Roles of voltage‑gated potassium channels in the maintenance of pancreatic cancer stem cells

Siegel RL, Miller KD and Jemal A: Cancer statistics, 2017. CA Cancer J Clin. 67:7–30. 2017. View Article : Google Scholar

Ferlay J, Steliarova-Foucher E, Lortet-Tieulent J, Rosso S, Coebergh JW, Comber H, Forman D and Bray F: Cancer incidence and mortality patterns in Europe Estimates for 40 countries in 2012. Eur J Cancer. 49:1374–1403. 2013. View Article : Google Scholar

Ilic M and Ilic I: Epidemiology of pancreatic cancer. World J Gastroenterol. 22:9694–9705. 2016. View Article : Google Scholar

Ishiwata T, Matsuda Y, Yoshimura H, Sasaki N, Ishiwata S, Ishikawa N, Takubo K, Arai T and Aida J: Pancreatic cancer stem cells: Features and detection methods. Pathol Oncol Res. 2:797–805. 2018. View Article : Google Scholar

Moore MJ, Goldstein D, Hamm J, Figer A, Hecht JR, Gallinger S, Au HJ, Murawa P, Walde D, Wolff RA, et al: Erlotinib plus gemcitabine compared with gemcitabine alone in patients with advanced pancreatic cancer: A phase III trial of the national cancer institute of Canada clinical trials group. J Clin Oncol. 25:1960–1966. 2007. View Article : Google Scholar

Louvet C, Labianca R, Hammel P, Lledo G, Zampino MG, André T, Zaniboni A, Ducreux M, Aitini E, Taïeb J, et al: Gemcitabine in combination with oxaliplatin compared with gemcitabine alone in locally advanced or metastatic pancreatic cancer: Results of a GERCOR and GISCAD phase III trial. J Clin Oncol. 23:3509–3516. 2005. View Article : Google Scholar

Hu G, Li F, Ouyang K, Xie F, Tang X, Wang K, Han S, Jiang Z, Zhu M, Wen D, et al: Intrinsic gemcitabine resistance in a novel pancreatic cancer cell line is associated with cancer stem cell-like phenotype. Int J Oncol. 40:798–806. 2012.

Clarke MF, Dick JE, Dirks PB, Eaves CJ, Jamieson CH, Jones DL, Visvader J, Weissman IL and Wahl GM: Cancer stem cells-perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res. 66:9339–9344. 2006. View Article : Google Scholar

Visvader JE and Lindeman GJ: Cancer stem cells in solid tumours: Accumulating evidence and unresolved questions. Nat Rev Cancer. 8:755–768. 2008. View Article : Google Scholar

Toh TB, Lim JJ and Chow EK: Epigenetics in cancer stem cells. Mol Cancer. 16:292017. View Article : Google Scholar

Long A, Giroux V, Whelan K A, Hamilton KE, Tetreault MP, Tanaka K, Lee JS, Klein-Szanto AJ, Nakagawa H and Rustgi AK: WNT10A promotes an invasive and self-renewing phenotype in esophageal squamous cell carcinoma. Carcinogenesis. 36:598–606. 2015. View Article : Google Scholar

Chen Q, Song S, Wei S, Liu B, Honjo S, Scott A, Jin J, Ma L, Zhu H, Skinner HD, et al: ABT-263 induces apoptosis and synergizes with chemotherapy by targeting stemness pathways in esophageal cancer. Oncotarget. 6:25883–25896. 2015. View Article : Google Scholar

Yue D, Zhang Z, Li J, Chen X, Ping Y, Liu S, Shi X, Li L, Wang L, Huang L, et al: Transforming growth factor-betal promotes the migration and invasion of sphere-forming stem-like cell subpopulations in esophageal cancer. Exp Cell Res. 336:141–149. 2015. View Article : Google Scholar

Brungs D, Aghmesheh M, Vine KL, Becker TM, Carolan MG and Ranson M: Gastric cancer stem cells: Evidence, potential markers, and clinical implications. J Gastroenterol. 51:313–326. 2016. View Article : Google Scholar

Li Y, Rogoff HA, Keates S, Gao Y, Murikipudi S, Mikule K, Leggett D, Li W, Pardee AB and Li CJ: Suppression of cancer relapse and metastasis by inhibiting cancer stemness. Proc Natl Acad Sci USA. 112:1839–1844. 2015. View Article : Google Scholar

Shiozaki A, Ichikawa D, Otsuji E and Marunaka Y: Cellular physiological approach for treatment of gastric cancer. World J Gastroenterol. 20:11560–11566. 2014. View Article : Google Scholar

