Proton-dependent inhibition of the cardiac sodium channel Nav1.5 by ranolazine

Frontiers in Pharmacology

Volumn 4 JUN, Issue , 2013, Pages

  Sokolov, S ^a   Peters, C H ^a   Rajamani, S ^b   Ruben, P C ^a  

^a SIMON FRASER UNIVERSITY   (Canada)

^b GILEAD SCIENCES   (United States)

Author keywords

Acidosis; Cardiac sodium channel; Electrophysiology; Nav1.5; Ranolazine

Indexed keywords

CARDIAC SODIUM CHANNEL NAV1.5; RANOLAZINE; SODIUM CHANNEL NAV1.5; UNCLASSIFIED DRUG;

ACIDIFICATION; ARTICLE; BIOLOGICAL ACTIVITY; CONTROLLED STUDY; DEPOLARIZATION; DRUG ACTIVITY; HUMAN; HUMAN CELL; PH; PROTEIN CONFORMATION; PROTEIN INTERACTION; PROTON DEPENDENT INHIBITION; SODIUM CURRENT; STEADY STATE;

EID: 84881608904     PISSN: None     EISSN: 16639812     Source Type: Journal    
DOI: 10.3389/fphar.2013.00078     Document Type: Article

References (55)

1. Amin, A., Asghari-Roodsari, A., and Tan, H. (2010). Cardiac sodium channelopathies. Pflugers Arch. 460, 223-237. doi: 10.1007/s00424-009-0761-0.
2. Antzelevitch, C., Burashnikov, A., Sicouri, S., and Belardinelli, L. (2011). Electrophysiologic basis for the antiarrhythmic actions of ranolazine. Heart Rhythm 8, 1281-1290. doi: 10.1016/j.hrthm.2011.03.045.
3. Belardinelli, L., Shryock, J., and Fraser, H. (2006). Inhibition of the late sodium current as a potential cardioprotective principle: effects of the late sodium current inhibitor ranolazine. Heart 92(Suppl. 4), iv6-iv14. doi: 10.1136/hrt.2005.078790.
4. Benitah, J., Balser, J., Marban, E., and Tomaselli, G. (1997). Proton inhibition of sodium channels: mechanism of gating shifts and reduced conductance. J. Membr. Biol. 155, 121-131. doi: 10.1007/s002329900164.
5. Burashnikov, A., and Antzelevitch, C. (2008). Atrial-selective sodium channel blockers: do they exist. J. Cardiovasc. Pharmacol. 52, 121-128. doi: 10.1097/FJC.0b013e31817618eb.
6. Burashnikov, A., and Antzelevitch, C. (2009). Atrial-selective sodium channel block for the treatment of atrial fibrillation. Expert Opin. Emerg. Drugs 14, 233-249. doi: 10.1517/14728210902997939.
7. Burashnikov, A., and Antzelevitch, C. (2010). New development in atrial antiarrhythmic drug therapy. Nat. Rev. Cardiol. 7, 139-148. doi: 10.1038/nrcardio.2009.245.
8. Burashnikov, A., Diego, J. D., Zygmunt, A., Belardinelli, L., and Antzelevitch, C. (2007). Atrium-selective sodium channel block as a strategy for suppression of atrial fibrillation: differences in sodium channel inactivation between atria and ventricles and the role of ranolazine. Circulation 116, 1449-1457. doi: 10.1161/CIRCULATIONAHA.107.704890.
9. Carmeliet, E. (1999). Cardiac ionic currents and acute ischemia: from channels to arrhythmias. Physiol. Rev. 79, 917-1017.
10. Chaitman, M. D. (2006). Ranolazine for the treatment of chronic angina and potential use in other cardiovascular conditions. Circulation 113, 2462-2472. doi: 10.1161/CIRCULATIONAHA.105.597500.
11. ++ overload and left ventricular mechanical dysfunction. J. Cardiovasc. Electrophysiol. 17, 141-148. doi: 10.1111/j.1540-8167.2006.00395.x.
