The role of mitochondria for the regulation of cardiac alternans

Frontiers in Physiology

Volumn 1 NOV, Issue , 2010, Pages

  Florea, Stela M ^a   Blatter, Lothar A ^b  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b RUSH UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Ca alternans; Electron transport chain; Intracellular Ca ; Mitochondria; Mitochondrial ca cycling; Permeability transition pore; TCA cycle

Indexed keywords

EID: 84861768802     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2010.00141     Document Type: Article

References (92)

1. 2+ 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. Altschafl, B. A., Beutner, G., Sharma, V. K., Sheu, S. S., and Valdivia, H. H. (2007). The mitochondrial ryanodine receptor in rat heart: a pharmaco-kinetic profile. Biochim. Biophys. Acta 1768, 1784-1795.
4. Armoundas, A. A. (2009). Mechanism of abnormal sarcoplasmic reticulum calcium release in canine left-ventricular myocytes results in cellular alternans. IEEE Trans. Biomed. Eng. 56, 220-228.
5. Badeer, H. S., Ryo, U. Y., Gassner, W. F., Kass, E. J., Cavaluzzi, J., Gilbert, J. L., and Brooks, C. M. (1967). Factors affecting pulsus alternans in the rapidly driven heart and papillary muscle. Am. J. Physiol. 213, 1095-1101.
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, C1313-1319.
7. Belevych, A. E., Terentyev, D., Viatchenko-Karpinski, S., Terentyeva, R, Sridhar, A., Nishijima, Y., Wilson LD, Cardounel, A. J., Laurita, K. R., Carnes, C. A., Billman, G. E., and Gyorke, S. (2009). Redox modification of ryanodine receptors underlies calcium alternans in a canine model of sudden cardiac death. Cardiovasc. Res. 84, 387-395.
8. Berger, R. D. (2000). Repolarization alternans: toward a unifying theory of reentrant arrhythmia induction. Circ. Res. 87, 1083-1084.
9. Beutner, G., Sharma, V. K., Giovannucci, D. R., Yule, D. I., and Sheu, S. S. (2001). Identification of a ryanodine receptor in rat heart mitochondria. J. Biol. Chem. 276, 21482-21488.
10. Beutner, G., Sharma, V. K., Lin, L., Ryu, S. Y., Dirksen, R. T., and Sheu, S. S. (2005). Type 1 ryanodine receptor in cardiac mitochondria: transducer of excitation-metabolism coupling. Biochim. Biophys. Acta. 1717, 1-10.
11. Blatter, L. A., Kockskamper, J., Sheehan, K. A., Zima, A. V., Huser, J., and Lipsius, S. L. (2003). Local calcium gradients during excitation-contraction coupling and alternans in atrial myocytes. J. Physiol. 546, 19-31.
12. Buntinas, L., Gunter, K. K., Sparagna, G. C., and Gunter, T. E. (2001). The rapid mode of calcium uptake into heart mitochondria (RaM): comparison to RaM in liver mitochondria. Biochim. Biophys. Acta 1504, 248-261.
13. Clusin, W. T. (2008). Mechanisms of calcium transient and action potential alternans in cardiac cells and tissues. Am. J. Physiol. Heart Circ. Physiol. 294, H1-H10.
14. Cordeiro, J. M., Malone, J. E., Di Diego, J. M., 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.
15. 2+ exchange of heart mitochondria by benzothiazepine CGP-37157. J. Cardiovasc. Pharmacol. 21, 595-599.
16. Crompton, M. (1999). The mitochondrial permeability transition pore and its role in cell death. Biochem. J. 341 (Pt 2), 233-249.
17. 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.
18. de Diego, C., Chen, F., Xie, L. H., Dave, A. S., Thu, M., Rongey, C., Weiss, J. N., and Valderrabano, M. (2008). Cardiac alternans in embryonic mouse ventricles. Am. J. Physiol. Heart Circ. Physiol. 294, H433-H440.
19. (2+) and the heart. Cell Calcium 44, 77-91.
20. 2+ transient in rat ventricular myocytes. Circ. Res. 91, 585-593.
