Roles of hyperpolarization-activated current If in sinoatrial node pacemaking: Insights from bifurcation analysis of mathematical models

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 298, Issue 6, 2010, Pages

  Kurata, Yasutaka ^a   Matsuda, Hiroyuki ^b   Hisatome, Ichiro ^c   Shibamoto, Toshishige ^a  

^a KANAZAWA MEDICAL UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c TOTTORI UNIVERSITY   (Japan)

Author keywords

Biological pacemaker; Computer simulation; Electrotonic modulation; Nonlinear dynamics

Indexed keywords

ACETYLCHOLINE; SODIUM CHANNEL;

ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; COMPUTER SIMULATION; CONTROLLED STUDY; HEART CONDUCTION; HEART STIMULATION; HYPERPOLARIZATION; MEMBRANE STEADY POTENTIAL; MOLECULAR STABILITY; NONHUMAN; OSCILLATION; POTASSIUM TRANSPORT; PRIORITY JOURNAL; RABBIT; SINUS NODE; SODIUM CURRENT; STEADY STATE;

ACETYLCHOLINE; ANIMALS; COMPUTER SIMULATION; CYCLIC NUCLEOTIDE-GATED CATION CHANNELS; DOSE-RESPONSE RELATIONSHIP, DRUG; HEART ATRIA; HEART CONDUCTION SYSTEM; MEMBRANE POTENTIALS; MODELS, ANIMAL; MODELS, BIOLOGICAL; MODELS, THEORETICAL; POTASSIUM CHANNELS; RABBITS; SINOATRIAL NODE; SODIUM CHANNELS;

EID: 77952599931     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00729.2009     Document Type: Article

References (60)

