Dynamical description of sinoatrial node pacemaking: Improved mathematical model for primary pacemaker cell

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 283, Issue 5 52-5, 2002, Pages

  Kurata, Yasutaka ^a,b   Hisatome, Ichiro ^a,b   Imanishi, Sunao ^a,b   Shibamoto, Toshishige ^a,b  

^a KANAZAWA MEDICAL UNIVERSITY   (Japan)

^b TOTTORI UNIVERSITY   (Japan)

Author keywords

Bifurcation diagram; Computer simulation; Nonlinear dynamical system; Rabbit sinoatrial node

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); CALCIUM CHANNEL L TYPE; CALCIUM ION; CHLORIDE ION; POTASSIUM CHANNEL; POTASSIUM ION; SODIUM ION;

ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; HUMAN; HUMAN CELL; MATHEMATICAL MODEL; MEMBRANE POTENTIAL; NONHUMAN; PACEMAKER; PATCH CLAMP; PRIORITY JOURNAL; RABBIT; SARCOLEMMA; SARCOPLASMIC RETICULUM; SINUS NODE; SODIUM CALCIUM EXCHANGE;

EID: 0036838501     PISSN: 03636135     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpheart.00900.2001     Document Type: Article

References (130)

1. 2+ channels and ryanodine receptors in rat ventricular myocytes. J Gen Physiol 108: 435-454, 1996.
2. Anumonwo JMB, Freeman LC, Kwok WM, and Kass RS. Delayed rectification in single cells isolated from guinea pig sinoatrial node. Am J Physiol Heart Circ Physiol 262: H921-H925, 1992.
3. Baruscotti M, DiFrancesco D, and Robinson RB. A TTX-sensitive inward sodium current contributes to spontaneous activity in newborn rabbit sino-atrial node cells. J Physiol 492: 21-30, 1996.
4. + current contribution to the diastolic depolarization in newborn rabbit SA node cells. Am J Physiol Heart Circ Physiol 279: H2303-H2309, 2000.
5. Bers DM and Perez-Reyes E. Ca channels in cardiac myocytes: Structure and function in Ca influx and intracellular Ca release. Cardiovasc Res 42: 339-360, 1999.
6. 2- exchanger: Molecular partners in pacemaker regulation. Circ Res 88: 1254-1258, 2001.
7. Boyett MR, Honjo H, Yamamoto M, Nikmaram MR, Niwa R, and Kodama I. Regional differences in effects of 4-aminopyridine within the sinoatrial node. Am J Physiol Heart Circ Physiol 275: H1158-H1168, 1998.
8. Boyett MR, Honjo H, Yamamoto M, Nikmaram MR, Niwa R, and Kodama I. Downward gradient in action potential duration along conduction path in and around the sinoatrial node. Am J Physiol Heart Circ Physiol 276: H686-H698, 1999.
9. 2+. Experiments and modelling. Philos Trans R Soc Lond A Math Phys Sci 359: 1091-1110, 2001.
10. Brown HF, Kimura J, Noble D, Noble SJ, and Taupignon A. The ionic currents underlying pacemaker activity in rabbit sino-atrial node: Experimental results and computer simulations. Proc R Soc Lond B Biol Sci 222: 329-347, 1984.
11. Campbell DL, Giles WR, Hume JR, Noble D, and Shibata EF. Reversal potential of the calcium current in bull-frog atrial myocytes. J Physiol 403: 267-286, 1988.
12. Cannell MB and Allen DG. Model of calcium movements during activation in the sarcomere of frog skeletal muscle. Biophys J 45: 913-925, 1984.
13. - in cardiac cells? Cardiovasc Res 26: 433-442, 1992.
14. Clancy CE and Rudy Y. Cellular consequences of HERG mutations in the long QT syndrome: precursors to sudden cardiac death. Cardiovasc Res 50: 301-313, 2001.
