Non-linear dynamics of cardiac alternans: Subcellular to tissue-level mechanisms of arrhythmia

Frontiers in Physiology

Volumn 3 MAY, Issue , 2012, Pages

  Gaeta, Stephen A ^a   Christini, David J ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Calcium handling; Cardiac alternans; Repolarization alternans; Subcellular alternans; T wave alternans.

Indexed keywords

EID: 84866369684     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2012.00157     Document Type: Review

References (104)

1. Aistrup, G. L., Kelly, J. E., Kapur, S., Kowalczyk, M., Sysman-Wolpin, I., Kadish, A. H., and Wasserstrom, J. A. (2006). Pacing-induced heterogeneities in intracellular Ca2+ signaling, cardiac alternans, and ventricular arrhythmias in intact rat heart. Circ. Res. 99, e65-e73.
2. Aistrup, G. L., Shiferaw, Y., Kapur, S., Kadish, A. H., and Wasserstrom, J. A. (2009). Mechanisms underlying the formation and dynamics of subcellular calcium alternans in the intact rat heart. Circ. Res. 104, 639-649.
3. Banville, I., Chattipakorn, N., and Gray, R. A. (2004). Restitution dynamics during pacing and arrhythmias in isolated pig hearts. J. Cardiovasc. Electrophysiol. 15,455-463.
4. Banville, I., and Gray, R. A. (2002). Effect of action potential duration and conduction velocity restitution and their spatial dispersion on alternans and the stability of arrhythmias. J. Cardiovasc. Electrophysiol. 13, 1141-1149.
5. Bass, B. G. (1975). Restitution of the action potential in cat papillary muscle. Am. J. Physiol. 228, 1717-1724.
6. Bassani, J. W., Yuan, W., and Bers, D. M. (1995). Fractional sr ca release is regulated by trigger ca and sr ca content in cardiac myocytes. Am. J. Physiol. 268(Pt 1), C1313-C1319.
7. Bayer, J. D.,Narayan, S. M., Lalani,G. G., and Trayanova, N. A. (2010). Rate-dependent action potential alternans in human heart failure implicates abnormal intracellular calcium handling. Heart Rhythm 7, 1093-1101.
8. Bers, D. M. (2002). Cardiac excitation-contraction coupling. Nature 415, 198-205.
9. Bers, D. M. (2008). Calcium cycling and signaling in cardiac myocytes. Annu. Rev. Physiol. 70, 23-49.
10. Blatter, L. A. (2003). Local calcium gradients during excitation-contraction coupling and alternans in atrial myocytes. J. Physiol. (Lond.) 546, 19-31.
11. Brette, F., and Orchard, C. (2003). T-tubule function in mammalian cardiac myocytes. Circ. Res. 92, 1182-1192.
12. Cheng, H., and Lederer, W. J. (2008). Calcium sparks. Physiol. Rev. 88, 1491-1545.
13. Chinushi, M., Kozhevnikov, D., Caref, E. B., Restivo, M., and El-Sherif, N. (2003). Mechanism of discordant t wave alternans in the in vivo heart. J. Cardiovasc. Electrophysiol. 14, 632-638.
14. Chinushi, M., Restivo, M., Caref, E. B., and El-Sherif, N. (1998). Electro-physiological basis of arrhythmo-genicity of qt/t alternans in the long-qt syndrome: tridimensional analysis of the kinetics of cardiac repolar-ization. Circ. Res. 83, 614-628.
15. Christini, D. J., Riccio, M. L., Culianu, C. A., Fox, J. J., Karma, A., and Gilmour, R. F. (2006). Control of electrical alternans in canine cardiac Purkinje fibers. Phys. Rev. Lett. 96, 104101.
16. Chudin, E., Goldhaber, J., Garfinkel, A., Weiss, J., and Kogan,B. (1999). Intracellular Ca(2+) dynamics and the stability of ventricular tachycardia. Biophys. J.77, 2930-2941.
