Eag and HERG potassium channels as novel therapeutic targets in cancer

World Journal of Surgical Oncology

Volumn 8, Issue , 2010, Pages

  Asher, Viren ^a   Sowter, Heidi ^b   Shaw, Robert ^a   Bali, Anish ^a   Khan, Raheela ^a  

^a ROYAL DERBY HOSPITAL   (United Kingdom)

^b UNIVERSITY OF DERBY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ASTEMIZOLE; BIOLOGICAL MARKER; IMIPRAMINE; MONOCLONAL ANTIBODY; POTASSIUM CHANNEL HERG; SMALL INTERFERING RNA; VOLTAGE GATED POTASSIUM CHANNEL; ANTINEOPLASTIC AGENT; ERG1 POTASSIUM CHANNEL;

ANTINEOPLASTIC ACTIVITY; CANCER CELL; CANCER INHIBITION; CARCINOGENESIS; CELL CYCLE PROGRESSION; CELL PROLIFERATION; GENE EXPRESSION; GENE IDENTIFICATION; GENE TARGETING; HUMAN; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PROGNOSIS; PROTEIN STRUCTURE; REGULATORY MECHANISM; REVIEW; TUMOR GROWTH; ANIMAL; DRUG ANTAGONISM; METABOLISM; NEOPLASM; PATHOLOGY;

ANIMALS; ANTINEOPLASTIC AGENTS; ETHER-A-GO-GO POTASSIUM CHANNELS; HUMANS; NEOPLASMS;

EID: 78650589673     PISSN: None     EISSN: 14777819     Source Type: Journal    
DOI: 10.1186/1477-7819-8-113     Document Type: Review

References (96)