15. Courtemanche M, Ramirez RJ, and Nattel S. Ionic mechanisms underlying human atrial action potential properties: Insights from a mathematical model. Am J Physiol Heart Circ Physiol 275: H301-H321, 1998.
16. Demir SS, Clark JW, and Giles WR. Parasympathetic modulation of sinoatrial node pacemaker activity in rabbit heart: A unifying model. Am J Physiol Heart Circ Physiol 276: H2221-H2244, 1999.
17. Demir SS, Clark JW, Murphey CR, and Giles WR. A mathematical model of a rabbit sinoatrial node cell. Am J Physiol Cell Physiol 266: C832-C852, 1994.
18. f. J Physiol 429: 401-409, 1990.
19. Denyer JC and Brown HF. Rabbit sino-atrial node cells: Isolation and electrophysiological properties. J Physiol 428: 405-424, 1990.
20. f) to generation of spontaneous activity in rabbit sino-atrial node myocytes. J Physiol 434: 23-40, 1991.
21. f) in cells isolated from the rabbit sino-atrial node. J Physiol 377: 61-88, 1986.
22. DiFrancesco D and Noble D. A model of cardiac electrical activity incorporating ionic pumps and concentration changes. Philos Trans R Soc Lond B Biol Sci 307: 353-398, 1985.
23. Doerr T, Denger R, and Trautwein W. Calcium currents in single SA nodal cells of the rabbit heart studied with action potential clamp. Pflügers Arch 413: 599-603, 1989.
24. Dokos S, Celler B, and Lovell N. Ion currents underlying sinoatrial node pacemaker activity: A new single cell mathematical model. J Theor Biol 181: 245-272, 1996.
25. Dokos S, Celler B, and Lovell N. Vagal control of sinoatrial rhythm: A mathematical model. J Theor Biol 182: 21-44, 1996.
26. Egan T and Noble D. Acetylcholine and the mammalian "slow inward" current: A computer investigation. Proc R Soc Lond B Biol Sci 230: 315-337, 1987.
27. Fermini B and Nathan R. Removal of sialic acid alters both T- and L-type calcium currents in cardiac myocytes. Am J Physiol Heart Circ Physiol 260: H735-H743, 1991.
28. Giles WR and van Ginneken ACG. A transient outward current in isolated cells from the crista terminalis of rabbit heart. J Physiol 368: 243-264, 1985.
29. 2+ release from the sarcoplasmic reticulum: A computer model. Ann Biomed Eng 26: 213-229, 1998.
30. Guevara MR and Jongsma HJ. Three ways of abolishing automaticity in sinoatrial node: Ionic modeling and nonlinear dynamics. Am J Physiol Heart Circ Physiol 262: H1268-H1286, 1992.
31. Guo J, Mitsuiye T, and Noma A. The sustained inward current in sino-atrial node cells of guinea-pig heart. Pflügers Arch 433: 390-396, 1997.
32. Guo J, Ono K, and Noma A. A sustained inward current activated at the diastolic potential range in rabbit sino-atrial node cells. J Physiol 483: 1-13, 1995.
33. Guo J, Ono K, and Noma A. Monovalent cation conductance of the sustained inward current in rabbit sinoatrial node cells. Pflügers Arch 433: 209-211, 1996.
34. Habuchi Y, Han X, and Giles WR. Comparison of the hyperpolarization-activated and delayed rectifier currents in rabbit atrioventricular node and sinoatrial node. Heart Vessels Suppl 9: 203-206, 1995.
35. 2+ channels in guinea-pig ventricular myocytes through independent mechanisms. J Physiol 444: 257-268, 1991.
36. Hagiwara N and Irisawa H. Na-Ca exchange current in sinoatrial node cell of rabbit (Abstract). Circulation, Suppl 78: 490a, 1988.
37. Hagiwara N, Irisawa H, and Kameyama M. Contribution of two types of calcium currents to the pacemaker potentials of rabbit sino-atrial node cells. J Physiol 395: 233-253, 1988.
