Mathematical simulations of ligand-gated and cell-type specific effects on the action potential of human atrium

Progress in Biophysics and Molecular Biology

Volumn 98, Issue 2-3, 2008, Pages 161-170

  Maleckar, Mary M ^a   Greenstein, Joseph L ^a   Trayanova, Natalia A ^a   Giles, Wayne R ^b  

^a Johns Hopkins University School of Medicine   (United States)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

Acetylcholine; Fibroblast; Human atrium; Mathematical model; Natriuretic peptides

Indexed keywords

ACETYLCHOLINE; ATRIAL NATRIURETIC FACTOR; ION CHANNEL;

ACTION POTENTIAL; ARTICLE; BIOLOGICAL MODEL; CHANNEL GATING; CYTOLOGY; DRUG EFFECT; FIBROBLAST; HEART ATRIUM; HEART ATRIUM FUNCTION; HEART MUSCLE CELL; HUMAN; PHYSIOLOGY; THEORETICAL MODEL;

ACETYLCHOLINE; ACTION POTENTIALS; ATRIAL FUNCTION; ATRIAL NATRIURETIC FACTOR; FIBROBLASTS; HEART ATRIA; HUMANS; ION CHANNEL GATING; ION CHANNELS; MODELS, CARDIOVASCULAR; MODELS, THEORETICAL; MYOCYTES, CARDIAC;

MAMMALIA;

EID: 61849157383     PISSN: 00796107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbiomolbio.2009.01.010     Document Type: Article

References (71)

