Antifibrillatory agents and potassium channels in the atria: Pore block versus channel trafficking

Molecular Interventions

Volumn 9, Issue 2, 2009, Pages 79-86

  McEwen, Dyke P ^a,b   Martens, Jeffrey R ^a,c  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b Essen Instruments Inc   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2' (4 METHOXYPHENYLACETAMIDOMETHYL) N [2 (3 PYRIDYL)ETHYL] 2 BIPHENYLCARBOXAMIDE; AMIODARONE; ANTIARRHYTHMIC AGENT; AVE 1231; FLECAINIDE; ION CHANNEL; POTASSIUM CHANNEL; QUINIDINE; UNCLASSIFIED DRUG; VERNAKALANT; VOLTAGE GATED POTASSIUM CHANNEL;

CELL DENSITY; CELL MEMBRANE PERMEABILITY; HEART ARRHYTHMIA; HEART ATRIUM FIBRILLATION; HEART MUSCLE POTENTIAL; HEART REPOLARIZATION; HUMAN; ION TRANSPORT; LIVER TOXICITY; LUNG TOXICITY; PERIPHERAL NEUROPATHY; REVIEW;

ANIMALS; ANTI-ARRHYTHMIA AGENTS; ATRIAL FIBRILLATION; BIOLOGICAL TRANSPORT; HEART ATRIA; HUMANS; PERMEABILITY; POTASSIUM CHANNEL BLOCKERS; POTASSIUM CHANNELS;

EID: 65949092763     PISSN: 15340384     EISSN: 15432548     Source Type: Journal    
DOI: 10.1124/mi.9.2.7     Document Type: Review

References (89)

1. Center for Disease Control Atrial Fibrillation Fact Sheet. Age-adjusted death rates for atrial-fibrillation as a contributing cause-United States, 1999. http://www.cdc.gov/dhdsp/library/pdfs/fs-atrial-fibrillation.pdf (accessed April 2, 2009).
2. Nattel, S. and Carlsson, L. Innovative approaches to anti-arrhythmic drug therapy. Nat. Rev. Drug Discov. 5, 1034-1049 (2006).
3. Waldo, A.L. A perspective on antiarrhythmic drug therapy to treat atrial fibrillation: There remains an unmet need. Am. Heart. J. 151, 771-778 (2006).
4. Lafuente-Lafuente, C., Mouly, S., Longas-Tejero, M.A., and Bergmann, J.. Antiarrhythmics for maintaining sinus rhythm after cardioversion of atrial fibrillation. Cochrane Database Syst. Rev. CD005049 (2007).
5. Lafuente-Lafuente, C., Mouly, S., Longas-Tejero, M.A., Mahe, I., and Bergmann, J.F. Antiarrhythmic drugs for maintaining sinus rhythm after cardioversion of atrial fibrillation: A systematic review of randomized controlled trials. Arch. Intern. Med. 166, 719-728 (2006).
6. van der Heyden, M.A., Smits, M.E., and Vos, M.A. Drugs and trafficking of ion channels: A new pro-arrhythmic threat on the horizon? Br. J. Pharmacol. 153, 406-409 (2008).
7. Nattel, S. New ideas about atrial fibrillation 50 years on. Nature 415, 219-226 (2002).
8. Andalib, A., Brugada, R., and Nattel, S. Atrial fibrillation: Evidence for genetically determined disease. Curr. Opin. Cardiol. 23, 176-183 (2008).
9. Dobrev, D. and Ravens, U. Remodeling of cardiomyocyte ion channels in human atrial fibrillation. Basic Res. Cardiol. 98, 137-148 (2003).
10. Ravens, U. Potassium channels in atrial fibrillation: targets for atrial and pathology-specific therapy? Heart Rhythm 5, 758-759 (2008).
11. Burstein, B. and Nattel, S. Atrial structural remodeling as an antiarrhythmic target. J. Cardiovasc. Pharmacol. 52, 4-10 (2008).
12. Cleutjens, J.P., Verluyten, M.J., Smiths, J.F., and Daemen, M.J. Collagen remodeling after myocardial infarction in the rat heart. Am. J. Pathol. 147, 325-338 (1995).
