Long-term channel block is required to inhibit cellular transformation by human ether-à-go-go-related gene (hERG1) potassium channels

Molecular Pharmacology

Volumn 86, Issue 2, 2014, Pages 211-221

  Pier, David M ^a,e   Shehatou, George S G ^a,c   Giblett, Susan ^a   Pullar, Christine E ^a   Trezise, Derek J ^b,d   Pritchard, Catrin A ^a   Challiss, R A John ^a   Mitcheson, John S ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

^b GLAXOSMITHKLINE   (United Kingdom)

^c MANSOURA UNIVERSITY   (Egypt)

^d Welwyn Garden City   (United Kingdom)

^e UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHOTERICIN B; DOFETILIDE; IONOPHORE; NYSTATIN; POTASSIUM CHANNEL HERG; POTASSIUM CHANNEL HERG1; UNCLASSIFIED DRUG; ACTIN; POTASSIUM CHANNEL BLOCKING AGENT;

ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CELL ADHESION; CELL CONTACT; CELL DENSITY; CELL GROWTH; CELL MIGRATION; CELL POLARITY; CELL PROLIFERATION; CELL SIZE; CELL STRUCTURE; CELL SURVIVAL; CELL TRANSFORMATION; COLONY FORMATION; CONTROLLED STUDY; FIBROBLAST; HUMAN; LONG TERM EXPOSURE; MALIGNANT TRANSFORMATION; MEMBRANE STEADY POTENTIAL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SPINDLE CELL; STRESS FIBER; WESTERN BLOTTING; WOUND CLOSURE; 3T3 CELL LINE; ANIMAL; CELL LINE; CELL MOTION; DRUG ANTAGONISM; DRUG EFFECT; FOCAL ADHESION; GENETIC TRANSFECTION; METABOLISM; NUDE MOUSE;

ACTINS; ANIMALS; CELL LINE; CELL MOVEMENT; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; ETHER-A-GO-GO POTASSIUM CHANNELS; FIBROBLASTS; FOCAL ADHESIONS; HUMANS; MICE; MICE, NUDE; NIH 3T3 CELLS; POTASSIUM CHANNEL BLOCKERS; STRESS FIBERS; TRANSFECTION;

EID: 84905978523     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.113.091439     Document Type: Article

References (51)