Shiozaki A, Ariyoshi Y, Iitaka D, Kosuga T, Shimizu H, Kudou M, Konishi T, Shoda K, Arita T, Konishi H, et al: Functional analysis and clinical significance of sodium iodide symporter expression in gastric cancer. Gastric Cancer. 22:473–485. 2019. View Article : Google Scholar

Kosuga T, Shiozaki A, Kudou M, Yamazato Y, Ichikawa D, Komatsu S, Konishi H, Okamoto K, Shoda K, Arita T, et al: Blockade of potassium ion transports enhances hypotonicity-induced cytocidal effects in gastric cancer. Oncotarget. 8:101394–101405. 2017. View Article : Google Scholar

Kudou M, Shiozaki A, Yamazato Y, Katsurahara K, Kosuga T, Shoda K, Arita T, Konishi H, Komatsu S, Kubota T, et al: The expression and role of TRPV2 in esophageal squamous cell carcinoma. Sci Rep. 9:160552019. View Article : Google Scholar

Shiozaki A, Kudou M, Ichikawa D, Fujiwara H, Shimizu H, Ishimoto T, Arita T, Kosuga T, Konishi H, Komatsu S, et al: Esophageal cancer stem cells are suppressed by tranilast, a TRPV2 channel inhibitor. J Gastroenterol. 53:197–207. 2018. View Article : Google Scholar

Darakhshan S and Pour AB: Tranilast: A review of its therapeutic applications. Pharmacol Res. 91:15–28. 2015. View Article : Google Scholar

Almanaa TN, Geusz ME and Jamasbi RJ: A new method for identifying stem-like cells in esophageal cancer cell lines. J Cancer. 4:536–548. 2013. View Article : Google Scholar

Johnson S, Chen H and Lo PK: In vitro tumorsphere formation assays. Bio Protoc. 3:e3252013. View Article : Google Scholar

Miyazaki H, Shiozaki A, Niisato N and Marunaka Y: Physiological significance of hypotonicity-induced regulatory volume decrease: Reduction in intracellular Cl⁻ concentration acting as an intracellular signaling. Am J Physiol Renal Physiol. 292:F1411–F1417. 2007. View Article : Google Scholar

Fan P, Zhang Y, Liu L, Zhao Z, Yin Y, Xiao X, Bauer N, Gladkich J, Mattern J, Gao C, et al: Continuous exposure of pancreatic cancer cells to dietary bioactive agents does not induce drug resistance unlike chemotherapy. Cell Death Dis. 7:e22462016. View Article : Google Scholar

Rasheed ZA and Matsui W: Biological and clinical relevance of stem cells in pancreatic adenocarcinoma. J Gastroenterol Hepatol. 27(Suppl 2): S15–S18. 2012. View Article : Google Scholar

Matsuda Y, Kure S and Ishiwata T: Nestin and other putative cancer stem cell markers in pancreatic cancer. Med Mol Morphol. 45:59–65. 2012. View Article : Google Scholar

Miyazaki H, Shiozaki A, Niisato N, Ohsawa R, Itoi H, Ueda Y, Otsuji E, Yamagishi H, Iwasaki Y, Nakano T, et al: Chloride ions control the G1/S cell-cycle checkpoint by regulating the expression of p21 through a p53-independent pathway in human gastric cancer cells. Biochem Biophys Res Commun. 366:506–512. 2008. View Article : Google Scholar

Ohsawa R, Miyazaki H, Niisato N, Shiozaki A, Iwasaki Y, Otsuji E and Marunaka Y: Intracellular chloride regulates cell proliferation through the activation of stress-activated protein kinases in MKN28 human gastric cancer cells. J Cell Physiol. 223:764–770. 2010.

Shiozaki A, Otsuji E and Marunaka Y: Intracellular chloride regulates the G(1)/S cell cycle progression in gastric cancer cells. World J Gastrointest Oncol. 3:119–122. 2011. View Article : Google Scholar

Tanaka S, Miyazaki H, Shiozaki A, Ichikawa D, Otsuji E and Marunaka Y: Cytosolic Cl⁻ affects the anticancer activity of paclitaxel in the gastric cancer cell line, MKN28 cell. Cell Physiol Biochem. 42:68–80. 2017. View Article : Google Scholar

Rausch V, Liu L, Kallifatidis G, Baumann B, Mattern J, Gladkich J, Wirth T, Schemmer P, Büchler MW, Zoller M, et al: Synergistic activity of sorafenib and sulforaphane abolishes pancreatic cancer stem cell characteristics. Cancer Res. 70:5004–5013. 2010. View Article : Google Scholar

Kim MP, Fleming JB, Wang H, Abbruzzese JL, Choi W, Kopetz S, McConkey DJ, Evans DB and Gallick GE: ALDH activity selectively defines an enhanced tumor-initiating cell population relative to CD133 expression in human pancreatic adenocarcinoma. PLoS One. 6:e206362011. View Article : Google Scholar