12. Crampin, E. J., Smith, N. P., Langham, A. E., Clayton, R. H., and Orchard, C. H. (2006). Acidosis in models of cardiac ventricular myocytes. Philos. Trans. A Math. Phys. Eng. Sci. 364, 1171-1186. doi: 10.1098/rsta.2006.1763.
13. + currents in human lymphocytes by pH. J. Physiol. 413, 399-413.
14. Dobrev, D., and Nattel, S. (2010). New antiarrhythmic drugs for treatment of atrial fibrillation. Lancet 375, 1212-1223. doi: 10.1016/S0140-6736(10)60096-7.
15. El-Bizri, N., Kahlig, K., Shyrock, J., George, A. L. J., Belardinelli, L., and Rajamani, S. (2011). Ranolazine block of human Nav1.4 sodium channels and paramyotonia congenita mutants. Channels 5, 161-172. doi: 10.4161/chan.5.2.14851.
16. Errington, A. C., Stoehr, T., Heers, C., and Lees, G. (2008). The investigational anticonvulsant lacosamide selectively enhances slow inactivation of voltage-gated sodium channels. Mol. Pharmacol. 73, 157-169. doi: 10.1124/mol.107.039867.
17. Estacion, M., Waxman, S. G., and Dib-Hajj, S. D. (2010). Effects of ranolazine on wild-type and mutant hNav1.7 channels and on DRG neuron excitability. Mol. Pain 6, 1-13. doi: 10.1186/1744-8069-6-35.
18. Fozzard, H., Lee, P., and Lipkind, G. (2005). Mechanism of local anesthetic drug action on voltage-gated sodium channels. Curr. Pharm. Des. 11, 2671-2686. doi: 10.2174/1381612054546833.
19. Fredj, S., Sampson, K., Liu, H., and Kass, R. (2006). Molecular basis of ranolazine block of LQT-3 mutant sodium channels: evidence for site of action. Br. J. Pharmacol. 148, 16-24. doi: 10.1038/sj.bjp.0706709.
20. Gould, H., Garrett, C., Donahue, R., Paul, D., Diamond, I., and Taylor, B. (2009). Ranolazine attenuates behavioral signs of neuropathic pain. Behav. Pharmacol. 20, 755-758. doi: 10.1097/FBP.0b013e3283323c90.
21. Hale, S., Leeka, J., and Kloner, R. (2006). Improved left ventricular function and reduced necrosis after myocardial ischemia/reperfusion in rabbits treated with ranolazine, an inhibitor of the late sodium channel. J. Pharmacol. Exp. Ther. 318, 418-423. doi: 10.1124/jpet.106.103242.
22. Hale, S., Shryock, J., Belardinelli, L., Sweeney, M., and Kloner, R. (2008). Late sodium current inhibition as a new cardioprotective approach. J. Mol. Cell. Cardiol. 44, 954-967. doi: 10.1016/j.yjmcc.2008.03.019.
23. Hille, B. (1968). Charges and potentials at the nerve surface. divalent ions and pH. J. Gen. Physiol. 51, 221-236. doi: 10.1085/jgp.51.2.221.
24. Hille, B. (1977). Local anesthetics: hydrophilic and hydrophobic pathways for the drug-receptor reaction. J. Gen. Physiol. 69, 497-515. doi: 10.1085/jgp.69.4.497.
25. + currents and suppression of action potentials in embryonic rat dorsal root ganglion neurons by ranolazine. Neuropharmacology 62, 2251-2260. doi: 10.1016/j.neuropharm.2012.01.021.
26. + current and potentiates ranolazine inhibition of Nav1.5 channels. Am. J. Physiol. Heart Circ. Physiol. 300, H288-H299. doi: 10.1152/ajpheart.00539.2010.
27. Jerling, M., and Abdallah, H. (2005). Effect of renal impairment on multiple-dose pharmacokinetics of extended-release ranolazine. Clin. Pharmacol. Ther. 78, 288-297. doi: 10.1016/j.clpt.2005.05.004.