38. Hagiwara N, Irisawa H, Kasanuki H, and Hosoda S. Background current in sino-atrial node cells of the rabbit heart. J Physiol 448: 53-72, 1992.
39. 2+ release from sarcoplasmic reticulum in the regulation of sinoatrial node automaticity. Heart Vessels 11: 234-241, 1996.
40. Ks in guinea-pig isolated ventricular myocytes. Exp Physiol 81: 605-621, 1996.
41. Hess P and Tsien RW. Mechanism of ion permeation through calcium channels. Nature 309: 453-456, 1984.
42. Hilgemann DW and Noble D. Excitation-contraction coupling and extracellular calcium transients in rabbit atrium: Reconstruction of basic cellular mechanisms. Proc R Soc Lond B Biol Sci 230: 163-205, 1987.
43. 2+. J Physiol 494: 727-742, 1996.
44. Honjo H, Boyett MR, Kodama I, and Toyama J. Correlation between electrical activity and the size of rabbit sino-atrial node cells. J Physiol 496: 795-808, 1996.
45. Honjo H, Kodama I, Zang WJ, and Boyett MR. Desensitization to acetylcholine in single sinoatrial node cells isolated from rabbit hearts. Am J Physiol Heart Circ Physiol 263: H1779-H1789, 1992.
46. Honjo H, Lei M, Boyett MR, and Kodama I. Heterogeneity of 4-aminopyridine-sensitive current in rabbit sinoatrial node cells. Am J Physiol Heart Circ Physiol 276: H1295-H1304, 1999.
47. 2- release contributes to automaticity in cat atrial pacemaker cells. J Physiol 524: 415-422, 2000.
48. + channel in rabbit sinoatrial node cells. Am J Physiol Heart Circ Physiol 269: H443-H452, 1995.
49. - channels in rabbit sino-atrial node cells. J Physiol 476: 55-68, 1994.
50. 2+ dynamics: The roles of ryanodine receptor adaptation and sarcoplasmic reticulum load. Biophys J 74: 1149-1168, 1998.
51. Janiak R, Lewartowski B, and Langer GA. Functional coupling between sarcoplasmic reticulum and Na/Ca exchange in single myocytes of guinea-pig and rat heart. J Mol Cell Cardiol 28: 253-264, 1996.
52. Janvier NC and Boyett MR. The role of Na-Ca exchange current in the cardiac action potential. Cardiovasc Res 32: 69-84, 1996.
53. 2+ exchange current in isolated toad pacemaker cells. J Physiol 508: 153-166, 1998.
54. Kawano S and Hiraoka M. Transient outward currents and action potential alterations in rabbit ventricular myocytes. J Mol Cell Cardiol 23: 681-693, 1991.
55. Kodama I, and Boyett MR. Regional differences in the electrical activity of the rabbit sinus node. Pflügers Arch 404: 214-226, 1985.
56. Kodama I, Boyett MR, Nikmaram MR, Yamamoto M, Honjo H, and Niwa R. Regional differences in effects of E-4031 within the sinoatrial node. Am J Physiol Heart Circ Physiol 276: H793-H802, 1999.
57. + currents in pacemaker activity in the sinoatrial node. Am J Physiol Heart Circ Physiol 272: H2793-H2806, 1997.
58. Kohlhardt M, Figulla HR, and Tripathi O. The slow membrane channel as the predominant mediator of the excitation process of the sinoatrial pacemaker cell. Basic Res Cardiol 71: 17-26, 1976.
59. Kreitner D. Electrophysiological study of the two main pacemaker mechanisms in the rabbit sinus node. Cardiovasc Res 19: 304-318, 1985.
60. Lacampagne A, Caputo C, and Argibay J. Effect of ryanodine on cardiac calcium current and calcium channel gating current. Biophys J 70: 370-375, 1996.
61. Langer GA and Peskoff A. Calcium concentration and movement in the diadic cleft space of the cardiac ventricular cell. Biophys J 70: 1169-1182, 1996.