Rasheed ZA, Yang J, Wang Q, Kowalski J, Freed I, Murter C, Hong SM, Koorstra JB, Rajeshkumar NV, He X, et al: Prognostic significance of tumorigenic cells with mesenchymal features in pancreatic adenocarcinoma. J Natl Cancer Ins. 102:340–351. 2010. View Article : Google Scholar

Wu HY, Yang MC, Ding LY, Chen CS and Chu PC: p21-Activated kinase 3 promotes cancer stem cell phenotypes through activating the Akt-GSK3ß-ß-catenin signaling pathway in pancreatic cancer cells. Cancer Lett. 456:13–22. 2019. View Article : Google Scholar

Comes N, Serrano-Albarras A, Capera J, Serrano-Novillo C, Condom E, Ramon Y, Cajal S, Ferreres JC and Felipe A: Involvement of potassium channels in the progression of cancer to a more malignant phenotype. Biochim Biophys Acta. 1848:2477–2492. 2015. View Article : Google Scholar

Rao VR, Perez-Neut M, Kaja S and Gentile S: Voltage-gated ion channels in cancer cell proliferation. Cancers (Basel). 7:849–875. 2015. View Article : Google Scholar

Serrano-Novillo C, Capera J, Colomer-Molera M, Condom E, Ferreres JC and Felipe A: Implication of voltage-gated potassium channels in neoplastic cell proliferation. Cancers (Basel). 11:2872019. View Article : Google Scholar

Brevet M, Fucks D, Chatelain D, Regimbeau JM, Delcenserie R, Sevestre H and Ouadid-Ahidouch H: Deregulation of 2 potassium channels in pancreas adenocarcinomas: Implication of KV1.3 gene promoter methylation. Pancreas. 38:649–654. 2009. View Article : Google Scholar

Leanza L, Zoratti M, Gulbins E and Szabo I: Mitochondrial ion channels as oncological targets. Oncogene. 33:5569–5581. 2014. View Article : Google Scholar

Zaccagnino A, Manago A, Leanza L, Gontarewitz A, Linder B, Azzolini M, Biasutto L, Zoratti M, Peruzzo R, Legler K, et al: Tumor-reducing effect of the clinically used drug clofazimine in a SCID mouse model of pancreatic ductal adenocarcinoma. Oncotarget. 8:38276–38293. 2017. View Article : Google Scholar

Leanza L, Romio M, Becker KA, Azzolini M, Trentin L, Manago A, Venturini E, Zaccagnino A, Mattarei A, Carraretto L, et al: Direct pharmacological targeting of a mitochondrial ion channel selectively kills tumor cells in vivo. Cancer Cell. 31:516–531.e10. 2017. View Article : Google Scholar

Szabo I, Trentin L, Trimarco V, Semenzato G and Leanza L: Biophysical characterization and expression analysis of Kv1.3 potassium channel in primary human leukemic B cells. Cell Physiol Biochem. 37:965–978. 2015. View Article : Google Scholar

Aissaoui D, Mlayah-Bellalouna S, Jebali J, Abdelkafi-Koubaa Z, Souid S, Moslah W, Othman H, Luis J, ElAyeb M, Marrakchi N, et al: Functional role of Kv1.1 and Kv1.3 channels in the neoplastic progression steps of three cancer cell lines, elucidated by scorpion peptides. Int J Biol Macromol. 111:1146–1155. 2018. View Article : Google Scholar

Martinez R, Stühmer W, Martin S, Schell J, Reichmann A, Rohde V and Pardo L: Analysis of the expression of Kv10.1 potassium channel in patients with brain metastases and glioblastoma multiforme: Impact on survival. BMC Cancer. 15:8392015. View Article : Google Scholar

Sette A, Spadavecchia J, Landoulsi J, Casale S, Haye B, Crociani O and Arcangeli A: Development of novel anti-Kv 11.1 antibody-conjugated PEG-TiO₂ nanoparticles for targeting pancreatic ductal adenocarcinoma cells. J Nanopart Res. 15:21112013. View Article : Google Scholar

Crociani O, Lastraioli E, Boni L, Pillozzi S, Romoli MR, D'Amico M, Stefanini M, Crescioli S, Masi A, Taddei A, et al: hERG1 channels regulate VEGF-A secretion in human gastric cancer: Clinicopathological correlations and therapeutical implications. Clin Cancer Res. 20:1502–1512. 2014. View Article : Google Scholar

Wang SP, Wang JA, Luo RH, Cui WY and Wang H: Potassium channel currents in rat mesenchymal stem cells and their possible roles in cell proliferation. Clin Exp Pharmacol Physiol. 35:1077–1084. 2008. View Article : Google Scholar

