Kv3.4 potassium channel-mediated electrosignaling controls cell cycle and survival of irradiated leukemia cells

Pflugers Archiv European Journal of Physiology

Volumn 465, Issue 8, 2013, Pages 1209-1221

  Palme, Daniela ^a   Misovic, Milan ^a   Schmid, Evi ^a   Klumpp, Dominik ^a   Salih, Helmut R ^a   Rudner, Justine ^a,b   Huber, Stephan M ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b UNIVERSITY HOSPITAL ESSEN   (Germany)

Author keywords

Calcium signaling; Cell cycle; Ion channels; K562 human erythroid leukemia cells; Patch clamp whole cell recording; Primary chronic myeloid leukemia cells

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CYCLIN DEPENDENT KINASE 1; PHOSPHATASE; POTASSIUM CHANNEL; POTASSIUM CHANNEL KV3.4; PROTEIN CDC25B; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL CYCLE; CELL CYCLE PROGRESSION; CELL SURVIVAL; CHRONIC MYELOID LEUKEMIA; CLONOGENESIS; CONTROLLED STUDY; DOWN REGULATION; G2 PHASE CELL CYCLE CHECKPOINT; HUMAN; HUMAN CELL; IONIZING RADIATION; IRRADIATION; LEUKEMIA CELL; M PHASE CELL CYCLE CHECKPOINT; PRIORITY JOURNAL; PROTEIN EXPRESSION; RADIOSENSITIVITY; SIGNAL TRANSDUCTION;

APOPTOSIS; CALCIUM; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CDC25 PHOSPHATASES; CELL CYCLE; CELL DIVISION; CELL LINE, TUMOR; CELL SURVIVAL; CELLS, CULTURED; CYCLIN B; G2 PHASE; HUMANS; K562 CELLS; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; POTASSIUM CHANNELS, VOLTAGE-GATED; RADIATION TOLERANCE; SHAW POTASSIUM CHANNELS;

EID: 84881479780     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-013-1249-5     Document Type: Article

References (67)