1. Jemal A, et al. Cancer statistics, 2010. CA Cancer J Clin 2010, 60(5):277-300. 10.3322/caac.20073, 20610543.
2. Fiske JL, et al. Voltage-sensitive ion channels and cancer. Cancer Metastasis Rev 2006, 25(3):493-500. 10.1007/s10555-006-9017-z, 17111226.
3. Swartz KJ. Sensing voltage across lipid membranes. Nature 2008, 456(7224):891-7. 10.1038/nature07620, 2629456, 19092925.
4. Brayden JE, Nelson MT. Regulation of arterial tone by activation of calcium-dependent potassium channels. Science 1992, 256(5056):532-5. 10.1126/science.1373909, 1373909.
5. Darszon A, et al. Ion channels in sperm motility and capacitation. Soc Reprod Fertil Suppl 2007, 65:229-44.
6. Lang F. Mechanisms and significance of cell volume regulation. J Am Coll Nutr 2007, 26(5 Suppl):613S-623S.
7. Sontheimer H. An unexpected role for ion channels in brain tumor metastasis. Exp Biol Med (Maywood) 2008, 233(7):779-91. 10.3181/0711-MR-308, 2557067, 18445774.
8. Blackiston DJ, McLaughlin KA, Levin M. Bioelectric controls of cell proliferation: ion channels, membrane voltage and the cell cycle. Cell Cycle 2009, 8(21):3519-28. 2862582, 19823012.
9. Perrin MJ, et al. Human ether-a-go-go related gene (hERG) K+ channels: function and dysfunction. Prog Biophys Mol Biol 2008, 98(2-3):137-48. 10.1016/j.pbiomolbio.2008.10.006, 19027781.
10. Pardo LA, et al. Role of voltage-gated potassium channels in cancer. J Membr Biol 2005, 205(3):115-24. 10.1007/s00232-005-0776-1, 16362499.
11. Conti M. Targeting K+ channels for cancer therapy. J Exp Ther Oncol 2004, 4(2):161-6.
12. Catsch A. Eine erbliche storung des Bewegungsmechanismus be Drosophila Melanogaster. Z Ind Abst Vererb 1944, 82:62-66.
13. Kaplan WD, Trout WE. The behavior of four neurological mutants of Drosophila. Genetics 1969, 61(2):399-409. 1212165, 5807804.
14. Ganetzky B, Wu CF. Drosophila mutants with opposing effects on nerve excitability: genetic and spatial interactions in repetitive firing. J Neurophysiol 1982, 47(3):501-14.
15. Warmke JW, Ganetzky B. A family of potassium channel genes related to eag in Drosophila and mammals. Proc Natl Acad Sci USA 1994, 91(8):3438-42. 10.1073/pnas.91.8.3438, 43592, 8159766.
16. Harmar AJ, et al. IUPHAR-DB: the IUPHAR database of G protein-coupled receptors and ion channels. Nucleic Acids Res 2009, (37 Database):D680-5. 10.1093/nar/gkn728, 2686540, 18948278.
17. Ludwig J, et al. Functional expression of a rat homologue of the voltage gated ether a go-go potassium channel reveals differences in selectivity and activation kinetics between the Drosophila channel and its mammalian counterpart. EMBO J 1994, 13(19):4451-8. 395377, 7925287.
18. Frings S, et al. Characterization of ether-a-go-go channels present in photoreceptors reveals similarity to IKx, a K+ current in rod inner segments. J Gen Physiol 1998, 111(4):583-99. 10.1085/jgp.111.4.583, 2217119, 9524140.
19. Occhiodoro T, et al. Cloning of a human ether-a-go-go potassium channel expressed in myoblasts at the onset of fusion. FEBS Lett 1998, 434(1-2):177-82. 10.1016/S0014-5793(98)00973-9, 9738473.
20. Bijlenga P, et al. T-type alpha 1 H Ca2+ channels are involved in Ca2+ signaling during terminal differentiation (fusion) of human myoblasts. Proc Natl Acad Sci USA 2000, 97(13):7627-32. 10.1073/pnas.97.13.7627, 16596, 10861024.
21. Curran ME, et al. A molecular basis for cardiac arrhythmia: HERG mutations cause long QT syndrome. Cell 1995, 80(5):795-803. 10.1016/0092-8674(95)90358-5, 7889573.
22. Pardo LA, et al. Oncogenic potential of Eag K channels. EMBO J 1999, 18(20):5540-7. 10.1093/emboj/18.20.5540, 1171622, 10523298.
23. Martin S, et al. Eag1 potassium channel immunohistochemistry in the CNS of adult rat and selected regions of human brain. Neuroscience 2008, 155(3):833-44. 10.1016/j.neuroscience.2008.05.019, 18650019.
24. Wu CF, et al. Potassium currents in Drosophila: different components affected by mutations of two genes. Science 1983, 220(4601):1076-8. 10.1126/science.6302847, 6302847.
25. Bergquist S, Dickman DK, Davis GW. A hierarchy of cell intrinsic and target-derived homeostatic signaling. Neuron 2010, 66(2):220-34. 10.1016/j.neuron.2010.03.023, 20434999.