1. Afrasiabi E, Hietamäki M, Viitanen T, Sukumaran P, Bergelin N, and Törnquist K (2010) Expression and significance of HERG (KCNH2) potassium channels in the regulation of MDA-MB-435S melanoma cell proliferation and migration. Cell Signal 22:57-64.
2. Arcangeli A, Becchetti A, Cherubini A, Crociani O, Defilippi P, Guasti L, Hofmann G, Pillozzi S, Olivotto M, and Wanke E (2004) Physical and functional interaction between integrins and hERG potassium channels. Biochem Soc Trans 32:826-827. (Pubitemid 39524389)
3. Arcangeli A, Crociani O, Lastraioli E, Masi A, Pillozzi S, and Becchetti A (2009) Targeting ion channels in cancer: a novel frontier in antineoplastic therapy. Curr Med Chem 16:66-93.
4. Becchetti A (2011) Ion channels and transporters in cancer. 1. Ion channels and cell proliferation in cancer. Am J Physiol Cell Physiol 301:C255-C265.
5. Bianchi L, Wible B, Arcangeli A, Taglialatela M, Morra F, Castaldo P, Crociani O, Rosati B, Faravelli L, and Olivotto M et al. (1998) herg encodes a K+ current highly conserved in tumors of different histogenesis: a selective advantage for cancer cells? Cancer Res 58:815-822.
6. Cherubini A, Hofmann G, Pillozzi S, Guasti L, Crociani O, Cilia E, Di Stefano P, Degani S, Balzi M, and Olivotto M et al. (2005) Human ether-a-go-go-related gene 1 channels are physically linked to beta1 integrins and modulate adhesion-dependent signaling. Mol Biol Cell 16:2972-2983. (Pubitemid 40741240)
7. Cherubini A, Pillozzi S, Hofmann G, Crociani O, Guasti L, Lastraioli E, Polvani S, Masi A, Becchetti A, Wanke E, et al.(2002) HERG K+ channels and beta 1 integrins interact through the assembly of a macromolecular complex, Ann N Y Acad Sci 973:559-561.
8. Cherubini A, Taddei GL, Crociani O, Paglierani M, Buccoliero AM, Fontana L, Noci I, Borri P, Borrani E, and Giachi M et al. (2000) HERG potassium channels are more frequently expressed in human endometrial cancer as compared to non-cancerous endometrium. Br J Cancer 83:1722-1729. (Pubitemid 32001720)
9. Cockerill S, Tobin A, Willars G, Standen N, and Mitcheson J (2007) Modulation of hERG potassium currents by protein kinase C: evidence for the direct phosphorylation of pore forming subunits. J Physiol 581:479-493. (Pubitemid 46831751)
10. Crociani O, Guasti L, Balzi M, Becchetti A, Wanke E, Olivotto M, Wymore RS, and Arcangeli A (2003) Cell cycle-dependent expression of HERG1 and HERG1B isoforms in tumor cells. J Biol Chem 278:2947-2955. (Pubitemid 36801200)
11. Ding XW, Luo HS, Luo B, Xu DQ, and Gao S (2008) Overexpression of hERG1 in resected esophageal squamous cell carcinomas: a marker for poor prognosis. J Surg Oncol 97:57-62.
12. Dolderer JH, Schuldes H, Bockhorn H, Altmannsberger M, Lambers C, von Zabern D, Jonas D, Schwegler H, Linke R, and Schröder UH (2010) HERG1 gene expression as a specific tumor marker in colorectal tissues. Eur J Surg Oncol 36:72-77.
13. Downie BR, Sánchez A, Knötgen H, Contreras-Jurado C, Gymnopoulos M, Weber C, Stühmer W, and Pardo LA (2008) Eag1 expression interferes with hypoxia homeostasis and induces angiogenesis in tumors. J Biol Chem 283:36234-36240.
14. Fraser SP, Grimes JA, Diss JK, Stewart D, Dolly JO, and Djamgoz MB (2003) Predominant expression of Kv1.3 voltage-gated K+ channel subunit in rat prostate cancer cell lines: electrophysiological, pharmacological and molecular characterisation. Pflugers Arch 446:559-571.
15. Fraser SP and Pardo LA (2008) Ion channels: functional expression and therapeutic potential in cancer. Colloquium on Ion Channels and Cancer. EMBO Rep 9: 512-515. (Pubitemid 351772910)
16. Glassmeier G, Hempel K, Wulfsen I, Bauer CK, Schumacher U, and Schwarz JR (2012) Inhibition of HERG1 K+ channel protein expression decreases cell proliferation of human small cell lung cancer cells. Pflugers Arch 463:365-376.