62. Lederer WJ, Niggli E, and Hadley RW. Sodium-calcium exchange in excitable cells: Fuzzy space. Science 248: 283, 1990.
63. Lee AJ and Allen DJ. EMD 53988 sensitizes the contractile proteins to calcium in intact ferret ventricular muscle. Circ Res 69: 927-936, 1991.
64. K, in rabbit sino-atrial node cells. Exp Physiol 81: 725-741, 1996.
65. + current in rabbit sinoatrial node cells. Cardiovasc Res 46: 433-441, 2000.
66. + current in human ventricular myocytes. Circ Res 78: 689-696, 1996.
67. Li J, Qu J, and Nathan RD. Ionic basis of ryanodine's negative chronotropic effect on pacemaker cells isolated from the sinoatrial node. Am J Physiol Heart Circ Physiol 273: H2481-H2489, 1997.
68. Lindblad DS, Murphey CR, Clark JW, and Giles WR. A model of the action potential and underlying membrane currents in a rabbit atrial cell. Am J Physiol Heart Circ Physiol 271: H1666-H1696, 1996.
69. Liu S and Rasmusson RL. Hodgkin-Huxley and partially coupled inactivation models yield different voltage dependence of block. Am J Physiol Heart Circ Physiol 272: H2013-H2022, 1997.
70. K in rabbit sinoatrial node myocytes: Implications for SA node automaticity. J Cardiovasc Pharmacol 32: 783-790, 1998.
71. Luo CH and Rudy Y. A dynamic model of the cardiac ventricular action potential. I. Simulations of ionic currents and concentration changes. Circ Res 74: 1071-1096, 1994.
72. Mangoni ME, Fontanaud P, Noble PJ, Noble D, Benkemoun H, Nargeot J, and Richard S. Facilitation of the L-type calcium current in rabbit sino-atrial cells: Effect on cardiac automaticity. Cardiovasc Res 48: 375-392, 2000.
73. Maruoka F, Nakashima Y, Takano M, Ono K, and Noma A. Cation-dependent gating of the hyperpolarization-activated cation current in the rabbit sino-atrial node cells. J Physiol 477: 423-435, 1994.
74. Matsuoka S and Hilgemann DW. Steady-state and dynamic properties of cardiac sodium-calcium exchange: Ion and voltage dependencies of the transport cycle. J Gen Physiol 100: 963-1001, 1992.
75. 2+, and regulation of ion pumps in ventricular myocyte. Biophys J 81: 614-629, 2001.
76. Mironov SL. Conformational model for ion permeation in membrane channels: A comparison with multi-ion models and applications to calcium channel permeability. Biophys J 63: 485-496, 1992.
77. +-mediated single channel currents in guinea-pig sinoatrial node pacemaker cells. J Physiol 521: 69-79, 1999.
78. Mitsuiye T, Shinagawa Y, and Noma A. Sustained inward current during pacemaker depolarization in mammalian sinoatrial node cells. Circ Res 87: 88-91, 2000.
79. ++ reduction in rabbit sinoatrial node cell treated with K-free medium. J Kanazawa Med Univ 16: 406-412, 1991.
80. + current in pacemaker cells isolated from rabbit sinoatrial node. Am J Physiol Heart Circ Physiol 270: H2108-H2119, 1996.
81. Nakayama T, Kurachi Y, Noma A, and Irisawa H. Action potential and membrane currents of single pacemaker cells of the rabbit heart. Pflügers Arch 402: 248-257, 1984.
82. Nathan RD. Two electrophysiologically distinct types of cultured pacemaker cells from rabbit sinoatrial node. Am J Physiol Heart Circ Physiol 250: H325-H329, 1986.
83. -, UL-FS-49, and ZD-7288 within sinoatrial node. Am J Physiol Heart Circ Physiol 272: H2782-H2792, 1997.
