Intracellular Ca2+ oscillations, a potential pacemaking mechanism in early embryonic heart cells

Journal of General Physiology

Volumn 130, Issue 2, 2007, Pages 133-144

  Sasse, Philipp ^a   Zhang, Jianbao ^b,c   Cleemann, Lars ^d   Morad, Martin ^d   Hescheler, Juergen ^b   Fleischmann, Bernd K ^a  

^a UNIVERSITY OF BONN   (Germany)

^b UNIVERSITY OF COLOGNE   (Germany)

^c XI'AN JIAOTONG UNIVERSITY   (China)

^d GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; INOSITOL 1,4,5 TRISPHOSPHATE; RYANODINE RECEPTOR; SODIUM CALCIUM EXCHANGE PROTEIN; ION CHANNEL;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM SIGNALING; CONTROLLED STUDY; EMBRYO; HEART MUSCLE CELL; MECHANOTRANSDUCTION; MEMBRANE DEPOLARIZATION; MEMBRANE POTENTIAL; MOUSE; NONHUMAN; SARCOPLASMIC RETICULUM; ANIMAL; BIOLOGICAL RHYTHM; CELL COMMUNICATION; CELL CULTURE; ELECTROPHYSIOLOGY; HEART; METABOLISM; MUSCLE CONTRACTION; PATCH CLAMP; PHYSIOLOGY; PRENATAL DEVELOPMENT;

ACTION POTENTIALS; ANIMALS; BIOLOGICAL CLOCKS; CALCIUM; CELL COMMUNICATION; CELLS, CULTURED; ELECTROPHYSIOLOGY; HEART; ION CHANNELS; MICE; MUSCLE CONTRACTION; MYOCYTES, CARDIAC; PATCH-CLAMP TECHNIQUES; SODIUM-CALCIUM EXCHANGER;

EID: 34547624122     PISSN: 00221295     EISSN: 00221295     Source Type: Journal    
DOI: 10.1085/jgp.200609575     Document Type: Article

References (44)