21. Diaz, M. E., O'Neill, S. C., and Eisner, D. A. (2004). Sarcoplasmic reticulum calcium content fluctuation is the key to cardiac alternans. Circ. Res. 94, 650-656.
22. Dilly, S. G., and Lab, M. J. (1988). Electrophysiological alternans and restitution during acute regional ischaemia in myocardium of anaesthetized pig. J. Physiol. 402, 315-333.
23. Dumitrescu, C., Narayan, P., Efimov, I. R., Cheng, Y., Radin, M. J., McCune, S. A., and Altschuld, R. A. (2002). Mechanical alternans and restitution in failing SHHF rat left ventricles. Am. J. Physiol. Heart Circ. Physiol. 282, H1320-H1326.
24. Eisner, D. A., Choi, H. S., Diaz, M. E., O'Neill, S. C., and Trafford, A. W. (2000). Integrative analysis of calcium cycling in cardiac muscle. Circ Res. 87, 1087-1094.
25. Eisner, D. A., Diaz, M. E., Li, Y., O'Neill, S. C., and Trafford, A. W. (2005). Stability and instability of regulation of intracellular calcium. Exp. Physiol. 90, 3-12.
26. Eisner, D. A., Li, Y., and O'Neill, S. C. (2006). Alternans of intracellular calcium: mechanism and significance. Heart Rhythm 3, 743-745.
27. Euler, D. E. (1999). Cardiac alternans: mechanisms and pathophysiological significance. Cardiovasc. Res. 42, 583-590.
28. 2+ alternans modulation in atrial myocytes. Biophys. J. 88, 135a.
29. Fox, J. J., McHarg, J. L., and Gilmour, R. F. Jr. (2002). Ionic mechanism of electrical alternans. Am. J. Physiol. Heart Circ. Physiol. 282, H516-H530.
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. Gunter, T. E., Buntinas, L., Sparagna, G., Eliseev, R., and Gunter, K. (2000). Mitochondrial calcium transport: mechanisms and functions. Cell Calcium 28, 285-296.
32. Hayashi, H., Shiferaw, Y., Sato, D., Nihei, M., Lin, S. F., Chen, P. S., Garfinkel, A., Weiss, J. N., and Qu, Z. (2007). Dynamic origin of spatially discordant alternans in cardiac tissue. Biophys. J. 92, 448-460.
33. Hiromoto, K., Shimizu, H., Furukawa, Y., Kanemori, T., Mine, T., Masuyama, T., and Ohyanagi, M. (2005). Discordant repolarization alternans-induced atrial fibrillation is suppressed by verapamil. Circ. J. 69, 1368-1373.
34. Huser, J., Blatter, L. A., and Sheu. S. S. (2000a). Mitochondrial calcium in heart cells: beat-to-beat oscillations or slow integration of cytosolic transients? J. Bioenerg. Biomembr. 32, 27-33.
35. Huser, J., Wang, Y. G., Sheehan, K. A., Cifuentes, F., Lipsius, S. L., and Blatter, L. A. (2000b). Functional coupling between glycolysis and excitation-contraction coupling underlies alternans in cat heart cells. J. Physiol. 524 (Pt 3), 795-806.
36. Huser, J., Lipsius, S. L., and Blatter, L. A. (1996). Calcium gradients during excitation-contraction coupling in cat atrial myocytes. J. Physiol. 494 (Pt 3), 641-651.
37. Huser, J., Rechenmacher, C. E., and Blatter, L. A. (1998). Imaging the permeability pore transition in single mitochondria. Biophys. J. 74, 2129-2137.
38. Isenberg, G., Han, S., Schiefer, A., and Wendt-Gallitelli, M. F. (1993). Changes in mitochondrial calcium concentration during the cardiac contraction cycle. Cardiovasc. Res. 27, 1800-1809.
39. Jordan, P. N., and Christini, D. J. (2007). Characterizing the contribution of voltage-and calcium-dependent coupling to action potential stability: implications for repolarization altern-ans. Am. J. Physiol. Heart Circ. Physiol. 293, H2109-H2118.
40. (2+) pump function to electrical and mechanical alternans. J. Electrocardiol. 36, 125-135.
41. 2+ transient alternans and repolarization alternans susceptibility in the intact rat heart. Am. J. Physiol. Heart Circ. Physiol. 296, H1491-H1512.
42. 2+ handling is the primary cause of mechanical alternans: study in ferret ventricular muscles. Am. J. Physiol. 261, H1746-H1755.
