CAS  PubMed  PubMed Central  Google Scholar 

  • Augustine GJ, Santamaria F, Tanaka K (2003) Local calcium signaling in neurons. Neuron 40(2):331–346

    CAS  PubMed  Google Scholar 

  • Azimi I, Milevskiy MJG, Kaemmerer E, Turner D, Yapa KTDS, Brown MA, Thompson EW, Roberts-Thomson SJ, Monteith GR (2017) TRPC1 is a differential regulator of hypoxia-mediated events and Akt signalling in PTEN-deficient breast cancer cells. J Cell Sci 130(14):2292–2305

    CAS  PubMed  Google Scholar 

  • Bae Y, Kim A, Cho C-H, Kim D, Jung H-G, Kim S-S, Yoo J, Park J-Y, Hwang EM (2019) TTYH1 and TTYH2 serve as LRRC8A-independent volume-regulated anion channels in cancer cells. Cell 8(6):562

    CAS  Google Scholar 

  • Barnum KJ, O’Connell MJ (2014) Cell cycle regulation by checkpoints. Methods Mol Biol 1170:29–40

    PubMed  PubMed Central  Google Scholar 

  • Bartlett PJ, Metzger W, Gaspers LD, Thomas AP (2015) Differential regulation of multiple steps in inositol 1,4,5-trisphosphate signaling by protein kinase C shapes hormone-stimulated Ca2+ oscillations. J Biol Chem 290(30):18519–18533

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bergson P, Lipkind G, Lee SP, Duban M-E, Hanck DA (2011) Verapamil block of T-type calcium channels. Mol Pharmacol 79(3):411–419

    CAS  PubMed  PubMed Central  Google Scholar 

  • Berkefeld H, Fakler B, Schulte U (2010) Ca2+-activated K+ channels: from protein complexes to function. Physiol Rev 90(4):1437–1459

    CAS  PubMed  Google Scholar 

  • Berridge MJ (2006) Calcium microdomains: organization and function. Cell Calcium 40(5–6):405–412

    CAS  PubMed  Google Scholar 

  • Berridge MJ, Lipp P, Bootman MD (2000) The versatility and universality of calcium signalling: abstract: nature reviews molecular cell biology. Nat Rev Mol Cell 1(October):11–21

    CAS  Google Scholar 

  • Berridge MJ, Bootman MD, Llewelyn Roderick H (2003) Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 4(7):517–529

    CAS  PubMed  Google Scholar 

  • Bilmen JG, Wootton LL, Michelangeli F (2002) The mechanism of inhibition of the sarco/endoplasmic reticulum Ca2+ ATPase by paxilline. Arch Biochem Biophys 406(1):55–64

    CAS  PubMed  Google Scholar 

  • Bomben VC, Sontheimer HW (2008) Inhibition of transient receptor potential canonical channels impairs cytokinesis in human malignant gliomas. Cell Prolif 41(1):98–121

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bomben VC, Sontheimer H (2010) Disruption of transient receptor potential canonical channel 1 causes incomplete cytokinesis and slows the growth of human malignant gliomas. Glia 58(10):1145–1156

    PubMed  PubMed Central  Google Scholar 

  • Bomben VC, Turner KL, Barclay T-TC, Sontheimer H (2011) Transient receptor potential canonical channels are essential for chemotactic migration of human malignant gliomas. J Cell Physiol 226(7):1879–1888

    CAS  PubMed  Google Scholar 

  • Bordey A, Sontheimer H, Trouslard J (2000) Muscarinic activation of BK channels induces membrane oscillations in glioma cells and leads to inhibition of cell migration. J Membr Biol 176(1):31–40

    CAS  PubMed  Google Scholar 

  • Borowiec A-S, Bidaux G, Pigat N, Goffin V, Bernichtein S, Capiod T (2014) Calcium channels, external calcium concentration and cell proliferation. Eur J Pharmacol 739:19–25

    CAS  PubMed  Google Scholar 

  • Brennan CW, Verhaak RGW, McKenna A, Campos B, Noushmehr H, Salama SR, Zheng S, Chakravarty D, Sanborn JZ, Berman SH, Beroukhim R, Bernard B, Wu CJ, Genovese G, Shmulevich I, Barnholtz-Sloan J, Zou L, Vegesna R, Shukla SA, Ciriello G, Yung WK, Zhang W, Sougnez C, Mikkelsen T, Aldape K, Bigner DD, Van Meir EG, Prados M, Sloan A, Black KL, Eschbacher J, Finocchiaro G, Friedman W, Andrews DW, Guha A, Iacocca M, O’Neill BP, Foltz G, Myers J, Weisenberger DJ, Penny R, Kucherlapati R, Perou CM, Hayes DN, Gibbs R, Marra M, Mills GB, Lander ES, Spellman P, Wilson R, Sander C, Weinstein J, Meyerson M, Gabriel S, Laird PW, Haussler D, Getz G, Chin L, Benz C, Barrett W, Ostrom Q, Wolinsky Y, Bose B, Boulos PT, Boulos M, Brown J, Czerinski C, Eppley M, Kempista T, Kitko T, Koyfman Y, Rabeno B, Rastogi P, Sugarman M, Swanson P, Yalamanchii K, Otey IP, Liu YS, Xiao Y, Auman JT, Chen PC, Hadjipanayis A, Lee E, Lee S, Park PJ, Seidman J, Yang L, Kalkanis S, Poisson LM, Raghunathan A, Scarpace L, Bressler R, Eakin A, Iype L, Kreisberg RB, Leinonen K, Reynolds S, Rovira H, Thorsson V, Annala MJ, Paulauskis J, Curley E, Hatfield M, Mallery D, Morris S, Shelton T, Shelton C, Sherman M, Yena P, Cuppini L, DiMeco F, Eoli M, Maderna E, Pollo B, Saini M, Balu S, Hoadley KA, Li L, Miller CR, Shi Y, Topal MD, Wu J, Dunn G, Giannini C, Aksoy BA, Antipin Y, Borsu L, Cerami E, Gao J, Gross B, Jacobsen A, Ladanyi M, Lash A, Liang Y, Reva B, Schultz N, Shen R, Socci ND, Viale A, Ferguson ML, Chen QR, Demchok JA, Dillon LAL, Mills Shaw KR, Sheth M, Tarnuzzer R, Wang Z, Yang L, Davidsen T, Guyer MS, Ozenberger BA, Sofia HJ, Bergsten J, Eckman J, Harr J, Smith C, Tucker K, Winemiller C, Zach LA, Ljubimova JY, Eley G, Ayala B, Jensen MA, Kahn A, Pihl TD, Pot DA, Wan Y, Hansen N, Hothi P, Lin B, Shah N, Yoon JG, Lau C, Berens M, Ardlie K, Carter SL, Cherniack AD, Noble M, Cho J, Cibulskis K, DiCara D, Frazer S, Gabriel SB, Gehlenborg N, Gentry J, Heiman D, Kim J, Jing R, Lawrence M, Lin P, Mallard W, Onofrio RC, Saksena G, Schumacher S, Stojanov P, Tabak B, Voet D, Zhang H, Dees NN, Ding L, Fulton LL, Fulton RS, Kanchi KL, Mardis ER, Wilson RK, Baylin SB, Harshyne L, Cohen ML, Devine K, Sloan AE, Van Den Berg SR, Berger MS, Carlin D, Craft B, Ellrott K, Goldman M, Goldstein T, Grifford M, Singer MA, Sam NG, Stuart J, Swatloski T, Waltman P, Zhu J, Foss R, Frentzen B, McTiernan R, Yachnis A, Mao Y, Akbani R, Bogler O, Fuller GN, Liu W, Liu Y, Lu Y, Protopopov A, Ren X, Sun Y, Yung WKA, Zhang J, Chen K, Weinstein JN, Bootwalla MS, Lai PH, Triche TJ, Van Den Berg DJ, Gutmann DH, Lehman NL, Brat D, Olson JJ, Mastrogianakis GM, Devi NS, Zhang Z, Lipp E, McLendon R (2013) The somatic genomic landscape of glioblastoma. Cell 155(2):462

    CAS  PubMed  PubMed Central  Google Scholar 

  • Carafoli E (2002) Calcium signaling: a tale for all seasons. Proc Natl Acad Sci U S A 99(3):1115–1122

    CAS  PubMed  PubMed Central  Google Scholar 

  • Caramia M, Sforna L, Franciolini F, Catacuzzeno L (2019) The volume-regulated anion channel in glioblastoma. Cancers 11(3):307

    CAS  PubMed Central  Google Scholar 

  • Castle NA, London DO, Creech C, Fajloun Z, Stocker JW, Sabatier JM (2003) Maurotoxin: a potent inhibitor of intermediate conductance Ca2+-activated potassium channels. Mol Pharmacol 63(2):409–418

