Novel roles for hERG K + channels in cell proliferation and apoptosis

Cell Death and Disease

Volumn 2, Issue 8, 2011, Pages

  Jehle, J ^a   Schweizer, P A ^a   Katus, H A ^a   Thomas, D ^a  

^a UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

Author keywords

Anticancer therapy; Apoptosis; Cell proliferation; hERG; K + channel

Indexed keywords

1 [2 (6 METHYL 2 PYRIDYL)ETHYL] 4 (4 METHYLSULFONYLAMINOBENZOYL)PIPERIDINE; 10 HYDROXYCAMPTOTHECIN; ASTEMIZOLE; DOXAZOSIN; ERYTHROMYCIN; PACLITAXEL; POTASSIUM CHANNEL BLOCKING AGENT; POTASSIUM CHANNEL HERG; TUMOR MARKER; TUMOR NECROSIS FACTOR ALPHA RECEPTOR; VINCRISTINE; VOLTAGE GATED POTASSIUM CHANNEL;

ACTION POTENTIAL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; CANCER CELL CULTURE; CANCER PATIENT; CELL CYCLE REGULATION; CELL DEATH; CELL MEMBRANE; CELL PROLIFERATION; COLON CANCER; CONGESTIVE HEART FAILURE; DIAGNOSTIC VALUE; ELECTROCARDIOGRAPHY; ENDOPLASMIC RETICULUM; HEART ELECTROPHYSIOLOGY; HEART VENTRICLE ARRHYTHMIA; HUMAN; HYPERTENSION; MEMBRANE POTENTIAL; MUSCLE CELL; NEOPLASM; NONHUMAN; ONTOGENY; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; QT INTERVAL; REPOLARIZATION; REVIEW; URINARY TRACT DISEASE; DRUG ANTAGONISM; DRUG EFFECT; METABOLISM;

APOPTOSIS; CELL PROLIFERATION; ETHER-A-GO-GO POTASSIUM CHANNELS; HUMANS; NEOPLASMS; POTASSIUM CHANNEL BLOCKERS;

EID: 80052338033     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2011.77     Document Type: Review

References (73)

