CaMKII-dependent regulation of cardiac Na+ homeostasis

Frontiers in Pharmacology

Volumn 5 MAR, Issue , 2014, Pages

  Grandi, Eleonora ^a   Herren, Anthony W ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Arrhythmia; CaMKII; DADs

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; REACTIVE OXYGEN METABOLITE; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; SODIUM CHANNEL NAV1.5;

BRUGADA SYNDROME; CALCIUM TRANSPORT; CHANNEL GATING; EXCITATION CONTRACTION COUPLING; GENE MUTATION; HEART ARRHYTHMIA; HEART FAILURE; HEART MUSCLE POTENTIAL; HUMAN; LONG QT SYNDROME; NONHUMAN; OXIDATIVE STRESS; PROTEIN PHOSPHORYLATION; REVIEW; SODIUM BALANCE; SODIUM CELL LEVEL; SODIUM CURRENT; SODIUM TRANSPORT;

EID: 84897943657     PISSN: None     EISSN: 16639812     Source Type: Journal    
DOI: 10.3389/fphar.2014.00041     Document Type: Review

References (81)

1. Abriel, H. (2010). Cardiac sodium channel Na(v)1.5 and interacting proteins: physiology and pathophysiology. J. Mol. Cell. Cardiol. 48, 2-11. doi: 10.1016/j.yjmcc.2009.08.025.
2. 2+ exchanger function. J. Physiol. 575, 845-854. doi: 10.1113/jphysiol.2006.111252.
3. Anderson, M. E., Brown, J. H., and Bers, D. M. (2011). CaMKII in myocardial hypertrophy and heart failure. J. Mol. Cell. Cardiol. 51, 468-473. doi: 10.1016/j.yjmcc.2011.01.012.
4. 2+/calmodulin-dependent protein kinase II (CaMKII) regulates cardiac sodium channel NaV1.5 gating by multiple phosphorylation sites. J. Biol. Chem. 287, 19856-19869. doi: 10.1074/jbc.M111.322537.
5. +]i and underlies disturbed calcium handling in the rabbit pressure and volume overload heart failure model. Cardiovasc. Res. 57, 1015-1024. doi: 10.1016/S0008-6363(02)00809-X.
6. Bayer, K. U., Lebel, E., Mcdonald, G. L., O'Leary, H., Schulman, H., and De Koninck, P. (2006). Transition from reversible to persistent binding of CaMKII to postsynaptic sites and NR2B. J. Neurosci. 26, 1164-1174. doi: 10.1523/JNEUROSCI.3116-05.2006.
7. Beltran-Alvarez, P., Pagans, S., and Brugada, R. (2011). The cardiac sodium channel is post-translationally modified by arginine methylation. J. Proteome Res. 10, 3712-3719. doi: 10.1021/pr200339n.
8. +-ATPase alpha1 and alpha2 subunits in T-tubule and surface sarcolemmal membranes. Cardiovasc. Res. 73, 92-100. doi: 10.1016/j.cardiores.2006.11.006.
9. Bers, D. M., and Grandi, E. (2009). Calcium/calmodulin-dependent kinase II regulation of cardiac ion channels. J. Cardiovasc. Pharmacol. 54, 180-187. doi: 10.1097/FJC.0b013e3181a25078.
10. Bezzina, C., Veldkamp, M. W., Van Den Berg, M. P., Postma, A. V., Rook, M. B., Viersma, J. W., et al. (1999). A single Na(+) channel mutation causing both long-QT and Brugada syndromes. Circ. Res. 85, 1206-1213. doi: 10.1161/01.RES.85.12.1206.
11. Biet, M., Barajas-Martinez, H., Ton, A. T., Delabre, J. F., Morin, N., and Dumaine, R. (2012). About half of the late sodium current in cardiac myocytes from dog ventricle is due to non-cardiac-type Na(+) channels. J. Mol. Cell. Cardiol. 53, 593-598. doi: 10.1016/j.yjmcc.2012.06.012.
12. Bossuyt, J., Ai, X., Moorman, J. R., Pogwizd, S. M., and Bers, D. M. (2005). Expression and phosphorylation of the na-pump regulatory subunit phospholemman in heart failure. Circ. Res. 97, 558-565. doi: 10.1161/01.RES.0000181172.27931.c3.