17. Cordeiro, J. M., Malone, J. E., Diego, J. M. D., Scornik, F. S., Aistrup, G. L., Antzelevitch, C., and Wasserstrom, J. A. (2007). Cellular and subcellular alternans in the canine left ventricle. Am. J. Physiol. Heart Circ. Physiol. 293, H3506-H3516.
18. Cutler, M. J., and Rosenbaum, D. S. (2009). Explaining the clinical manifestations of t wave alternans in patients at risk for sudden cardiac death. Heart Rhythm 6(Suppl.), S22-S28.
19. Cutler, M. J., Wan, X., Laurita, K. R., Hajjar, R. J., and Rosenbaum, D. S. (2009). Targeted serca2a gene expression identifies molecular mechanism and therapeutic target for arrhythmogenic cardiac alternans. Circ. Arrhythm. Electrophysiol. 2, 686-694.
20. Díaz, M. E., Eisner, D. A., and O'Neill, S. C. (2002). Depressed ryanodine receptor activity increases variability and duration of the systolic Ca2+ transient in rat ventricular myocytes. Circ. Res. 91,585-593.
21. Díaz, M. E., O'Neill, S. C., and Eisner, D. A. (2004). Sarcoplasmic reticu-lum calcium content fluctuation is the key to cardiac alternans. Circ. Res. 94, 650-656.
22. Diego, C. D., Pai, R. K., Dave, A. S., Lynch, A., Thu, M., Chen, F., Xie, L-H., Weiss, J. N., and Valderrábano, M. (2008). Spatially discordant alternans in cardiomyocyte monolayers. Am. J. Physiol. Heart Circ. Physiol. 294, 1417-1425.
23. Echebarria, B., and Karma, A. (2007). Amplitude equation approach to spatiotemporal dynamics of cardiac alternans. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 76(Pt 1), 051911.
24. Euler, D. E. (1999). Cardiac alternans: mechanisms and pathophysiologi-cal significance. Cardiovasc. Res. 42, 583-590.
25. Ferrari, G. M. D., Viola, M. C., D'Amato, E., Antolini, R., and Forti, S. (1995). Distinct patterns of calcium transients during early and delayed after-depolarizations induced by isopro-terenol in ventricular myocytes. Circulation 91,2510-2515.
26. Fox, J. J., McHarg, J. L., and Gilmour, R. F. (2002a). Ionic mechanism of electrical alternans. Am. J. Physiol. Heart Circ. Physiol. 282,H516-H530.
27. Fox, J. J., Riccio, M. L., Hua, F., Bodenschatz, E., and Gilmour, R. F. (2002b). Spatiotemporal transition to conduction block in canine ventricle. Circ. Res. 90, 289-296.
28. Franz, M. R. (2003). The electrical restitution curve revisited: steep or flat slope-which is better? J. Cardiovasc. Electrophysiol. 14, S140-S147.
29. Fujiwara, K., Tanaka, H., Mani, H., Nakagami, T., and Takamatsu, T. (2008). Burst emergence of intracel-lular Ca2+waves evokes arrhythmo-genic oscillatory depolarization via the Na+-Ca2+ exchanger: simultaneous confocal recording of membrane potential and intracellular Ca2+ in the heart. Circ. Res. 103, 509-518.
30. Gaeta, S. A., Bub, G., Abbott, G. W., and Christini, D. J. (2009). Dynamical mechanism for subcellular alternans in cardiac myocytes. Circ. Res. 105, 335-342.
31. Gaeta, S. A., Krogh-Madsen, T., and Christini, D. J. (2010). Feedback-control induced pattern formation in cardiac myocytes: a mathematical modeling study. J. Theor. Biol. 266, 408-418.
32. Garfinkel, A., Kim, Y. H., Voroshilovsky, O., Qu, Z., Kil, J. R., Lee, M. H., Karagueuzian, H. S., Weiss, J. N.,and Chen, P. S. (2000). Preventing ventricular fibrillation by flattening cardiac restitution. Proc. Natl. Acad. Sci. U.S.A. 97, 6061-6066.