1. Amos G.J., Wettwer E., Metzger F., Li Q., Himmel H.M., and Ravens U. Differences between outward currents of human atrial and subepicardial ventricular myocytes. J. Physiol. 491 Pt 1 (1996) 31-50
2. Allessi R., Nusynowitz M., Abildskov J.A., and Moe G.K. Nonuniform distribution of vagal effects on dog atria. Circ. Res. 194 (1958) 406-410
3. Blaauw Y., Schotten U., van Hunnik A., Neuberger H.R., and Allessie M.A. Cardioversion of persistent atrial fibrillation by a combination of atrial-specific and non-specific class III drugs in the goat. Cardiovasc. Res. 75 (2007) 89-98
4. Baudino T.A., Carver W., Giles W., and Borg T.K. Cardiac fibroblasts: friend or foe?. Am. J. Physiol. Heart Circ. Physiol. 291 (2006) H1015-H1026
5. + current in human atrial fibrillation. Their possible role in post operative atrial fibrillation. J. Mol. Cell Cardiol. 32 (2000) 1885-1896
6. Brown R.D., Ambler S.K., Mitchell M.D., and Long C.S. The cardiac fibroblast: therapeutic target in myocardial remodeling and failure. Annu. Rev. Pharmacol. Toxicol. 45 (2005) 657-687
7. Boyett M.R., Kodama I., Honjo H., Arai A., Suzuki R., and Toyama J. Ionic basis of the chronotropic effect of acetylcholine on the rabbit sinoatrial node. Cardiovasc. Res. 29 (1995) 867-878
8. Burashnikov A., and Antzelevitch C. Late-phase 3 EAD. A unique mechanism contributing to initiation of atrial fibrillation. PACE 29 (2006) 290-295
9. Burstein B., and Nattel S. Atrial fibrosis: mechanisms and clinical relevance in atrial fibrillation. J. Am. Coll. Cardiol. 51 (2008) 802-809
10. Cabo C. Modulation of impulse propagation by fibroblasts. Am. J. Physiol. Heart Circ. Physiol. 294 (2008) H1992-H1993
11. Camelliti P., Borg T.K., and Kohl P. Structural and functional characterization of cardiac fibroblasts. Cardiovasc. Res. 65 (2005) 40-51
12. Chilton L., Giles W.R., and Smith G.L. Evidence of intercellular coupling between co-cultured adult rabbit ventricular myocytes and myofibroblasts. J. Physiol. 583 (2007) 225-236
13. K,ACh blocker AVE0118 on ion channels in human chronic atrial fibrillation. Br. J. Pharmacol. 154 (2008) 1619-1630
14. Courtemanche M., Ramirez R.J., and Nattel S. Ionic mechanisms underlying human atrial action potential properties: insights from a mathematical model. Am. J. Physiol. 275 (1998) H301-H321
15. Dawodu A.A., Monti F., Iwashiro K., Schiariti M., Chiavarelli R., and Puddu P.E. The shape of human atrial action potential accounts for different frequency-related changes in vitro. Int. J. Cardiol. 54 (1996) 237-249
16. Demir S.S., Clark J.W., and Giles W.R. Parasympathetic modulation of sinoatrial node pacemaker activity in rabbit heart: a unifying model. Am. J. Physiol. 276 (1999) H2221-H2244
17. D'Souza S.P., Davis M., and Baxter G.F. Autocrine and paracrine actions of natriuretic peptides in the heart. Pharmacol. Ther. 101 (2004) 113-129
18. + current (IK,ACh) in chronic human atrial fibrillation: decrease in GIRK4 mRNA correlates with reduced IK,ACh and muscarinic receptor-mediated shortening of action potentials. Circulation 104 (2001) 2551-2557
19. + channel current. Circ. Res. 73 (1993) 210-216
20. Feng J., Xu D., Wang Z., and Nattel S. Ultrarapid delayed rectifier current inactivation in human atrial myocytes: properties and consequences. Am. J. Physiol. 275 (1998) H1717-H1725
21. Feng J., Wang Z., Li G.R., and Nattel S. Effects of class III antiarrhythmic drugs on transient outward and ultra-rapid delayed rectifier currents in human atrial myocytes. J. Pharmacol. Exp. Ther. 281 (1997) 384-392
22. Fermini B., Wang Z., Duan D., and Nattel S. Differences in rate dependence of transient outward current in rabbit and human atrium. Am. J. Physiol. 263 (1992) H1747-H1754
23. + currents to repolarization assessed using mathematical models of human ventricular myocytes. Philos. Trans. A: Math. Phys. Eng. Sci. 364 (2006) 1207-1222
24. + current to repolarization of the human ventricular action potential. Prog. Biophys. 96 (2008) 357-376
25. Gaborit N., Le Bouter S., Szuts V., Varro A., Escande D., Nattel S., and Demolombe S. Regional and tissue specific transcript signatures of ion channel genes in the non-diseased human heart. J. Physiol. 582 (2007) 675-693
