Novel electrophysiological properties of dronedarone: Inhibition of human cardiac two-pore-domain potassium (K2P) channels

Naunyn-Schmiedeberg's Archives of Pharmacology

Volumn 385, Issue 10, 2012, Pages 1003-1016

  Schmidt, Constanze ^a   Wiedmann, Felix ^a   Schweizer, Patrick A ^a   Becker, Rüdiger ^a   Katus, Hugo A ^a   Thomas, Dierk ^a  

^a UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

Author keywords

Action potential; Atrial fibrillation; Class III antiarrhythmic drug; Dronedarone; K2P channel

Indexed keywords

CARDIAC TWO PORE DOMAIN POTASSIUM CHANNEL 2.1; CARDIAC TWO PORE DOMAIN POTASSIUM CHANNEL 3.1; DRONEDARONE; POTASSIUM CHANNEL; THREONINE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ANTIARRHYTHMIC ACTIVITY; ARTICLE; CELL MEMBRANE POTENTIAL; CHANNEL GATING; CHO CELL; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFECT; DRUG SENSITIVITY; ELECTRODE; FEMALE; IC 50; MEMBRANE ELECTROPHYSIOLOGY; MUTAGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE; PATCH CLAMP; POTASSIUM CURRENT; SCREENING; VOLTAGE CLAMP; XENOPUS;

AMIODARONE; ANIMALS; ATRIAL FIBRILLATION; CHO CELLS; CRICETINAE; CRICETULUS; DOSE-RESPONSE RELATIONSHIP, DRUG; ION CHANNEL GATING; MEMBRANE POTENTIALS; MYOCARDIUM; OOCYTES; PATCH-CLAMP TECHNIQUES; POTASSIUM CHANNEL BLOCKERS; POTASSIUM CHANNELS, TANDEM PORE DOMAIN; TRANSFECTION; XENOPUS LAEVIS;

EID: 84866735590     PISSN: 00281298     EISSN: 14321912     Source Type: Journal    
DOI: 10.1007/s00210-012-0780-9     Document Type: Article

References (56)