1. Abbott GW, Butler MH, Bendahhou S, Dalakas MC, Ptacek LJ, Goldstein SA (2001) MiRP2 forms potassium channels in skeletal muscle with Kv3.4 and is associated with periodic paralysis. Cell 104:217-231
2. Abbott GW, Butler MH, Goldstein SA (2006) Phosphorylation and protonation of neighboring MiRP2 sites: function and pathophysiology of MiRP2-Kv3.4 potassium channels in periodic paralysis. FASEB J 20:293-301
3. Arcangeli A (2005) Expression and role of hERG channels in cancer cells. Novartis Found Symp 266:225-232, discussion 232-224
4. Arcangeli A (2011) Ion channels and transporters in cancer. 3. Ion channels in the tumor cell-microenvironment cross talk. Am J Physiol Cell Physiol 301:C762-C771
5. Barry PH, Lynch JW (1991) Liquid junction potentials and small cell effects in patch-clamp analysis. J Membr Biol 121:101-117
6. 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
7. Beck EJ, Sorensen RG, Slater SJ, Covarrubias M (1998) Interactions between multiple phosphorylation sites in the inactivation particle of a K+ channel. Insights into the molecular mechanism of protein kinase C action. J Gen Physiol 112:71-84
8. Bielanska J, Hernandez-Losa J, Moline T, Somoza R, Cajal SR, Condom E, Ferreres JC, Felipe A (2012) Increased voltage-dependent K(+) channel Kv1.3 and Kv1.5 expression correlates with leiomyosarcoma aggressiveness. Oncol Lett 4:227-230
9. Bolanz KA, Hediger MA, Landowski CP (2008) The role of TRPV6 in breast carcinogenesis. Mol Cancer Ther 7:271-279
10. Boutros R, Dozier C, Ducommun B (2006) The when and wheres of CDC25 phosphatases. Curr Opin Cell Biol 18:185-191
11. Choi KH, Song C, Shin D, Park S (2011) hERG channel blockade by externally applied quaternary ammonium derivatives. Biochim Biophys Acta 1808:1560-1566
12. 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:C541-C549
13. D'Angiolella V, Palazzo L, Santarpia C, Costanzo V, Grieco D (2007) Role for non-proteolytic control of M-phase promoting factor activity at M-phase exit. PLoS One 2:e247
14. Diochot S, Schweitz H, Beress L, Lazdunski M (1998) Sea anemone peptides with a specific blocking activity against the fast inactivating potassium channel Kv3.4. J Biol Chem 273:6744-6749
15. Dittmann K, Mayer C, Kehlbach R, Rothmund MC, Peter Rodemann H (2009) Radiation-induced lipid peroxidation activates src kinase and triggers nuclear EGFR transport. Radiother Oncol 92:379-382
16. Duan S, Yao Z, Hou D, Wu Z, Zhu WG, Wu M (2007) Phosphorylation of Pirh2 by calmodulin-dependent kinase II impairs its ability to ubiquitinate p53. EMBO J 26:3062-3074
17. Fiorio Pla A, Avanzato D, Munaron L, Ambudkar IS (2012) Ion channels and transporters in cancer. 6. Vascularizing the tumor: TRP channels as molecular targets. Am J Physiol Cell Physiol 302:C9-C15
18. Glover-Collins K, Thompson ME (2008) Nuclear export of BRCA1 occurs during early S phase and is calcium-dependent. Cell Signal 20:958-968
19. Gu C, Gu Y (2011) Clustering and activity tuning of Kv1 channels in myelinated hippocampal axons. J Biol Chem 286:25835-25847
20. Hadley JK, Noda M, Selyanko AA, Wood IC, Abogadie FC, Brown DA (2000) Differential tetraethylammonium sensitivity of KCNQ1-4 potassium channels. Br J Pharmacol 129:413-415
21. Heise N, Palme D, Misovic M, Koka S, Rudner J, Lang F, Salih HR, Huber SM, Henke G (2010) Non-selective cation channel-mediated Ca2+ - entry and activation of Ca2+/calmodulin-dependent kinase II contribute to G2/M cell cycle arrest and survival of irradiated leukemia cells. Cell Physiol Biochem 26:597-608
22. Hemmerlein B, Weseloh RM, Mello de Queiroz F, Knotgen H, Sanchez A, Rubio ME, Martin S, Schliephacke T, Jenke M, Heinz Joachim R, Stuhmer W, Pardo LA (2006) Overexpression of Eag1 potassium channels in clinical tumours. Mol Cancer 5:41
23. Holmfeldt P, Zhang X, Stenmark S, Walczak CE, Gullberg M (2005) CaMKIIgamma-mediated inactivation of the Kin I kinesin MCAK is essential for bipolar spindle formation. EMBO J 24:1256-1266
24. Huber SM (2013) Oncochannels. Cell Calcium. doi: 10.1016/j.ceca.2013.01. 001
25. Huber SM, Misovic M, Mayer C, Rodemann HP, Dittmann K (2012) EGFR-mediated stimulation of sodium/glucose cotransport promotes survival of irradiated human A549 lung adenocarcinoma cells. Radiother Oncol 103:373-379