    CAS  PubMed  Google Scholar 

  • Catacuzzeno L, Franciolini F (2018) Role of KCa3.1 channels in modulating Ca2+ oscillations during glioblastoma cell migration and invasion. Int J Mol Sci 19(10):2970

    PubMed Central  Google Scholar 

  • Catacuzzeno L, Aiello F, Fioretti B, Sforna L, Castigli E, Ruggieri P, Tata AM, Calogero A, Franciolini F (2011) Serum-activated K and Cl currents underlay U87-MG glioblastoma cell migration. J Cell Physiol 226(7):1926–1933

    CAS  PubMed  Google Scholar 

  • Catacuzzeno L, Fioretti B, Franciolini F (2012) A theoretical study on the role of Ca2+-activated K+ channels in the regulation of hormone-induced Ca2+ oscillations and their synchronization in adjacent cells. J Theor Biol 309:103–112

    CAS  PubMed  Google Scholar 

  • Catacuzzeno L, Michelucci A, Sforna L, Aiello F, Sciaccaluga M, Fioretti B, Castigli E, Franciolini F (2014) Identification of key signaling molecules involved in the activation of the swelling-activated chloride current in human glioblastoma cells. J Membr Biol 247(1):45–55

    CAS  PubMed  Google Scholar 

  • Catacuzzeno L, Caramia M, Sforna L, Belia S, Guglielmi L, D’Adamo MC, Pessia M, Franciolini F (2015) Reconciling the discrepancies on the involvement of large-conductance Ca2+-activated K channels in glioblastoma cell migration. Front Cell Neurosci 9(APR):152

    PubMed  PubMed Central  Google Scholar 

  • Catterall WA (2011) Voltage-gated calcium channels. Cold Spring Harb Perspect Biol 3(8):1–23

    Google Scholar 

  • Chairoungdua A, Kanai Y, Matsuo H, Inatomi J, Kim DK, Endou H (2001) Identification and characterization of a novel member of the heterodimeric amino acid transporter family presumed to be associated with an unknown heavy chain. J Biol Chem 276(52):49390–49399

    CAS  PubMed  Google Scholar 

  • Chen C, Tao T, Cheng W, He W-Q, Qiao Y-N, Gao Y-Q, Chen X, Wang P, Chen C-P, Zhao W, Chen H-Q, Ye A-P, Peng Y-J, Zhu M-S (2014) Myosin light chain kinase (MLCK) regulates cell migration in a myosin regulatory light chain phosphorylation-independent mechanism. J Biol Chem 289(41):28478–28488

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng Y, Zhao J, Qiao W, Chen K (2014) Recent advances in diagnosis and treatment of gliomas using chlorotoxin-based bioconjugates. Am J Nucl Med Mol Imaging 4(5):385–405

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cheong A, Bingham AJ, Li J, Kumar B, Sukumar P, Munsch C, Buckley NJ, Neylon CB, Porter KE, Beech DJ, Wood IC (2005) Downregulated REST transcription factor is a switch enabling critical potassium channel expression and cell proliferation. Mol Cell 20(1):45–52

    CAS  PubMed  Google Scholar 

  • Chianale F, Cutrupi S, Rainero E, Baldanzi G, Porporato PE, Traini S, Filigheddu N, Gnocchi VF, Santoro MM, Parolini O, van Blitterswijk WJ, Sinigaglia F, Graziani A (2007) Diacylglycerol kinase-alpha mediates hepatocyte growth factor-induced epithelial cell scatter by regulating Rac activation and membrane ruffling. Mol Biol Cell 18(12):4859–4871

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chigurupati S, Venkataraman R, Barrera D, Naganathan A, Madan M, Paul L, Pattisapu JV, Kyriazis GA, Sugaya K, Bushnev S, Lathia JD, Rich JN, Chan SL (2010) Receptor channel TRPC6 is a key mediator of notch-driven glioblastoma growth and invasiveness. Cancer Res 70(1):418–427

    CAS  PubMed  Google Scholar 

  • Chuang HH, Prescott ED, Kong H, Shields S, Jordt SE, Basbaum AI, Chao MV, Julius D (2001) Bradykinin and nerve growth factor release the capsaicin receptor from PtdIns(4,5)P2-mediated inhibition. Nature 411(6840):957–962

    CAS  PubMed  Google Scholar 

  • Coleman N, Brown BM, Oliván-Viguera A, Singh V, Olmstead MM, Valero MS, Köhler R, Wulff H (2014) New positive Ca2+-activated K+ channel gating modulators with selectivity for KCa3.1. Mol Pharmacol 86(3):342–357

    PubMed  PubMed Central  Google Scholar 

  • Crunelli V, Tóth TI, Cope DW, Blethyn K, Hughes SW (2005) The “window” T-type calcium current in brain dynamics of different behavioural states. J Physiol 562(Pt 1):121–129

    CAS  PubMed  Google Scholar 

  • Cuddapah VA, Sontheimer H (2010) Molecular interaction and functional regulation of ClC-3 by Ca2+/calmodulin-dependent protein kinase II (CaMKII) in human malignant glioma. J Biol Chem 285(15):11188–11196

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cuddapah VA, Sontheimer H (2011) Ion channels and transporters [corrected] in cancer. 2. Ion channels and the control of cancer cell migration. Am J Physiol Cell Physiol 301(3):C541–C549

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cuddapah VA, Habela CW, Watkins S, Moore LS, Barclay TTC, Sontheimer H (2012) Kinase activation of ClC-3 accelerates cytoplasmic condensation during mitotic cell rounding. Am J Physiol Cell Physiol 302(3):C527–C538

    CAS  PubMed  Google Scholar 

  • Cuddapah VA, Turner KL, Sontheimer H (2013) Calcium entry via TRPC1 channels activates chloride currents in human glioma cells. Cell Calcium 53(3):187–194

    CAS  PubMed  Google Scholar 

  • D’Alessandro G, Catalano M, Sciaccaluga M, Chece G, Cipriani R, Rosito M, Grimaldi A, Lauro C, Cantore G, Santoro A, Fioretti B, Franciolini F, Wulff H, Limatola C (2013) KCa3.1 channels are involved in the infiltrative behavior of glioblastoma in vivo. Cell Death Dis 4:e773

    PubMed  PubMed Central  Google Scholar 

  • D’Alessandro G, Grimaldi A, Chece G, Porzia A, Esposito V, Santoro A, Salvati M, Mainiero F, Ragozzino D, Di Angelantonio S, Wulff H, Catalano M, Limatola C (2016) KCa3.1 channel inhibition sensitizes malignant gliomas to temozolomide treatment. Oncotarget 7(21):30781–30796

    PubMed  PubMed Central  Google Scholar 

  • D’Alessandro G, Monaco L, Catacuzzeno L, Antonangeli F, Santoro A, Esposito V, Franciolini F, Wulff H, Limatola C (2019) Radiation increases functional KCa3.1 expression and invasiveness in glioblastoma. Cancers 11(3):279

    PubMed Central  Google Scholar 

  • Danial NN, Korsmeyer SJ (2004) Cell death: critical control points. Cell 116(2):205–219

    CAS  PubMed  Google Scholar 

  • DeBin JA, Maggio JE, Strichartz GR (1993) Purification and characterization of chlorotoxin, a chloride channel ligand from the venom of the scorpion. Am J Physiol Cell Physiol 264(2 Pt 1):361–369

    Google Scholar 

  • Debska G, Kicinska A, Dobrucki J, Dworakowska B, Nurowska E, Skalska J, Dolowy K, Szewczyk A (2003) Large-conductance K+ channel openers NS1619 and NS004 as inhibitors of mitochondrial function in glioma cells. Biochem Pharmacol 65(11):1827–1834

    CAS  PubMed  Google Scholar 

  • Déliot N, Constantin B (2015) Plasma membrane calcium channels in cancer: alterations and consequences for cell proliferation and migration. Biochim Biophys Acta 1848(10 Pt B):2512–2522

    PubMed  Google Scholar 

  • Demuro A, Parker I (2006) Imaging single-channel calcium microdomains. Cell Calcium 40(5–6):413–422

    CAS  PubMed  PubMed Central  Google Scholar 

  • Deneka D, Sawicka M, Lam AKM, Paulino C, Dutzler R (2018) Structure of a volume-regulated anion channel of the LRRC8 family. Nature 558(7709):254–259

    CAS  PubMed  Google Scholar 

  • Deshane J, Garner CC, Sontheimer H (2003) Chlorotoxin inhibits glioma cell invasion via matrix metalloproteinase-2. J Biol Chem 278(6):4135–4144