1. Shapovalov G, Lehen'kyi V, Skryma R, Prevarskaya N. TRP channels in cell survival and cell death in normal and transformed cells. Cell Calcium 2011; e-pub ahead of print 29 May 2011; doi:10.1016/j.ceca.2011.05.006.
2. Lau YT, Wong CK, Luo J, Leung LH, Tsang PF, Bian ZX et al. Effects of hyperpolarizationactivated cyclic nucleotide-gated (HCN) channel blockers on the proliferation and cell cycle progression of embryonic stem cells. Pflugers Arch 2011; 461: 191-202.
3. Shieh CC, Coghlan M, Sullivan JP, Gopalakrishnan M. Potassium channels: molecular defects, diseases, and therapeutic opportunities. Pharmacol Rev 2000; 52: 557-594.
4. Lang F, Föller M, Lang KS, Lang PA, Ritter M, Gulbins E et al. Ion channels in cell proliferation and apoptotic cell death. J Membr Biol 2005; 205: 147-157. (Pubitemid 41803692)
5. Chou CC, Lunn CA, Murgolo NJ. KCa3.1: target and marker for cancer, autoimmune disorder and vascular inflammation? Expert Rev Mol Diagn 2008; 8: 179-187. (Pubitemid 351469437)
6. Srivastava S, Zhdanova O, Di L, Li Z, Albaqumi M, Wulff H et al. Protein histidine phosphatase 1 negatively regulates CD4 T cells by inhibiting the K+ channel KCa3.1. Proc Natl Acad Sci USA 2008; 105: 14442-14446.
7. Toyama K, Wulff H, Chandy KG, Azam P, Raman G, Saito T et al. The intermediateconductance calcium-activated potassium channel KCa3.1 contributes to atherogenesis in mice and humans. J Clin Invest 2008; 118: 3025-3037.
8. Grgic I, Kiss E, Kaistha BP, Busch C, Kloss M, Sautter J et al. Renal fibrosis is attenuated by targeted disruption of KCa3.1 potassium channels. Proc Natl Acad Sci USA 2009; 106: 14518-14523.
9. Jang SH, Choi SY, Ryu PD, Lee SY. Anti-proliferative effect of Kv1.3 blockers in A549 human lung adenocarcinoma in vitro and in vivo. Eur J Pharmacol 2011; 651: 26-32.
10. Alvarez-Baron CP, Jonsson P, Thomas C, Dryer SE, Williams C. The two-pore domain potassium channel KCNK5: induction by estrogen receptor {alpha} and role in proliferation of breast cancer cells. Mol Endocrinol 2011; 25: 1326-1336.
11. Sanguinetti MC, Jurkiewicz NK. Two components of delayed rectifier K+ current. J Gen Physiol 1990; 96: 195-215.
12. Warmke JW, Ganetzky B. A family of potassium channel genes related to eag in Drosophila and mammals. Proc Natl Acad Sci USA 1994; 91: 3438-3442. (Pubitemid 24130252)
13. Sanguinetti MC, Jiang C, Curran ME, Keating MT. A mechanistic link between an inherited and an acquired cardiac arrhythmia: HERG encodes the IKr potassium channel. Cell 1995; 81: 299-307.
14. Sanguinetti MC, Tristani-Firouzi M. hERG potassium channels and cardiac arrhythmia. Nature 2006; 440: 463-469.
15. Thomas D, Karle CA, Kiehn J. The cardiac hERG/IKr potassium channel as pharmacological target: structure, function, regulation, and clinical applications. Curr Pharm Des 2006; 12: 2271-2283. (Pubitemid 43891399)
16. Staudacher I, Schweizer PA, Katus HA, Thomas D. hERG: protein trafficking and potential for therapy and drug side effects. Curr Opin Drug Discov Devel 2010; 13: 23-30.
17. Gonzalez-Juanatey JR, Iglesias MJ, Alcaide C, Pineiro R, Lago F. Doxazosin induces apoptosis in cardiomyocytes cultured in vitro by a mechanism that is independent of alpha1-adrenergic blockade. Circulation 2003; 107: 127-131. (Pubitemid 36070944)
18. Dolderer JH, Schuldes H, Bockhorn H, Altmannsberger M, Lambers C, von Zabern D et al. HERG1 gene expression as a specific tumor marker in colorectal tissues. Eur J Surg Oncol 2010; 36: 72-77.
19. Gong JH, Liu XJ, Shang BY, Chen SZ, Zhen YS. HERG K+ channel related chemosensitivity to sparfloxacin in colon cancer cells. Oncol Rep 2010; 23: 1747-1756.