13. Weber, K.T., Pick, R., Silver, M.A., Moe, G.W., Janicki, J.S., Zucker, I.H., and Armstrong, P.W. Fibrillar collagen and remodeling of dilated canine left ventricle. Circulation 82, 1387-1401 (1990).
14. Korantzopoulos, P., Kolettis, T., Siogas, K., and Goudevenos, J. Atrial fibrillation and electrical remodeling: the potential role of inflammation and oxidative stress. Med. Sci. Monit. 9, RA225-229 (2003). (Pubitemid 37303894)
15. Fox, C.S., Parise, H., D'Agostino, R.B., Sr., Lloyd-Jones, D.M., Vasan, R.S., Wang, T.J., Levy, D., Wolf, P.A., and Benjamin, E.J. Parental atrial fibrillation as a risk factor for atrial fibrillation in offspring. J. Am. Med. Assoc. 291, 2851-2855 (2004).
16. Ellinor, P.T., Yi, B.A., and MacRae, C.A. Genetics of atrial fibrillation. Med. Clin. North Am. 92, 41-51 (2008). (Pubitemid 350176580)
17. Nerbonne, J.M. and Kass, R.S. Molecular physiology of cardiac repolar- ization. Physiol Rev. 85, 1205-1253 (2005).
18. Brendel, J. and Peukert, S. Blockers of the Kv1.5 channel for the treatment of atrial arrhythmias. Curr. Med. Chem. Cardiovasc. Hematol. Agents 1, 273-287 (2003).
19. Chen, Y.H., Xu, S.J., Bendahhou, S. et al. KCNQ1 gain-of-function mutation in familial atrial fibrillation. Science 299, 251-254 (2003).
20. Otway, R., Vandenberg, J.I., and Fatkin, D. Atrial fibrillation-A new cardiac channelopathy. Heart Lung Circ. 16, 356-360 (2007).
21. Brugada, R., Hong, K., Dumaine, R. et al. Sudden death associated with short-QT syndrome linked to mutations in HERG. Circulation 109, 30-35 (2004).
22. Hong, K., Bjerregaard, P., Gussak, I., and Brugada, R. Short QT syndrome and atrial fibrillation caused by mutation in KCNH2. J. Cardiovasc. Electrophysiol. 16, 394-396 (2005).
23. Xia, M., Jin, Q., Bendahhou, S. et al. A Kir2.1 gain-of-function mutation underlies familial atrial fibrillation. Biochem. Biophys. Res. Commun. 332, 1012-1019 (2005).
24. Yang, Y., Xia, M., Jin, Q. et al. Identification of a KCNE2 gain-of-function mutation in patients with familial atrial fibrillation. Am. J. Hum. Genet. 75, 899-905 (2004).
25. Ehrlich, J.R., Zicha, S., Coutu, P., Hebert, T.E., and Nattel, S. Atrial fibrillation-associated minK38G/S polymorphism modulates delayed rectifier current and membrane localization. Cardiovasc. Res. 67, 520-528 (2005). (Pubitemid 41019559)
26. Olson, T.M., Alekseev, A.E., Liu, X.K. et al. Kv1.5 channelopathy due to KCNA5 loss-of-function mutation causes human atrial fibrillation. Hum. Mol. Genet. 15, 2185-2191 (2006). (Pubitemid 43985509)
27. Bigi, M.A., Aslani, A., and Shahrzad, S. Clinical predictors of atrial fibrillation in Brugada syndrome. Europace 9, 947-950 (2007).
28. Chen, L.Y., Ballew, J.D., Herron, K.J., Rodeheffer, R.J., and Olson, T.M. A common polymorphism in SCN5A is associated with lone atrial fibrillation. Clin. Pharmacol. Ther. 81, 35-41 (2007).
29. Olson, T.M., Michels, V.V., Ballew, J.D., Reyna, S.P., Karst, M.L., Herron, K.J., Horton, S.C., Rodeheffer, R.J., and Anderson, J.L. Sodium channel mutations and susceptibility to heart failure and atrial fibrillation. J. Am. Med. Assoc. 293, 447-454 (2005).