13. Brette, F., and Orchard, C. H. (2006). Density and sub-cellular distribution of cardiac and neuronal sodium channel isoforms in rat ventricular myocytes. Biochem. Biophys. Res. Commun. 348, 1163-1166. doi: 10.1016/j.bbrc.2006.07.189.
14. Camors, E., Mohler, P. J., Bers, D. M., and Despa, S. (2012). Ankyrin-B reduction enhances Ca spark-mediated SR Ca release promoting cardiac myocyte arrhythmic activity. J. Mol. Cell. Cardiol. 52, 1240-1248. doi: 10.1016/j.yjmcc.2012.02.010.
15. + in cardiac cells? Cardiovasc. Res. 26, 433-442. doi: 10.1093/cvr/26.5.433.
16. Clancy, C. E., and Rudy, Y. (2002). Na(+) channel mutation that causes both Brugada and long-QT syndrome phenotypes: a simulation study of mechanism. Circulation 105, 1208-1213. doi: 10.1161/hc1002.105183.
17. Coppini, R., Ferrantini, C., Yao, L., Fan, P., Del Lungo, M., Stillitano, F., et al. (2013). Late sodium current inhibition reverses electromechanical dysfunction in human hypertrophic cardiomyopathy. Circulation 127, 575-584. doi: 10.1161/CIRCULATIONAHA.112.134932.
18. Coyan, F., Burel, S., Lichti, C. F., Brown, J. H., Charpentier, F., Nerbonne, J. M., et al. (2014). Phosphoproteomic identification of CaMKII-and heart failure-dependent phosphorylation sites on the native cardiac Nav1.5 channel protein. Biophys. J. 106, 37a.
19. Davis, R. P., Casini, S., Van Den Berg, C. W., Hoekstra, M., Remme, C. A., Dambrot, C., et al. (2012). Cardiomyocytes derived from pluripotent stem cells recapitulate electrophysiological characteristics of an overlap syndrome of cardiac sodium channel disease. Circulation 125, 3079-3091. doi: 10.1161/CIRCULATIONAHA.111.066092.
20. DeGrande, S., Nixon, D., Koval, O., Curran, J. W., Wright, P., Wang, Q., et al. (2012). CaMKII inhibition rescues proarrhythmic phenotypes in the model of human ankyrin-B syndrome. Heart Rhythm 9, 2034-2041. doi: 10.1016/j.hrthm.2012.08.026.
21. +-ATPase isoform distribution in rat ventricular myocytes. Am. J. Physiol. Cell Physiol. 293, C321-327. doi: 10.1152/ajpcell.00597.2006.
22. Despa, S., and Bers, D. M. (2013). Na(+) transport in the normal and failing heart-Remember the balance. J. Mol. Cell. Cardiol. 61, 2-10. doi: 10.1016/j.yjmcc.2013.04.011.
23. Despa, S., Islam, M. A., Weber, C. R., Pogwizd, S. M., and Bers, D. M. (2002). Intracellular Na(+) concentration is elevated in heart failure but Na/K pump function is unchanged. Circulation 105, 2543-2548. doi: 10.1161/01.CIR.0000016701.85760.97.
24. Edwards, A. G., Hake, J., Heller Brown, J., and McCulloch, A. D. (2012). βAr-stimulation causes EADs but not DADs in pre-failure CAMKIIdC transgenic myocytes. Biophys. J. 102, 98a. doi: 10.1016/j.bpj.2011.11.559.
25. Erickson, J. R., Joiner, M. L., Guan, X., Kutschke, W., Yang, J., Oddis, C. V., et al. (2008). A dynamic pathway for calcium-independent activation of CaMKII by methionine oxidation. Cell 133, 462-474. doi: 10.1016/j.cell.2008.02.048.
26. Gonano, L. A., Sepulveda, M., Rico, Y., Kaetzel, M., Valverde, C. A., Dedman, J., et al. (2011). Calcium-calmodulin kinase II mediates digitalis-induced arrhythmias. Circ. Arrhythm. Electrophysiol. 4, 947-957. doi: 10.1161/CIRCEP.111.964908.