26. Dubin AE, Liles MM, Harris GL. The K+ channel gene ether a go-go is required for the transduction of a subset of odorants in adult Drosophila melanogaster. J Neurosci 1998, 18(15):5603-13.
27. Titus SA, Warmke JW, Ganetzky B. The Drosophila erg K+ channel polypeptide is encoded by the seizure locus. J Neurosci 1997, 17(3):875-81.
28. Bauer CK, Schwarz JR. Physiology of EAG K+ channels. J Membr Biol 2001, 182(1):1-15.
29. Sanguinetti MC, et al. A mechanistic link between an inherited and an acquired cardiac arrhythmia: HERG encodes the IKr potassium channel. Cell 1995, 81(2):299-307. 10.1016/0092-8674(95)90340-2, 7736582.
30. Brugada R, et al. Sudden death associated with short-QT syndrome linked to mutations in HERG. Circulation 2004, 109(1):30-5. 10.1161/01.CIR.0000109482.92774.3A, 14676148.
31. Warmke J, Drysdale R, Ganetzky B. A distinct potassium channel polypeptide encoded by the Drosophila eag locus. Science 1991, 252(5012):1560-2. 10.1126/science.1840699, 1840699.
32. Yellen G. The voltage-gated potassium channels and their relatives. Nature 2002, 419(6902):35-42. 10.1038/nature00978, 12214225.
33. Morais Cabral JH, et al. Crystal structure and functional analysis of the HERG potassium channel N terminus: a eukaryotic PAS domain. Cell 1998, 95(5):649-55. 10.1016/S0092-8674(00)81635-9, 9845367.
34. Semenza GL. Hypoxia-inducible factor 1 and the molecular physiology of oxygen homeostasis. J Lab Clin Med 1998, 131(3):207-14. 10.1016/S0022-2143(98)90091-9, 9523843.
35. Downie BR, et al. Eag1 expression interferes with hypoxia homeostasis and induces angiogenesis in tumors. J Biol Chem 2008, 283(52):36234-40. 10.1074/jbc.M801830200, 2606018, 18927085.
36. Ludwig J, Owen D, Pongs O. Carboxy-terminal domain mediates assembly of the voltage-gated rat ether-a-go-go potassium channel. EMBO J 1997, 16(21):6337-45. 10.1093/emboj/16.21.6337, 1170240, 9400421.
37. Jenke M, et al. C-terminal domains implicated in the functional surface expression of potassium channels. EMBO J 2003, 22(3):395-403. 10.1093/emboj/cdg035, 140720, 12554641.
38. Sun XX, Bostrom SL, Griffith LC. Alternative splicing of the eag potassium channel gene in Drosophila generates a novel signal transduction scaffolding protein. Mol Cell Neurosci 2009, 40(3):338-43. 10.1016/j.mcn.2008.11.005, 2646804, 19130887.
39. Ganetzky B, et al. The eag family of K+ channels in Drosophila and mammals. Ann N Y Acad Sci 1999, 868:356-69. 10.1111/j.1749-6632.1999.tb11297.x, 10414305.
40. Bianchi L, et al. herg encodes a K+ current highly conserved in tumors of different histogenesis: a selective advantage for cancer cells?. Cancer Res 1998, 58(4):815-22.
41. Toral C, et al. Effect of extracellular matrix on adhesion, viability, actin cytoskeleton and K+ currents of cells expressing human ether a go-go channels. Life Sci 2007, 81(3):255-65. 10.1016/j.lfs.2007.05.014, 17586530.
42. Meyer R, et al. Identification of ether a go-go and calcium-activated potassium channels in human melanoma cells. J Membr Biol 1999, 171(2):107-15. 10.1007/s002329900563, 10489423.
43. Meyer R, Heinemann SH. Characterization of an eag-like potassium channel in human neuroblastoma cells. J Physiol 1998, 508(Pt 1):49-56. 2230852, 9490815.
44. Patt S, et al. Expression of ether a go-go potassium channels in human gliomas. Neurosci Lett 2004, 368(3):249-53. 10.1016/j.neulet.2004.07.001, 15364405.
45. Farias LM, et al. Ether a go-go potassium channels as human cervical cancer markers. Cancer Res 2004, 64(19):6996-7001. 10.1158/0008-5472.CAN-04-1204, 15466192.
46. Ousingsawat J, et al. Expression of voltage-gated potassium channels in human and mouse colonic carcinoma. Clin Cancer Res 2007, 13(3):824-31. 10.1158/1078-0432.CCR-06-1940, 17289873.
47. Ding XW, et al. Aberrant expression of Eag1 potassium channels in gastric cancer patients and cell lines. Med Oncol 2007, 24(3):345-50. 10.1007/s12032-007-0015-y, 17873312.
48. Mello de Queiroz F, et al. Ether a go-go potassium channel expression in soft tissue sarcoma patients. Mol Cancer 2006, 5:42. 10.1186/1476-4598-5-42, 1618397, 17022811.