43. 2+ waves in cat atrial myocytes. J. Physiol. 545, 65-79.
44. 2+ release by glycolysis in cat atrial myocytes. J. Physiol. 564, 697-714.
45. Konta, T., Ikeda, K., Yamaki, M., Nakamura, K., Honma, K., Kubota, I., and Yasui, S. (1990). Significance of discordant ST alternans in ventricular fibrillation. Circulation 82, 2185-2189.
46. (2+) release in subepicardial myocytes of intact beating mouse hearts: effect of exogenous buffers. Am. J. Physiol. Heart Circ. Physiol. 298, H2138-H2153.
47. Lab, M. J., and Lee, J. A. (1990). Changes in intracellular calcium during mechanical alternans in isolated ferret ventricular muscle. Circ. Res. 66, 585-595.
48. Lab, M. J., and Seed, W. A. (1993). Pulsus alternans. Cardiovasc. Res. 27, 1407-1412.
49. 2+ alternans in rat ventricular myocytes. J. Physiol. 587, 1283-1292.
50. 2+ and electrical alternans in cardiac myocytes: role of CAMKII and repolarizing currents. Am. J. Physiol. Heart Circ. Physiol. 292, H2854-H2866.
51. Luss, I., Boknik, P., Jones, L. R., Kirchhefer, U., Knapp, J., Linck, B., Luss, H., Meissner, A., Muller, F. U., Schmitz, W., Vahlensieck, U., and Neumann, J. (1999). Expression of cardiac calcium regulatory proteins in atrium v ventricle in different species. J. Mol. Cell Cardiol. 31, 1299-1314.
52. 2+ uptake during excitation-contraction coupling and impairs energetic adaptation in cardiac myocytes. Circ. Res. 99, 172-182.
53. Mahajan, A., Shiferaw, Y., Sato, D., Baher, A., Olcese, R., Xie, L. H., Yang, M. J., Chen, P. S., Restrepo, J. G., Karma, A., Grafinkel, A., Qu, Z., and Weiss, J. (2008). A rabbit ventricular action potential model replicating cardiac dynamics at rapid heart rates. Biophys. J. 94, 392-410.
54. 2+ uptake into mitochondria in vitro and in situ in single cardiac myocytes. J. Biol. Chem. 273, 10223-10231.
55. 2+concentration in living single rat cardiac myocytes. Am. J. Physiol. 261, H1123-H1134.
56. Moravec, C. S., and Bond, M. (1991). Calcium is released from the junctional sarcoplasmic reticulum during cardiac muscle contraction. Am. J. Physiol. 260, H989-H997.
57. Myles, R. C., Burton, F. L., Cobbe, S. M., and Smith, G. L. (2008). The link between repolarisation alternans and ventricular arrhythmia: does the cellular phenomenon extend to the clinical problem? J. Mol. Cell Cardiol. 45, 1-10.
58. Narayan, S. M., Bode, F., Karasik, P. L., and Franz, M. R. (2002). Alternans of atrial action potentials during atrial flutter as a precursor to atrial fibrillation. Circulation 106, 1968-1973.
59. Nattel, S. (2002). New ideas about atrial fibrillation 50 years on. Nature 415, 219-226.
60. 2+ uptake: tortoise or hare? J. Mol. Cell Cardiol. 46, 767-774.
61. Orchard, C. H., McCall, E., Kirby, M. S., and Boyett, M .R. (1991). Mechanical alternans during acidosis in ferret heart muscle. Circ. Res. 68, 69-76.
62. Pastore, J. M., Girouard, S. D., Laurita, K. R., Akar, F. G., and Rosenbaum, D.S. (1999). Mechanism linking T-wave alternans to the genesis of cardiac fibrillation. Circulation 99, 1385-1394.
63. Pastore, J. M., and Rosenbaum, D. S. (2000). Role of structural barriers in the mechanism of alternans-induced reentry. Circ. Res. 87, 1157-1163.
64. 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.
65. Restrepo, J. G., Weiss, J. N., and Karma, A. (2008). Calsequestrin-mediated mechanism for cellular calcium transient alternans. Biophys. J. 95, 3767-3789.
66. 2+] in cardiac cells. EMBO J. 20, 4998-5007.
67. Rosenbaum, D. S. (2001). T wave alter-nans: a mechanism of arrhythmo-genesis comes of age after 100 years. J. Cardiovasc. Electrophysiol. 12, 207-209.