84. Nilius B. Possible functional significance of a novel type of cardiac Ca channel. Biomed Biochim Acta 45: 37-45, 1986.
85. Noble D and Noble SJ. A model of sino-atrial node electrical activity based on a modification of the DiFrancesco-Noble (1984) equations. Proc R Soc Lond B Biol Sci 222: 295-304, 1984.
86. Ks, and length- and tension-dependent processes. Can J Cardiol 14: 123-134, 1998.
87. Noma A, Morad M, and Irisawa H. Does the "pacemaker current" generate the diastolic depolarization in the rabbit SA node cells? Pflügers Arch 397: 190-194, 1983.
88. + currents in repolarization. Circ Res 82: 63-81, 1998.
89. Oei HI, van Ginneken ACG, Jongsma HJ, and Bouman LN. Mechanisms of impulse generation in isolated cells from the rabbit sinoatrial node. J Mol Cell Cardiol 21: 1137-1149, 1989.
90. + current in sinoatrial pacemaker activity. Am J Physiol Heart Circ Physiol 269: H453-H462, 1995.
91. Priebe L and Beuckelmann DJ. Simulation study of cellular electric properties in heart failure. Circ Res 82: 1206-1223, 1998.
92. Puglisi JL and Bers DM. LabHEART: An interactive computer model of rabbit ventricular myocyte ion channels and Ca transport. Am J Physiol Cell Physiol 281: C2049-C2060, 2001.
93. 2+ release in the functional unit of the cardiac diadic space. Biophys J 77: 1871-1884, 1999.
94. Rigg L and Terrer DA. Possible role of calcium release from the sarcoplasmic reticulum in pacemaking in guinea-pig sinoatrial node. Exp Physiol 81: 877-880, 1996.
95. 2+. Biophys J 34: 559-569, 1981.
96. Rubenstein DS, Fox LM, McNulty JA, and Lipsius SL. Electrophysiology and ultrastructure of Eustachian ridge from cat right atrium: A comparison with SA node. J Mol Cell Cardiol 19: 965-976, 1987.
97. Rubenstein DS and Lipsius SL. Mechanisms of automaticity in subsidiary pacemakers from cat right atrium. Circ Res 64: 648-657, 1989.
98. Saint DA. Pacemaking in the heart: The interplay of ionic currents. Clin Exp Pharmacol Physiol 25: 841-846, 1998.
99. Sakai R, Hagiwara N, Matsuda N, Kasanuki H, and Hosoda S. Sodium-potassium pump current in rabbit sinoatrial node cells. J Physiol 490: 51-62, 1996.
100. - current: Differential sensitivity to block by class III antiarrhythmic agents. J Gen Physiol 96: 195-215, 1990.
101. + current is composed of two currents in guinea pig atrial cells. Am J Physiol Heart Circ Physiol 260: H393-H399, 1991.
102. Satoh H. Ouabain actions on the spontaneous activity and ionic currents in rabbit sino-atrial node cells. Gen Pharmacol 25: 1591-1598, 1994.
103. 2+ channel inhibitors in the pace-maker depolarization in rabbit sino-atrial nodal cells. Gen Pharmacol 26: 581-587, 1995.
104. Satoh H. Electrophysiological actions of ryanodine on single rabbit sinoatrial nodal cells. Gen Pharmacol 28: 31-38, 1997.
105. 2+. Biophys J 69: 1847-1857, 1995.
106. 2+ signaling. J Physiol 500: 285-295, 1997.
107. Shannon TR and Bers DM. Assessment of intra-SR free [Ca] and buffering in rat heart. Biophys J 73: 1524-1531, 1997.
108. Shibasaki T. Conductance and kinetics of delayed rectifier potassium channels in nodal cells of the rabbit heart. J Physiol 387: 227-250, 1987.
109. + current in pacemaker cells disociated from rat sinoatrial node. J Physiol 523: 593-605, 2000.
110. 2+ exchange. Circ Res 81: 1034-1044, 1997.
111. 2+ channel. Biophys J 71: 3064-3072, 1996.
