Slow [Na]i Changes and Positive Feedback between Membrane Potential and [Ca]i Underlie Intermittent Early Afterdepolarizations and Arrhythmias

Circulation: Arrhythmia and Electrophysiology

Volumn 8, Issue 6, 2015, Pages 1472-1480

  Xie, Yuanfang ^a   Liao, Zhandi ^a   Grandi, Eleonora ^a   Shiferaw, Yohannes ^b   Bers, Donald M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CALIFORNIA STATE UNIVERSITY   (United States)

Author keywords

Action potentials; arrhythmias; calcium; cardiac; feedback; sodium

Indexed keywords

CALCIUM; SODIUM; SODIUM CALCIUM EXCHANGE PROTEIN;

ACTION POTENTIAL DURATION; ARTICLE; CALCIUM CELL LEVEL; DEPOLARIZATION; FEEDBACK SYSTEM; HEART ARRHYTHMIA; HEART MUSCLE CELL; HEART REPOLARIZATION; ION CURRENT; MATHEMATICAL MODEL; MEMBRANE POTENTIAL; NEGATIVE FEEDBACK; POSITIVE FEEDBACK; PRIORITY JOURNAL; SIMULATION; SODIUM CELL LEVEL; SYSTEM ANALYSIS; ANIMAL; ARRHYTHMIAS, CARDIAC; BIOLOGICAL MODEL; CALCIUM SIGNALING; CARDIAC MUSCLE CELL; COMPUTER SIMULATION; HEART MUSCLE CONDUCTION SYSTEM; HEART PACING; HEART RATE; IN VITRO STUDY; KINETICS; MALE; METABOLISM; PATHOPHYSIOLOGY; RABBIT;

ANIMALS; ARRHYTHMIAS, CARDIAC; CALCIUM; CALCIUM SIGNALING; CARDIAC PACING, ARTIFICIAL; COMPUTER SIMULATION; FEEDBACK, PHYSIOLOGICAL; HEART CONDUCTION SYSTEM; HEART RATE; IN VITRO TECHNIQUES; KINETICS; MALE; MEMBRANE POTENTIALS; MODELS, CARDIOVASCULAR; MYOCYTES, CARDIAC; RABBITS; SODIUM;

EID: 84950131464     PISSN: 19413149     EISSN: 19413084     Source Type: Journal    
DOI: 10.1161/CIRCEP.115.003085     Document Type: Article

References (40)