    CAS  PubMed  Google Scholar 

  • Devor DC, Singh AK, Frizzell RA, Bridges RJ (1996) Modulation of Cl- secretion by benzimidazolones. I. Direct activation of a Ca(2+)-dependent K+ channel. Am J Phys 271(5 Pt 1):L775–L784

    CAS  Google Scholar 

  • Dickson EJ, Falkenburger BH, Hille B (2013) Quantitative properties and receptor reserve of the IP(3) and calcium branch of G(q)-coupled receptor signaling. J Gen Physiol 141(5):521–535

    CAS  PubMed  PubMed Central  Google Scholar 

  • Droogmans G, Prenen J, Eggermont J, Voets T, Nilius B (1998) Voltage-dependent block of endothelial volume-regulated anion channels by calix[4]arenes. Am J Phys 275(3):C646–C652

    CAS  Google Scholar 

  • Dupont G, Lokenye EFL, Challiss RAJ (2011) A model for Ca2+ oscillations stimulated by the type 5 metabotropic glutamate receptor: an unusual mechanism based on repetitive, reversible phosphorylation of the receptor. Biochimie 93(12):2132–2138

    CAS  PubMed  Google Scholar 

  • Dziegielewska B, Gray LS, Dziegielewski J (2014) T-type calcium channels blockers as new tools in cancer therapies. Pflugers Archiv Eur J Physiol 466(4):801–810

    CAS  Google Scholar 

  • Engbers JDT, Anderson D, Asmara H, Renata R, Hamish Mehaffey W, Hameed S, McKay BE, Kruskic M, Zamponi GW, Turner RW (2012) Intermediate conductance calcium-activated potassium channels modulate summation of parallel fiber input in cerebellar Purkinje cells. Proc Natl Acad Sci U S A 109(7):2601–2606

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ernest NJ, Sontheimer H (2007) Extracellular glutamine is a critical modulator for regulatory volume increase in human glioma cells. Brain Res 1144:231–238

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ernest NJ, Weaver AK, Van Duyn LB, Sontheimer HW (2005) Relative contribution of chloride channels and transporters to regulatory volume decrease in human glioma cells. Am J Physiol Cell Physiol 288(6):C1451–C1460

    CAS  PubMed  Google Scholar 

  • Ernest NJ, Habela CW, Sontheimer H (2008) Cytoplasmic condensation is both necessary and sufficient to induce apoptotic cell death. J Cell Sci 121(Pt 3):290–297

    CAS  PubMed  Google Scholar 

  • Fabian A, Fortmann T, Dieterich P, Riethmüller C, Schön P, Mally S, Nilius B, Schwab A (2008) TRPC1 channels regulate directionality of migrating cells. Pflugers Arch Eur J Physiol 457(2):475–484

    CAS  Google Scholar 

  • Fanger CM, Ghanshani S, Logsdon NJ, Rauer H, Kalman K, Zhou J, Kathy B, George Chandy K, Cahalan MD, Aiyar J (1999) Calmodulin mediates calcium-dependent activation of the intermediate conductance K(Ca) channel, IKCa1. J Biol Chem 274(9):5746–5754

    CAS  PubMed  Google Scholar 

  • Feustel PJ, Jin Y, Kimelberg HK (2004) Volume-regulated anion channels are the predominant contributors to release of excitatory amino acids in the ischemic cortical penumbra. Stroke 35(5):1164–1168

    CAS  PubMed  Google Scholar 

  • Fioretti B, Castigli E, Micheli MR, Bova R, Sciaccaluga M, Harper A, Franciolini F, Catacuzzeno L (2006) Expression and modulation of the intermediate- conductance Ca2+-activated K+ channel in glioblastoma GL-15 cells. Cell Physiol Biochem 18(1–3):47–56

    CAS  PubMed  Google Scholar 

  • Fioretti B, Catacuzzeno L, Sforna L, Aiello F, Pagani F, Ragozzino D, Castigli E, Franciolini F (2009) Histamine hyperpolarizes human glioblastoma cells by activating the intermediate-conductance Ca2+-activated K+ channel. Am J Physiol Cell Physiol 297(1)

    Google Scholar 

  • Foyouzi-Youssefi R, Arnaudeau S, Borner C, Kelley WL, Tschopp J, Lew DP, Demaurex N, Krause KH (2000) Bcl-2 decreases the free Ca2+ concentration within the endoplasmic reticulum. Proc Natl Acad Sci U S A 97(11):5723–5728

    CAS  PubMed  PubMed Central  Google Scholar 

  • Furukawa T, Nukada T, Namiki Y, Miyashita Y, Hatsuno K, Ueno Y, Yamakawa T, Isshiki T (2009) Five different profiles of dihydropyridines in blocking T-type Ca(2+) channel subtypes (Ca(v)3.1 (alpha(1G)), Ca(v)3.2 (alpha(1H)), and Ca(v)3.3 (alpha(1I))) expressed in xenopus oocytes. Eur J Pharmacol 613(1–3):100–107

    CAS  PubMed  Google Scholar 

  • Gaitán-Peñas H, Gradogna A, Laparra-Cuervo L, Solsona C, Fernández-Dueñas V, Barrallo-Gimeno A, Ciruela F, Lakadamyali M, Pusch M, Estévez R (2016) Investigation of LRRC8-mediated volume-regulated anion currents in xenopus oocytes. Biophys J 111(7):1429–1443

    PubMed  PubMed Central  Google Scholar 

  • Galizia L, Flamenco MP, Rivarola V, Capurro C, Ford P (2008) Role of AQP2 in activation of calcium entry by hypotonicity: implications in cell volume regulation. Am J Physiol Renal Physiol 294(3):F582–F590

    CAS  PubMed  Google Scholar 

  • Gaudet R (2008) TRP channels entering the structural era. J Physiol 586(15):3565–3575

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ge W, Ren J (2009) Combined L-/T-type calcium channel blockers: ready for prime time. Hypertension 53(4):592–594

    CAS  PubMed  Google Scholar 

  • Ge L, Hoa NT, Cornforth AN, Bota DA, Mai A, In Kim D, Chiou S-K, Hickey MJ, Kruse CA, Jadus MR (2012) Glioma big potassium channel expression in human cancers and possible T cell epitopes for their immunotherapy. J Immunol 189(5):2625–2634

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gees M, Owsianik G, Nilius B, Voets T (2012) TRP channels. Compr Physiol 2(1):563–608

    PubMed  Google Scholar 

  • Ghanshani S, Wulff H, Miller MJ, Rohm H, Neben A, Gutman GA, Cahalan MD, George Chandy K (2000) Up-regulation of the IKCa1 potassium channel during T-cell activation: molecular mechanism and functional consequences. J Biol Chem 275(47):37137–37149

    CAS  PubMed  Google Scholar 

  • Giangiacomo KM, Garcia ML, McManus OB (1992) Mechanism of iberiotoxin block of the large-conductance calcium-activated potassium channel from bovine aortic smooth muscle. Biochemistry 31(29):6719–6727

    CAS  PubMed  Google Scholar 

  • Gimple RC, Bhargava S, Dixit D, Rich JN (2019) Glioblastoma stem cells: lessons from the tumor hierarchy in a lethal cancer. Genes Dev 33(11–12):591–609

    CAS  PubMed  PubMed Central  Google Scholar 

  • González C, Baez-Nieto D, Valencia I, Oyarzún I, Rojas P, Naranjo D, Latorre R (2012) K+ channels: function-structural overview. Compr Physiol 2(3):2087–2149

    PubMed  Google Scholar 

  • Graves AR, Curran PK, Smith CL, Mindell JA (2008) The Cl-/H+ antiporter ClC-7 is the primary chloride permeation pathway in lysosomes. Nature 453(7196):788–792

    CAS  PubMed  Google Scholar 

  • Guéguinou M, ChantÔme A, Fromont G, Bougnoux P, Vandier C, Potier-Cartereau M (2014) KCa and Ca2+ channels: the complex thought. Biochim Biophys Acta Mol Cell Res 1843(10):2322–2333

    Google Scholar 

  • Günther W, Piwon N, Jentsch TJ (2003) The ClC-5 chloride channel knock-out mouse - an animal model for dent’s disease. Pflugers Arch Eur J Physiol 445(4):456–462

    Google Scholar 

  • Guzman RE, Grieschat M, Fahlke C, Alekov AK (2013) ClC-3 is an intracellular chloride/proton exchanger with large voltage-dependent nonlinear capacitance. ACS Chem Neurosci 4(6):994–1003

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guzman RE, Miranda-Laferte E, Franzen A, Fahlke C (2015) Neuronal ClC-3 splice variants differ in subcellular localizations, but mediate identical transport functions. J Biol Chem 290(43):25851–25862

    CAS  PubMed  PubMed Central  Google Scholar 

  • Habela CW, Sontheimer H (2007) Cytoplasmic volume condensation is an integral part of mitosis. Cell Cycle 6(13):1613–1620