26. Hutchins JR, Dikovskaya D, Clarke PR (2003) Regulation of Cdc2/cyclin B activation in Xenopus egg extracts via inhibitory phosphorylation of Cdc25C phosphatase by Ca(2+)/calmodulin-dependent protein [corrected] kinase II. Mol Biol Cell 14:4003-4014
27. Jang SH, Kang KS, Ryu PD, Lee SY (2009) Kv1.3 voltage-gated K(+) channel subunit as a potential diagnostic marker and therapeutic target for breast cancer. BMB Reports 42:535-539
28. Jang SH, Choi SY, Ryu PD, Lee SY (2011) Anti-proliferative effect of Kv1.3 blockers in A549 human lung adenocarcinoma in vitro and in vivo. Eur J Pharmacol 651:26-32
29. Kim HJ, Jang SH, Jeong YA, Ryu PD, Kim DY, Lee SY (2010) Involvement of Kv4.1 K(+) channels in gastric cancer cell proliferation. Biol Pharm Bull 33:1754-1757
30. Kunzelmann K (2005) Ion channels and cancer. J Membr Biol 205:159-173
31. Kuo SS, Saad AH, Koong AC, Hahn GM, Giaccia AJ (1993) Potassium-channel activation in response to low doses of gamma-irradiation involves reactive oxygen intermediates in nonexcitatory cells. Proc Natl Acad Sci U S A 90:908-912
32. Lee JM, Davis FM, Roberts-Thomson SJ, Monteith GR (2011) Ion channels and transporters in cancer. 4. Remodeling of Ca(2+) signaling in tumorigenesis: role of Ca(2+) transport. Am J Physiol Cell Physiol 301:C969-C976
33. Lee GW, Park HS, Kim EJ, Cho YW, Kim GT, Mun YJ, Choi EJ, Lee JS, Han J, Kang D (2012) Reduction of breast cancer cell migration via up-regulation of TASK-3 two-pore domain K+ channel. Acta Physiol (Oxf) 204:513-524
34. Lehen'kyi V, Flourakis M, Skryma R, Prevarskaya N (2007) TRPV6 channel controls prostate cancer cell proliferation via Ca(2+)/NFAT-dependent pathways. Oncogene 26:7380-7385
35. Lehen'kyi V, Shapovalov G, Skryma R, Prevarskaya N (2011) Ion channels and transporters in cancer. 5. Ion channels in control of cancer and cell apoptosis. Am J Physiol Cell Physiol 301:C1281-C1289
36. Li H, Liu L, Guo L, Zhang J, Du W, Li X, Liu W, Chen X, Huang S (2008) 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 87:387-392
37. Li N, Wang C, Wu Y, Liu X, Cao X (2009) Ca(2+)/calmodulin-dependent protein kinase II promotes cell cycle progression by directly activating MEK1 and subsequently modulating p27 phosphorylation. J Biol Chem 284:3021-3027
38. Logsdon NJ, Kang J, Togo JA, Christian EP, Aiyar J (1997) A novel gene, hKCa4, encodes the calcium-activated potassium channel in human T lymphocytes. J Biol Chem 272:32723-32726
39. Lozzio CB, Lozzio BB (1975) Human chronic myelogenous leukemia cell-line with positive Philadelphia chromosome. Blood 45:321-334
40. Ma S, Yang Y, Wang C, Hui N, Gu L, Zhong H, Cai Z, Wang Q, Zhang Q, Li N, Cao X (2009) Endogenous human CaMKII inhibitory protein suppresses tumor growth by inducing cell cycle arrest and apoptosis through down-regulation of the phosphatidylinositide 3-kinase/Akt/HDM2 pathway. J Biol Chem 284:24773-24782
41. MacDonnell SM, Weisser-Thomas J, Kubo H, Hanscome M, Liu Q, Jaleel N, Berretta R, Chen X, Brown JH, Sabri AK, Molkentin JD, Houser SR (2009) CaMKII negatively regulates calcineurin-NFAT signaling in cardiac myocytes. Circ Res 105:316-325
42. Maga G, Mossi R, Fischer R, Berchtold MW, Hubscher U (1997) Phosphorylation of the PCNA binding domain of the large subunit of replication factor C by Ca2+/calmodulin-dependent protein kinase II inhibits DNA synthesis. Biochemistry 36:5300-5310
43. Matsumoto Y, Maller JL (2002) Calcium, calmodulin, and CaMKII requirement for initiation of centrosome duplication in Xenopus egg extracts. Science 295:499-502
44. Menendez ST, Rodrigo JP, Allonca E, Garcia-Carracedo D, Alvarez-Alija G, Casado-Zapico S, Fresno MF, Rodriguez C, Suarez C, Garcia-Pedrero JM (2010) Expression and clinical significance of the Kv3.4 potassium channel subunit in the development and progression of head and neck squamous cell carcinomas. J Pathol 221:402-410
45. Miguel-Velado E, Perez-Carretero FD, Colinas O, Cidad P, Heras M, Lopez-Lopez JR, Perez-Garcia MT (2010) Cell cycle-dependent expression of Kv3.4 channels modulates proliferation of human uterine artery smooth muscle cells. Cardiovasc Res 86:383-391