30. Callans, D.J. In the clinic. Atrial fibrillation. Ann. Intern. Med. 149, ITC5-1- 15; quiz ITC15-16 (2008).
31. d'Avila, A. and Ruskin, J.N. Nonpharmacologic strategies: the evolving story of ablation and hybrid therapy. Am. J. Cardiol. 102, 20H-24H (2008).
32. Jais, P., Pappone, C., Kuck, K.H. et al. European experience of atrial fibrillation ablation. Heart Rhythm 271(suppl), S87 (2004).
33. Cappato, R., Calkins, H., Chen, S.A. et al. Worldwide survey on the methods, efficacy, and safety of catheter ablation for human atrial fibrillation. Circulation 111, 1100-1105 (2005).
34. Bagwe, S., Leonardi, M., and Bissett, J. Novel pharmacological therapies for atrial fibrillation. Curr. Opin. Cardiol. 22, 450-457 (2007).
35. Ford, J.W. and Milnes, J.T. New drugs targeting the cardiac ultra-rapid delayed-rectifier current (I Kur): rationale, pharmacology and evidence for potential therapeutic value. J. Cardiovasc. Pharmacol. 52, 105-120 (2008).
36. Vassallo, P. and Trohman, R.G. Prescribing amiodarone: An evidence- based review of clinical indications. J. Am. Med. Assoc. 298, 1312-1322 (2007).
37. Camm, A.J. Safety considerations in the pharmacological management of atrial fibrillation. Int. J. Cardiol. 127, 299-306 (2008).
38. Camm, A.J. and Savelieva, I. Advances in antiarrhythmic drug treatment of atrial fibrillation: Where do we stand now? Heart Rhythm 1, 244-246 (2004).
39. Mays, D.J., Foose, J.M., Philipson, L.H., and Tamkun, M.M. Localization of the Kv1.5 K+ channel protein in explanted cardiac tissue. J. Clin. Invest. 96, 282-292 (1995).
40. Amos, G.J., Wettwer, E., Metzger, F., Li, Q., Himmel, H.M., and Ravens, U. Differences between outward currents of human atrial and subepicardial ventricular myocytes. J. Physiol. 491 (Pt 1), 31-50 (1996).
41. Wang, Z., Fermini, B., and Nattel, S. Sustained depolarization-induced outward current in human atrial myocytes. Evidence for a novel delayed rectifier K+ current similar to Kv1.5 cloned channel currents. Circ. Res. 73, 1061-1076 (1993). (Pubitemid 23340202)
42. Brundel, B.J., Van Gelder, I.C., Henning, R.H., Tuinenburg, A.E., Wietses, M., Grandjean, J.G., Wilde, A.A., Van Gilst, W.H., and Crijns, H.J. Alterations in potassium channel gene expression in atria of patients with persistent and paroxysmal atrial fibrillation: Differential regulation of protein and mRNA levels for K+ channels. J. Am. Coll. Cardiol. 37, 926-932 (2001). (Pubitemid 32202465)
43. Michelakis, E.D. and Weir, E.K. The pathobiology of pulmonary hypertension. Smooth muscle cells and ion channels. Clin. Chest. Med. 22, 419-432 (2001).
44. Sweeney, M. and Yuan, J.X. Hypoxic pulmonary vasoconstriction: role of voltage-gated potassium channels. Respir. Res. 1, 40-48 (2000).
45. Decher, N., Kumar, P., Gonzalez, T., Pirard, B., and Sanguinetti, M.C. Binding site of a novel Kv1.5 blocker: a "foot in the door" against atrial fibrillation. Mol. Pharmacol. 70, 1204-1211 (2006).
46. Schram, G., Pourrier, M., Melnyk, P., and Nattel, S. Differential distribution of cardiac ion channel expression as a basis for regional specialization in electrical function. Circ. Res. 90, 939-950 (2002). (Pubitemid 34633859)
47. Gogelein, H., Brendel, J., Steinmeyer, K., Strubing, C., Picard, N., Rampe, D., Kopp, K., Busch, A.E., and Bleich, M. Effects of the atrial antiarrhythmic drug AVE0118 on cardiac ion channels. Naunyn Schmiedebergs Arch. Pharmacol. 370, 183-192 (2004).