    CAS  PubMed  Google Scholar 

  • Habela CW, Ernest NJ, Swindall AF, Sontheimer H (2009) Chloride accumulation drives volume dynamics underlying cell proliferation and migration. J Neurophysiol 101(2):750–757

    CAS  PubMed  Google Scholar 

  • Hajnóczky G, Davies E, Madesh M (2003) Calcium signaling and apoptosis. Biochem Biophys Res Commun 304(3):445–454

    PubMed  Google Scholar 

  • Hara-Chikuma M, Yang B, Sonawane ND, Sasaki S, Uchida S, Verkman AS (2005) ClC-3 chloride channels facilitate endosomal acidification and chloride accumulation. J Biol Chem 280(2):1241–1247

    CAS  PubMed  Google Scholar 

  • Hirose Y, Berger MS, Pieper RO (2001) Abrogation of the Chk1-mediated G(2) checkpoint pathway potentiates temozolomide-induced toxicity in a P53-independent manner in human glioblastoma cells. Cancer Res 61(15):5843–5849

    CAS  PubMed  Google Scholar 

  • Hite RK, Tao X, MacKinnon R (2017) Structural basis for gating the high-conductance Ca2+-activated K+ channel. Nature 541(7635):52–57

    CAS  PubMed  Google Scholar 

  • Hoffmann EK, Lambert IH, Pedersen SF (2009) Physiology of cell volume regulation in vertebrates. Physiol Rev 89(1):193–277

    CAS  PubMed  Google Scholar 

  • Holt MEV, King SA, Cala PM, Pedersen SF (2006) Regulation of the Pleuronectes americanus Na+/H+ exchanger by osmotic shrinkage, β-adrenergic stimuli, and inhibition of Ser/Thr protein phosphatases. Cell Biochem Biophys 45(1):1–18

    CAS  PubMed  Google Scholar 

  • Hyzinski-García MC, Rudkouskaya A, Mongin AA (2014) LRRC8A protein is indispensable for swelling-activated and ATP-induced release of excitatory amino acids in rat astrocytes. J Physiol 592(22):4855–4862

    PubMed  PubMed Central  Google Scholar 

  • Iamshanova O, Pla AF, Prevarskaya N (2017) Molecular mechanisms of tumour invasion: regulation by calcium signals. J Physiol 595(10):3063–3075

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ise T, Shimizu T, Lee EL, Inoue H, Kohno K, Okada Y (2005) Roles of volume-sensitive Cl- channel in cisplatin-induced apoptosis in human epidermoid cancer cells. J Membr Biol 205(3):139–145

    CAS  PubMed  Google Scholar 

  • Ishii TM, Silvia C, Hirschberg B, Bond CT, Adelman JP, Maylie J (1997) A human intermediate conductance calcium-activated potassium channel. Proc Natl Acad Sci U S A 94(21):11651–11656

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jantaratnotai N, McLarnon JG (2011) Calcium dependence of purinergic subtype P2Y1 receptor modulation of C6 glioma cell migration. Neurosci Lett 497(2):80–84

    CAS  PubMed  Google Scholar 

  • Jentsch TJ (2007) Chloride and the endosomal-lysosomal pathway: emerging roles of CLC chloride transporters. J Physiol 578(3):633–640

    CAS  PubMed  Google Scholar 

  • Jentsch TJ, Pusch M (2018) CLC chloride channels and transporters: structure, function, physiology, and disease. Physiol Rev 98(3):1493–1590

    CAS  PubMed  Google Scholar 

  • Jentsch TJ, Steinmeyer K, Schwarz G (1990) Primary structure of Torpedo marmorata chloride channel isolated by expression cloning in xenopus oocytes. Nature 348(6301):510–514

    CAS  PubMed  Google Scholar 

  • Jiang Y, Pico A, Cadene M, Chait BT, MacKinnon R (2001) Structure of the RCK domain from the E. coli K+ channel and demonstration of its presence in the human BK channel. Neuron 29(3):593–601

    CAS  PubMed  Google Scholar 

  • Joiner WJ, Wang LUY, Tang MD, Kaczmarek LK (1997) HSK4, a member of a novel subfamily of calcium-activated potassium channels. Proc Natl Acad Sci U S A 94(20):11013–11018

    CAS  PubMed  PubMed Central  Google Scholar 

  • Joseph SK, Hajnóczky G (2007) IP3 receptors in cell survival and apoptosis: Ca2+ release and beyond. Apoptosis 12(5):951–968

    CAS  PubMed  Google Scholar 

  • Joseph JV, Van Roosmalen IAM, Busschers E, Tomar T, Conroy S, Eggens-Meijer E, Fajardo NP, Pore MM, Balasubramanyian V, Wagemakers M, Copray S, Den Dunnen WFA, Kruyt FAE (2015) Serum-induced differentiation of glioblastoma neurospheres leads to enhanced migration/invasion capacity that is associated with increased MMP9. PLoS One 10(12)

    Google Scholar 

  • Kaczmarek LK, Aldrich RW, George Chandy K, Grissmer S, Wei AD, Wulff H (2017) International union of basic and clinical pharmacology. C. Nomenclature and properties of calcium-activated and sodium-activated potassium channels. Pharmacol Rev 69(1):1–11

    CAS  PubMed  Google Scholar 

  • Kang YJ, Kim IY, Kim EH, Yoon MJ, Kim SU, Kwon TK, Choi KS (2011) Paxilline enhances TRAIL-mediated apoptosis of glioma cells via modulation of c-FLIP, survivin and DR5. Exp Mol Med 43(1):24–34

    CAS  PubMed  Google Scholar 

  • Kanzawa T, Germano IM, Komata T, Ito H, Kondo Y, Kondo S (2004) Role of autophagy in temozolomide-induced cytotoxicity for malignant glioma cells. Cell Death Differ 11(4):448–457

    CAS  PubMed  Google Scholar 

  • Kaushal V, Koeberle PD, Wang Y, Schlichter LC (2007) The Ca2+-activated K+ channel KCNN4/KCa3.1 contributes to microglia activation and nitric oxide-dependent neurodegeneration. J Neurosci 27(1):234–244

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kefauver JM, Saotome K, Dubin AE, Pallesen J, Cottrell CA, Cahalan SM, Qiu Z, Hong G, Crowley CS, Whitwam T, Lee WH, Ward AB, Patapoutian A (2018) Structure of the human volume regulated anion channel. Elife 7

    Google Scholar 

  • Keizer J, Li YX, Stojilković S, Rinzel J (1995) InsP3-induced Ca2+ excitability of the endoplasmic reticulum. Mol Biol Cell 6(8):945–951

    CAS  PubMed  PubMed Central  Google Scholar 

  • Klumpp D, Frank SC, Klumpp L, Sezgin EC, Eckert M, Edalat L, Bastmeyer M, Zips D, Ruth P, Huber SM (2017) TRPM8 is required for survival and radioresistance of glioblastoma cells. Oncotarget 8(56):95896–95913

    PubMed  PubMed Central  Google Scholar 

  • Komuro H, Kumada T (2005) Ca2+ transients control CNS neuronal migration. Cell Calcium 37(5):387–393

    CAS  PubMed  Google Scholar 

  • Kovalevskaya NV, Bokhovchuk FM, Vuister GW (2012) The TRPV5/6 calcium channels contain multiple calmodulin binding sites with differential binding properties. J Struct Funct Genom 13(2):91–100

    CAS  Google Scholar 

  • Kraft R, Krause P, Jung S, Basrai D, Liebmann L, Bolz J, Patt S (2003) BK channel openers inhibit migration of human glioma cells. Pflugers Arch Eur J Physiol 446(2):248–255

    CAS  Google Scholar 

  • Lang F, Busch GL, Ritter M, Völkl H, Waldegger S, Gulbins E, Häussinger D (1998) Functional significance of cell volume regulatory mechanisms. Physiol Rev 78(1):247–306

    CAS  PubMed  Google Scholar 

  • Lang F, Lang KS, Wieder T, Myssina S, Birka C, Lang PA, Kaiser S, Kempe D, Duranton C, Huber SM (2003) Cation channels, cell volume and the death of an erythrocyte. Pflugers Arch Eur J Physiol 447(2):121–125

    CAS  Google Scholar 

  • Launay P, Fleig A, Perraud AL, Scharenberg AM, Penner R, Kinet JP (2002) TRPM4 is a Ca2+-activated nonselective cation channel mediating cell membrane depolarization. Cell 109(3):397–407

    CAS  PubMed  Google Scholar 

  • Lee C-H, MacKinnon R (2018) Activation mechanism of a human SK-calmodulin channel complex elucidated by cryo-EM structures. Science 360(6388):508–513