49. Arcangeli A, et al. A novel inward-rectifying K+ current with a cell-cycle dependence governs the resting potential of mammalian neuroblastoma cells. J Physiol 1995, 489(Pt 2):455-71. 1156772, 8847640.
50. Hofmann G, et al. 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 2001, 276(7):4923-31. 10.1074/jbc.M005682200, 11080495.
51. Smith GA, et al. Functional up-regulation of HERG K+ channels in neoplastic hematopoietic cells. J Biol Chem 2002, 277(21):18528-34. 10.1074/jbc.M200592200, 11893742.
52. Crociani O, et al. Cell cycle-dependent expression of HERG1 and HERG1B isoforms in tumor cells. J Biol Chem 2003, 278(5):2947-55. 10.1074/jbc.M210789200, 12431979.
53. Suzuki T, Takimoto K. Selective expression of HERG and Kv2 channels influences proliferation of uterine cancer cells. Int J Oncol 2004, 25(1):153-9.
54. Shao XD, et al. 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(3):295-301. 10.4161/cbt.4.3.1500, 15846098.
55. Masi A, et al. hERG1 channels are overexpressed in glioblastoma multiforme and modulate VEGF secretion in glioblastoma cell lines. Br J Cancer 2005, 93(7):781-92. 10.1038/sj.bjc.6602775, 2361632, 16175187.
56. Cherubini A, et al. HERG potassium channels are more frequently expressed in human endometrial cancer as compared to non-cancerous endometrium. Br J Cancer 2000, 83(12):1722-9. 10.1054/bjoc.2000.1497, 2363441, 11104572.
57. Pillozzi S, 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(9):1791-8. 10.1038/sj.leu.2402572, 12200695.
58. Bauer CK, et al. HERG K(+) currents in human prolactin-secreting adenoma cells. Pflugers Arch 2003, 445(5):589-600.
59. Lastraioli E, et al. herg1 gene and HERG1 protein are overexpressed in colorectal cancers and regulate cell invasion of tumor cells. Cancer Res 2004, 64(2):606-11. 10.1158/0008-5472.CAN-03-2360, 14744775.
60. Shao XD, et al. Expression and significance of HERG protein in gastric cancer. Cancer Biol Ther 2008, 7(1):45-50. 10.4161/cbt.7.1.5126, 17938585.
61. Afrasiabi E, et al. Expression and significance of HERG (KCNH2) potassium channels in the regulation of MDA-MB-435 S melanoma cell proliferation and migration. Cell Signal 22(1):57-64. 10.1016/j.cellsig.2009.09.010, 19765650.
62. Wadhwa S, et al. Differential expression of potassium ion channels in human renal cell carcinoma. Int Urol Nephrol 2008,
63. Ding XW, et al. Aberrant expression of ether a go-go potassium channel in colorectal cancer patients and cell lines. World J Gastroenterol 2007, 13(8):1257-61.
64. Agarwal JR, et al. The potassium channel Ether a go-go is a novel prognostic factor with functional relevance in acute myeloid leukemia. Mol Cancer 2010, 9:18. 10.1186/1476-4598-9-18, 2835655, 20105281.
65. Diaz L, et al. Estrogens and human papilloma virus oncogenes regulate human ether-a-go-go-1 potassium channel expression. Cancer Res 2009, 69(8):3300-7. 10.1158/0008-5472.CAN-08-2036, 19351862.
66. Borowiec AS, 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(3):690-701. 10.1002/jcp.21065, 17520698.
67. Gavrilova-Ruch O, Schonherr R, Heinemann SH. Activation of hEAG1 potassium channels by arachidonic acid. Pflugers Arch 2007, 453(6):891-903. 10.1007/s00424-006-0173-3, 17120019.
68. Stuhmer W, et al. Potassium channels as tumour markers. FEBS Lett 2006, 580(12):2850-2. 10.1016/j.febslet.2006.03.062, 16783874.
69. Bruggemann A, Stuhmer W, Pardo LA. Mitosis-promoting factor-mediated suppression of a cloned delayed rectifier potassium channel expressed in Xenopus oocytes. Proc Natl Acad Sci USA 1997, 94(2):537-42. 10.1073/pnas.94.2.537, 19548, 9012819.
70. Pardo LA, et al. Cell cycle-related changes in the conducting properties of r-eag K+ channels. J Cell Biol 1998, 143(3):767-75. 10.1083/jcb.143.3.767, 2148139, 9813096.
71. Camacho J, et al. Cytoskeletal interactions determine the electrophysiological properties of human EAG potassium channels. Pflugers Arch 2000, 441(2-3):167-74. 10.1007/s004240000420, 11211100.
72. Arcangeli A. Expression and role of hERG channels in cancer cells. Novartis Found Symp 2005, 266:225-32. discussion 232-4, full_text, 16050271.