1. Aimond F, Beck L, Gautier P, Chérif OK, Davy JM, Lorente P, Nisato D, Vassort G (2000) Cellular and in vivo electrophysiological effects of dronedarone in normal and postmyocardial infarcted rats. J Pharmacol Exp Ther 292:415-424
2. Altomare C, Barbuti A, Viscomi C, Baruscotti M, DiFrancesco D (2000) Effects of dronedarone on acetylcholine-activated current in rabbit SAN cells. Br J Pharmacol 130:1315-1320
3. Bayliss DA, Sirois JE, Talley EM (2003) The TASK family: two-pore domain background K+ channels. Mol Interv 4:205-219
4. Bockenhauer D, Zilberberg N, Goldstein SA (2001) KCNK2: reversible conversion of a hippocampal potassium leak into a voltage-dependent channel. Nat Neurosci 4:486-491
5. Bogdan R, Goegelein H, Ruetten H (2011) Effect of dronedarone on Na+, Ca2+ and HCN channels. Naunyn Schmiedeberg's Arch Pharmacol 383:347-356
6. Brohawn SG, del Mármol J, MacKinnon R (2012) Crystal structure of the human K2P TRAAK, a lipid- and mechano-sensitive K + ion channel. Science 335:436-441
7. Connolly SJ, Camm AJ, Halperin JL, Joyner C, Alings M, Amerena J, Atar D, Avezum Á, Blomström P, Borggrefe M, Budaj A, Chen SA, Ching CK, Commerford P, Dans A, Davy JM, Delacrétaz E, Di Pasquale G, Diaz R, Dorian P, Flaker G, Golitsyn S, Gonzalez-Hermosillo A, Granger CB, Heidbüchel H, Kautzner J, Kim JS, Lanas F, Lewis BS, Merino JL, Morillo C, Murin J, Narasimhan C, Paolasso E, Parkhomenko A, Peters NS, Sim KH, Stiles MK, Tanomsup S, Toivonen L, Tomcsányi J, Torp-Pedersen C, Tse HF, Vardas P, Vinereanu D, Xavier D, Zhu J, Zhu JR, Baret-Cormel L, Weinling E, Staiger C, Yusuf S, Chrolavicius S, Afzal R, Hohnloser SH, Investigators PALLAS (2011) Dronedarone in high-risk permanent atrial fibrillation. N Engl J Med 365:2268-2276
8. Decher N, Maier M, DittrichW, Gassenhuber J, Brüggemann A, Busch AE, Steinmeyer K (2001) Characterization of TASK-4, a novel member of the pH-sensitive, two-pore domain potassium channel family. FEBS Lett 492:84-89
9. Decher N, Wemhöner K, Rinné S, Netter MF, Zuzarte M, Aller MI, Kaufmann SG, Li XT, Meuth SG, Daut J, Sachse FB, Maier SK (2011) Knock-out of the potassium channel TASK-1 leads to a prolonged QT interval and a disturbed QRS complex. Cell Physiol Biochem 28:77-86
10. Dobrev D, Nattel S (2010) New antiarrhythmic drugs for treatment of atrial fibrillation. Lancet 375:1212-1223
11. Donner BC, Schullenberg M, Geduldig N, Hüning A, Mersmann J, Zacharowski K, Kovacevic A, Decking U, Aller MI, Schmidt KG (2011) Functional role of TASK-1 in the heart: studies in TASK-1 deficient mice show prolonged cardiac repolarization and reduced heart variability. Basic Res Cardiol 106:75-87
12. Dorian P (2010) Clinical pharmacology of dronedarone: implications for the therapy of atrial fibrillation. J Cardiovasc Pharmacol Ther 15:15S-18S
13. Ehrlich JR, Biliczki P, Hohnloser SH, Nattel S (2008) Atrial-selective approaches for the treatment of atrial fibrillation. J Am Coll Cardiol 51:787-792
14. Ehrlich JR, Nattel S (2009) Novel approaches for pharmacological management of atrial fibrillation. Drugs 69:757-774
15. Ellinghaus P, Scheubel RJ, Dobrev D, Ravens U, Holtz J, Huetter J, Nielsch U, Morawietz H (2005) Comparing the global mRNA expression profile of human atrial and ventricular myocardium with high-density oligonucleotide arrays. J Thorac Cardiovasc Surg 129:1383-1390
16. Feliciangeli S, Bendahhou S, Sandoz G, Gounon P, Reichold M, Warth R, Lazdunski M, Barhanin J, Lesage F (2007) Does sumoylation control K2P1/TWIK1 background K+ channels? Cell 130:563-569
17. Gautier P, Guillemare E, Marion A, Bertrand JP, Tourneur Y, Nisato D (2003) Electrophysiologic characterization of dronedarone in guinea pig ventricular cells. J Cardiovasc Pharmacol 41:191-202
18. Gierten J, Ficker E, Bloehs R, Schlömer K, Kathöfer S, Scholz E, Zitron E, Kiesecker C, Bauer A, Becker R, Katus HA, Karle CA, Thomas D (2008) Regulation of two-pore-domain (K2P) potassium leak channels by the tyrosine kinase inhibitor genistein. Br J Pharmacol 154:1680-1690