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lee EL, Shimizu T, Ise T, Numata T, Kohno K, Okada Y (2007) Impaired activity of volume-sensitive Cl- channel is involved in cisplatin resistance of cancer cells. J Cell Physiol 211(2):513–521

    CAS  PubMed  Google Scholar 

  • Leist M, Single B, Castoldi AF, Kühnle S, Nicotera P (1997) Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis. J Exp Med 185(8):1481–1486

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lepannetier S, Zanou N, Yerna X, Emeriau N, Dufour I, Masquelier J, Muccioli G, Tajeddine N, Gailly P (2016) Sphingosine-1-phosphate-activated TRPC1 channel controls chemotaxis of glioblastoma cells. Cell Calcium 60(6):373–383

    CAS  PubMed  Google Scholar 

  • Li N, Wang C, Wu Y, Liu X, Cao X (2009) Ca2+/calmodulin-dependent protein kinase II promotes cell cycle progression by directly activating MEK1 and subsequently modulating P27 phosphorylation. J Biol Chem 284(5):3021–3027

    CAS  PubMed  Google Scholar 

  • Lippiat JD, Standen NB, Harrow ID, Phillips SC, Davies NW (2003) Properties of BK(Ca) channels formed by bicistronic expression of HSloalpha and Beta1-4 subunits in HEK293 cells. J Membr Biol 192(2):141–148

    CAS  PubMed  Google Scholar 

  • Liu T, Stauber T (2019) The volume-regulated anion channel LRRC8/VRAC is dispensable for cell proliferation and migration. Int J Mol Sci 20(11)

    Google Scholar 

  • Liu X, Chang Y, Reinhart PH, Sontheimer H (2002) Cloning and characterization of glioma BK, a novel BK channel isoform highly expressed in human glioma cells. J Neurosci 22(5):1840–1849

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lukacs V, Thyagarajan B, Varnai P, Balla A, Balla T, Rohacs T (2007) Dual regulation of TRPV1 by phosphoinositides. J Neurosci 27(26):7070–7080

    CAS  PubMed  PubMed Central  Google Scholar 

  • MacKinnon R, Miller C (1988) Mechanism of charybdotoxin block of the high-conductance, Ca2+−activated K+ channel. J Gen Physiol 91(3):335–349

    CAS  PubMed  Google Scholar 

  • Maeno E, Ishizaki Y, Kanaseki T, Hazama A, Okada Y (2000) Normotonic cell shrinkage because of disordered volume regulation is an early prerequisite to apoptosis. Proc Natl Acad Sci U S A 97(17):9487–9492

    CAS  PubMed  PubMed Central  Google Scholar 

  • Maertens C, Droogmans G, Chakraborty P, Nilius B (2001) Inhibition of volume-regulated anion channels in cultured endothelial cells by the anti-oestrogens clomiphene and nafoxidine. Br J Pharmacol 132(1):135–142

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mak DOD, McBride S, Foskett JK (1998) Inositol 1,4,5-tris-phosphate activation of inositol tris-phosphate receptor Ca2+ channel by ligand tuning of Ca2+ inhibition. Proc Natl Acad Sci U S A 95(26):15821–15825

    CAS  PubMed  PubMed Central  Google Scholar 

  • Manning TJ, Parker JC, Sontheimer H (2000) Role of lysophosphatidic acid and rho in glioma cell motility. Cell Motil Cytoskeleton 45(3):185–199

    CAS  PubMed  Google Scholar 

  • Mao J, Chen L, Xu B, Wang L, Li H, Guo J, Li W, Nie S, Jacob TJC, Wang L (2008) Suppression of ClC-3 channel expression reduces migration of nasopharyngeal carcinoma cells. Biochem Pharmacol 75(9):1706–1716

    CAS  PubMed  Google Scholar 

  • Mariggio MA, Mazzoleni G, Pietrangelo T, Guarnieri S, Morabito C, Steimberg N, Fano G (2001) Calcium-mediated transductive systems and functionally active gap junctions in astrocyte-like GL15 cells. BMC Physiol 1:4

    CAS  PubMed  PubMed Central  Google Scholar 

  • Matsuda JJ, Filali MS, Volk KA, Collins MM, Moreland JG, Lamb FS (2008) Overexpression of CLC-3 in HEK293T cells yields novel currents that are PH dependent. Am J Physiol Cell Physiol 294(1)

    Google Scholar 

  • McCoy E, Sontheimer H (2007) Expression and function of water channels (aquaporins) in migrating malignant astrocytes. Glia 55(10):1034–1043

    PubMed  PubMed Central  Google Scholar 

  • Meera P, Wallner M, Song M, Toro L (1997) Large conductance voltage- and calcium-dependent K+ channel, a distinct member of voltage-dependent ion channels with seven N-terminal transmembrane segments (SO-S6), an extracellular N terminus, and an intracellular (S9-S10) C terminus. Proc Natl Acad Sci U S A 94(25):14066–14071

    CAS  PubMed  PubMed Central  Google Scholar 

  • Milenkovic A, Brandl C, Milenkovic VM, Jendryke T, Sirianant L, Wanitchakool P, Zimmermann S, Reiff CM, Horling F, Schrewe H, Schreiber R, Kunzelmann K, Wetzel CH, Weber BHF (2015) Bestrophin 1 is indispensable for volume regulation in human retinal pigment epithelium cells. Proc Natl Acad Sci U S A 112(20):E2630–E2639

    CAS  PubMed  PubMed Central  Google Scholar 

  • Min XJ, Li H, Hou SC, He W, Liu J, Hu B, Wang J (2011) Dysfunction of volume-sensitive chloride channels contributes to cisplatin resistance in human lung adenocarcinoma cells. Exp Biol Med 236(4):483–491

    CAS  Google Scholar 

  • Minton K (2014) Cell migration: coordinating calcium signalling. Nat Rev Mol Cell Biol 15(3):152

    CAS  PubMed  Google Scholar 

  • Montana V, Sontheimer H (2011) Bradykinin promotes the chemotactic invasion of primary brain tumors. J Neurosci 31(13):4858–4867

    CAS  PubMed  PubMed Central  Google Scholar 

  • Monteith GR, Davis FM, Roberts-Thomson SJ (2012) Calcium channels and pumps in cancer: changes and consequences. J Biol Chem 287(38):31666–31673

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nilius B, Szallasi A (2014) Transient receptor potential channels as drug targets: from the science of basic research to the art of medicine. Pharmacol Rev 66(3):676–814

    PubMed  Google Scholar 

  • Nilius B, Prenen J, Kamouchi M, Viana F, Voets T, Droogmans G (1997) Inhibition by mibefradil, a novel calcium channel antagonist, of Ca(2+)- and volume-activated Cl- channels in macrovascular endothelial cells. Br J Pharmacol 121(3):547–555

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nilius B, Prenen J, Janssens A, Owsianik G, Wang C, Zhu MX, Voets T (2005) The selectivity filter of the cation channel TRPM4. J Biol Chem 280(24):22899–22906

    CAS  PubMed  Google Scholar 

  • Numata T, Shimizu T, Okada Y (2007) TRPM7 is a stretch- and swelling-activated cation channel involved in volume regulation in human epithelial cells. Am J Physiol Cell Physiol 292(1):C460–C467

    CAS  PubMed  Google Scholar 

  • Núñez R, Sancho-Martínez SM, Novoa JML, López-Hernández FJ (2010) Apoptotic volume decrease as a geometric determinant for cell dismantling into apoptotic bodies. Cell Death Differ 17(11):1665–1671

    PubMed  Google Scholar 

  • Okada T, Akita T, Sato-Numata K, Islam MR, Okada Y (2014) A newly cloned ClC-3 isoform, ClC-3d, as well as ClC-3a mediates Cd-sensitive outwardly rectifying anion currents. Cell Physiol Biochem 33(3):539–556

    CAS  PubMed  Google Scholar 

  • Olesen SP, Munch E, Moldt P, Drejer J (1994) Selective activation of Ca(2+)-dependent K+ channels by novel benzimidazolone. Eur J Pharmacol 251(1):53–59

    CAS  PubMed  Google Scholar 

  • Olsen ML, Schade S, Lyons SA, Amaral MD, Sontheimer H (2003) Expression of voltage-gated chloride channels in human glioma cells. J Neurosci 23(13):5572–5582

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ostrom QT, Bauchet L, Davis FG, Deltour I, Fisher JL, Langer CE, Pekmezci M, Schwartzbaum JA, Turner MC, Walsh KM, Wrensch MR, Barnholtz-Sloan JS (2015) Response to “the epidemiology of glioma in adults: a ‘state of the science’ review”. Neuro-Oncology 17(4):624–626