26. Gaudesius G., Miragoli M., Thomas S.P., and Rohr S. Coupling of cardiac electrical activity over extended distances by fibroblasts of cardiac origin. Circ. Res. 93 (2003) 421-428
27. Horio T., Tokudome T., Maki T., Yoshihara F., Suga S., Nishikimi T., Kojima M., Kawano Y., and Kangawa K. Gene expression, secretion, and autocrine action of C-type natriuretic peptide in cultured adult rat cardiac fibroblasts. Endocrinology 144 (2003) 2279-2284
28. Hund T.J., Kucera J.P., Otani N.F., and Rudy Y. Ionic charge conservation and long-term steady state in the Luo-Rudy dynamic cell model. Biophys. J. 81 (2001) 3324-3331
29. Imai Y., Jiang B., and Pappano A.J. Mechanism for muscarinic inhibition of I(Ca(L)) is determined by the path for elevating cyclic AMP in cardiac myocytes. Cardiovasc. Res. 51 (2001) 331-343
30. Jacquemet V. Steady-state solutions in mathematical models of atrial cell electrophysiology and their stability. Math. Biosci. 208 (2007) 241-269
31. Jacquemet V., and Henriquez C.S. Modelling cardiac fibroblasts: interactions with myocytes and their impact on impulse propagation. Europace 9 (2007) v129-v137
32. Jacquemet V., and Henriquez C.S. Loading effect of fibroblast-myocyte coupling on resting potential, impulse propagation and repolarization: insights from a microstructure model. Am. J. Physiol. Heart Circ. Physiol. 294 (2008) H2040-H2052
33. Joyner R.W. Effects of the discrete pattern of electrical coupling on propagation through an electrical syncytium. Circ. Res. 50 (1982) 192-200
34. Joyner R.W., and van Capelle F.J. Propagation through electrically coupled cells. How a small SA node drives a large atrium. Biophys. J. 50 (1986) 1157-1164
35. Joyner R.W., Wang Y.G., Wilders R., Golod D.A., Wagner M.B., Kumar R., and Goolsby W.N. A spontaneously active focus drives a model atrial sheet more easily than a model ventricular sheet. Am. J. Physiol. Heart Circ. Physiol. 279 (2000) H752-H763
36. Joyner R.W., Wilders R., and Wagner M.B. Propagation of pacemaker activity. Med. Biol. Eng. Comput. 45 (2007) 177-187
37. Kamkin A., Kiseleva I., Wagner K.D., Lammerich A., Bohm J., Persson P.B., and Gunther J. Mechanically induced potentials in fibroblasts from human right atrium. Exp. Physiol. 84 (1999) 347-356
38. Kawara T., Derksen R., de Groot J.R., Coronel R., Tasseron S., Linnenbank A.C., Hauer R.N., Kirkels H., Janse M.J., and de Bakker J.M. Activation delay after premature stimulation in chronically diseased human myocardium relates to the architecture of interstitial fibrosis. Circulation 104 (2001) 3069-3075
39. Kneller J., Zou R., Vigmond E., Wang Z., Leon L.J., and Nattel S. Cholinergic atrial fibrillation in a computer model of a two-dimensional sheet of canine atrial cells with realistic ionic properties. Circ. Res. 17 (2002) E73-E87
40. Kohl P., Camelliti P., Burton F.L., and Smith G.L. Electrical coupling of fibroblasts and myocytes: relevance for cardiac propagation. J. Electrocardiol. 38 (2005) 45-50
41. Kuhn M. Molecular physiology of natriuretic peptide signalling. Basic Res. Cardiol. 99 (2004) 76-82
42. Li D., Zhang L., Kneller J., and Nattel S. Potential ionic mechanism for repolarization differences between canine right and left atrium. Circ. Res. 88 (2001) 1168-1175
43. + current in adult mouse atria. Br. J. Pharmacol. 140 (2003) 576-584
44. MacCannell K.A., Bazzazi H., Chilton L., Shibukawa Y., Clark R.B., and Giles W.R. A mathematical model of electrotonic interactions between ventricular myocytes and fibroblasts. Biophys. J. 92 (2007) 4121-4132
45. Maleckar, M.M., Greenstein, J.L., Giles, W.R., Trayanova, N.A. Mechanisms of rate dependence in an updated model of the human atrial myocyte. Am. J. Physiol., submitted for publication-a.
46. Maleckar, M.M., Greenstein, J.L., Giles, W.R., Trayanova, N.A. Electrotonic coupling between human atrial myocytes and fibroblasts alters myocyte excitability and repolarization. Biophys. J., submitted for publication-b.
47. Miragoli M., Gaudesius G., and Rohr S. Electrotonic modulation of cardiac impulse conduction by myofibroblasts. Circ. Res. 98 (2006) 801-810
48. Nattel S., and Opie L.H. Controversies in atrial fibrillation. Lancet 367 (2006) 262-272
49. Ninomiya I. Direct evidence of nonuniform distribution of vagal effects on dog atria. Circ. Res. 19 (1966) 576-583