33. Gierer, A., and Meinhardt, H. (1972). A theory of biological pattern formation. Kybernetik 12, 30-39.
34. Gilmour, R. F., Otani, N. F., and Watan-abe, M. A. (1997). Memory and complex dynamics in cardiac Purk-inje fibers. Am. J. Physiol. 272(Pt 2), H1826-H1832.
35. Goldhaber, J. I., Xie, L.-H., Duong, T., Motter, C., Khuu, K., and Weiss, J. N. (2005). Action potential duration restitution and alternans in rabbit ventricular myocytes: the key role of intracellular calcium cycling. Circ. Res. 96, 459-466.
36. Greenstein, J. L., and Winslow, R. L. (2002). An integrative model of the cardiac ventricular myocyte incorporating local control of Ca2+ release. Biophys. J. 83, 2918-2945.
37. Guevara, M., Ward, G., Shrier, A., and Glass, L. (1984). Electrical alternans and period doubling bifurcations. Comput. Cardiol. 167-170.
38. Hall, G., Bahar, S., and Gauthier, D. (1999). Prevalence of rate-dependent behaviors in cardiac muscle. Phys. Rev. Lett. 82, 2995-2998.
39. Hüser, J., Wang, Y. G., Sheehan, K. A., Cifuentes, F., Lipsius, S. L., and Blatter, L. A. (2000). Functional coupling between glycolysis and excitation-contraction coupling underlies alternans in cat heart cells. J. Physiol. (Lond.) 524(Pt 3), 795-806.
40. Jordan, P. N., and Christini, D. J. (2007). Characterizing the contribution of voltage- and calcium-dependent coupling to action potential stability: implications for repo-larization alternans. Am. J. Physiol. Heart Circ. Physiol. 293, H2109-H2118.
41. Kanu, U. B., Iravanian, S., Gilmour, R. F., and Christini, D. J. (2011). Control of action potential duration alternans in canine cardiac ventricular tissue. IEEE Trans. Biomed. Eng. 58, 894-904.
42. Kapur, S., Wasserstrom, J. A., Kelly, J. E., Kadish, A. H., and Aistrup, G. L. (2009). Acidosis and ischemia increase cellular Ca2+ transient alternans and repolarization alternans susceptibility in the intact rat heart. Am. J. Physiol. Heart Circ. Physiol. 296,H1491-H1512.
43. Karma, A., and Gilmour, R. (2007). Nonlinear dynamics of heart rhythm disorders. Phys. Today 60, 51.
44. Katz, A. (2005). Physiology of the Heart. Philadelphia: Lippincott Williams & Wilkins.
45. Keurs, H. E. D. J. T., and Boyden, P. A. (2007). Calcium and arrhythmoge-nesis. Physiol. Rev. 87,457-506.
46. Knot, H. J., Laher, I., Sobie, E. A., Guati-mosim, S., Gomez-Viquez, L., Hart-mann, H., Song, L.-S., Lederer, W J., Graier, W E, Malli, R., Frieden, M., and Petersen, O. H. (2005). Twenty years of calcium imaging: cell physiology to dye for. Mol. Interv. 5, 112-127.
47. Kockskämper, J., and Blatter, L. A. (2002). Subcellular Ca2+alternans represents a novel mechanism for the generation of arrhythmogenic Ca2+waves in cat atrial myocytes. J. Physiol. (Lond.) 545(Pt 1), 65-79.
48. Koller, M. L., Maier, S. K. G., Gelzer, A. R., Bauer, W R., Meesmann, M., and Gilmour, R. E (2005). Altered dynamics of action potential restitution and alternans in humans with structural heart disease. Circulation 112,1542-1548.
49. Koller, M. L., Riccio, M. L., and Gilmour, R. E (1998). Dynamic restitution of action potential duration during electrical alternans and ventricular fibrillation. Am. J. Physiol. 275(Pt 2), H1635-H1642.
50. Krogh-Madsen, T., and Christini, D. J. (2007). Action potential duration dispersion and alternans in simulated heterogeneous cardiac tissue with a structural barrier. Biophys. J. 92,1138-1149.