1. Altomare C, Bucchi A, Camatini E, Baruscotti M, Viscomi C, Moroni A, DiFrancesco D. Integrated allosteric model of voltage gating of HCN channels. J Gen Physiol 117: 519-532, 2001. (Pubitemid 32552261)
2. Altomare C, Terragni B, Brioschi C, Milanesi R, Pagliuca C, Viscomi C, Moroni A, Baruscotti M, DiFrancesco D. Heteromeric HCN1-HCN4 channels: a comparison with native pacemaker channels from the rabbit sinoatrial node. J Physiol 549: 347-359, 2003. (Pubitemid 36701749)
3. Azene EM, Xue T, Marbán E, Tomaselli GF, Li RA. Non-equilibrium behavior of HCN channels: insights into the role of HCN channels in native and engineered pacemakers. Cardiovasc Res 67: 263-273, 2005. (Pubitemid 40943619)
4. Chay TR, Lee YS. Phase resetting and bifurcation in the ventricular myocardium. Biophys J 47: 641-651, 1985.
5. Chay TR, Lee YS. Bursting, beating, and chaos by two functionally distinct inward current inactivations in excitable cells. Ann N Y Acad Sci 591: 328-350, 1990.
6. + activity and pacemaker potential in rabbit SA node cells. Am J Physiol Heart Circ Physiol 276: H205-H214, 1999.
7. Demir SS, Clark JW, 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.
8. Dhooge A, Govaerts W, Kuznetsov YuA, Mestrom W, Riet AM, Sautois B. MATCONT and CL-MATCONT: Continuation Toolboxes in MATLAB (Online). http://www.matcont.ugent.be/matcont.html [2006].
9. f) to generation of spontaneous activity in rabbit sino-atrial node myocytes. J Physiol 434: 23-40, 1991.
10. DiFrancesco D. Dual allosteric modulation of pacemaker (f) channels by cAMP and voltage in rabbit SA node. J Physiol 515: 367-376, 1999. (Pubitemid 29129208)
11. DiFrancesco D, 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.
12. Garny A, Kohl P, Hunter PJ, Boyett MR, Noble D. One-dimensional rabbit sinoatrial node models: benefits and limitations. J Cardiovasc Electrophysiol 14: S121-S132, 2003.
13. Gepstein L, Feld Y, Yankelson L. Somatic gene and cell therapy strategies for the treatment of cardiac arrhythmias. Am J Physiol Heart Circ Physiol 286: H815-H822, 2004.
14. Gibb WJ, Wagner MB, Lesh MD. Effects of simulated potassium blockade on the dynamics of triggered cardiac activity. J Theor Biol 168: 245-257, 1994.
15. Guevara MR, 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.
16. Herrmann S, Stieber J, Stöckl G, Hofmann F, Ludwig A. HCN4 provides a "depolarization reserve" and is not required for heart rate acceleration in mice. EMBO J 26: 4423-4432, 2007. (Pubitemid 350036626)
17. Jalife J, Antzelevitch C. Phase resetting and annihilation of pacemaker activity in cardiac tissue. Science 206: 695-697, 1979. (Pubitemid 10203219)
18. Joyner RW, van Capelle FJL. Propagation through electrically coupled cells: how a small SA node drives a large atrium. Biophys J 50: 1157-1164, 1986.
19. Joyner RW, Wang YG, Wilders R, Golod DA, Wagner MB, Kumar R, Goolsby WN. A spontaneously active focus drives a model atrial sheet more easily than a model ventricular sheet. Am J Physiol Heart Circ Physiol 279: H752-H763, 2000.
20. Krogh-Madsen T, Schaffer P, Skriver AD, Taylor LK, Pelzmann B, Koidl B, Guevara MR. An ionic model for rhythmic activity in small clusters of embryonic chick ventricular cells. Am J Physiol Heart Circ Physiol 289: H398-H413, 2005.
21. Kurata Y, Hisatome I, Imanishi S, Shibamoto T. Dynamical description of sinoatrial node pacemaking: improved mathematical model for primary pacemaker cell. Am J Physiol Heart Circ Physiol 283: H2074-H2101, 2002.
22. + currents in sinoatrial node pacemaking: insights from stability and bifurcation analyses of a mathematical model. Am J Physiol Heart Circ Physiol 285: H2804-H2819, 2003.
23. K1-downregulated human ventricular myocytes: insights from bifurcation analyses of a mathematical model. Biophys J 89: 2865-2887, 2005.
24. Kurata Y, Matsuda H, Hisatome I, Shibamoto T. Effects of pacemaker currents on creation and modulation of human ventricular pacemaker: theoretical study with application to biological pacemaker engineering. Am J Physiol Heart Circ Physiol 292: H701-H718, 2007.
25. + channel current. Biophys J 95: 951-977, 2008.
26. Kuznetsov YA. Elements of Applied Bifurcation Theory (3rd Ed). New York: Springer-Verlag, 2003.
27. Lakatta EG, DiFrancesco D. What keeps us ticking: a funny current, a calcium clock, or both? J Mol Cell Cardiol 47: 157-170, 2009.
28. 2+ cycling and surface membrane ion channel activation entrains normal automaticity in cells of the heart's pacemaker. Ann N Y Acad Sci 1080: 178-206, 2006.
29. Landau M, Lorente P, Michaels D, Jalife J. Bistabilities and annihilation phenomena in electrophysiological cardiac models. Circ Res 66: 1658-1672, 1990.
30. Li J, Qu J, 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.