50. + currents in repolarization. Circ. Res. 82 (1998) 63-81
51. Nygren A., Leon L.J., and Giles W.R. Simulations of the human atrial action potential. Phil. Trans. R. Soc. Lond. A 359 (2001) 1111-1125
52. Oliver P.M., Fox J.E., Kim R., Rockman H.A., Kim H.S., Reddick R.L., Pandey K.N., Milgram S.L., Smithies O., and Maeda N. Hypertension, cardiac hypertrophy, and sudden death in mice lacking natriuretic peptide receptor A. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 14730-14735
53. Pappano A.J., and Mubagwa K. Muscarinic agonist-induced actions on potassium and calcium channels in atrial myocytes: differential desensitization. Eur. Heart J. 12 Suppl. F (1991) 70-75
54. Pijnappels D.A., van Tuyn J., Devries A.A.F., Grauss R.W., van der Laarse A., Ypey D.L., Atsma D.E., and Chalij M.J. Resynchronization of separated rat cardiomyocyte fields with genetically modified human ventricular scar fibroblasts. Circulation 116 (2007) 2018-2028
55. Ramirez R.J., Nattel S., and Courtemanche M. Mathematical analysis of canine atrial action potentials: rate, regional factors, and electrical remodeling. Am. J. Physiol. Heart Circ. Physiol. 279 (2000) H1767-H1785
56. + channel cloned from human heart. Mol. Pharmacol. 44 (1993) 642-648
57. Rook M.B., van Ginnekin A.C., de Jonge B., el Aoumari A., Gros D., and Jongsma H.J. Differences in gap junction channels between cardiac myocytes, fibroblasts, and heterologous pairs. Am. J. Physiol. 263 (1992) C959-C977
58. Rose R.A., Hatano N., Ohya S., Imaizumi Y., and Giles W.R. C-type natriuretic peptide activates a non-selective cation current in acutely isolated rat cardiac fibroblasts via natriuretic peptide C receptor-mediated signalling. J. Physiol. 580 (2007) 255-274
59. Rose R.A., and Giles W.R. Natriuretic peptide C receptor signaling in the heart and vasculature. J. Physiol. 586 (2008) 353-366
60. Sachse F.B., Moreno A.P., and Abildskov J.A. Electrophysiological modeling of fibroblasts and their interaction with myocytes. Ann. Biomed. Eng. 36 (2008) 41-56
61. Schuessler R.B., Grayson T.M., Bromberg B.I., Cox J.L., and Boineau J.P. Cholinergically mediated tachyarrhythmias induced by a single extrastimulus in the isolated canine right atrium. Circ. Res. 71 (1992) 1254-1267
62. Shibata E.F., Brown T.L.Y., Washburn Z.W., Bai J., Revak T.J., and Butters C.A. Autonomic regulation of voltage-gated cardiac ion channels. J. Cardiovasc. Electrophysiol. 17 (2006) S34-S42
63. Shibata E.F., Drury T., Refsum H., Aldrete V., and Giles W. Contributions of a transient outward current to repolarization in human atrium. Am. J. Physiol. 257 (1989) H1773-H1781
64. + currents activated by depolarization in cardiac fibroblasts. Biophys. J. 88 (2005) 3924-3935
65. Shiroshita-Takeshita A., Bianca J.J., Brundel M., and Nattel S. Atrial fibrillation: basic mechanisms, remodeling and triggers. J. Card. Electrophysiol. 13 (2005) 181-193
66. Spach M.S., and Boineau J.P. Microfibrosis produces electrical load variations due to loss of side-to-side cell connections: a major mechanism of structural heart disease arrhythmias. Pacing Clin. Electrophysiol. 20 (1997) 397-413
67. Spach M.S., Miller III W.T., Geselowitz D.B., Barr R.C., Kootsey J.M., and Johnson E.A. The discontinuous nature of propagation in normal canine cardiac muscle. Evidence for recurrent discontinuities of intracellular resistance that affect the membrane currents. Circ. Res. 48 (1981) 39-54
68. Van Wagoner D.R., and Nerbonne J.M. Molecular basis of electrical remodeling in atrial fibrillation. J. Mol. Cell Cardiol. 32 (2000) 1101-1117
69. Wang S., Bondarenko V.E., Qu Y.J., Bett G.C., Morales M.J., Rasmusson R.L., and Strauss H.C. Time- and voltage-dependent components of Kv4.3 inactivation. Biophys. J. 89 (2005) 3026-3041
70. Wang Y., Xu H., Kumar R., Tipparaju S.M., Wagner M.B., and Joyner R.W. Differences in transient outward current properties between neonatal and adult human atrial myocytes. J. Mol. Cell Cardiol. 35 (2003) 1083-1092
71. Zlochiver S., Muñoz V., Vikstrom K.L., Taffet S.M., Berenfeld O., and Jalife J. Electrotonic myofibroblast-to-myocyte coupling increases propensity to reentrant arrhythmias in two-dimensional cardiac monolayers. Biophys. J. 95 (2008) 446-4480