19. Gierten J, Ficker E, Bloehs R, Schweizer PA, Zitron E, Scholz E, Karle C, Katus HA, Thomas D (2010) The human cardiac K2P3.1 (TASK-1) potassium leak channel is a molecular target for the class III antiarrhythmic drug amiodarone. Naunyn Schmiedeberg's Arch Pharmacol 381:261-270
20. Gierten J, Hassel D, Schweizer PA, Becker R, Katus HA, Thomas D (2012) Identification and functional characterization of zebrafish K2P10.1 (TREK2) two-pore-domain K+ channels. Biochim Biophys Acta 1818:33-41
21. Goonetilleke L, Quayle J (2012) TREK-1 K+ channels in the cardiovascular system: their significance and potential as a therapeutic target. Cardiovasc Ther 30:e23-e29
22. Guillemare E, Marion A, Nisato D, Gautier P (2000) Inhibitory effects of dronedarone on muscarinic K + current in guinea pig atrial cells. J Cardiovasc Pharmacol 36:802-805
23. Gurney A, Manoury B (2009) Two-pore potassium channels in the cardiovascular system. Eur Biophys J 38:305-318
24. Hohnloser SH, Crijns HJ, van Eickels M, Gaudin C, Page RL, Torp-Pedersen C, Connolly SJ, Investigators ATHENA (2009) Effect of dronedarone on cardiovascular events in atrial fibrillation. N Engl J Med 360:668-678
25. Iwasaki YK, Nishida K, Kato T, Nattel S (2011) Atrial fibrillation pathophysiology: implications for management. Circulation 124:2264-2274
26. Kathofer S, Thomas D, Karle CA (2005) The novel antiarrhythmic drug dronedarone: comparison with amiodarone. Cardiovasc Drug Rev 23:217-230
27. Lalevée N, Nargeot J, Barrére-Lemaire S, Gautier P, Richard S (2003) Effects of amiodarone and dronedarone on voltage-dependent sodium current in human cardiomyocytes. J Cardiovasc Electrophysiol 14:885-890
28. Lalevée N, Monier B, Sénatore S, Perrin L, Sémériva M (2006) Control of cardiac rhythm by ORK1, a Drosophila two-pore domain potassium channel. Curr Biol 16:1502-1508
29. Limberg SH, Netter MF, Rolfes C, Rinné S, Schlichthörl G, Zuzarte M, Vassiliou T, Moosdorf R, Wulf H, Daut J, Sachse FB, Decher N (2011) TASK-1 channels may modulate action potential duration of human atrial cardiomyocytes. Cell Physiol Biochem 28:613-624
30. Liu W, Saint DA (2004) Heterogeneous expression of tandem-pore K+ channel genes in adult and embryonic rat heart quantified by realtime polymerase chain reaction. Clin Exp Pharmacol Physiol 31:174-178
31. Lopes CM, Gallagher PG, Buck ME, Butler MH, Goldstein SA (2000) Proton block and voltage gating are potassium-dependent in the cardiac leak channel Kcnk3. J Biol Chem 275:16969-16978
32. Marban E (2002) Cardiac channelopathies. Nature 415:213-218
33. Milac AL, Anishkin A, Fatakia SN, Chow CC, Sukharev S, Guy HR (2011) Structural models of TREK channels and their gating mechanism. Channels (Austin) 5:23-33
34. Miller AN, Long SB (2012) Crystal structure of the human two-pore domain potassium channel K2P1. Science 335:432-436
35. Obers S, Staudacher I, Ficker E, Dennis A, Koschny R, Erdal H, Bloehs R, Kisselbach J, Karle CA, Schweizer PA, Katus HA, Thomas D (2010) Multiple mechanisms of hERG liability: K+ current inhibition, disruption of protein trafficking, and apoptosis induced by amoxapine. Naunyn Schmiedeberg's Arch Pharmacol 381:385-400
36. Patel A, Honore E (2001) Properties and regulation of mammalian 2P domain K+ channels. Trends Neurosci 24:339-346
37. Putzke C, Wemhöner K, Sachse FB, Rinné S, Schlichthörl G, Li XT, Jaé L, Eckhardt I, Wischmeyer E, Wulf H, Preisig-Müller R, Daut J, Decher N (2007) The acid-sensitive potassium channel TASK-1 in rat cardiac muscle. Cardiovasc Res 75:59-68
38. Rahm AK, Gierten J, Kisselbach J, Staudacher I, Staudacher K, Schweizer PA, Becker R, Katus HA, Thomas D (2012) Protein kinase C-dependent activation of human K2P18.1 K+ channels. Br J Pharmacol 166:764-773
39. Rajan S, Plant LD, Rabin ML, Butler MH, Goldstein SA (2005) Sumoylation silences the plasma membrane leak K+ channel K2P1. Cell 121:37-47