20. Lastraioli E, Guasti L, Crociani O, Polvani S, Hofmann G, Witchel H et al. herg1 gene and HERG1 protein are overexpressed in colorectal cancers and regulate cell invasion of tumor cells. Cancer Res 2004; 64: 606-611. (Pubitemid 38120900)
21. Shao XD, Wu KC, Guo XZ, Xie MJ, Zhang J, Fan DM. Expression and significance of HERG protein in gastric cancer. Cancer Biol Ther 2008; 7: 45-50. (Pubitemid 351590451)
22. Ding XW, Luo HS, Luo B, Xu DQ, Gao S. Overexpression of hERG1 in resected esophageal squamous cell carcinomas: a marker for poor prognosis. J Surg Oncol 2008; 97: 57-62.
23. Cherubini A, Taddei GL, Crociani O, Paglierani M, Buccoliero AM, Fontana L et al. HERG potassium channels are more frequently expressed in human endometrial cancer as compared to non-cancerous endometrium. Br J Cancer 2000; 83: 1722-1729. (Pubitemid 32001720)
24. Pillozzi S, Brizzi MF, Balzi M, Crociani O, Cherubini A, Guasti L et al. HERG potassium channels are constitutively expressed in primary human acute myeloid leukemias and regulate cell proliferation of normal and leukemic hemopoietic progenitors. Leukemia 2002; 16: 1791-1798.
25. Smith GA, Tsui HW, Newell EW, Jiang X, Zhu XP, Tsui FW et al. Functional up-regulation of HERG K+ channels in neoplastic hematopoietic cells. J Biol Chem 2002; 277: 18528-18534. (Pubitemid 34952403)
26. Li H, Liu L, Guo L, Zhang J, Du W, Li X et al. HERG K+ channel expression in CD34+/ CD38-/CD123(high) cells and primary leukemia cells and analysis of its regulation in leukemia cells. Int J Hematol 2008; 87: 387-392.
27. Masi A, Becchetti A, Restano-Cassulini R, Polvani S, Hofmann G, Buccoliero AM et al. hERG1 channels are overexpressed in glioblastoma multiforme and modulate VEGF secretion in glioblastoma cell lines. Br J Cancer 2005; 93: 781-792. (Pubitemid 41486438)
28. Patt S, Preussat K, Beetz C, Kraft R, Schrey M, Kalff R et al. Expression of ether a go-go potassium channels in human gliomas. Neurosci Lett 2004; 368: 249-253. (Pubitemid 39214962)
29. Chen SZ, Jiang M, Zhen YS. HERG K+ channel expression-related chemosensitivity in cancer cells and its modulation by erythromycin. Cancer Chemother Pharmacol 2005; 56: 212-220. (Pubitemid 40884277)
30. Lin H, Xiao J, Luo X, Wang H, Gao H, Yang B et al. Overexpression HERG K(+) channel gene mediates cell-growth signals on activation of oncoproteins SP1 and NF-kappaB and inactivation of tumor suppressor Nkx3.1. J Cell Physiol 2007; 212: 137-147. (Pubitemid 46867595)
31. Bianchi L, Wible B, Arcangeli A, Taglialatela M, Morra F, Castaldo P et al. herg encodes a K+ current highly conserved in tumors of different histogenesis: a selective advantage for cancer cells? Cancer Res 1998; 58: 815-822. (Pubitemid 28099497)
32. Roy J, Vantol B, Cowley EA, Blay J, Linsdell P. Pharmacological separation of hEAG and hERG K+ channel function in the human mammary carcinoma cell line MCF-7. Oncol Rep 2008; 19: 1511-1516.
33. Wang H, Zhang Y, Cao L, Han H, Wang J, Yang B et al. HERG K+ channel, a regulator of tumor cell apoptosis and proliferation. Cancer Res 2002; 62: 4843-4848. (Pubitemid 34984401)
34. Afrasiabi E, Hietamaki M, Viitanen T, Sukumaran P, Bergelin N, Tornquist K. Expression and significance of HERG (KCNH2) potassium channels in the regulation of MDA-MB- 435S melanoma cell proliferation and migration. Cell Signal 2010; 22: 57-64.
35. Crociani O, Guasti L, Balzi M, Becchetti A, Wanke E, Olivotto M et al. Cell cycle-dependent expression of HERG1 and HERG1B isoforms in tumor cells. J Biol Chem 2003; 278: 2947-2955. (Pubitemid 36801200)
36. Zhao J, Wei XL, Jia YS, Zheng JQ. Silencing of herg gene by shRNA inhibits SH-SY5Y cell growth in vitro and in vivo. Eur J Pharmacol 2008; 579: 50-57.
37. Cherubini A, Hofmann G, Pillozzi S, Guasti L, Crociani O, Cilia E et al. Human ether-a-gogo- related gene 1 channels are physically linked to beta1 integrins and modulate adhesiondependent signaling. Mol Biol Cell 2005; 16: 2972-2983. (Pubitemid 40741240)