    PubMed  PubMed Central  Google Scholar 

  • Parekh AB (2011) Decoding cytosolic Ca2+ oscillations. Trends Biochem Sci 36(2):78–87

    CAS  PubMed  Google Scholar 

  • Parkash J, Asotra K (2010) Calcium wave signaling in cancer cells. Life Sci 87(19–22):587–595

    CAS  PubMed  PubMed Central  Google Scholar 

  • Parsons DW, Jones S, Zhang X, Lin JCH, Leary RJ, Angenendt P, Mankoo P, Hannah C, Mei Siu I, Gallia GL, Olivi A, Roger ML, Ahmed Rasheed B, Keir S, Nikolskaya T, Nikolsky Y, Busam DA, Tekleab H, Diaz LA, Hartigan J, Smith DR, Strausberg RL, Marie SKN, Shinjo SMO, Yan H, Riggins GJ, Bigner DD, Karchin R, Papadopoulos N, Parmigiani G, Vogelstein B, Velculescu VE, Kenneth W. Kinzler. (2008) An integrated genomic analysis of human glioblastoma multiforme. Science 321(5897):1807–1812

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pedersen EA, Menon R, Bailey KM, Thomas DG, Van Noord RA, Tran J, Wang H, Ping Ping Q, Hoering A, Fearon ER, Chugh R, Lawlor ER (2016) Activation of Wnt/b-catenin in Ewing sarcoma cells antagonizes EWS/ETS function and promotes phenotypic transition to more metastatic cell states. Cancer Res 76(17):5040–5053

    CAS  PubMed  PubMed Central  Google Scholar 

  • Peña TL, Chen SH, Konieczny SF, Rane SG (2000) Ras/MEK/ERK up-regulation of the fibroblast K(Ca) channel FIK is a common mechanism for basic fibroblast growth factor and transforming growth factor-$β$ suppression of myogenesis. J Biol Chem 275(18):13677–13682

    PubMed  Google Scholar 

  • Perez-Reyes E (2003) Molecular physiology of low-voltage-activated T-type calcium channels. Physiol Rev 83(1):117–161

    CAS  PubMed  Google Scholar 

  • Perez-Reyes E, Van Deusen AL, Vitko I (2009) Molecular pharmacology of human Cav3.2 T-type Ca2+ channels: block by antihypertensives, antiarrhythmics, and their analogs. J Pharmacol Exp Ther 328(2):621–627

    CAS  PubMed  Google Scholar 

  • Picollo A, Pusch M (2005) Chloride/proton antiporter activity of mammalian CLC proteins ClC-4 and ClC-5. Nature 436(7049):420–423

    CAS  PubMed  Google Scholar 

  • Pinton P, Rizzuto R (2006) Bcl-2 and Ca2+ homeostasis in the endoplasmic reticulum. Cell Death Differ 13(8):1409–1418

    CAS  PubMed  Google Scholar 

  • Planells-Cases R, Lutter D, Guyader C, Gerhards NM, Ullrich F, Elger DA, Kucukosmanoglu A, Xu G, Voss FK, Momsen Reincke S, Stauber T, Blomen VA, Vis DJ, Wessels LF, Brummelkamp TR, Borst P, Rottenberg S, Jentsch TJ (2015) Subunit composition of VRAC channels determines substrate specificity and cellular resistance to Pt-based anti-cancer drugs. EMBO J 34(24):2993–3008

    CAS  PubMed  PubMed Central  Google Scholar 

  • Poulsen KA, Andersen EC, Hansen CF, Klausen TK, Hougaard C, Lambert IH, Hoffmann EK (2010) Deregulation of apoptotic volume decrease and ionic movements in multidrug-resistant tumor cells: role of chloride channels. Am J Physiol Cell Physiol 298(1):C14–C25

    CAS  PubMed  Google Scholar 

  • Prevarskaya N, Ouadid-Ahidouch H, Skryma R, Shuba Y (2014) Remodelling of Ca2+ transport in Cancer: how it contributes to Cancer hallmarks? Philos Trans R Soc Lond Ser B Biol Sci 369(1638):20130097

    Google Scholar 

  • Priebe L, Friedrich M, Benndorf K (1996) Functional interaction between K(ATP) channels and the Na(+)-K(+) pump in metabolically inhibited heart cells of the Guinea-pig. J Physiol 492(Pt 2):405–417

    CAS  PubMed  PubMed Central  Google Scholar 

  • Qin C, He B, Dai W, Lin Z, Zhang H, Wang X, Wang J, Zhang X, Wang G, Yin L, Zhang Q (2014) The impact of a chlorotoxin-modified liposome system on receptor MMP-2 and the receptor-associated protein ClC-3. Biomaterials 35(22):5908–5920

    CAS  PubMed  Google Scholar 

  • Qiu Z, Dubin AE, Mathur J, Buu T, Reddy K, Miraglia LJ, Reinhardt J, Orth AP, Patapoutian A (2014) SWELL1, a plasma membrane protein, is an essential component of volume-regulated anion channel. Cell 157(2):447–458

    CAS  PubMed  PubMed Central  Google Scholar 

  • Quast S-A, Berger A, Buttstädt N, Friebel K, Schönherr R, Eberle J (2012) General sensitization of melanoma cells for TRAIL-induced apoptosis by the potassium channel inhibitor TRAM-34 depends on release of SMAC. PLoS One 7(6):e39290

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rampling R, Cruickshank G, Lewis AD, Fitzsimmons SA, Workman P (1994) Direct measurement of PO2 distribution and bioreductive enzymes in human malignant brain tumors. Int J Radiat Oncol Biol Phys 29(3):427–431

    CAS  PubMed  Google Scholar 

  • Ransom CB, Sontheimer H (2001) BK channels in human glioma cells. J Neurophysiol 85(2):790–803

    CAS  PubMed  Google Scholar 

  • Ransom CB, O’Neal JT, Sontheimer H (2001) Volume-activated chloride currents contribute to the resting conductance and invasive migration of human glioma cells. J Neurosci 21(19):7674–7683

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ransom CB, Liu X, Sontheimer H (2002) BK channels in human glioma cells have enhanced calcium sensitivity. Glia 38(4):281–291

    PubMed  Google Scholar 

  • Robert SM, Sontheimer H (2014) Glutamate transporters in the biology of malignant gliomas. Cell Mol Life Sci CMLS 71(10):1839–1854

    CAS  PubMed  Google Scholar 

  • Rondé P, Giannone G, Gerasymova I, Stoeckel H, Takeda K, Haiech J (2000) Mechanism of calcium oscillations in migrating human astrocytoma cells. Biochim Biophys Acta Mol Cell Res 1498(2–3):273–280

    Google Scholar 

  • Rosa P, Sforna L, Carlomagno S, Mangino G, Miscusi M, Pessia M, Franciolini F, Calogero A, Catacuzzeno L (2017) Overexpression of large-conductance calcium-activated potassium channels in human glioblastoma stem-like cells and their role in cell migration. J Cell Physiol 232(9):2478–2488

    CAS  PubMed  Google Scholar 

  • Rothstein JD, Dykes-Hoberg M, Pardo CA, Bristol LA, Lin J, Kuncl RW, Kanai Y, Hediger MA, Wang Y, Schielke JP, Welty DF (1996) Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 16(3):675–686

    CAS  PubMed  Google Scholar 

  • Rouzaire-Dubois B, Milandri JB, Bostel S, Dubois JM (2000) Control of cell proliferation by cell volume alterations in rat C6 glioma cells. Pflugers Arch Eur J Physiol 440(6):881–888

    CAS  Google Scholar 

  • Ruggieri P, Mangino G, Fioretti B, Catacuzzeno L, Puca R, Ponti D, Miscusi M, Franciolini F, Ragona G, Calogero A (2012) The inhibition of KCa3.1 channels activity reduces cell motility in glioblastoma derived cancer stem cells. PLoS One 7(10):e47825

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sanchez M, McManus OB (1996) Paxilline inhibition of the alpha-subunit of the high-conductance calcium-activated potassium channel. Neuropharmacology 35(7):963–968

    CAS  PubMed  Google Scholar 

  • Scheel O, Zdebik AA, Lourdel S, Jentsch TJ (2005) Voltage-dependent electrogenic chloride/proton exchange by endosomal CLC proteins. Nature 436(7049):424–427

    CAS  PubMed  Google Scholar 

  • Schreiber M, Salkoff L (1997) A novel calcium-sensing domain in the BK channel. Biophys J 73(3):1355–1363

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schwab A, Stock C (2014) Ion channels and transporters in tumour cell migration and invasion. Philos Trans R Soc Lond Ser B Biol Sci 369(1638):20130102