28. Jones, D. K., Peters, C. H., Tolhurst, S. A., Claydon, T. W., and Ruben, P. C. (2011). Extracellular proton modulation of the cardiac voltage-gated sodium channel, Nav1.5. Biophys. J. 101, 2147-2156. doi: 10.1016/j.bpj.2011.08.056.
29. Kahlig, K. M., Lepist, I., Leung, K., Rajamani, S., and George, A. L. (2010). Ranolazine selectively blocks persistent current evoked by epilepsy-associated Nav1.1 mutations. Br. J. Pharmacol. 161, 1414-1426. doi: 10.1111/j.1476-5381.2010.00976.x.
30. 2+. J. Physiol. 541, 9-24. doi: 10.1113/jphysiol.2001.014456.
31. Khan, A., Kyle, J., Hanck, D., Lipkind, G., and Fozzard, H. (2006). Isoform-dependent interaction of voltage-gated sodium channels with protons. J. Physiol. 576, 493-501. doi: 10.1113/jphysiol.2006.115659.
32. Khan, A., Romantseva, L., Lam, A., Lipkind, G., and Fozzard, H. (2002). Role of outer ring carboxylates of the rat skeletal muscle sodium channel pore in proton block. J. Physiol. 543, 71-84. doi: 10.1113/jphysiol.2002.021014.
33. Magyar, J., Kiper, C. E., Dumaine, R., Burgess, D. E., Bányász, T., and Satin, J. (2004). Divergent action potential morphologies reveal nonequilibrium properties of human cardiac Na channels. Cardiovasc Res. 64, 477-487. doi: 10.1016/j.cardiores.2004.07.014.
34. Maruki, Y., Koehler, R. C., Eleff, S. M., and Traystman, R. J. (1993). Intracellular pH during reperfusion influences evoked potential recovery after complete cerebral ischemia. Stroke 24, 697-703. doi: 10.1161/01.STR.24.5.697.
35. Moreno, J. D., Zhu, Z. I., Yang, P. C., Bankston, J. R., Jeng, M. T., Kang, C., et al. (2011). A computational model to predict the effects of class I anti-arrhythmic drugs on ventricular rhythms. Sci. Transl. Med. 3, 98ra83. doi: 10.1126/scitranslmed.3002588.
36. Moss, A. J., Zareba, W., Schwarz, K. Q., Rosero, S., McNitt, S., and Robinson, J. L. (2008). Ranolazine shortens repolarization in patients with sustained inward sodium current due to type-3 long-QT syndrome. J. Cardiovasc. Electrophysiol. 19, 1289-1293. doi: 10.1111/j.1540-8167.2008.01246.x.
37. + current in the canine left ventricle. Am. J. Physiol. Heart Circ. Physiol. 301, H936-H944. doi: 10.1152/ajpheart.00204.2011.
38. Peters, C., Sokolov, S., Rajamani, S., and Ruben, P. C. (2013). The actions of the antianginal drug, Ranolazine, on the brain sodium channel NaV1.2 and its modulation by extracellular protons. Br. J. Pharmacol. 169, 704-716. doi: 10.1111/bph.12150.
39. Rajamani, S., El-Bizri, N., Shryock, J. C., Makielski, J. C., and Belardinelli, L. (2009). Use-dependent block of cardiac late Na(+) current by ranolazine. Heart Rhythm 6, 1625-1631. doi: 10.1016/j.hrthm.2009.07.042.
40. Rajamani, S., Shryock, J. C., and Belardinelli, L. (2008). Block of tetrodotoxin-sensitive, Nav1.7 and tetrodotoxin-resistant, Nav1.8, Na channels by ranolazine. Channels 2, 449-460. doi: 10.4161/chan.2.6.7362.
41. Reddy, B., Weintraub, H., and Schwartzbard, A. (2010). Ranolazine: a new approach to treating an old problem. Tex. Heart Inst. J. 37, 641-647.