46. Ouadid-Ahidouch H, Chaussade F, Roudbaraki M, Slomianny C, Dewailly E, Delcourt P, Prevarskaya N (2000) KV1.1 K(+) channels identification in human breast carcinoma cells: involvement in cell proliferation. Biochem Biophys Res Commun 278:272-277
47. Patel AJ, Lazdunski M (2004) The 2P-domain K+ channels: role in apoptosis and tumorigenesis. Pflugers Arch 448:261-273
48. Patel R, Holt M, Philipova R, Moss S, Schulman H, Hidaka H, Whitaker M (1999) Calcium/calmodulin-dependent phosphorylation and activation of human Cdc25-C at the G2/M phase transition in HeLa cells. J Biol Chem 274:7958-7968
49. Pillozzi S, Brizzi MF, Balzi M, Crociani O, Cherubini A, Guasti L, Bartolozzi B, Becchetti A, Wanke E, Bernabei PA, Olivotto M, Pegoraro L, Arcangeli A (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
50. Pillozzi S, Brizzi MF, Bernabei PA, Bartolozzi B, Caporale R, Basile V, Boddi V, Pegoraro L, Becchetti A, 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
51. Planas-Silva MD, Means AR (1992) Expression of a constitutive form of calcium/calmodulin dependent protein kinase II leads to arrest of the cell cycle in G2. EMBO J 11:507-517
52. Schroter KH, Ruppersberg JP, Wunder F, Rettig J, Stocker M, Pongs O (1991) Cloning and functional expression of a TEA-sensitive A-type potassium channel from rat brain. FEBS Lett 278:211-216
53. Semenova SB, Vassilieva IO, Fomina AF, Runov AL, Negulyaev YA (2009) Endogenous expression of TRPV5 and TRPV6 calcium channels in human leukemia K562 cells. Am J Physiol Cell Physiol 296:C1098-C1104
54. Si J, Collins SJ (2008) Activated Ca2+/calmodulin-dependent protein kinase IIgamma is a critical regulator of myeloid leukemia cell proliferation. Cancer Res 68:3733-3742
55. Smith GA, Tsui HW, Newell EW, Jiang X, Zhu XP, Tsui FW, Schlichter LC (2002) Functional up-regulation of HERG K+ channels in neoplastic hematopoietic cells. J Biol Chem 277:18528-18534
56. Soliman EM, Rodrigues MA, Gomes DA, Sheung N, Yu J, Amaya MJ, Nathanson MH, Dranoff JA (2009) Intracellular calcium signals regulate growth of hepatic stellate cells via specific effects on cell cycle progression. Cell Calcium 45:284-292
57. Spitzner M, Ousingsawat J, Scheidt K, Kunzelmann K, Schreiber R (2007) Voltage-gated K+ channels support proliferation of colonic carcinoma cells. FASEB J 21:35-44
58. Steinhardt RA, Alderton J (1988) Intracellular free calcium rise triggers nuclear envelope breakdown in the sea urchin embryo. Nature 332:364-366
59. 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 101:122-126
60. Taylor JT, Zeng XB, Pottle JE, Lee K, Wang AR, Yi SG, Scruggs JA, Sikka SS, Li M (2008) Calcium signaling and T-type calcium channels in cancer cell cycling. World J Gastroenterol 14:4984-4991
61. Torricelli C, Fortino V, Capurro E, Valacchi G, Pacini A, Muscettola M, Soucek K, Maioli E (2008) Rottlerin inhibits the nuclear factor kappaB/cyclin-D1 cascade in MCF-7 breast cancer cells. Life Sci 82:638-643
62. Voloshyna I, Besana A, Castillo M, Matos T, Weinstein IB, Mansukhani M, Robinson RB, Cordon-Cardo C, Feinmark SJ (2008) TREK-1 is a novel molecular target in prostate cancer. Cancer Res 68:1197-1203
63. Vullhorst D, Jockusch H, Bartsch JW (2001) The genomic basis of K(V)3.4 potassium channel mRNA diversity in mice. Gene 264:29-35
64. Wang C, Li N, Liu X, Zheng Y, Cao X (2008) A novel endogenous human CaMKII inhibitory protein suppresses tumor growth by inducing cell cycle arrest via p27 stabilization. J Biol Chem 283:11565-11574
65. Yeung SY, Thompson D, Wang Z, Fedida D, Robertson B (2005) Modulation of Kv3 subfamily potassium currents by the sea anemone toxin BDS: significance for CNS and biophysical studies. J Neurosci 25:8735-8745
66. Yuan K, Chung LW, Siegal GP, Zayzafoon M (2007) alpha-CaMKII controls the growth of human osteosarcoma by regulating cell cycle progression. Lab Investig J Tech Methods Pathol 87:938-950
67. Zhanping W, Xiaoyu P, Na C, Shenglan W, Bo W (2007) Voltage-gated K+ channels are associated with cell proliferation and cell cycle of ovarian cancer cell. Gynecol Oncol 104:455-460