    Google Scholar 

  • Schwab A, Wojnowski L, Gabriel K, Oberleithner H (1994) Oscillating activity of a Ca(2+)-sensitive K+ channel. A prerequisite for migration of transformed Madin-Darby canine kidney focus cells. J Clin Invest 93(4):1631–1636

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schwab A, Nechyporuk-Zloy V, Fabian A, Stock C (2007) Cells move when ions and water flow. Pflugers Arch Eur J Physiol 453(4):421–432

    CAS  Google Scholar 

  • Schwab A, Fabian A, Hanley PJ, Stock C (2012) Role of ion channels and transporters in cell migration. Physiol Rev 92(4):1865–1913

    CAS  PubMed  Google Scholar 

  • Schwaller B (2010) Cytosolic Ca2+ buffers. Cold Spring Harb Perspect Biol 2(11):a004051

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 (2010) CXCL12-induced glioblastoma cell migration requires intermediate conductance Ca2+-activated K+ channel activity. Am J Physiol Cell Physiol 299(1):C175–C184

    CAS  PubMed  Google Scholar 

  • Sforna L, Cenciarini M, Belia S, D’Adamo MC, Pessia M, Franciolini F, Catacuzzeno L (2014) The role of ion channels in the hypoxia-induced aggressiveness of glioblastoma. Front Cell Neurosci 8:467

    PubMed  Google Scholar 

  • Sforna L, Cenciarini M, Belia S, Michelucci A, Pessia M, Franciolini F, Catacuzzeno L (2017) Hypoxia modulates the swelling-activated cl current in human glioblastoma cells: role in volume regulation and cell survival. J Cell Physiol 232(1):91–100

    CAS  PubMed  Google Scholar 

  • Singh S, Syme CA, Singh AK, Devor DC, Bridges RJ (2001) Benzimidazolone activators of chloride secretion: potential therapeutics for cystic fibrosis and chronic obstructive pulmonary disease. J Pharmacol Exp Ther 296(2):600–611

    CAS  PubMed  Google Scholar 

  • Sirianant L, Wanitchakool P, Ousingsawat J, Benedetto R, Zormpa A, Cabrita I, Schreiber R, Kunzelmann K (2016) Non-essential contribution of LRRC8A to volume regulation. Pflugers Arch Eur J Physiol 468(5):805–816

    CAS  Google Scholar 

  • Sontheimer H (2008) An unexpected role for ion channels in brain tumor metastasis. Exp Biol Med 233(7):779–791

    CAS  Google Scholar 

  • Soroceanu L, Yancey G, Khazaeli MB, Sontheimer H (1998) Use of chlorotoxin for targeting of primary brain tumors. Cancer Res 58(21):4871–4879

    CAS  PubMed  Google Scholar 

  • Soroceanu L, Manning TJ, Sontheimer H (1999) Modulation of glioma cell migration and invasion using Cl- and K+ ion channel blockers. J Neurosci 19(14):5942–5954

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stauber T, Weinert S, Jentsch TJ (2012) Cell biology and physiology of CLC chloride channels and transporters. Compr Physiol 2(3):1701–1744

    PubMed  Google Scholar 

  • Stegen B, Butz L, Klumpp L, Zips D, Dittmann K, Ruth P, Huber SM (2015) Ca2+-activated IK K+ channel blockade radiosensitizes glioblastoma cells. Mol Cancer Res 13(9):1283–1295

    CAS  PubMed  Google Scholar 

  • Steinbach JP, Wolburg H, Klumpp A, Probst H, Weller M (2003) Hypoxia-induced cell death in human malignant glioma cells: energy deprivation promotes decoupling of mitochondrial cytochrome c release from caspase processing and necrotic cell death. Cell Death Differ 10(7):823–832

    CAS  PubMed  Google Scholar 

  • Steinle M, Palme D, Misovic M, Rudner J, Dittmann K, Lukowski R, Ruth P, Huber SM (2011) Ionizing radiation induces migration of glioblastoma cells by activating BK K(+) channels. Radiother Oncol 101(1):122–126

    CAS  PubMed  Google Scholar 

  • Steinmeyer K, Ortland C, Jentsch TJ (1991) Primary structure and functional expression of a developmentally regulated skeletal muscle chloride channel. Nature 354(6351):301–304

    CAS  PubMed  Google Scholar 

  • Stobrawa SM, Breiderhoff T, Takamori S, Engel D, Schweizer M, Zdebik AA, Bösl MR, Ruether K, Jahn H, Draguhn A, Jahn R, Jentsch TJ (2001) Disruption of CIC-3, a chloride channel expressed on synaptic vesicles, leads to a loss of the hippocampus. Neuron 29(1):185–196

    CAS  PubMed  Google Scholar 

  • Strange K, Yamada T, Denton JS (2019) A 30-year journey from volume-regulated anion currents to molecular structure of the LRRC8 channel. J Gen Physiol 151(2):100–117

    CAS  PubMed  PubMed Central  Google Scholar 

  • Strøbaek D, Teuber L, Jørgensen TD, Ahring PK, Kjaer K, Hansen RS, Olesen SP, Christophersen P, Skaaning-Jensen B (2004) Activation of human IK and SK Ca2+ −activated K+ channels by NS309 (6,7-Dichloro-1H-Indole-2,3-Dione 3-Oxime). Biochim Biophys Acta 1665(1–2):1–5

    PubMed  Google Scholar 

  • Stupp R, van den Bent MJ, Hegi ME (2005a) Optimal role of temozolomide in the treatment of malignant gliomas. Curr Neurol Neurosci Rep 5(3):198–206

    CAS  PubMed  Google Scholar 

  • Stupp R, Mason WP, Van Den Bent MJ, Weller M, Fisher B, Taphoorn MJB, Belanger K, Brandes AA, Marosi C, Bogdahn U, Curschmann J, Janzer RC, Ludwin SK, Gorlia T, Allgeier A, Lacombe D, Cairncross JG, Eisenhauer E, Mirimanoff RO (2005b) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352(10):987–996

    CAS  PubMed  Google Scholar 

  • Stupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJB, Janzer RC, Ludwin SK, Allgeier A, Fisher B, Belanger K, Hau P, Brandes AA, Gijtenbeek J, Marosi C, Vecht CJ, Mokhtari K, Wesseling P, Villa S, Eisenhauer E, Gorlia T, Weller M, Lacombe D, Cairncross JG, Mirimanoff RO (2009) Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol 10(5):459–466

    CAS  PubMed  Google Scholar 

  • Syeda R, Qiu Z, Dubin AE, Murthy SE, Florendo MN, Mason DE, Mathur J, Cahalan SM, Peters EC, Montal M, Patapoutian A (2016) LRRC8 proteins form volume-regulated anion channels that sense ionic strength. Cell 164(3):499–511

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tao X, Hite RK, MacKinnon R (2017) Cryo-EM structure of the open high-conductance Ca2+−activated K+ channel. Nature 541(7635):46–51

    CAS  PubMed  Google Scholar 

  • Taylor CW, Laude AJ (2002) IP3 receptors and their regulation by calmodulin and cytosolic Ca2+. Cell Calcium 32(5–6):321–334

    CAS  PubMed  Google Scholar 

  • Taylor CW, Thorn P (2001) Calcium signalling: IP3 rises again... and again. Curr Biol 11(9)

    Google Scholar 

  • Ternovsky VI, Okada Y, Sabirov RZ (2004) Sizing the pore of the volume-sensitive anion channel by differential polymer partitioning. FEBS Lett 576(3):433–436

    CAS  PubMed  Google Scholar 

  • Thore S, Dyachok O, Tengholm A (2004) Oscillations of phospholipase C activity triggered by depolarization and Ca2+ influx in insulin-secreting cells. J Biol Chem 279(19):19396–19400

    CAS  PubMed  Google Scholar 

  • Turner KL, Sontheimer H (2014) Cl- and K+ channels and their role in primary brain tumour biology. Philos Trans R Soc B Biol Sci 369(1638)

    Google Scholar 

  • Turner KL, Honasoge A, Robert SM, McFerrin MM, Sontheimer H (2014) A proinvasive role for the Ca(2+) -activated K(+) channel KCa3.1 in malignant glioma. Glia 62(6):971–981

    PubMed  PubMed Central  Google Scholar 

  • Turner RW, Asmara H, Engbers JDT, Miclat J, Rizwan AP, Sahu G, Zamponi GW (2016) Assessing the role of IKCa channels in generating the SAHP of CA1 hippocampal pyramidal cells. Channels 10(4):313–319

    PubMed  PubMed Central  Google Scholar 

  • Valerie NCK, Dziegielewska B, Hosing AS, Augustin E, Gray LS, Brautigan DL, Larner JM, Dziegielewski J (2013) Inhibition of T-type calcium channels disrupts Akt signaling and promotes apoptosis in glioblastoma cells. Biochem Pharmacol 85(7):888–897