48. Wettwer, E., Hala, O., Christ, T., Heubach, J.F., Dobrev, D., Knaut, M., Varro, A., and Ravens, U. Role of IKur in controlling action potential shape and contractility in the human atrium: Influence of chronic atrial fibrillation. Circulation 110, 2299-2306 (2004). (Pubitemid 39407330)
49. Schotten, U., de Haan, S., Verheule, S., Harks, E.G., Frechen, D., Bodewig, E., Greiser, M., Ram, R., Maessen, J., Kelm, M., Allessie, M., and van Wagoner, D.R. Blockade of atrial-specific K+-currents increases atrial but not ventricular contractility by enhancing reverse mode Na+/ Ca2+-exchange. Cardiovasc. Res. 73, 37-47 (2007).
50. Lofberg, L., Jacobson, I., and Carlsson, L. Electrophysiological and anti- arrhythmic effects of the novel antiarrhythmic agent AZD7009: A comparison with azimilide and AVE0118 in the acutely dilated right atrium of the rabbit in vitro. Europace 8, 549-557 (2006). (Pubitemid 43985496)
51. Gross, M.F., Beaudoin, S., McNaughton-Smith, G., Amato, G.S., Castle, N.A., Huang, C., Zou, A., and Yu, W. Aryl sulfonamido indane inhibitors of the Kv1.5 ion channel. Bioorg. Med. Chem. Lett. 17, 2849-2853 (2007).
52. Eldstrom, J., Wang, Z., Xu, H., Pourrier, M., Ezrin, A., Gibson, K., and Fedida, D. The molecular basis of high-affinity binding of the antiar- rhythmic compound vernakalant (RSD1235) to Kv1.5 channels. Mol. Pharmacol. 72, 1522-1534 (2007). (Pubitemid 350146089)
53. Fedida, D. Vernakalant (RSD1235): A novel, atrial-selective antifibrillatory agent. Expert Opin. Investig. Drugs 16, 519-532 (2007).
54. Fedida, D., Orth, P.M., Chen, J.Y., Lin, S., Plouvier, B., Jung, G., Ezrin, A.M., and Beatch, G.N. The mechanism of atrial antiarrhythmic action of RSD1235. J. Cardiovasc. Electrophysiol. 16, 1227-1238 (2005).
55. Mao, Z.L., Wheeler, J.J., Clohs, L., Beatch, G.N., and Keirns, J. Pharmacokinetics of the novel atrial-selective antiarrhythmic agent vernakalant hydrochloride injection (RSD1235): Influence of CYP2D6 expression and other factors. J. Clin. Pharmacol. 17-29 (2009).
56. Yeung, K.S. and. Meanwell, N. Inhibition of hERG channel trafficking: an under-explored mechanism for drug-induced QT prolongation. ChemMedChem 3, 1501-1502 (2008).
57. Dennis, A., Wang, L., Wan, X., and Ficker, E. hERG channel trafficking: novel targets in drug-induced long QT syndrome. Biochem. Soc. Trans. 35, 1060-1063 (2007).
58. Ficker, E., Kuryshev, Y.A., Dennis, A.T., Obejero-Paz, C., Wang, L., Hawryluk, P., Wible, B.A., and Brown, A.M. Mechanisms of arsenic- induced prolongation of cardiac repolarization. Mol. Pharmacol. 66, 33-44 (2004).
59. Ficker, E., Dennis, A.T., Wang, L., and Brown, A.M. Role of the cytosolic chaperones Hsp70 and Hsp90 in maturation of the cardiac potassium channel HERG. Circ. Res. 92, e87-100 (2003).
60. Ficker, E., Dennis, A., Kuryshev, Y., Wible, B.A., and Brown, A.M. HERG channel trafficking. Novartis Found. Symp. 266, 57-69; discussion 70-54, 95-159 (2005).