27. 2+ model: sinus rhythm and chronic atrial fibrillation. Circ. Res. 109, 1055-1066. doi: 10.1161/CIRCRESAHA.111.253955.
28. Grandi, E., Pasqualini, F. S., and Bers, D. M. (2010). A novel computational model of the human ventricular action potential and Ca transient. J. Mol. Cell. Cardiol. 48, 112-121. doi: 10.1016/j.yjmcc.2009.09.019.
29. Grandi, E., Puglisi, J. L., Wagner, S., Maier, L. S., Severi, S., and Bers, D. M. (2007). Simulation of Ca-calmodulin-dependent protein kinase II on rabbit ventricular myocyte ion currents and action potentials. Biophys. J. 93, 3835-3847. doi: 10.1529/biophysj.107.114868.
30. Grant, A. O., Carboni, M. P., Neplioueva, V., Starmer, C. F., Memmi, M., Napolitano, C., et al. (2002). Long QT syndrome, Brugada syndrome, and conduction system disease are linked to a single sodium channel mutation. J. Clin. Invest. 110, 1201-1209. doi: 10.1172/JCI0215570.
31. Herren, A. W., Bers, D. M., and Grandi, E. (2013). Post-translational modifications of the cardiac Na channel: contribution of CaMKII-dependent phosphorylation to acquired arrhythmias. Am. J. Physiol. Heart Circ. Physiol. 305, H431-H445. doi: 10.1152/ajpheart.00306.2013.
32. Hund, T. J., Koval, O. M., Li, J., Wright, P. J., Qian, L., Snyder, J. S., et al. (2010). A beta(IV)-spectrin/CaMKII signaling complex is essential for membrane excitability in mice. J. Clin. Invest. 120, 3508-3519. doi: 10.1172/JCI43621.
33. Jayasinghe, I. D., Cannell, M. B., and Soeller, C. (2009). Organization of ryanodine receptors, transverse tubules, and sodium-calcium exchanger in rat myocytes. Biophys. J. 97, 2664-2673. doi: 10.1016/j.bpj.2009.08.036.
34. Kapa, S., Tester, D. J., Salisbury, B. A., Harris-Kerr, C., Pungliya, M. S., Alders, M., et al. (2009). Genetic testing for long-QT syndrome: distinguishing pathogenic mutations from benign variants. Circulation 120, 1752-1760. doi: 10.1161/CIRCULATIONAHA.109.863076.
35. Kapplinger, J. D., Tester, D. J., Alders, M., Benito, B., Berthet, M., Brugada, J., et al. (2010). An international compendium of mutations in the SCN5A-encoded cardiac sodium channel in patients referred for Brugada syndrome genetic testing. Heart Rhythm 7, 33-46. doi: 10.1016/j.hrthm.2009.09.069.
36. + channel in cardiac disease. Circulation 126, 2084-2094. doi: 10.1161/CIRCULATIONAHA.112.105320.
37. Li, L., Louch, W. E., Niederer, S. A., Aronsen, J. M., Christensen, G., Sejersted, O. M., et al. (2012). Sodium accumulation in SERCA knockout-induced heart failure. Biophys. J. 102, 2039-2048. doi: 10.1016/j.bpj.2012.03.045.
38. Lin, X., Liu, N., Lu, J., Zhang, J., Anumonwo, J. M., Isom, L. L., et al. (2011). Subcellular heterogeneity of sodium current properties in adult cardiac ventricular myocytes. Heart Rhythm 8, 1923-1930. doi: 10.1016/j.hrthm.2011.07.016.
39. Litwin, S. E., Li, J., and Bridge, J. H. (1998). Na-Ca exchange and the trigger for sarcoplasmic reticulum Ca release: studies in adult rabbit ventricular myocytes. Biophys. J. 75, 359-371. doi: 10.1016/S0006-3495(98)77520-4.
40. 2+ uptake in myocytes from failing hearts restores energy supply and demand matching. Circ. Res. 103, 279-288. doi: 10.1161/CIRCRESAHA.108.175919.