17. Green JM, Alvero AB, Kohen F, and Mor G (2009) 7-(O)-Carboxymethyl daidzein conjugated to N-t-Boc-hexylenediamine: a novel compound capable of inducing cell death in epithelial ovarian cancer stem cells. Cancer Biol Ther 8:1747-1753.
18. Hardy ME, Lawrence CL, Standen NB, and Rodrigo GC (2006) Can optical recordings of membrane potential be used to screen for drug-induced action potential prolongation in single cardiac myocytes? J Pharmacol Toxicol Methods 54:173-182. (Pubitemid 44382686)
19. Hegle AP, Marble DD, and Wilson GF (2006) A voltage-driven switch for ion-independent signaling by ether-à-go-go K+ channels. Proc Natl Acad Sci USA 103: 2886-2891.
20. Herren B, Garton KJ, Coats S, Bowen-Pope DF, Ross R, and Raines EW (2001) ADAM15 overexpression in NIH3T3 cells enhances cell-cell interactions. Exp Cell Res 271:152-160. (Pubitemid 33071002)
21. Hofmann G, Bernabei PA, Crociani O, Cherubini A, Guasti L, Pillozzi S, Lastraioli E, Polvani S, Bartolozzi B, and Solazzo V, et al. (2001) HERG K+ channels activation during beta(1) integrin-mediated adhesion to fibronectin induces an up-regulation of alpha(v)beta(3) integrin in the preosteoclastic leukemia cell line FLG 29.1. J Biol Chem 276:4923-4931.
22. Huang C, Rajfur Z, Borchers C, Schaller MD, and Jacobson K (2003) JNK phosphorylates paxillin and regulates cell migration. Nature 424:219-223. (Pubitemid 36858692)
23. Huang X, Dubuc AM, Hashizume R, Berg J, He Y, Wang J, Chiang C, Cooper MK, Northcott PA, and Taylor MD, et al. (2012) Voltage-gated potassium channel EAG2 controls mitotic entry and tumor growth in medulloblastoma via regulating cell volume dynamics. Genes Dev 26:1780-1796.
24. Jehle J, Schweizer PA, Katus HA, and Thomas D (2011) Novel roles for hERG K(+) channels in cell proliferation and apoptosis. Cell Death Dis 2:e193.
25. Kamiya K, Niwa R, Mitcheson JS, and Sanguinetti MC (2006) Molecular determinants of HERG channel block. Mol Pharmacol 69:1709-1716.
26. Lampugnani MG (1999) Cell migration into a wounded area in vitro. Methods Mol Biol 96:177-182.
27. Lastraioli E, Bencini L, Bianchini E, Romoli MR, Crociani O, Giommoni E, Messerini L, Gasperoni S, Moretti R, and Di Costanzo F et al. (2012) hERG1 channels and Glut-1 as independent prognostic indicators of worse outcome in stage I and II colorectal cancer: a pilot study. Transl Oncol 5:105-112.
28. Lastraioli E, Guasti L, Crociani O, Polvani S, Hofmann G, Witchel H, Bencini L, Calistri M, Messerini L, and Scatizzi M et al. (2004) herg1 gene and HERG1 protein are overexpressed in colorectal cancers and regulate cell invasion of tumor cells. Cancer Res 64:606-611. (Pubitemid 38120900)
29. Lastraioli E, Taddei A, Messerini L, Comin CE, Festini M, Giannelli M, Tomezzoli A, Paglierani M, Mugnai G, and De Manzoni G et al. (2006) hERG1 channels in human esophagus: evidence for their aberrant expression in the malignant progression of Barrett's esophagus. J Cell Physiol 209:398-404. (Pubitemid 44484630)
30. Lees-Miller JP, Kondo C, Wang L, and Duff HJ (1997) Electrophysiological characterization of an alternatively processed ERG K+ channel in mouse and human hearts. Circ Res 81:719-726.
31. London B, Trudeau MC, Newton KP, Beyer AK, Copeland NG, Gilbert DJ, Jenkins NA, Satler CA, and Robertson GA (1997) Two isoforms of the mouse ether-a-go-go-related gene coassemble to form channels with properties similar to the rapidly activating component of the cardiac delayed rectifier K+ current. Circ Res 81:870-878. (Pubitemid 27467223)
32. Masi A, Becchetti A, Restano-Cassulini R, Polvani S, Hofmann G, Buccoliero AM, Paglierani M, Pollo B, Taddei GL, and Gallina P et al. (2005) hERG1 channels are overexpressed in glioblastoma multiforme and modulate VEGF secretion in glioblastoma cell lines. Br J Cancer 93:781-792. (Pubitemid 41486438)