42. Sokolov, S., Kraus, R., Scheuer, T., and Catterall, W. (2008). Inhibition of sodium channel gating by trapping the domain II voltage sensor with protoxin II. Mol. Pharmacol. 73, 1020-1028. doi: 10.1124/mol.107.041046.
43. + currents in atrial fibrillation: effects of ranolazine on arrhythmias and contractility in human atrial myocardium. J. Am. Coll. Cardiol. 55, 2330-2342. doi: 10.1016/j.jacc.2009.12.055.
44. Sossalla, S., Wagner, S., Rasenack, E. C., Ruff, H., Weber, S. L., Schondube, F. A., et al. (2008). Ranolazine Improves diastolic dysfunction in isolated myocardium from failing human hearts-role of late sodium current and intracellular ion accumulation. J. Mol. Cell. Cardiol. 45, 32-43. doi: 10.1016/j.yjmcc.2008.03.006.
45. Stone, P. H., Chaitman, B. R., Stocke, K., Sano, J., DeVault, A., and Koch, G. G. (2010). The anti-ischemic mechanism of action of ranolazine in stable ischemic heart disease. J. Am. Coll. Cardiol. 56, 934-942. doi: 10.1016/j.jacc.2010.04.042.
46. + channels. Neuron 18, 675-682. doi: 10.1016/S0896-6273(00)80307-4.
47. Trapani, J. G., and Korn, S. J. (2003). Effect of external pH on activation of the Kv1.5 potassium channel. Biophys. J. 84, 195-204. doi: 10.1016/S0006-3495(03)74842-5.
48. Undrovinas, A. I., Belardinelli, L., Undrovinas, N. A., and Sabbah, H. N. (2006). Ranolazine improves abnormal repolarization and contraction in left ventricular myocytes of dogs with heart failure by inhibiting late sodium current. J. Cardiovasc. Electrophysiol. 17, S169-S177. doi: 10.1111/j.1540-8167.2006.00401.x.
49. 2+ accumulation in chronic heart failure. J. Physiol. Sci. 60, 245-257. doi: 10.1007/s12576-010-0092-0.
50. Vilin, Y. Y., Peters, C. H., and Ruben, P. C. (2012). Acidosis differentially modulates inactivation in Nav1.2, Nav1.4, and Nav1.5 channels. Front. Pharmacol. 3:109. doi: 10.3389/fphar.2012.00109.
51. Wang, G. K., Calderon, J., and Wang, S.-Y. (2008). State- and use-dependent block of muscle Nav1.4 and neuronal Nav1.7 voltage-gated Na channel isoforms by ranolazine. Mol. Pharmacol. 73, 940-948. doi: 10.1124/mol.107.041541.
52. + channel voltage sensor. Proc. Natl. Acad. Sci. U.S.A. 108, 15426-15431. doi: 10.1073/pnas.1112320108.
53. Wasserstrom, J. A., Sharma, R., O'Toole, M. J., Zheng, J., Kelly, J. E., Shryock, J., et al. (2009). Ranolazine antagonizes the effects of increased late sodium current on intracellular calcium cycling in rat isolated intact heart. J. Pharmacol. Exper. Ther. 331, 382-391. doi: 10.1124/jpet.109.156471.
54. Wu, L., Shryock, J. C., Song, Y., Li, Y., Antzelevitch, C., and Belardinelli, L. (2004). Antiarrhythmic effects of ranolazine in a guinea pig in vitro model of long-QT syndrome. J. Pharmacol. Exper. Ther. 310, 599-605. doi: 10.1124/jpet.104.066100.
55. Zhang, J., Yarov-Yarovoy, V., Scheuer, T., Karbat, I., Cohen, L., Gordon, D., et al. (2011). Structure-function map of the receptor site for β-scorpion toxins in domain II of voltage-gated sodium channels. J. Biol. Chem. 86, 33641-33651. doi: 10.1074/jbc.M111.282509.