40. Ravens U (2010) Novel pharmacological approaches for antiarrhythmic therapy. Naunyn Schmiedeberg's Arch Pharmacol 381:187-193
41. Ridley JM, Milnes JT, Witchel HJ, Hancox JC (2004) High affinity HERG K(+) channel blockade by the antiarrhythmic agent dronedarone: resistance to mutations of the S6 residues Y652 and F656. Biochem Biophys Res Commun 325:883-891
42. Schweizer PA, Becker R, Katus HA, Thomas D (2011) Dronedarone: current evidence for its safety and efficacy in the management of atrial fibrillation. Drug Des Devel Ther 5:27-39
43. Seyler C, Duthil-Straub E, Zitron E, Gierten J, Scholz EP, Fink RH, Karle CA, Becker R, Katus HA, Thomas D (2012) TASK1 (K2P3.1) K+ current inhibition by endothelin-1 is mediated by Rho kinase-dependent channel phosphorylation. Br J Pharmacol 165:1467-1475
44. Staudacher K, Baldea I, Kisselbach J, Staudacher I, Rahm AK, Schweizer PA, Becker R, Katus HA, Thomas D (2011a) Alternative splicing determines mRNA translation initiation and function of human K2P10.1 K+ channels. J Physiol 589:3709-3720
45. Staudacher K, Staudacher I, Ficker E, Seyler C, Gierten J, Kisselbach J, Rahm AK, Trappe K, Schweizer PA, Becker R, Katus HA, Thomas D (2011b) Carvedilol targets human K2P3.1 (TASK1) K+ leak channels. Br J Pharmacol 163:1099-1110
46. Staudacher I, Wang L, Wan X, Obers S, Wenzel W, Tristram F,Koschny R, Staudacher K, Kisselbach J, Koelsch P, Schweizer PA, Katus HA, Ficker E, Thomas D (2011c) hERG K+ channelassociated cardiac effects of the antidepressant drug desipramine. Naunyn Schmiedeberg's Arch Pharmacol 383:119-139
47. Streit AK, Netter MF, Kempf F, Walecki M, Rinné S, Bollepalli MK, Preisig-Müller R, Renigunta V, Daut J, Baukrowitz T, Sansom MS, Stansfeld PJ, Decher N (2011) A specific two-pore domain potassium channel blocker defines the structure of the TASK-1 open pore. J Biol Chem 286:13977-13984
48. Thomas D, Goldstein SAN (2009) Two-P-domain (K2P) potassium channels: leak conductance regulators of excitability. In: Squire LR (ed) Encyclopedia of neuroscience. Academic Press, Oxford, pp 1207-1220
49. Thomas D, Kathofer S, ZhangW,Wu K,Wimmer AB, Zitron E, Kreye VA, Katus HA, Schoels W, Karle CA, Kiehn J (2003) Acute effects of dronedarone on both components of the cardiac delayed rectifier K+ current, HERG and KvLQT1/minK potassium channels. Br J Pharmacol 140:996-1002
50. Thomas D, Plant LD, Wilkens CM, McCrossan ZA, Goldstein SAN (2008) Alternative translation initiation in rat brain yields K2P2.1 potassium channels permeable to sodium. Neuron 58:859-870
51. Thomas D, Wendt-Nordahl G, Röckl K, Ficker E, Brown AM, Kiehn J (2001) High-affinity blockade of human ether-a-gogo-related gene human cardiac potassium channels by the novel antiarrhythmic drug BRL-32872. J Pharmacol Exp Ther 297:753-761
52. Varró A, Takács J, Németh M, Hála O, Virág L, Iost N, Baláti B, Agoston M, Vereckei A, Pastor G, Delbruyère M, Gautier P, Nisato D, Papp JG (2001) Electrophysiological effects of dronedarone (SR 33589), a noniodinated amiodarone derivative in the canine heart: comparison with amiodarone. Br J Pharmacol 133:625-634
53. Voigt N, Rozmaritsa N, Trausch A, Zimniak T, Christ T, Wettwer E, Matschke K, Dobrev D, Ravens U (2010) Inhibition of IK, ACh current may contribute to clinical efficacy of class I and class III antiarrhythmic drugs in patients with atrial fibrillation. Naunyn Schmiedeberg's Arch Pharmacol 381:251-259
54. Watanabe Y, Kimura J (2008) Acute inhibitory effect of dronedarone, a noniodinated benzofuran analogue of amiodarone, on Na+/Ca2+ exchange current in guinea pig cardiac ventricular myocytes. Naunyn Schmiedeberg's Arch Pharmacol 377:371-376
55. Xian Tao L, Dyachenko V, Zuzarte M, Putzke C, Preisig-Müller R, Isenberg G, Daut J (2006) The stretch-activated potassium channel TREK-1 in rat cardiac ventricular muscle. Cardiovasc Res 69:86-97
56. Zhang YH, Colenso CK, Sessions RB, Dempsey CE, Hancox JC (2011) The hERG K(+) channel S4 domain L532P mutation: characterization at 37 °C. Biochim Biophys Acta 1808:2477-2487