73. Xia Z, et al. The antidepressants imipramine, clomipramine, and citalopram induce apoptosis in human acute myeloid leukemia HL-60 cells via caspase-3 activation. J Biochem Mol Toxicol 1999, 13(6):338-47. 10.1002/(SICI)1099-0461(1999)13:6<338::AID-JBT8>3.0.CO;2-7, 10487422.
74. Wang H, et al. HERG K+ channel, a regulator of tumor cell apoptosis and proliferation. Cancer Res 2002, 62(17):4843-8.
75. Nilius B, Schwarz G, Droogmans G. Control of intracellular calcium by membrane potential in human melanoma cells. Am J Physiol 1993, 265(6 Pt 1):C1501-10.
76. Whitaker M, Patel R. Calcium and cell cycle control. Development 1990, 108(4):525-42.
77. Rouzaire-Dubois B, Dubois JM. A quantitative analysis of the role of K+ channels in mitogenesis of neuroblastoma cells. Cell Signal 1991, 3(4):333-9. 10.1016/0898-6568(91)90062-Y, 1931483.
78. Rouzaire-Dubois B, Dubois JM. K+ channel block-induced mammalian neuroblastoma cell swelling: a possible mechanism to influence proliferation. J Physiol 1998, 510(Pt 1):93-102. 10.1111/j.1469-7793.1998.093bz.x, 2231012, 9625869.
79. Abbott NJ. Astrocyte-endothelial interactions and blood-brain barrier permeability. J Anat 2002, 200(6):629-38. 10.1046/j.1469-7580.2002.00064.x, 1570746, 12162730.
80. Bender AS, et al. Ionic mechanisms in glutamate-induced astrocyte swelling: role of K+ influx. J Neurosci Res 1998, 52(3):307-21. 10.1002/(SICI)1097-4547(19980501)52:3<307::AID-JNR7>3.0.CO;2-H, 9590439.
81. Bertout JA, Patel SA, Simon MC. The impact of O2 availability on human cancer. Nat Rev Cancer 2008, 8(12):967-75. 10.1038/nrc2540, 18987634.
82. Hegle AP, Marble DD, Wilson GF. A voltage-driven switch for ion-independent signaling by ether-a-go-go K+ channels. Proc Natl Acad Sci USA 2006, 103(8):2886-91. 10.1073/pnas.0505909103, 1413768, 16477030.
83. Sun XX, et al. The eag potassium channel binds and locally activates calcium/calmodulin-dependent protein kinase II. J Biol Chem 2004, 279(11):10206-14. 10.1074/jbc.M310728200, 14699099.
84. Colomer J, Means AR. Physiological roles of the Ca2+/CaM-dependent protein kinase cascade in health and disease. Subcell Biochem 2007, 45:169-214. full_text, 18193638.
85. Hemmerlein B, et al. Overexpression of Eag1 potassium channels in clinical tumours. Mol Cancer 2006, 5:41. 10.1186/1476-4598-5-41, 1621079, 17022810.
86. Pardo LA, Stuhmer W. Eag1: an emerging oncological target. Cancer Res 2008, 68(6):1611-3. 10.1158/0008-5472.CAN-07-5710, 18339837.
87. Garcia-Ferreiro RE, et al. Mechanism of block of hEag1 K+ channels by imipramine and astemizole. J Gen Physiol 2004, 124(4):301-17. 10.1085/jgp.200409041, 2233905, 15365094.
88. Gavrilova-Ruch O, et al. Effects of imipramine on ion channels and proliferation of IGR1 melanoma cells. J Membr Biol 2002, 188(2):137-49. 10.1007/s00232-001-0181-3, 12172639.
89. Gomez-Varela D, et al. Monoclonal antibody blockade of the human Eag1 potassium channel function exerts antitumor activity. Cancer Res 2007, 67(15):7343-9. 10.1158/0008-5472.CAN-07-0107, 17671204.
90. Weber C, et al. Silencing the activity and proliferative properties of the human EagI Potassium Channel by RNA Interference. J Biol Chem 2006, 281(19):13030-7. 10.1074/jbc.M600883200, 16537547.
91. Zhao J, et al. Silencing of herg gene by shRNA inhibits SH-SY5Y cell growth in vitro and in vivo. Eur J Pharmacol 2008, 579(1-3):50-7. 10.1016/j.ejphar.2007.10.008, 17976575.
92. Furlan F, et al. ERG conductance expression modulates the excitability of ventral horn GABAergic interneurons that control rhythmic oscillations in the developing mouse spinal cord. J Neurosci 2007, 27(4):919-28. 10.1523/JNEUROSCI.4035-06.2007, 17251434.
93. Overholt JL, et al. HERG-Like potassium current regulates the resting membrane potential in glomus cells of the rabbit carotid body. J Neurophysiol 2000, 83(3):1150-7.
94. Farrelly AM, et al. Expression and function of KCNH2 (HERG) in the human jejunum. Am J Physiol Gastrointest Liver Physiol 2003, 284(6):G883-95.
95. Gullo F, et al. ERG K+ channel blockade enhances firing and epinephrine secretion in rat chromaffin cells: the missing link to LQT2-related sudden death?. FASEB J 2003, 17(2):330-2.
96. Rosati B, 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(15):2601-10. 10.1096/fj.00-0077com, 11099479.