68. Rosenbaum, D. S., Jackson, L. E., Smith, J. M., Garan, H., Ruskin, J. N., and Cohen, R. J. (1994). Electrical alter-nans and vulnerability to ventricular arrhythmias. N. Engl. J. Med. 330, 235-241.
69. Rovetti, R., Cui, X., Garfinkel, A., Weiss, J. N., and Qu, Z. (2010). Spark-induced sparks as a mechanism of intracellular calcium alternans in cardiac myocytes. Circ. Res. 106, 1582-1591.
70. Rubenstein, D. S., and Lipsius, S. L. (1995). Premature beats elicit a phase reversal of mechanoelectrical alternans in cat ventricular myocytes. A possible mechanism for reentrant arrhythmias. Circulation 91, 201-214.
71. Sato, D., Shiferaw, Y., Garfinkel, A., Weiss, J. N., Qu, Z., and Karma, A. (2006). Spatially discordant alternans in car-diac tissue: role of calcium cycling. Circ. Res. 99, 520-527.
72. 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.
73. 2+ signals by mitochondria in cat ventricular myocytes. Am. J. Physiol. Cell Physiol. 291, C840-C850.
74. Sheehan, K. A., and Blatter, L. A. (2003). Regulation of junctional and non-junctional sarcoplasmic reticulum calcium release in excitation-contraction coupling in cat atrial myocytes. J. Physiol. 546, 119-135.
75. 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.
76. Shiferaw, Y., Watanabe, M. A., Garfinkel, A., Weiss, J. N., and Karma, A. (2003). Model of intracellular calcium cycling in ventricular myocytes. Biophys. J. 85, 3666-3686.
77. Shimizu, W., and Antzelevitch, C. (1999). Cellular and ionic basis for T-wave alternans under long-QT conditions. Circulation 99, 1499-1507.
78. Smith, J. M., Clancy, E. A., Valeri, C. R., Ruskin, J. N., and Cohen, R. J. (1988). Electrical alternans and cardiac electrical instability. Circulation 77, 110-121.
79. Sparagna, G. C., Gunter, K. K., Sheu, S. S., and Gunter, T. E. (1995). Mitochondrial calcium uptake from physiological-type pulses of calcium. A description of the rapid uptake mode. J. Biol. Chem. 270, 27510-27515.
80. Spencer, C. I., Lab, M. J., and Seed, W. A. (1992). Mechanical restitution during alternans in guinea pig papillary muscles. Cardiovasc. Res. 26, 779-782.
81. Surawicz, B., and Fisch, C. (1992). Cardiac alternans: diverse mechanisms and clinical manifestations. J. Am. Coll. Cardiol. 20, 483-499.
82. Uno, K. (1991). Mechanisms of pulsus alternans: its relation to alternation of regional contraction and elevated ST segment. Am. Heart J. 122, 1694-1700.
83. Verrier, R. L., and Nearing, B. D. (1994). Electrophysiologic basis for T wave alternans as an index of vulnerability to ventricular fibrillation. J. Cardiovasc. Electrophysiol. 5, 445-461.
84. 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.
85. 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.
86. Wohlfart, B. (1982). Analysis of mechanical alternans in rabbit papillary muscle. Acta. Physiol. Scand. 115, 405-414.
87. Wu, J. Y., Vereecke, J., Carmeliet, E., and Lipsius, S. L. (1991). Ionic currents activated during hyperpolarization of single right atrial myocytes from cat heart. Circ. Res. 68, 1059-1069.
88. Wu, Y., and Clusin, W. T. (1997). Calcium transient alternans in blood-perfused ischemic hearts: observations with fluorescent indicator fura red. Am. J. Physiol. 273, H2161-H2169.
89. Xie, L. H., Sato, D., Garfinkel, A., Qu, Z., and Weiss, J. N. (2008). Intracellular Ca alternans: coordinated regulation by sarcoplasmic reticulum release, uptake, and leak. Biophys. J. 95, 3100-3110.
90. Xie, L. H., and Weiss, J. N. (2009). Arrhythmogenic consequences of intracellular calcium waves. Am. J. Physiol. Heart Circ. Physiol. 297, H997-H1002.
91. 2+ transport. Circ. Res. 77, 88-97.
92. (2+) signalling in cat atrial excitation-contraction coupling and arrhythmias. J. Physiol. 555, 607-615.