51. Krogh-Madsen, T., Karma, A., Riccio, M. L., Jordan, P. N., Christini, D. J., and Gilmour, R. E (2010). Off-site control of repolarization alternans in cardiac fibers. Phys. Rev. E 81 (Pt 1),011915.
52. Livshitz, L. M., and Rudy, Y. (2007). Regulation of Ca2+ and electrical alternans in cardiac myocytes: role of camkii and repolarizing currents. Am. J. Physiol. Heart Circ. Physiol. 292, H2854-H2866.
53. Mahajan, A., Sato, D., Shiferaw, Y., Baher, A., Xie, L.-H., Peralta, R., Olcese, R., Garfinkel, A., Qu, Z., and Weiss, J. N. (2008). Modifying l-type calcium current kinetics: consequences for cardiac excitation and arrhythmia dynamics. Biophys. J. 94, 411-423.
54. Minamikawa, T., Cody, S. H., and Williams, D. A. (1997). In situ visualization of spontaneous calcium waves within perfused whole rat heart by confocal imaging. Am. J. Physiol. 272(Pt 2), H236-H243.
55. Miura, M., Ishide, N., Oda, H., Sakurai, M., Shinozaki, T., and Takishima, T. (1993). Spatial features of calcium transients during early and delayed afterdepolarizations. Am. J. Physiol. 265(Pt2),H439-H444.
56. Narayan, S. (2006). T-wave alternans and the susceptibility to ventricular arrhythmias. J. Am. Coll. Cardiol. 47, 269-281.
57. Narayan, S. M. (2008). T-wave alternans testing for ventricular arrhythmias. Prog. Cardiovasc. Dis. 51,118-127.
58. Narayan, S. M., Bayer, J. D., Lalani, G., and Trayanova, N. A. (2008). Action potential dynamics explain arrhythmic vulnerability in human heart failure: a clinical and modeling study implicating abnormal calcium handling. J. Am. Coll. Cardiol. 52, 1782-1792.
59. Narayan, S. M., Franz, M. R., Clop-ton, P., Pruvot, E. J., and Krummen, D. E. (2011). Repolarization alternans reveals vulnerability to human atrial fibrillation. Circulation 123, 2922-2930.
60. Nieminen, T., and Verrier, R. L. (2010). Usefulness of T-wave alternans in sudden death risk stratification and guiding medical therapy. Ann. Non-invasive Electrocardiol. 15, 276-288.
61. Nolasco, J. B.,andDahlen,R. W. (1968). A graphic method for the study of alternation in cardiac action potentials. J. Appl. Physiol. 25,191-196.
62. O'Hara, T., Virág, L., Varró, A., and Rudy, Y. (2011). Simulation of the undiseased human cardiac ventricular action potential: model formulation and experimental validation. PLoS Comput. Biol. 7, e1002061. doi:10.1371/journal.pcbi.1002061
63. Orchard, C. H., Pásek, M., and Brette, E (2009). The role of mammalian cardiac t-tubules in excitation-contraction coupling: experimental and computational approaches. Exp. Physiol. 94,509-519.
64. Otani, N. F., and Gilmour, R. E (1997). Memory models for the electrical properties of local cardiac systems. J. Theor. Biol. 187,409-436.
65. Pastore, J. M., Girouard, S. D., Lau-rita, K. R., Akar, F. G., and Rosen-baum,D. S. (1999). Mechanism linking t-wave alternans to the genesis of cardiac fibrillation. Circulation 99, 1385-1394.
66. Peterson, B. Z., DeMaria, C. D., Adel-man, J. P., and Yue, D. T. (1999). Calmodulin is the Ca2+ sensor for Ca2+-dependent inactivation of L-type calcium channels. Neuron 22, 549-558.
67. Picht, E., DeSantiago, J., Blatter, L. A., and Bers, D. M. (2006). Cardiac alternans do not rely on diastolic sarcoplasmic reticulum calcium content fluctuations. Circ. Res. 99, 740-748.