112. Smith PD, Liesegang GW, Berger RL, Czerlinski G, and Podolsky RJ. A stopped-flow investigation of calcium ion binding by ethylene glycol bis (β-aminoethyl ether)-N,N-tetraacetic acid. Anal Biochem 143: 188-195, 1984.
113. 2+ control. Biophys J 79: 94-115, 2000.
114. Soeller C and Cannell MB. Numerical simulation of local calcium movements during L-type calcium channel gating in the cardiac diad. Biophys J 73: 97-111, 1997.
115. Stern MD, Song LS, Cheng H, Sham JSK, Yang HT, Boheler KR, and Rios E. Local control models of cardiac excitation-contraction coupling: A possible role for allosteric interactions between ryanodine receptors. J Gen Physiol 113: 469-489, 1999.
116. 2+ channel in rat ventricular myocytes: Ion selectivity and inactivation mechanisms. J Physiol 529: 139-158, 2000.
117. Uese K, Hagiwara N, Miyawaki T, and Kasanuki H. Properties of the transient outward current in rabbit sino-atrial node cells. J Mol Cell Cardiol 31: 1975-1984, 1999.
118. Van Ginneken ACG and Giles WR. Voltage clamp measurements of the hyperpolarization-activated inward current If in single cells from rabbit sino-atrial node. J Physiol 434: 57-83, 1991.
119. Verheijck EE, van Ginneken ACG, Bourier J, and Bouman LN. Effects of delayed rectifier current blockade by E-4031 on impulse generation in single sinoatrial nodal myocytes of the rabbit. Circ Res 76: 607-615, 1995.
120. 2+ current to electrical activity in sinoatrial nodal myocytes of rabbits. Am J Physiol Heart Circ Physiol 276: H1064-H1077, 1999.
121. Verheijck EE, Wessels A, van Ginneken ACG, Bourier J, Markman MWM, Vermeulen JLM, de Bakker JMT, Lamers WH, Opthof T, and Bouman LN. Distribution of atrial and nodal cells within the rabbit sinoatrial node: Models of sinoatrial transition. Circulation 97: 1623-1631, 1998.
122. 2+/calmodulin-dependent protein kinase II activation. Circ Res 87: 760-767, 2000.
123. Wang Z, Fermini B, and Nattel S. Rapid and slow components of delayed rectifier current in human atrial myocytes. Cardiovasc Res 28: 1540-1546, 1994.
124. Wilders R, Jongsma HJ, and van Ginneken ACG. Pacemaker activity of the rabbit sinoatrial node: A comparison of mathematical models. Biophys J 60: 1202-1216, 1991.
125. Wu J, Schuessler RB, Rodefeld MD, Saffitz JE, and Boineau JP. Morphological and membrane characteristics of spider and spindle cells isolated from rabbit sinus node. Am J Physiol Heart Circ Physiol 280: H1232-H1240, 2001.
126. Yanagihara K and Irisawa H. Potassium current during the pacemaker depolarization in rabbit sinoatrial node cell. Pflügers Arch 388: 255-260, 1980.
127. You Y, Pelzer DJ, and Pelzer S. Trypsin and forskolin decrease the sensitivity of L-type calcium current to inhibition by cytoplasmic free calcium in guinea pig heart muscle cells. Biophys J 69: 1838-1846, 1995.
128. 2+ buffering in guinea pig ventricular cardiomyocytes. Biophys J 72: 175-187, 1997.
129. Zaza A, Micheletti M, Brioschi A, and Rocchetti M. Ionic currents during sustained pacemaker activity in rabbit sinoatrial myocytes. J Physiol 505: 677-688, 1997.
130. Zhang H, Holden AV, Kodama I, Honjo H, Lei M, Varghese T, and Boyett MR. Mathematical models of action potentials in the periphery and center of the rabbit sinoatrial node. Am J Physiol Heart Circ Physiol 279: H397-H421, 2000.