1. Abi-Gerges, N., G.J. Ji, Z.J. Lu, R. Fischmeister, J. Hescheler, and B.K. Fleischmann. 2000. Functional expression and regulation of the hyperpolarization activated non-selective cation current in embryonic stem cell-derived cardiomyocytes. J. Physiol. 523:377-389.
2. 2+ channels and ryanodine receptors in rat ventricular myocytes. J. Gen. Physiol. 108:435-454.
3. Atri, A., J. Amundson, D. Clapham, and J. Sneyd. 1993. A single-pool model for intracellular calcium oscillations and waves in the Xenopus laevis oocyte. Biophys. J. 65:1727-1739.
4. Baruscotti, M., and D. DiFrancesco. 2004. Pacemaker channels. Ann. N. Y. Acad. Sci. 1015:111-121.
5. Blatter, L.A., J. Kockskamper, K.A. Sheehan, A.V. Zima, J. Huser, and S.L. Lipsius. 2003. Local calcium gradients during excitation-contraction coupling and alternans in atrial myocytes. J. Physiol. 546:19-31.
6. 2+ oscillations in cardiac cells. J. Cell Biol. 152:717-728.
7. 2+ release sites in rat cardiac myocytes. Proc. Natl. Acad. Sci. USA. 95:10984-10989.
8. Clusin, W.T. 2003. Calcium and cardiac arrhythmias: DADs, EADs, and alternans. Crit. Rev. Clin. Lab. Sci. 40:337-375.
9. 2+ response amplitude and duration. Nature. 386:855-858.
10. Dumollard, R., J. Carroll, G. Dupont, and C. Sardet. 2002. Calcium wave pacemakers in eggs. J. Cell Sci. 115:3557-3564.
11. Fabiato, A. 1983. Calcium-induced release of calcium from the cardiac sarcoplasmic reticulum. Am. J. Physiol. 245:C1-14.
12. Fleischmann, B.K., Y. Duan, Y. Fan, T. Schoneberg, A. Ehlich, N. Lenka, S. Viatchenko-Karpinski, L. Pott, J. Hescheler, and B. Fakler. 2004. Differential subunit composition of the G protein-activated inward-rectifier potassium channel during cardiac development. J. Clin. Invest. 114:994-1001.
13. 2+ oscillations and for their frequency encoding through protein phosphorylation. Proc. Natl. Acad. Sci. USA. 87:1461-1465.
14. Healy, J.I., R.E. Dolmetsch, L.A. Timmerman, J.G. Cyster, M.L. Thomas, G.R. Crabtree, R.S. Lewis, and C.C. Goodnow. 1997. Different nuclear signals are activated by the b cell receptor during positive versus negative signaling. Immunity. 6:419-428.
15. Herr, C., N. Smyth, S. Ullrich, F. Yun, P. Sasse, J. Hescheler, B. Fleischmann, K. Lasek, K. Brixius, R.H. Schwinger, et al. 2001. Loss of annexin A7 leads to alterations in frequency-induced shortening of isolated murine cardiomyocytes. Mol. Cell. Biol. 21:4119-4128.
16. Janse, M.J. 2004. Electrophysiological changes in heart failure and their relationship to arrhythmogenesis. Cardiovasc. Res. 61:208-217.
17. Kamino, K. 1991. Optical approaches to ontogeny of electrical activity and related functional organization during early heart development. Physiol. Rev. 71:53-91.
18. Katra, R.P., and K.R. Laurita. 2005. Cellular mechanism of calcium-mediated triggered activity in the heart. Circ. Res. 96:535-542.
19. 2+ oscillations. Biophys. J. 71:3477-3487.
20. Kolossov, E., B.K. Fleischmann, Q. Liu, W. Bloch, S. Viatchenko- Karpinski, O. Manzke, G.J. Ji, H. Bohlen, K. Addicks, and J. Hescheler. 1998. Functional characteristics of ES cell-derived cardiac precursor cells identified by tissue-specific expression of the green fluorescent protein. J. Cell Biol. 143:2045-2056.
21. Kolossov, E., Z. Lu, I. Drobinskaya, N. Gassanov, Y. Duan, H. Sauer, O. Manzke, W. Bloch, H. Bohlen, J. Hescheler, and B.K. Fleischmann. 2005. Identification and characterization of embryonic stem cell-derived pacemaker and atrial cardiomyocytes. FASEB J. 19:577-579.
22. Koushik, S.V., J. Wang, R. Rogers, D. Moskophidis, N.A. Lambert, T.L. Creazzo, and S.J. Conway. 2001. Targeted inactivation of the sodium-calcium exchanger (Ncx1) results in the lack of a heartbeat and abnormal myofibrillar organization. FASEB J. 15:1209-1211.