1. Toivonen L. Spontaneous variability in the frequency of ventricular premature complexes over prolonged intervals and implications for antiarrhythmic treatment. Am J Cardiol. 1987;60:608-612.
2. Morganroth J, Michelson EL, Horowitz LN, Josephson ME, Pearlman AS, Dunkman WB. Limitations of routine long-term electrocardiographic monitoring to assess ventricular ectopic frequency. Circulation. 1978;58(3 Pt 1):408-414.
3. Weiss JN, Garfinkel A, Karagueuzian HS, Chen PS, Qu Z. Early afterdepolarizations and cardiac arrhythmias. Heart Rhythm. 2010;7:1891-1899. doi: 10.1016/j.hrthm.2010.09.017.
4. Clancy CE, Tateyama M, Liu H, Wehrens XH, Kass RS. Nonequilibrium gating in cardiac Na+ channels: an original mechanism of arrhythmia. Circulation. 2003;107:2233-2237. doi: 10.1161/01. CIR.0000069273.51375.BD.
5. Edwards AG, Grandi E, Hake JE, Patel S, Li P, Miyamoto S, Omens JH, Heller Brown J, Bers DM, McCulloch AD. Nonequilibrium reactivation of Na+ current drives early afterdepolarizations in mouse ventricle. Circ Arrhythm Electrophysiol. 2014;7:1205-1213. doi: 10.1161/CIRCEP.113.001666.
6. Sato D, Xie LH, Nguyen TP, Weiss JN, Qu Z. Irregularly appearing early afterdepolarizations in cardiac myocytes: random fluctuations or dynamical chaos Biophys J. 2010;99:765-773. doi: 10.1016/j. bpj.2010.05.019.
7. Priori SG, Corr PB. Mechanisms underlying early and delayed afterdepolarizations induced by catecholamines. Am J Physiol. 1990;258(6 Pt 2):H1796-H1805.
8. Lerma C, Krogh-Madsen T, Guevara M and Glass L. Stochastic aspects of cardiac arrhythmias. J Stat Phys. 2007;128:347-374.
9. Tran DX, Sato D, Yochelis A, Weiss JN, Garfinkel A, Qu Z. Bifurcation and chaos in a model of cardiac early afterdepolarizations. Phys Rev Lett. 2009;102:258103.
10. Tanskanen AJ, Greenstein JL, O'Rourke B, Winslow RL. The role of stochastic and modal gating of cardiac L-type Ca2+ channels on early after-depolarizations. Biophys J. 2005;88:85-95. doi: 10.1529/biophysj.104.051508.
11. Bers DM. Cardiac excitation-contraction coupling. Nature. 2002;415:198-205. doi: 10.1038/415198a.
12. Clusin WT. Calcium and cardiac arrhythmias: DADs, EADs, and alternans. Crit Rev Clin Lab Sci. 2003;40:337-375. doi: 10.1080/713609356.
13. Xie LH, Weiss JN. Arrhythmogenic consequences of intracellular calcium waves. Am J Physiol Heart Circ Physiol. 2009;297:H997-H1002. doi: 10.1152/ajpheart.00390.2009.
14. Restrepo JG, Karma A. Spatiotemporal intracellular calcium dynamics during cardiac alternans. Chaos. 2009;19:037115. doi: 10.1063/1.3207835.
15. Johnson DM, Heijman J, Bode EF, Greensmith DJ, van der Linde H, Abi-Gerges N, Eisner DA, Trafford AW, Volders PG. Diastolic spontaneous calcium release from the sarcoplasmic reticulum increases beatto-beat variability of repolarization in canine ventricular myocytes after-adrenergic stimulation. Circ Res. 2013;112:246-256. doi: 10.1161/CIRCRESAHA.112.275735.
16. Antzelevitch C, Sun ZQ, Zhang ZQ, Yan GX. Cellular and ionic mechanisms underlying erythromycin-induced long QT intervals and torsade de pointes. J Am Coll Cardiol. 1996;28:1836-1848. doi: 10.1016/S0735-1097(96)00377-4.
17. Liu GX, Choi BR, Ziv O, Li W, de Lange E, Qu Z, Koren G. Differential conditions for early after-depolarizations and triggered activity in cardiomyocytes derived from transgenic LQT1 and LQT2 rabbits. J Physiol. 2012;590(Pt 5):1171-1180. doi: 10.1113/jphysiol.2011.218164.
18. Grandi E, Pasqualini FS, Bers DM. A novel computational model of the human ventricular action potential and Ca transient. J Mol Cell Cardiol. 2010;48:112-121. doi: 10.1016/j.yjmcc.2009.09.019.
19. Despa S, Islam MA, Weber CR, Pogwizd SM, Bers DM. Intracellular Na(+) concentration is elevated in heart failure but Na/K pump function is unchanged. Circulation. 2002;105:2543-2548.
20. Ginsburg KS, Weber CR, Bers DM. Cardiac Na+-Ca2+ exchanger: dynamics of Ca2+-dependent activation and deactivation in intact myocytes. J Physiol. 2013;591(Pt 8):2067-2086. doi: 10.1113/jphysiol.2013.252080.
21. Shannon TR, Wang F, Puglisi J, Weber C, Bers DM. A mathematical treatment of integrated Ca dynamics within the ventricular myocyte. Biophys J. 2004;87:3351-3371. doi: 10.1529/biophysj.104.047449.