38. D'Amico M, Biagiotti T, Fontana L, Restano-Cassulini R, Lasagna N, Arcangeli A et al. HERG current sustains a cardiac-type action potential in neuroblastoma S cells. Biochem Biophys Res Commun 2003; 302: 101-108. (Pubitemid 36268925)
39. Meves H. Slowing of ERG current deactivation in NG108-15 cells by the histidine-specific reagent diethylpyrocarbonate. Neuropharmacology 2001; 41: 220-228. (Pubitemid 32728093)
40. Pancrazio JJ, Ma W, Grant GM, Shaffer KM, Kao WY, Liu QY et al. A role for inwardly rectifying K+ channels in differentiation of NG108-15 neuroblastoma x glioma cells. J Neurobiol 1999; 38: 466-474. (Pubitemid 29102833)
41. Hofmann G, Bernabei PA, Crociani O, Cherubini A, Guasti L, Pillozzi S et al. HERG K+ channels activation during beta(1) integrin-mediated adhesion to fibronectin induces an upregulation of alpha(v)beta(3) integrin in the preosteoclastic leukemia cell line FLG 29.1. J Biol Chem 2001; 276: 4923-4931.
42. Agarwal JR, Griesinger F, Stuhmer W, Pardo LA. The potassium channel Ether a go-go is a novel prognostic factor with functional relevance in acute myeloid leukemia. Mol Cancer 2010; 9: 18.
43. Rosati B, Marchetti P, Crociani O, Lecchi M, Lupi R, Arcangeli A et al. Glucose- and arginine-induced insulin secretion by human pancreatic beta-cells: the role of HERG K(+) channels in firing and release. FASEB J 2000; 14: 2601-2610.
44. Pond AL, Scheve BK, Benedict AT, Petrecca K, Wagoner RD, Shrier A et al. Expression of distinct ERG proteins in rat, mouse, and human heart. Relation to functional I(Kr) channels. J Biol Chem 2000; 275: 5997-6006. (Pubitemid 30115250)
45. Bauer CK, Wulfsen I, Schäfer R, Glassmeier G, Wimmers S, Flitsch J et al. HERG K(+) currents in human prolactin-secreting adenoma cells. Pflugers Arch 2003; 445: 589-600. (Pubitemid 36286894)
46. Staudacher I, Wang L, Wan X, Obers S, Wenzel W, Tristram F et al. hERG K+ channelassociated cardiac effects of the antidepressant drug desipramine. Naunyn Schmiedebergs Arch Pharmacol 2011; 383: 119-139.
47. Crociani O, Cherubini A, Piccini E, Polvani S, Costa L, Fontana L et al. Erg gene(s) expression during development of the nervous and muscular system of quail embryos. Mech Dev 2000; 95: 239-243. (Pubitemid 30440814)
48. Binggeli R, Weinstein RC. Membrane potentials and sodium channels: hypotheses for growth regulation and cancer formation based on changes in sodium channels and gap junctions. J Theor Biol 1986; 123: 377-401. (Pubitemid 17222826)
49. Ishihara K, Hiraoka M. Gating mechanism of the cloned inward rectifier potassium channel from mouse heart. J Membr Biol 1994; 142: 55-64. (Pubitemid 24339366)
50. Wonderlin WF, Strobl JS. Potassium channels, proliferation and G1 progression. J Membr Biol 1996; 154: 91-107. (Pubitemid 26413993)
51. Abbott GW, Sesti F, Splawski I, Buck ME, Lehmann MH, Timothy KW et al. MiRP1 forms IKr potassium channels with HERG and is associated with cardiac arrhythmia. Cell 1999; 97: 175-187.
52. Roepke TK, Purtell K, King EC, La Perle KM, Lerner DJ, Abbott GW. Targeted deletion of Kcne2 causes gastritis cystica profunda and gastric neoplasia. PLoS One 2010; 5: e11451.
53. Jones EMC, Roti Roti EC, Wang J, Delfosse SA, Robertson GA. Cardiac IKr channels minimally comprise hERG 1a and 1b subunits. J Biol Chem 2004; 279: 44690-44694. (Pubitemid 39430878)
54. Li H, Liu L, Guo T, Zhang J, Li X, Du W et al. Expression and functional role of HERG1, K+ channels in leukemic cells and leukemic stem cells. J Huazhong Univ Sci Technolog Med Sci 2007; 27: 257-260.
55. Fernando MA, Heaney AP. Alpha1-adrenergic receptor antagonists: novel therapy for pituitary adenomas. Mol Endocrinol 2005; 19: 3085-3096. (Pubitemid 41697723)