68. Pruvot, E. J., Katra, R. P., Rosenbaum, D. S., and Laurita, K. R. (2004). Role of calcium cycling versus restitution in the mechanism of repolarization alternans. Circ. Res. 94,1083-1090.
69. Pruvot, E., and Rosenbaum, D. (2003). T-wave alternans for risk stratification and prevention of sudden cardiac death. Curr. Cardiol Rep. 5, 350-357.
70. Qu, Z., Garfinkel, A., Chen, P. S., and Weiss, J. N. (2000). Mechanisms of discordant alternans and induction of reentry in simulated cardiac tissue. Circulation. 102,1664-1670.
71. Qu, Z., and Weiss, J. N. (2007). The chicken or the egg? Voltage and calcium dynamics in the heart. Am. J. Physiol. Heart Circ. Physiol. 293, H2054-H2055.
72. Restrepo, J. G., Weiss, J. N., and Karma, A. (2008). Calsequestrin-mediated mechanism for cellular calcium transient alternans. Biophys. J. 95, 3767-3789.
73. Riccio, M. L., Koller, M. L., and Gilmour, R. F. (1999). Electrical restitution and spatiotemporal organization during ventricular fibrillation. Circ. Res. 84, 955-963.
74. Rosenbaum, D. S., Jackson, L. E., Smith, J. M., Garan, H., Ruskin, J. N., and Cohen, R. J. (1994). Electrical alternans and vulnerability to ventricular arrhythmias. N. Engl. J. Med. 330, 235-241.
75. Rubenstein, D. S., and Lipsius, S. L. (1995). Premature beats elicit a phase reversal of mechanoelec-trical alternans in cat ventricular myocytes. A possible mechanism for reentrant arrhythmias. Circulation 91,201-214.
76. Salama, G. (2006). Arrhythmia genesis: aberrations of voltage or Ca2+ cycling? Heart Rhythm 3, 67-70.
77. Sato, D., Shiferaw, Y., Qu, Z., Garfinkel, A., Weiss, J. N., and Karma, A. (2007). Inferring the cellular origin of voltage and calcium alternans from the spatial scales of phase reversal during discordant alternans. Biophys. J. 92, L33-L35.
78. Shiferaw, Y., and Karma, A. (2006). Turing instability mediated by voltage and calcium diffusion in paced cardiac cells. Proc. Natl. Acad. Sci. U.S.A. 103,5670-5675.
79. Shiferaw, Y., Qu, Z., Garfinkel, A., Karma, A., and Weiss, J. (2006). Nonlinear dynamics of paced cardiac cells. Ann. N. Y. Acad. Sci. 1080, 376-394.
80. Shiferaw, Y., Sato, D., and Karma, A. (2005). Coupled dynamics of voltage and calcium in paced cardiac cells. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 71(Pt 1), 021903.
81. Shiferaw, Y.,Watanabe, M. A., Garfinkel, A., Weiss, J. N., and Karma, A. (2003). Model of intracellu-lar calcium cycling in ventricular myocytes. Biophys. J. 85, 3666-3686.
82. Shimizu, W., and Antzelevitch, C. (1999). Cellular and ionic basis for t-wave alternans under long-qt conditions. Circulation 99, 1499-1507.
83. Sipido, K. R. (2006). Calcium overload, spontaneous calcium release, and ventricular arrhythmias. Heart Rhythm 3, 977-979.
84. Stern, M. D. (1992). Theory of excitation-contraction coupling in cardiac muscle. Biophys. J. 63, 497-517.
85. Stern, M. D., Song, L. S., Cheng, H., Sham, J. S., Yang, H. T., Boheler, K. R., and Ríos, E. (1999). Local control models of cardiac excitation-contraction coupling. A possible role for allosteric interactions between ryanodine receptors. J. Gen. Physiol. 113,469-489.
86. Tolkacheva, E. G., Anumonwo, J. M. B., and Jalife, J. (2006). Action potential duration restitution portraits of mammalian ventricular myocytes: role of calcium current. Biophys. J. 91,2735-2745.