61. Takemasa, H., Nagatomo, T., Abe, H. et al. Coexistence of hERG current block and disruption of protein trafficking in ketoconazole-induced long QT syndrome. Br. J. Pharmacol. 153, 439-447 (2008).
62. Rajamani, S., Eckhardt, L.L., Valdivia, C.R. et al. Drug-induced long QT syndrome: hERG K+ channel block and disruption of protein trafficking by fluoxetine and norfluoxetine. Br. J. Pharmacol. 149, 481-489 (2006). (Pubitemid 44658508)
63. Cordes, J.S., Sun, Z., Lloyd, D.B., Bradley, J.A., Opsahl, A.C., Tengowski, M.W., Chen, X., and Zhou, J. Pentamidine reduces hERG expression to prolong the QT interval. Br. J. Pharmacol. 145, 15-23 (2005).
64. Kuryshev, Y.A., Ficker, E., Wang, L. et al. Pentamidine-induced long QT syndrome and block of hERG trafficking. J. Pharmacol. Exp. Ther. 312, 316-323 (2005).
65. Guo, J., Massaeli, H., Li, W., Xu, J., Luo, T., Shaw, J., Kirshenbaum, L.A., and Zhang, S. Identification of IKr and its trafficking disruption induced by probucol in cultured neonatal rat cardiomyocytes. J. Pharmacol. Exp. Ther. 321, 911-920 (2007).
66. Anderson, C.L., Delisle, B.P., Anson, B.D., Kilby, J.A., Will, M.L., Tester, D.J., Gong, Q., Zhou, Z., Ackerman, M.J., and January, C.T. Most LQT2 mutations reduce Kv11.1 (hERG) current by a class 2 (trafficking-defi- cient) mechanism. Circulation 113, 365-373 (2006). (Pubitemid 43803197)
67. Walker, V.E., Atanasiu, R., Lam, H., and Shrier, A. Co-chaperone FKBP38 promotes HERG trafficking. J. Biol. Chem. 282, 23509-23516 (2007). (Pubitemid 47311946)
68. Gong, Q., Jones, M.A., and Zhou, Z. Mechanisms of pharmacological rescue of trafficking-defective hERG mutant channels in human long QT syndrome. J. Biol. Chem. 281, 4069-4074 (2006). (Pubitemid 44378220)
69. Ellgaard, L. and Helenius, A. Quality control in the endoplasmic reticu- lum. Nat. Rev. Mol. Cell Biol. 4, 181-191 (2003).
70. Delisle, B.P., Underkofler, H.A., Moungey, B.M. et al. Small GTPase determinants for the golgi processing and plasmalemmal expression of human ether-a-go-go related (hERG) K+ channels. J. Biol. Chem. 2844-2853 (2009).
71. Barbuti, A., Gravante, B., Riolfo, M., Milanesi, R., Terragni, B., and DiFrancesco, D. Localization of pacemaker channels in lipid rafts regulates channel kinetics. Circ. Res. 94, 1325-1331 (2004).
72. Brainard, A.M., Miller, A.J., Martens, J.R., and England, S.K. Maxi-K channels localize to caveolae in human myometrium: a role for an actin- channel-caveolin complex in the regulation of myometrial smooth muscle K+ current. Am. J. Physiol. Cell Physiol. 289, C49-57 (2005). (Pubitemid 40880824)
73. Eldstrom, J., Van Wagoner, D.R., Moore, E.D., and Fedida, D. Localization of Kv1.5 channels in rat and canine myocyte sarcolemma. FEBS Lett. 6039-6046 (2006).
74. Martens, J.R., Navarro-Polanco, R., Coppock, E.A., Nishiyama, A., Parshley, L., Grobaski, T.D., and Tamkun, M.M. Differential targeting of Shaker-like potassium channels to lipid rafts. J. Biol. Chem. 275, 7443-7446 (2000).
75. Martens, J.R., O'Connell, K., and Tamkun, M. Targeting of ion channels to membrane microdomains: localization of KV channels to lipid rafts. Trends Pharmacol. Sci. 25, 16-21 (2004).