Zhang YY, Yue J, Che H, Sun HY, Tse HF and Li GR: BKCa and hEag1 channels regulate cell proliferation and differentiation in human bone marrow-derived mesenchymal stem cells. J Cell Physiol. 229:202–212. 2014. View Article : Google Scholar

Morokuma J, Blackiston D, Adams DS, Seebohm G, Trimmer B and Levin M: Modulation of potassium channel function confers a hyperproliferative invasive phenotype on embryonic stem cells. Proc Natl Acad Sci USA. 105:16608–16613. 2008. View Article : Google Scholar

Bai X, Ma J, Pan Z, Song YH, Freyberg S, Yan Y, Vykoukal D and Alt E: Electrophysiological properties of human adipose tissue-derived stem cells. Am J Physiol Cell Physiol. 293:C1539–C1550. 2007. View Article : Google Scholar

Jensen HB, Ravnborg M, Dalgas U and Stenager E: 4-Aminopyridine for symptomatic treatment of multiple sclerosis: A systematic review. Ther Adv Neurol Disord. 7:97–113. 2014. View Article : Google Scholar

Solari A, Uitdehaag B, Giuliani G, Pucci E and Taus C: Aminopyridines for symptomatic treatment in multiple sclerosis. Cochrane Database Syst Rev. 2002:CD0013302002.

Goodman AD, Brown TR, Edwards KR, Krupp LB, Schapiro RT, Cohen R, Marinucci LN and Blight AR; MSF204 Investigators: A phase 3 trial of extended release oral dalfampridine in multiple sclerosis. Ann Neurol. 68:494–502. 2010. View Article : Google Scholar

Goodman AD, Brown TR, Krupp LB, Schapiro RT, Schwid SR, Cohen R, Marinucci LN and Blight AR; Fampridine MS-F203 Investigators: Sustained-release oral fampridine in multiple sclerosis: A randomised, double-blind, controlled trial. Lancet. 373:732–738. 2009. View Article : Google Scholar

Rouzaire-Dubois B, Gerard V and Dubois JM: Involvement of K+ channels in the quercetin-induced inhibition of neuroblastoma cell growth. Pflugers Arch. 423:202–205. 1993. View Article : Google Scholar

Fieber LA, Gonzâlez DM, Wallace MR and Muir D: Delayed rectifier K currents in NF1 Schwann cells. Pharmacological block inhibits proliferation. Neurobiol Dis. 13:136–146. 2003. View Article : Google Scholar

Nilius B and Wohlrab W: Potassium Channels and Regulation of proliferation of human melanoma cells. J Physiol. 445:537–548. 1992. View Article : Google Scholar

Rybalchenko V, Prevarskaya N, Van Coppenolle F, Legrand G, Lemonnier L, Le Bourhis X and Skryma R: Verapamil inhibits proliferation of LNCaP human prostate cancer cells influencing K+ channel gating. Mol Pharmacol. 59:1376–1387. 2001. View Article : Google Scholar

Chin LS, Park CC, Zitnay KM, Sinha M, DiPatri AJ Jr, Perillan P and Simard JM: 4-Aminopyridine causes apoptosis and blocks an outward rectifier K+ channel in malignant astrocytoma cell lines. J Neurosci Res. 48:122–127. 1997. View Article : Google Scholar

Kim JA, Kang YS, Jung MW, Kang GH, Lee SH and Lee YS: Ca2⁺ influx mediates apoptosis induced by 4-aminopyridine, a K+ channel blocker, in HepG2 human hepatoblastoma cells. Pharmacology. 60:74–81. 2000. View Article : Google Scholar

Wang W, Xiao J, Adachi M, Liu Z and Zhou J: 4-aminopyridine induces apoptosis of human acute myeloid leukemia cells via increasing [Ca2⁺]i through P2X7 receptor pathway. Cell Physiol Biochem. 28:199–208. 2011. View Article : Google Scholar

Huang L, Li B, Li W, Guo H and Zou F: ATP-sensitive potassium channels control glioma cells proliferation by regulating ERK activity. Carcinogenesis. 30:737–744. 2009. View Article : Google Scholar

Ru Q, Li WL, Xiong Q, Chen L, Tian X and Li CY: Voltage-gated potassium channel blocker 4-aminopyridine induces glioma cell apoptosis by reducing expression of microRNA-10b-5p. Mol Biol Cell. 29:1125–1136. 2018. View Article : Google Scholar

Luo Z, Wang J, Li C, Qiu Y, Huang J, Huang Y, Gu H, Wu B, Hu Z and Zhen Y: Upregulation of phosphatase and tensin homolog is essential for the effect of 4-aminopyridine on A549/CDDP cells. Mol Med Rep. 17:5996–6001. 2018.