87. Tolkacheva, E. G., Romeo, M. M., Guer-raty, M., and Gauthier, D. J. (2004). Condition for alternans and its control in a two-dimensional mapping model of paced cardiac dynamics. Phys. Rev. EStat. Nonlin. Soft Matter Phys. 69(Pt 1), 031904.
88. Turing, A. M. (1952). The chemical basis of morphogenesis. Philos. Trans. R. Soc. Lond. B Biol. Sci. 237, 37-72.
89. Venetucci, L. A., Trafford, A. W., O'Neill, S. C., and Eisner, D. A. (2008). The sarcoplasmic reticulum and arrhyth-mogenic calcium release. Cardio-vasc. Res. 77, 285-292.
90. Verrier, R. L., Klingenheben, T., Malik, M., El-Sherif, N., Exner, D. V., Hohn-loser, S. H., Ikeda, T., Martínez, J. P., Narayan, S. M., Nieminen, T., and Rosenbaum, D. S. (2011). Microvolt T-wave alternans physiological basis, methods of measurement, and clinical utility-consensus guideline by International Society for Holter and Noninvasive Electrocardiology. J.Am. Coll. Cardiol. 58, 1309-1324.
91. Verrier, R. L., Kumar, K., and Near-ing, B. D. (2009). Basis for sudden cardiac death prediction by t-wave alternans from an integrative physiology perspective. Heart Rhythm 6, 416-422.
92. Verrier, R. L., and Nieminen, T. (2010). T-wave alternans as a therapeutic marker for antiarrhythmic agents. J. Cardiovasc. Pharmacol. 55, 544-554.
93. Walker, M. L., and Rosenbaum, D. S. (2003). Repolarization alternans: implications for the mechanism and prevention of sudden cardiac death. Cardiovasc. Res. 57, 599-614.
94. Wan, X., Laurita, K. R., Pruvot, E. J., and Rosenbaum, D. S. (2005). Molecular correlates of repolarization alternans in cardiac myocytes. J. Mol. Cell. Cardiol. 39,419-428.
95. Watanabe, M. A., Fenton, E H., Evans, 5. J., Hastings, H. M., and Karma, A. (2001). Mechanisms for discordant alternans. J. Cardiovasc. Electrophys-iol. 12, 196-206.
96. Weiss, J. N., Karma, A., Shiferaw, Y., Chen, P.-S., Garfinkel, A., and Qu, Z. (2006). From pulsus to pulseless: the saga of cardiac alternans. Circ. Res. 98,1244-1253.
97. Willms, A. R., Baro, D. J., Harris-Warrick, R. M., and Guckenheimer, J. (1999). An improved parameter estimation method for hodgkin-huxley models.J. Comput. Neurosci. 6, 145-168.
98. Wilson, L., and Rosenbaum, D. (2007). Mechanisms of arrythmogenic cardiac alternans. Europace vi77-vi82.
99. Wu, R., and Patwardhan, A. (2004). Restitution of action potential duration during sequential changes in diastolic intervals shows multimodal behavior. Circ. Res. 94, 634-641.
100. Wu, R., and Patwardhan, A. (2006). Mechanism of repolarization alternans has restitution of action potential duration dependent and independent components. J. Cardiovasc. Electrophysiol. 17, 87-93.
101. Wu, T.-J., Lin, S.-F., Weiss, J. N., Ting, C.-T., and Chen, P.-S. (2002). Two types of ventricular fibrillation in isolated rabbit hearts: importance of excitability and action potential duration restitution. Circulation 106, 1859-1866.
102. Xie, L.-H., Sato, D., Garfinkel, A., Qu, Z., and Weiss, J. N. (2008). Intracel-lular ca alternans: coordinated regulation by sarcoplasmic reticulum release, uptake, and leak. Biophys. J. 95,3100-3110.
103. Xie, L.-H., and Weiss, J. N. (2009). Arrhythmogenic consequences of intracellular calcium waves. Am. J. Physiol. Heart Circ. Physiol. 297, H997-H1002.
104. Zipes, D., and Jalife, J. (2004). Cardiac Electrophysiology: From Cell to Bedside. Philadelphia: Saunders.