    CAS  PubMed  Google Scholar 

  • Vandorpe DH, Shmukler BE, Jiang L, Lim B, Maylie J, Adelman JP, De Franceschi L, Domenica Cappellini M, Brugnara C, Alper SL (1998) CDNA cloning and functional characterization of the mouse Ca2+-gated K+ channel, MIK1. J Biol Chem 273(34):21542–21553

    CAS  PubMed  Google Scholar 

  • Vennekens R, Hoenderop JGJ, Prenen J, Stuiver M, Willems PHGM, Droogmans G, Nilius B, Bindels RJM (2000) Permeation and gating properties of the novel epithelial Ca2+ channel. J Biol Chem 275(6):3963–3969

    CAS  PubMed  Google Scholar 

  • Voets T, Droogmans G, Raskin G, Eggermont J, Nilius B (1999) Reduced intracellular ionic strength as the initial trigger for activation of endothelial volume-regulated anion channels. Proc Natl Acad Sci U S A 96(9):5298–5303

    CAS  PubMed  PubMed Central  Google Scholar 

  • Voss FK, Ullrich F, Mun̈ch J, Lazarow K, Lutte D, Mah N, Andrade-Navarro MA, Von Kries JP, Stauber T, Jentsch TJ (2014) Identification of LRRC8 heteromers as an essential component of the volume-regulated anion channel VRAC. Science 344(6184):634–638

    CAS  PubMed  Google Scholar 

  • Wang GX, Hatton WJ, Wang GL, Zhong J, Yamboliev I, Duan D, Hume JR (2003) 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 285(4 54–4)

    Google Scholar 

  • Wang D, Ragnarsson L, Lewis RJ (2018) Insight into T-type calcium channel structure, function and modulation. Curr Med Chem

    Google Scholar 

  • Warth R, Hamm K, Bleich M, Kunzelmann K, von Hahn T, Schreiber R, Ullrich E, Mengel M, Trautmann N, Kindle P, Schwab A, Greger R (1999) Molecular and functional characterization of the small Ca(2+)-regulated K+ channel (RSK4) of colonic crypts. Pflugers Arch Eur J Physiol 438(4):437–444

    CAS  Google Scholar 

  • Weaver AK, Liu X, Sontheimer H (2004) Role for calcium-activated potassium channels (BK) in growth control of human malignant glioma cells. J Neurosci Res 78(2):224–234

    CAS  PubMed  PubMed Central  Google Scholar 

  • Weaver AK, Bomben VC, Sontheimer H (2006) Expression and function of calcium-activated potassium channels in human glioma cells. Glia 54(3):223–233

    PubMed  PubMed Central  Google Scholar 

  • Weaver AK, Olsen ML, McFerrin MB, Sontheimer H (2007) BK channels are linked to inositol 1,4,5-triphosphate receptors via lipid rafts: a novel mechanism for coupling [Ca(2+)](i) to ion channel activation. J Biol Chem 282(43):31558–31568

    CAS  PubMed  Google Scholar 

  • Weiger T, Stevens DR, Wunder L, Haas HL (1997) Histamine H1 receptors in C6 glial cells are coupled to calcium-dependent potassium channels via release of calcium from internal stores. Naunyn Schmiedeberg's Arch Pharmacol 355(5):559–565

    CAS  Google Scholar 

  • Wondergem R, Bartley JW (2009) Menthol increases human glioblastoma intracellular Ca2+, BK channel activity and cell migration. J Biomed Sci 16:90

    PubMed  PubMed Central  Google Scholar 

  • Wondergem R, Ecay TW, Mahieu F, Owsianik G, Nilius B (2008) HGF/SF and menthol increase human glioblastoma cell calcium and migration. Biochem Biophys Res Commun 372(1):210–215

    CAS  PubMed  Google Scholar 

  • Wong R, Chen W, Zhong X, Rutka JT, Feng ZP, Sun HS (2018) Swelling-induced chloride current in glioblastoma proliferation, migration, and invasion. J Cell Physiol 233(1):363–370

    CAS  PubMed  Google Scholar 

  • Wrzosek A (2014) The potassium channel opener NS1619 modulates calcium homeostasis in muscle cells by inhibiting SERCA. Cell Calcium 56(1):14–24

    CAS  PubMed  Google Scholar 

  • Wulff H, Miller MJ, Hänsel W, Grissmer S, Cahalan MD, George Chandy K (2000) Design of a potent and selective inhibitor of the intermediate- conductance Ca2+-activated K+ channel, IKCa1: a potential immunosuppressant. Proc Natl Acad Sci U S A 97(14):8151–8156

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wulff H, Kolski-Andreaco A, Sankaranarayanan A, Sabatier J-M, Shakkottai V (2007) Modulators of small- and intermediate-conductance calcium-activated potassium channels and their therapeutic indications. Curr Med Chem 14(13):1437–1457

    CAS  PubMed  Google Scholar 

  • Yamada T, Wondergem R, Morrison R, Yin VP, Strange K (2016) Leucine-rich repeat containing protein LRRC8A is essential for swelling-activated Cl− currents and embryonic development in zebrafish. Physiol Rep 4(19)

    Google Scholar 

  • Ye ZC, Sontheimer H (1999) Glioma cells release excitotoxic concentrations of glutamate. Cancer Res 59(17):4383–4391

    CAS  PubMed  Google Scholar 

  • Yellen G (1984) Ionic permeation and blockade in Ca2+−activated K+ channels of bovine chromaffin cells. J Gen Physiol 84(2):157–186

    CAS  PubMed  Google Scholar 

  • Young KW, Nash MS, Challiss RAJ, Nahorski SR (2003) Role of Ca2+ feedback on single cell inositol 1,4,5-trisphosphate oscillations mediated by G-protein-coupled receptors. J Biol Chem 278(23):20753–20760

    CAS  PubMed  Google Scholar 

  • Zhang Y, Zhang H, Feustel PJ, Kimelberg HK (2008) DCPIB, a specific inhibitor of volume regulated anion channels (VRACs), reduces infarct size in MCAo and the release of glutamate in the ischemic cortical penumbra. Exp Neurol 210(2):514–520

    CAS  PubMed  Google Scholar 

  • Zhang Y, Zhang J, Jiang D, Dong Z, Qian Z, Liu C, Tao J (2012) Inhibition of T-type Ca 2+ channels by endostatin attenuates human glioblastoma cell proliferation and migration. Br J Pharmacol 166(4):1247–1260

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao W, Huimian X (2016) High expression of TRPM8 predicts poor prognosis in patients with osteosarcoma. Oncol Lett 12(2):1373–1379

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao Z, Li X, Hao J, Winston JH, Weinman SA (2007) The ClC-3 chloride transport protein traffics through the plasma membrane via interaction of an N-terminal dileucine cluster with clathrin. J Biol Chem 282(39):29022–29031

    CAS  PubMed  Google Scholar 

  • Zhou Y, Lingle CJ (2014) Paxilline inhibits BK channels by an almost exclusively closed-channel block mechanism. J Gen Physiol 144(5):415–440

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by Progetto Ricerca di Base 2017, Department of Chemistry, Biology and Biotechnology, University of Perugia and by Progetto Ricerca Finalizzata 2018 #RF-2018-12366215,

Author information

Authors and Affiliations

  1. Department of Chemistry, Biology and Biotechnology, University of Perugia, Perugia, Italy

    Luigi Catacuzzeno, Luigi Sforna & Fabio Franciolini

  2. Department of Human Neurosciences, Sapienza University of Rome, Rome, Italy

    Vincenzo Esposito

  3. Department of Physiology and Pharmacology, Sapienza University of Rome, Laboratory Associated to Istituto Pasteur Italia, Rome, Italy

    Cristina Limatola

  4. IRCCS Neuromed, Pozzilli, IS, Italy

    Cristina Limatola

Authors
  1. Luigi Catacuzzeno
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Luigi Sforna
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Vincenzo Esposito
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Cristina Limatola
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Fabio Franciolini
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Luigi Catacuzzeno .

Editor information

Editors and Affiliations

  1. Medizinische Hochschule Hannover, Zentrum für Innere Medizin, Hannover, Germany

    Christian Stock

  2. Max-Planck-Institut für Experimentelle Medizin, Göttingen, Germany

    Luis A. Pardo

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Catacuzzeno, L., Sforna, L., Esposito, V., Limatola, C., Franciolini, F. (2020). Ion Channels in Glioma Malignancy. In: Stock, C., Pardo, L.A. (eds) Transportome Malfunction in the Cancer Spectrum. Reviews of Physiology, Biochemistry and Pharmacology, vol 181. Springer, Cham. https://doi.org/10.1007/112_2020_44

Download citation

Publish with us

Policies and ethics

Search

Navigation