22. Yuan W, Bers DM. Protein kinase inhibitor H-89 reverses forskolin stimulation of cardiac L-type calcium current. Am J Physiol. 1995;268(3 Pt 1):C651-C659.
23. Madhvani RV, Xie Y, Pantazis A, Garfinkel A, Qu Z, Weiss JN, Olcese R. Shaping a new Ca2 conductance to suppress early afterdepolarizations in cardiac myocytes. J Physiol. 2011;589(Pt 24):6081-6092. doi: 10.1113/jphysiol.2011.219600.
24. Grandi E, Pandit SV, Voigt N, Workman AJ, Dobrev D, Jalife J, Bers DM. Human atrial action potential and Ca2+ model: sinus rhythm and chronic atrial fibrillation. Circ Res. 2011;109:1055-1066. doi: 10.1161/CIRCRESAHA.111.253955.
25. Yehia AR, Jeandupeux D, Alonso F, Guevara MR. Hysteresis and bistability in the direct transition from 1:1 to 2:1 rhythm in periodically driven single ventricular cells. Chaos. 1999;9:916-931. doi: 10.1063/1.166465.
26. Wang L, Myles RC, De Jesus NM, Ohlendorf AK, Bers DM, Ripplinger CM. Optical mapping of sarcoplasmic reticulum Ca2+ in the intact heart: ryanodine receptor refractoriness during alternans and fibrillation. Circ Res. 2014;114:1410-1421. doi: 10.1161/CIRCRESAHA.114.302505.
27. Wan X, Cutler M, Song Z, Karma A, Matsuda T, Baba A, Rosenbaum DS. New experimental evidence for mechanism of arrhythmogenic membrane potential alternans based on balance of electrogenic I(NCX)/I(Ca) currents. Heart Rhythm. 2012;9:1698-1705. doi: 10.1016/j.hrthm.2012.06.031.
28. Keener JP, Sneyd J. Mathematical Physiology. New York, NY: Springer; 1998.
29. Weiss JN, Qu Z, Chen PS, Lin SF, Karagueuzian HS, Hayashi H, Garfinkel A, Karma A. The dynamics of cardiac fibrillation. Circulation. 2005;112:1232-1240. doi: 10.1161/CIRCULATIONAHA.104.529545.
30. Kottkamp H, Tanner H, Kobza R, Schirdewahn P, Dorszewski A, Gerds-Li JH, Carbucicchio C, Piorkowski C, Hindricks G. Time courses and quantitative analysis of atrial fibrillation episode number and duration after circular plus linear left atrial lesions: trigger elimination or substrate modification: early or delayed cure J Am Coll Cardiol. 2004;44:869-877. doi: 10.1016/j.jacc.2004.04.049.
31. Faber GM, Rudy Y. Action potential and contractility changes in [Na(+)](i) overloaded cardiac myocytes: a simulation study. Biophys J. 2000;78:2392-2404. doi: 10.1016/S0006-3495(00)76783-X.
32. Chang MG, Chang CY, de Lange E, Xu L, O'Rourke B, Karagueuzian HS, Tung L, Marbán E, Garfinkel A, Weiss JN, Qu Z, Abraham MR. Dynamics of early afterdepolarization-mediated triggered activity in cardiac monolayers. Biophys J. 2012;102:2706-2714. doi: 10.1016/j.bpj.2012.05.011.
33. Despa S, Islam MA, Pogwizd SM, Bers DM. Intracellular [Na+] and Na+ pump rate in rat and rabbit ventricular myocytes. J Physiol. 2002;539(Pt 1):133-143.
34. Hund TJ, Rudy Y. Determinants of excitability in cardiac myocytes: mechanistic investigation of memory effect. Biophys J. 2000;79:3095-3104. doi: 10.1016/S0006-3495(00)76544-1.
35. Goldhaber JI, Xie LH, Duong T, Motter C, Khuu K, Weiss JN. Action potential duration restitution and alternans in rabbit ventricular myocytes: the key role of intracellular calcium cycling. Circ Res. 2005;96:459-466. doi: 10.1161/01.RES.0000156891.66893.83.
36. Bers DM, Despa S. Cardiac myocytes Ca2+ and Na+ regulation in normal and failing hearts. J Pharmacol Sci. 2006;100:315-322.
37. Pogwizd SM, Bers DM. Cellular basis of triggered arrhythmias in heart failure. Trends Cardiovasc Med. 2004;14:61-66. doi: 10.1016/j.tcm.2003.12.002.
38. Sato D, Xie LH, Sovari AA, Tran DX, Morita N, Xie F, Karagueuzian H, Garfinkel A, Weiss JN, Qu Z. Synchronization of chaotic early afterdepolarizations in the genesis of cardiac arrhythmias. Proc Natl Acad Sci USA. 2009;106:2983-2988. doi: 10.1073/pnas.0809148106.
39. Xie Y, Hu G, Sato D, Weiss JN, Garfinkel A, Qu Z. Dispersion of refractoriness and induction of reentry due to chaos synchronization in a model of cardiac tissue. Phys Rev Lett. 2007;99:118101.
40. Xie Y, Grandi E, Puglisi JL, Sato D, Bers DM.-adrenergic stimulation activates early afterdepolarizations transiently via kinetic mismatch of PKA targets. J Mol Cell Cardiol. 2013;58:153-161. doi: 10.1016/j.yjmcc.2013.02.009.