76. Martens, J.R., Sakamoto, N., Sullivan, S.A., Grobaski, T.D., and Tamkun, M.M. Isoform-specific localization of voltage-gated K+ channels to distinct lipid raft populations. Targeting of Kv1.5 to caveolae. J. Biol. Chem. 276, 8409-8414 (2001). (Pubitemid 37385653)
77. O'Connell, K.M., Martens, J.R., and Tamkun, M.M. Localization of ion channels to lipid Raft domains within the cardiovascular system. Trends Cardiovasc. Med. 14, 37-42 (2004).
78. Romanenko, V.G., Fang, Y., Byfield, F., Travis, A.J., Vandenberg, C.A., Rothblat, G.H., and Levitan, I. Cholesterol sensitivity and lipid raft targeting of Kir2.1 channels. Biophys. J. 87, 3850-3861 (2004).
79. Tanabe, Y., Hatada, K., Naito, N., Aizawa, Y., Chinushi, M., and Nawa, H. Over-expression of Kv1.5 in rat cardiomyocytes extremely shortens the duration of the action potential and causes rapid excitation. Biochem. Biophys. Res. Commun. 345, 1116-1121 (2006). (Pubitemid 43776519)
80. Van Wagoner, D.R., Pond, A.L., McCarthy, P.M., Trimmer, J.S., and Nerbonne, J.M. Outward K+ current densities and Kv1.5 expression are reduced in chronic human atrial fibrillation. Circ. Res. 80, 772-781 (1997).
81. Choi, W.S., Khurana, A., Mathur, R., Viswanathan, V., Steele, D.F., and Fedida, D. Kv1.5 surface expression is modulated by retrograde trafficking of newly endocytosed channels by the dynein motor. Circ. Res. 97, 363-371 (2005). (Pubitemid 41216141)
82. McEwen, D.P., Schumacher, S.M., Li, Q., Benson, M.D., Iniguez-Lluhi, J.A., Van Genderen, K.M., and Martens, J.R. Rab-GTPase-dependent endocytic recycling of KV1.5 in atrial yyocytes. J. Biol. Chem. 282, 29612-29620 (2007). (Pubitemid 350043393)
83. Zadeh, A.D., Xu, H., Loewen, M.E., Noble, G.P., Steele, D.F., and Fedida, D. Internalized Kv1.5 traffics via Rab-dependent pathways. J. Physiol. 586, 4793-4813 (2008).
84. Loewen, M.E., Wang, Z., Eldstrom, J., Dehghani Zadeh, A., Khurana, A., Steele, D.F., and Fedida, D. Shared requirement for dynein function and intact microtubule cytoskeleton for normal surface expression of cardiac potassium channels. Am. J. Physiol. Heart Circ. Physiol. 296, H71-83 (2009).
85. Seebohm, G., Strutz-Seebohm, N., Birkin, R. et al. Regulation of endocytic recycling of KCNQ1/KCNE1 potassium channels. Circ. Res. 686-692 (2007).
86. Seebohm, G., Strutz-Seebohm, N., Ureche, O.N. et al. Long QT syndrome-associated mutations in KCNQ and KCNE1 subunits disrupt normal endosomal recycling of IKs channels. Circ. Res. 103, 1451-1457 (2008).
87. Boehmer, C., Laufer, J., Jeyaraj, S., Klaus, F., Lindner, R., Lang, F., and Palmada, M. Modulation of the voltage-gated potassium channel Kv1.5 by the SGK1 protein kinase involves inhibition of channel ubiquitination. Cell. Physiol. Biochem. 22, 591-600 (2008).
88. Flowerdew, S.E. and Burgoyne, R.D. A VAMP7/Vti1a SNARE complex distinguishes a non-conventional traffic route to the cell surface used by KChIP1 and Kv4 potassium channels. Biochem. J. 529-540 (2009).
89. Zhou, Z., Gong, Q., and January, C.T. Correction of defective protein trafficking of a mutant HERG potassium channel in human long QT syndrome: Pharmacological and temperature effects. J. Biol. Chem. 274, 31123-31126 (1999).