41. Ma, J., Luo, A., Wu, L., Wan, W., Zhang, P., Ren, Z., et al. (2012). Calmodulin kinase II and protein kinase C mediate the effect of increased intracellular calcium to augment late sodium current in rabbit ventricular myocytes. Am. J. Physiol. Cell Physiol. 302, C1141-C1151. doi: 10.1152/ajpcell.00374.2011.
42. Makielski, J. C., and Farley, A. L. (2006). Na(+) current in human ventricle: implications for sodium loading and homeostasis. J. Cardiovasc. Electrophysiol. 17(Suppl. 1), S15-S20. doi: 10.1111/j.1540-8167.2006.00380.x.
43. + channel isoform Nav1.5 is modulated by its beta1 subunit. J. Physiol. Sci. 59, 217-225. doi: 10.1007/s12576-009-0029-7.
44. Marionneau, C., Lichti, C. F., Lindenbaum, P., Charpentier, F., Nerbonne, J. M., Townsend, R. R., et al. (2012). Mass spectrometry-based identification of native cardiac Nav1.5 channel alpha subunit phosphorylation sites. J. Proteome Res. 11, 5994-6007. doi: 10.1021/pr300702.
45. Mohler, P. J., Rivolta, I., Napolitano, C., Lemaillet, G., Lambert, S., Priori, S. G., et al. (2004). Nav1.5 E1053K mutation causing Brugada syndrome blocks binding to ankyrin-G and expression of Nav1.5 on the surface of cardiomyocytes. Proc. Natl. Acad. Sci. U.S.A. 101, 17533-17538. doi: 10.1073/pnas.0403711101.
46. Mohler, P. J., Schott, J. J., Gramolini, A. O., Dilly, K. W., Guatimosim, S., Dubell, W. H., et al. (2003). Ankyrin-B mutation causes type 4 long-QT cardiac arrhythmia and sudden cardiac death. Nature 421, 634-639. doi: 10.1038/nature01335.
47. Moreno, J. D., Yang, P. C., Bankston, J. R., Grandi, E., Bers, D. M., Kass, R. S., et al. (2013). Ranolazine for congenital and acquired late INa linked arrhythmias: in silico pharmacologic screening. Circ. Res. 113, e50-e61. doi: 10.1161/CIRCRESAHA.113.301971.
48. + loading and CaMKII. J. Physiol. doi: 10.1113/jphysiol.2013.266676 [Epub ahead of print].
49. Murphy, B. J., Rogers, J., Perdichizzi, A. P., Colvin, A. A., and Catterall, W. A. (1996). cAMP-dependent phosphorylation of two sites in the alpha subunit of the cardiac sodium channel. J. Biol. Chem. 271, 28837-28843. doi: 10.1074/jbc.271.46.28837.
50. Pandey, D., Gratton, J. P., Rafikov, R., Black, S. M., and Fulton, D. J. (2011). Calcium/calmodulin-dependent kinase II mediates the phosphorylation and activation of NADPH oxidase 5. Mol. Pharmacol. 80, 407-415. doi: 10.1124/mol.110.070193.
51. Petitprez, S., Zmoos, A. F., Ogrodnik, J., Balse, E., Raad, N., El-Haou, S., et al. (2011). SAP97 and dystrophin macromolecular complexes determine two pools of cardiac sodium channels Nav1.5 in cardiomyocytes. Circ. Res. 108, 294-304. doi: 10.1161/CIRCRESAHA.110.228312.
52. Pogwizd, S. M., Sipido, K. R., Verdonck, F., and Bers, D. M. (2003). Intracellular Na in animal models of hypertrophy and heart failure: contractile function and arrhythmogenesis. Cardiovasc. Res. 57, 887-896. doi: 10.1016/S0008-6363(02)00735-6.
53. Priori, S. G., Napolitano, C., Giordano, U., Collisani, G., and Memmi, M. (2000). Brugada syndrome and sudden cardiac death in children. Lancet 355, 808-809. doi: 10.1016/S0140-6736(99)05277-0.
54. Remme, C. A., Wilde, A. A., and Bezzina, C. R. (2008). Cardiac sodium channel overlap syndromes: different faces of SCN5A mutations. Trends Cardiovasc. Med. 18, 78-87. doi: 10.1016/j.tcm.2008.01.002.