23. Lehnart, S.E., C. Terrenoire, S. Reiken, X.H. Wehrens, L.S. Song, E.J. Tillman, S. Mancarella, J. Coromilas, W.J. Lederer, R.S. Kass, and A.R. Marks. 2006. Stabilization of cardiac ryanodine receptor prevents intracellular calcium leak and arrhythmias. Proc. Natl. Acad. Sci. USA. 103:7906-7910.
24. 2+ checkpoint in cardiac myofibrillogenesis. J. Cell Biol. 158:103-113.
25. Maltsev, V.A., T.M. Vinogradova, K.Y. Bogdanov, E.G. Lakatta, and M.D. Stern. 2004. Diastolic calcium release controls the beating rate of rabbit sinoatrial node cells: numerical modeling of the coupling process. Biophys. J. 86:2596-2605.
26. Maltsev, V.A., T.M. Vinogradova, and E.G. Lakatta. 2006. The emergence of a general theory of the initiation and strength of the heartbeat. J. Pharmacol. Sci. 100:338-369.
27. Maltsev, V.A., A.M. Wobus, J. Rohwedel, M. Bader, and J. Hescheler. 1994. Cardiomyocytes differentiated in vitro from embryonic stem cells developmentally express cardiac-specific genes and ionic currents. Circ. Res. 75:233-244.
28. Mery, A., F. Aimond, C. Menard, K. Mikoshiba, M. Michalak, and M. Puceat. 2005. Initiation of embryonic cardiac pacemaker activity by inositol 1,4,5-trisphosphate-dependent calcium signaling. Mol. Biol. Cell. 16:2414-2423.
29. 2+-activated cation channel TRPM4. J. Biol. Chem. 278:30813-30820.
30. 2+ exchanger in the embryonic mouse heart. J. Mol. Cell. Cardiol. 42:121-132.
31. Rubart, M., and D.P. Zipes. 2005. Mechanisms of sudden cardiac death. J. Clin. Invest. 115:2305-2315.
32. 2+ release causes myocyte depolarization. Underlying mechanism and threshold for triggered action potentials. Circ. Res. 87:774-780.
33. Schram, G., M. Pourrier, P. Melnyk, and S. Nattel. 2002. Differential distribution of cardiacion channel expression as a basis for regional specialization in electrical function. Circ. Res. 90:939-950.
34. Seisenberger, C., V. Specht, A. Welling, J. Platzer, A. Pfeifer, S. Kuhbandner, J. Striessnig, N. Klugbauer, R. Feil, and F. Hofmann. 2000. Functional embryonic cardiomyocytes after disruption of the L-type alpha 1C (Cav1.2) calcium channel gene in the mouse. J. Biol. Chem. 275:39193-39199.
35. Shih, H.T. 1994. Anatomy of the action potential in the heart. Tex. Heart Inst. J. 21:30-41.
36. Spitkovsky, D., P. Sasse, E. Kolossov, C. Bottinger, B.K. Fleischmann, J. Hescheler, and R.J. Wiesner. 2004. Activity of complex III of the mitochondrial electron transport chain is essential for early heart muscle cell differentiation. FASEB J. 18:1300-1302.
37. Stieber, J., S. Herrmann, S. Feil, J. Loster, R. Feil, M. Biel, F. Hofmann, and A. Ludwig. 2003. The hyperpolarization-activated channel HCN4 is required for the generation of pacemaker action potentials in the embryonic heart. Proc. Natl. Acad. Sci. USA. 100:15235-15240.
38. Takeshima, H., S. Komazaki, K. Hirose, M. Nishi, T. Noda, and M. Iino. 1998. Embryonic lethality and abnormal cardiac myocytes in mice lacking ryanodine receptor type 2. EMBO J. 17:3309-3316.
39. Verkerk, A.O., M.W. Veldkamp, A. Baartscheer, C.A. Schumacher, C. Klopping, A.C. van Ginneken, and J.H. Ravesloot. 2001. Ionic mechanism of delayed afterdepolarizations in ventricular cells isolated from human end-stage failing hearts. Circulation. 104:2728-2733.
40. 2+ oscillations drive spontaneous contractions in cardiomyocytes during early development. Proc. Natl. Acad. Sci. USA. 96:8259-8264.
41. 2+ releases during diastolic depolarization of sinoatrial pacemaker cells do not require membrane depolarization. Circ. Res. 94:802-809.
42. 2+ release in rat atrial myocytes: evidence from rapid 2-D confocal imaging. J. Physiol. 543:439-453.
43. 2+ release in rat atrial myocytes. Circ. Res. 92:e1-11.
44. Yang, H.T., D. Tweedie, S. Wang, A. Guia, T. Vinogradova, K. Bogdanov, P.D. Allen, M.D. Stern, E.G. Lakatta, and K.R. Boheler. 2002. The ryanodine receptor modulates the spontaneous beating rate of cardiomyocytes during development. Proc. Natl. Acad. Sci. USA. 99:9225-9230.