56. Borowiec AS, Hague F, Harir N, Guenin S, Guerineau F, Gouilleux F et al. IGF-1 activates hEAG K(+) channels through an Akt-dependent signaling pathway in breast cancer cells: role in cell proliferation. J Cell Physiol 2007; 212: 690-701. (Pubitemid 47267539)
57. Benning CM, Kyprianou N. Quinazoline-derived alpha1-adrenoceptor antagonists induce prostate cancer cell apoptosis via an alpha1-adrenoceptor- independent action. Cancer Res 2002; 62: 597-602. (Pubitemid 34106437)
58. Thomas D, Bloehs R, Koschny R, Ficker E, Sykora J, Kiehn J et al. Doxazosin induces apoptosis of cells expressing hERG K+ channels. Eur J Pharmacol 2008; 579: 98-103.
59. Davey M. Mechanism of alpha blockade for blood pressure control. Am J Cardiol 1987; 59: 18G-28G. (Pubitemid 17085540)
60. The ALLHAT Officers and Coordinators for the ALLHAT Collaborative Research Group. Major cardiovascular events in hypertensive patients randomized to doxazosin vs chlorthalidone: the antihypertensive and lipid-lowering treatment to prevent heart attack trial (ALLHAT). JAMA 2000; 283: 1967-1975.
61. Kang PM, Izumo S. Apoptosis and heart failure: a critical review of the literature. Circ Res 2000; 86: 1107-1113. (Pubitemid 30396034)
62. Kyprianou N, Vaughan TB, Michel MC. Apoptosis induction by doxazosin and other quinazoline alpha1-adrenoceptor antagonists: a new mechanism for cancer treatment? Naunyn Schmiedebergs Arch Pharmacol 2009; 380: 473-477.
63. Partin JV, Anglin IE, Kyprianou N. Quinazoline-based alpha 1-adrenoceptor antagonists induce prostate cancer cell apoptosis via TGF-beta signalling and I kappa B alpha induction. Br J Cancer 2003; 88: 1615-1621. (Pubitemid 36713791)
64. Eiras S, Fernandez P, Pineiro R, Iglesias MJ, Gonzalez-Juanatey JR, Lago F. Doxazosin induces activation of GADD153 and cleavage of focal adhesion kinase in cardiomyocytes en route to apoptosis. Cardiovasc Res 2006; 71: 118-128. (Pubitemid 43849671)
65. Oyadomari S, Mori M. Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ 2004; 11: 381-389. (Pubitemid 38489416)
66. Kornberg LJ. Focal adhesion kinase and its potential involvement in tumor invasion and metastasis. Head Neck 1998; 20: 745-752. (Pubitemid 28462832)
67. Walden PD, Globina Y, Nieder A. Induction of anoikis by doxazosin in prostate cancer cells is associated with activation of caspase-3 and a reduction of focal adhesion kinase. Urol Res 2004; 32: 261-265. (Pubitemid 39222602)
68. Zhao H, Lai F, Nonn L, Brooks JD, Peehl DM. Molecular targets of doxazosin in human prostatic stromal cells. Prostate 2005; 62: 400-410. (Pubitemid 40224145)
69. Pillozzi S, Brizzi MF, Bernabei PA, Bartolozzi B, Caporale R, Basile V et al. 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 2007; 110: 1238-1250. (Pubitemid 47281422)
70. Shao XD, Wu KC, Hao ZM, Hong L, Zhang J, Fan DM. The potent inhibitory effects of cisapride, a specific blocker for human ether-a-go-go-related gene (HERG) channel, on gastric cancer cells. Cancer Biol Ther 2005; 4: 295-301. (Pubitemid 41351289)
71. Thomas D, Wendt-Nordahl G, Röckl K, Ficker E, Brown AM, Kiehn J. High-affinity blockade of HERG human cardiac potassium channels by the novel antiarrhythmic drug BRL-32872. J Pharmacol Exp Ther 2001; 297: 753-761. (Pubitemid 32378009)
72. Thomas D, Gut B, Wendt-Nordahl G, Kiehn J. The antidepressant drug fluoxetine is an inhibitor of human ether-a-go-go-related gene (HERG) potassium channels. J Pharmacol Exp Ther 2002; 300: 543-548.
73. Zhang S, Zhou Z, Gong Q, Makielski JC, January CT. Mechanism of block and identification of the verapamil binding domain to HERG potassium channels. Circ Res 1999; 84: 989-998. (Pubitemid 29227678)