55. Sag, C. M., Wadsack, D. P., Khabbazzadeh, S., Abesser, M., Grefe, C., Neumann, K., et al. (2009). Calcium/calmodulin-dependent protein kinase II contributes to cardiac arrhythmogenesis in heart failure. Circ. Heart Fail. 2, 664-675. doi: 10.1161/CIRCHEARTFAILURE.109.865279.
56. +-ATPase inhibition by ouabain induces CaMKII-dependent apoptosis in adult rat cardiac myocytes. J. Mol. Cell. Cardiol. 49, 459-468. doi: 10.1016/j.yjmcc.2010.04.013.
57. Sato, P. Y., Coombs, W., Lin, X., Nekrasova, O., Green, K. J., Isom, L. L., et al. (2011). Interactions between ankyrin-G, Plakophilin-2, and Connexin43 at the cardiac intercalated disc. Circ. Res. 109, 193-201. doi: 10.1161/CIRCRESAHA.111.247023.
58. Sepulveda, M., Gonano, L. A., Back, T. G., Chen, S. R., and Vila Petroff, M. (2013). Role of CaMKII and ROS in rapid pacing-induced apoptosis. J. Mol. Cell. Cardiol. 63, 135-145. doi: 10.1016/j.yjmcc.2013.07.013.
59. Shryock, J. C., Song, Y., Rajamani, S., Antzelevitch, C., and Belardinelli, L. (2013). The arrhythmogenic consequences of increasing late INa in the cardiomyocyte. Cardiovasc. Res. 99, 600-611. doi: 10.1093/cvr/cvt145.
60. Song, Y., Shryock, J. C., and Belardinelli, L. (2008). An increase of late sodium current induces delayed afterdepolarizations and sustained triggered activity in atrial myocytes. Am. J. Physiol. Heart Circ. Physiol. 294, H2031-H2039. doi: 10.1152/ajpheart.01357.2007.
61. Sossalla, S., Maurer, U., Schotola, H., Hartmann, N., Didie, M., Zimmermann, W. H., et al. (2011). Diastolic dysfunction and arrhythmias caused by overexpression of CaMKIIdelta(C) can be reversed by inhibition of late Na(+) current. Basic Res. Cardiol. 106, 263-272. doi: 10.1007/s00395-010-0136-x.
62. Tan, H. L., Bink-Boelkens, M. T., Bezzina, C. R., Viswanathan, P. C., Beaufort-Krol, G. C., Van Tintelen, P. J., et al. (2001). A sodium-channel mutation causes isolated cardiac conduction disease. Nature 409, 1043-1047. doi: 10.1038/35059090.
63. Tester, D. J., Valdivia, C., Harris-Kerr, C., Alders, M., Salisbury, B. A., Wilde, A. A., et al. (2010). Epidemiologic, molecular, and functional evidence suggest A572D-SCN5A should not be considered an independent LQT3-susceptibility mutation. Heart Rhythm 7, 912-919. doi: 10.1016/j.hrthm.2010.04.014.
64. Tester, D. J., Will, M. L., Haglund, C. M., and Ackerman, M. J. (2005). Compendium of cardiac channel mutations in 541 consecutive unrelated patients referred for long QT syndrome genetic testing. Heart Rhythm 2, 507-517. doi: 10.1016/j.hrthm.2005.01.020.
65. Toischer, K., Hartmann, N., Wagner, S., Fischer, T. H., Herting, J., Danner, B. C., et al. (2013). Role of late sodium current as a potential arrhythmogenic mechanism in the progression of pressure-induced heart disease. J. Mol. Cell. Cardiol. 61, 111-122. doi: 10.1016/j.yjmcc.2013.03.021.
66. Veldkamp, M. W., Viswanathan, P. C., Bezzina, C., Baartscheer, A., Wilde, A. A., and Balser, J. R. (2000). Two distinct congenital arrhythmias evoked by a multidysfunctional Na(+) channel. Circ. Res. 86, E91-E97. doi: 10.1161/01.RES.86.9.e91.