33. Nilius B and Wohlrab W (1992) Potassium channels and regulation of proliferation of human melanoma cells. J Physiol 445:537-548.
34. Nobes CD and Hall A (1999) Rho GTPases control polarity, protrusion, and adhesion during cell movement. J Cell Biol 144:1235-1244. (Pubitemid 29157301)
35. Pardo LA, Contreras-Jurado C, Zientkowska M, Alves F, and Stühmer W (2005) Role of voltage-gated potassium channels in cancer. J Membr Biol 205:115-124. (Pubitemid 41803688)
36. Pardo LA, del Camino D, Sánchez A, Alves F, Brüggemann A, Beckh S, and Stühmer W (1999) Oncogenic potential of EAG K(+) channels. EMBO J 18:5540-5547.
37. Pei L, Wiser O, Slavin A, Mu D, Powers S, Jan LY, and Hoey T (2003) Oncogenic potential of TASK3 (Kcnk9) depends on K+ channel function. Proc Natl Acad Sci USA 100:7803-7807.
38. Perry M, de Groot MJ, Helliwell R, Leishman D, Tristani-Firouzi M, Sanguinetti MC, and Mitcheson J (2004) Structural determinants of HERG channel block by clofilium and ibutilide. Mol Pharmacol 66:240-249. (Pubitemid 38989480)
39. Perry M, Sanguinetti M, and Mitcheson J (2010) Revealing the structural basis of action of hERG potassium channel activators and blockers. J Physiol 588: 3157-3167.
40. Pillozzi S and Arcangeli A (2010) Physical and functional interaction between integrins and hERG1 channels in cancer cells. Adv Exp Med Biol 674:55-67.
41. Pillozzi S, Brizzi MF, Balzi M, Crociani O, Cherubini A, Guasti L, Bartolozzi B, Becchetti A, Wanke E, and Bernabei PA et al. (2002) HERG potassium channels are constitutively expressed in primary human acute myeloid leukemias and regulate cell proliferation of normal and leukemic hemopoietic progenitors. Leukemia 16:1791-1798.
42. Pillozzi S, Brizzi MF, Bernabei PA, Bartolozzi B, Caporale R, Basile V, Boddi V, Pegoraro L, Becchetti A, and Arcangeli A (2007) VEGFR-1 (FLT-1), beta1 integrin, and hERG K+ channel for a macromolecular signaling complex in acute myeloid leukemia: role in cell migration and clinical outcome. Blood 110:1238-1250. (Pubitemid 47281422)
43. Pillozzi S, Masselli M, De Lorenzo E, Accordi B, Cilia E, Crociani O, Amedei A, Veltroni M, D'Amico M, and Basso G et al. (2011) Chemotherapy resistance in acute lymphoblastic leukemia requires hERG1 channels and is overcome by hERG1 blockers. Blood 117:902-914.
44. Preussat K, Beetz C, Schrey M, Kraft R, Wölfl S, Kalff R, and Patt S (2003) Expression of voltage-gated potassium channels Kv1.3 and Kv1.5 in human gliomas. Neurosci Lett 346:33-36. (Pubitemid 36792187)
45. Schönherr R (2005) Clinical relevance of ion channels for diagnosis and therapy of cancer. J Membr Biol 205:175-184.
46. Shao XD, Wu KC, Guo XZ, Xie MJ, Zhang J, and Fan DM (2008) Expression and significance of HERG protein in gastric cancer. Cancer Biol Ther 7:45-50. (Pubitemid 351590451)
47. Smith GA, Tsui HW, Newell EW, Jiang X, Zhu XP, Tsui FW, and Schlichter LC (2002) Functional up-regulation of HERG K+ channels in neoplastic hematopoietic cells. J Biol Chem 277:18528-18534. (Pubitemid 34952403)
48. Suzuki T and Takimoto K (2004) Selective expression of HERG and Kv2 channels influences proliferation of uterine cancer cells. Int J Oncol 25:153-159.
49. Tajima N, Schönherr K, Niedling S, Kaatz M, Kanno H, Schönherr R, and Heinemann SH (2006) Ca2+-activated K+ channels in human melanoma cells are up-regulated by hypoxia involving hypoxia-inducible factor-1alpha and the von Hippel-Lindau protein. J Physiol 571:349-359.
50. Wang H, Zhang Y, Cao L, Han H, Wang J, Yang B, Nattel S, and Wang Z (2002) HERG K+ channel, a regulator of tumor cell apoptosis and proliferation. Cancer Res 62:4843-4848.
51. Yamazaki D, Kurisu S, and Takenawa T (2005) Regulation of cancer cell motility through actin reorganization. Cancer Sci 96:379-386. (Pubitemid 41179738)