31. Ludwig A, Budde T, Stieber J, Moosmang S, Wahl C, Holthoff K, Langebartels A, Wotjak C, Munsch T, Zong X, Feil S, Feil R, Lancel M, Chien KR, Konnerth A, Pape HC, Biel M, Hofmann F. Absence epilepsy and sinus dysrhythmia in mice lacking the pacemaker channel HCN2. EMBO J 22: 216-224, 2003. (Pubitemid 36119427)
32. Ludwig A, Herrmann S, Hoesl E, Stieber J. Mouse models for studying pacemaker channel function and sinus node arrhythmia. Prog Biophys Mol Biol 98: 179-185, 2008.
33. 2+ clocks and sarcolemmal voltage clocks confers robust and flexible pacemaker function in a novel pacemaker cell model. Am J Physiol Heart Circ Physiol 296: H594-H615, 2009.
34. Maltsev VA, Vinogradova TM, Lakatta EG. The emergence of a general theory of the initiation and strength of the heartbeat. J Pharm Sci 100: 338-369, 2006.
35. Mangoni ME, Nargeot J. Genesis and regulation of the heart automaticity. Physiol Rev 88: 919-982, 2008.
36. Marbán E, Cho HC. Creation of a biological pacemaker by gene- or cell-based approaches. Med Biol Eng Comput 45: 133-144, 2007. (Pubitemid 46291439)
37. Maruoka F, Nakashima Y, Takano M, Ono K, Noma A. Cation-dependent gating of the hyperpolarization-activated cation current in the rabbit sino-atrial node cells. J Physiol 477: 423-435, 1994. (Pubitemid 24211326)
38. +, UL-FS-49, and ZD-7288 within sinoatrial node. Am J Physiol Heart Circ Physiol 272: H2782-H2792, 1997.
39. Noble D. The surprising heart: a review of recent progress in cardiac electrophysiology. J Physiol 353: 1-50, 1984.
40. f in controlling and stabilizing pacemaker frequency of rabbit sino-atrial node cells. Proc Biol Sci 250: 199-207, 1992.
41. Noma A. Ionic mechanisms of the cardiac pacemaker potential. Jpn Heart J 37: 673-682, 1996. (Pubitemid 26358659)
42. Parker TS, Chua LO. Practical Numerical Algorithms For Chaotic Systems. New York: Springer-Verlag, 1989.
43. Qu J, Plotnikov AN, Danilo P Jr, Shlapakova I, Cohen IS, Robinson RB, Rosen MR. Expression and function of a biological pacemaker in canine heart. Circulation 107: 1106-1109, 2003. (Pubitemid 36297200)
44. Reiner VS, Antzelevitch C. Phase resetting and annihilation in a mathematical model of sinus node. Am J Physiol Heart Circ Physiol 249: H1143-H1153, 1985. (Pubitemid 16171199)
45. Rigg L, Terrar DA. Possible role of calcium release from the sarcoplasmic reticulum in pacemaking in guinea-pig sino-atrial node. Exp Physiol 81: 877-880, 1996. (Pubitemid 26332086)
46. f. Med Biol Eng Comput 45: 157-166, 2007.
47. Seydel R. Practical Bifurcation and Stability Analysis: From Equilibrium to Chaos (2nd Ed). New York: Springer-Verlag, 1994.
48. Tse HF, Xue T, Lau CP, Siu CW, Wang K, Zhang QY, Tomaselli GF, Akar FG, Li RA. Bioartificial sinus node constructed via in vivo gene transfer of an engineered pacemaker HCN channel reduces the dependence on electronic pacemaker in a sick-sinus syndrome model. Circulation 114: 1000-1011, 2006. (Pubitemid 44358876)
49. f in single cells from rabbit sino-atrial node. J Physiol 434: 57-83, 1991.
50. Varghese A, Winslow RL. Dynamics of abnormal pacemaking activity in cardiac Purkinje fibers. J Theor Biol 168: 407-420, 1994. (Pubitemid 24215459)
51. Verheijck EE, Wilders R, Bouman LN. Atrio-sinus interaction demonstrated by blockade of the rapid delayed rectifier current. Circulation 105: 880-885, 2002. (Pubitemid 34174931)
52. Vinet A, Roberge FA. A model study of stability and oscillations in the myocardial cell membrane. J Theor Biol 147: 377-412, 1990.
53. Viswanathan PC, Coles JA, Sharma V, Sigg DC. Recreating an artificial biological pacemaker: insights from a theoretical model. Heart Rhythm 3: 824-831, 2006. (Pubitemid 43960538)
54. Watanabe EI, Honjo H, Anno T, Boyett MR, Kodama I, Toyama J. Modulation of pacemaker activity of sinoatrial node cells by electrical load imposed by an atrial cell model. Am J Physiol Heart Circ Physiol 269: H1735-H1742, 1995.
55. Wilders R. Computer modeling of the sinoatrial node. Med Biol Eng Comput 45: 189-207, 2007.
56. f revealed by induction of ventricular automaticity by somatic gene transfer of gating- engineered pacemaker (HCN) channels. Circulation 115: 1839-1850, 2007.
57. Yamashita T, Nakajima T, Hazama H, Hamada E, Murakawa Y, Sawada K, Omata M. Regional differences in transient outward current density and inhomogeneities of repolarization in rabbit right atrium. Circulation 92: 3061-3069, 1995.
58. Yanagihara K, Noma A, Irisawa H. Reconstruction of sino-atrial node pacemaker potential based on the voltage clamp experiments. Jpn J Physiol 30: 841-857, 1980. (Pubitemid 11144691)
59. Zhang H, Holden AV, Kodama I, Honjo H, Lei M, Varghese T, 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.
60. Zhang H, Holden AV, Noble D, Boyett MR. Analysis of the chronotropic effect of acetylcholine on sinoatrial node cells. J Cardiovasc Electrophysiol 13: 465-474, 2002. (Pubitemid 34494267)