67. Vila-Petroff, M., Mundina-Weilenmann, C., Lezcano, N., Snabaitis, A. K., Huergo, M. A., Valverde, C. A., et al. (2010). Ca(2+)/calmodulin-dependent protein kinase II contributes to intracellular pH recovery from acidosis via Na(+)/H(+) exchanger activation. J. Mol. Cell. Cardiol. 49, 106-112. doi: 10.1016/j.yjmcc.2009.12.007.
68. Viswanathan, P. C., Benson, D. W., and Balser, J. R. (2003). A common SCN5A polymorphism modulates the biophysical effects of an SCN5A mutation. J. Clin. Invest. 111, 341-346. doi: 10.1172/JCI200316879.
69. + channels. J. Clin. Invest. 116, 3127-3138. doi: 10.1172/JCI26620.
70. Wagner, S., Ruff, H. M., Weber, S. L., Bellmann, S., Sowa, T., Schulte, T., et al. (2011). Reactive oxygen species-activated Ca/calmodulin kinase IIdelta is required for late I(Na) augmentation leading to cellular Na and Ca overload. Circ. Res. 108, 555-565. doi: 10.1161/CIRCRESAHA.110.221911.
71. Wan, X., Chen, S., Sadeghpour, A., Wang, Q., and Kirsch, G. E. (2001). Accelerated inactivation in a mutant Na(+) channel associated with idiopathic ventricular fibrillation. Am. J. Physiol. Heart Circ. Physiol. 280, H354-H360.
72. 2+ exchange current. Circ. Res. 92, 950-952. doi: 10.1161/01.RES.0000071747.61468.7F.
73. Weber, C. R., Piacentino, V. III, Houser, S. R., and Bers, D. M. (2003b). Dynamic regulation of sodium/calcium exchange function in human heart failure. Circulation 108, 2224-2229. doi: 10.1161/01.CIR.0000095274.72486.94.
74. + channel SCN5A associated with long-QT syndrome (LQT3): a role for the I-II linker in inactivation gating. Hum. Mutat. 21, 552. doi: 10.1002/humu.9136.
75. Wilde, A. A., and Brugada, R. (2011). Phenotypical manifestations of mutations in the genes encoding subunits of the cardiac sodium channel. Circ. Res. 108, 884-897. doi: 10.1161/CIRCRESAHA.110.238469.
76. Xi, Y., Wu, G., Yang, L., Han, K., Du, Y., Wang, T., et al. (2009). Increased late sodium currents are related to transcription of neuronal isoforms in a pressure-overload model. Eur. J. Heart Fail. 11, 749-757. doi: 10.1093/eurjhf/hfp092.
77. Yang, P., Kanki, H., Drolet, B., Yang, T., Wei, J., Viswanathan, P. C., et al. (2002). Allelic variants in long-QT disease genes in patients with drug-associated torsades de pointes. Circulation 105, 1943-1948. doi: 10.1161/01.CIR.0000014448.19052.4C.
78. Yang, T., Atack, T. C., Stroud, D. M., Zhang, W., Hall, L., and Roden, D. M. (2012). Blocking Scn10a channels in heart reduces late sodium current and is antiarrhythmic. Circ. Res. 111, 322-332. doi: 10.1161/CIRCRESAHA.112.265173.
79. + influx activates CaMKII in rat ventricular myocytes and N1325S mice. Am. J. Physiol. Cell Physiol. 301, C577-C586. doi: 10.1152/ajpcell.00125.2011.
80. Zhou, J., Yi, J., Hu, N., George, A. L. Jr., and Murray, K. T. (2000). Activation of protein kinase A modulates trafficking of the human cardiac sodium channel in Xenopus oocytes. Circ. Res. 87, 33-38. doi: 10.1161/01.RES.87.1.33.
81. Zhu, L. J., Klutho, P. J., Scott, J. A., Xie, L., Luczak, E. D., Dibbern, M. E., et al. (2014). Oxidative activation of the Ca/calmodulin-dependent protein kinase II (CaMKII) regulates vascular smooth muscle migration and apoptosis. Vascul. Pharmacol. 60, 75-83. doi: 10.1016/j.vph.2014.01.001.