Hyperpolarization-activated current, If, in mathematical models of rabbit sinoatrial node pacemaker cells

BioMed Research International

Volumn 2013, Issue , 2013, Pages

  Verkerk, Arie O ^a   Wilders, Ronald ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ACTION POTENTIAL; COMPUTER SIMULATION; CONDUCTANCE; DEPOLARIZATION; HYPERPOLARIZATION; ION CURRENT; MATHEMATICAL MODEL; MEMBRANE POTENTIAL; NONHUMAN; PACEMAKER; RABBIT; REVIEW; SINUS NODE; STEADY STATE; ANIMAL; ARTIFICIAL HEART PACEMAKER; THEORETICAL MODEL;

ANIMALS; COMPUTER SIMULATION; MODELS, THEORETICAL; PACEMAKER, ARTIFICIAL; RABBITS; SINOATRIAL NODE;

EID: 84880914083     PISSN: 23146133     EISSN: 23146141     Source Type: Journal    
DOI: 10.1155/2013/872454     Document Type: Review

References (94)

1. Irisawa H., Brown H. F., Giles W., Cardiac pacemaking in the sinoatrial node. Physiological Reviews 1993 73 1 197 227 2-s2.0-0027509511 (Pubitemid 23065438)
2. Boyett M. R., Honjo H., Kodama I., The sinoatrial node, a heterogeneous pacemaker structure. Cardiovascular Research 2000 47 4 658 687 2-s2.0-0033847605 10.1016/S0008-6363(00)00135-8
3. Satoh H., Sino-atrial nodal cells of mammalian hearts: ionic currents and gene expression of pacemaker ionic channels. Journal of Smooth Muscle Research 2003 39 5 175 193 2-s2.0-0347624077 10.1540/jsmr.39.175 (Pubitemid 38017644)
4. Couette B., Marger L., Nargeot J., Mangoni M. E., Physiological and pharmacological insights into the role of ionic channels in cardiac pacemaker activity. Cardiovascular & Hematological Disorders 2006 6 3 169 190 2-s2.0-33748609372 10.2174/187152906778249572 (Pubitemid 44377771)
5. Dobrzynski H., Boyett M. R., Anderson R. H., New insights into pacemaker activity: promoting understanding of sick sinus syndrome. Circulation 2007 115 14 1921 1932 2-s2.0-34247104908 10.1161/CIRCULATIONAHA.106.616011 (Pubitemid 46598906)
6. Maltsev V. A., Lakatta E. G., Normal heart rhythm is initiated and regulated by an intracellular calcium clock within pacemaker cells. Heart Lung & Circulation 2007 16 5 335 348 2-s2.0-34848845270 10.1016/j.hlc.2007.07.005 (Pubitemid 47504909)
7. Mangoni M. E., Nargeot J., Genesis and regulation of the heart automaticity. Physiological Reviews 2008 88 3 919 982 2-s2.0-50349096521 10.1152/physrev.00018.2007
8. Verkerk A. O., van Ginneken A. C. G., Wilders R., Pacemaker activity of the human sinoatrial node: role of the hyperpolarization-activated current, If. International Journal of Cardiology 2009 132 3 318 336 2-s2.0-60649086907 10.1016/j.ijcard.2008.12.196
9. 2+ clocks and surface membrane voltage clocks controls the timekeeping mechanism of the heart's pacemaker. Circulation Research 2010 106 4 659 673 2-s2.0-77949379471 10.1161/CIRCRESAHA.109.206078
10. Brown H., DiFrancesco D., Voltage-clamp investigations of membrane currents underlying pace-maker activity in rabbit sino-atrial node. Journal of Physiology 1980 308 331 351 2-s2.0-0019229267 (Pubitemid 11252754)
11. DiFrancesco D., Tortora P., Direct activation of cardiac pacemaker channels by intracellular cyclic AMP. Nature 1991 351 6322 145 147 2-s2.0-0025782740 10.1038/351145a0 (Pubitemid 21896552)
12. Brown H. F., DiFrancesco D., Noble S. J., How does adrenaline accelerate the heart? Nature 1979 280 5719 235 236 2-s2.0-0018387132 (Pubitemid 9227914)
13. Noma A., Irisawa H., Kokobun S., Slow current systems in the A-V node of the rabbit heart. Nature 1980 285 5762 228 229 2-s2.0-0019152633 (Pubitemid 10051019)
14. DiFrancesco D., A study of the ionic nature of the pace-maker current in calf Purkinje fibres. Journal of Physiology 1981 314 377 393 2-s2.0-0019393640
15. Roubille F., Tardif J. C., New therapeutic targets in cardiology: heart failure and arrhythmia: HCN channels. Circulation 2013 127 19 1986 1996
16. Chandler N. J., Greener I. D., Tellez J. O., Inada S., Musa H., Molenaar P., DiFrancesco D., Baruscotti M., Longhi R., Anderson R. H., Billeter R., Sharma V., Sigg D. C., Boyett M. R., Dobrzynski H., Molecular architecture of the human sinus node insights into the function of the cardiac pacemaker. Circulation 2009 119 12 1562 1575 2-s2.0-64749110218 10.1161/CIRCULATIONAHA.108. 804369
17. Schulze-Bahr E., Neu A., Friederich P., Kaupp U. B., Breithardt G., Pongs O., Isbrandt D., Pacemaker channel dysfunction in a patient with sinus node disease. Journal of Clinical Investigation 2003 111 10 1537 1545 2-s2.0-0037637420 10.1172/JCI200316387 (Pubitemid 38063286)
18. Ueda K., Nakamura K., Hayashi T., Inagaki N., Takahashi M., Arimura T., Morita H., Higashiuesato Y., Hirano Y., Yasunami M., Takishita S., Yamashina A., Ohe T., Sunamori M., Hiraoka M., Kimura A., Functional characterization of a trafficking-defective HCN4 mutation, D553N, associated with cardiac arrhythmia. Journal of Biological Chemistry 2004 279 26 27194 27198 2-s2.0-3042549234 10.1074/jbc.M311953200 (Pubitemid 38812556)
19. Milanesi R., Baruscotti M., Gnecchi-Ruscone T., DiFrancesco D., Familial sinus bradycardia associated with a mutation in the cardiac pacemaker channel. The New England Journal of Medicine 2006 354 2 151 157 2-s2.0-30444452695 10.1056/NEJMoa052475 (Pubitemid 43076712)
20. Nof E., Luria D., Brass D., Marek D., Lahat H., Reznik-Wolf H., Pras E., Dascal N., Eldar M., Glikson M., Point mutation in the HCN4 cardiac ion channel pore affecting synthesis, trafficking, and functional expression is associated with familial asymptomatic sinus bradycardia. Circulation 2007 116 5 463 470 2-s2.0-34548453724 10.1161/CIRCULATIONAHA.107.706887 (Pubitemid 47450254)
21. Laish-Farkash A., Glikson M., Brass D., Marek-Yagel D., Pras E., Dascal N., Antzelevitch C., Nof E., Reznik H., Eldar M., Luria D., A novel mutation in the HCN4 gene causes symptomatic sinus bradycardia in Moroccan Jews. Journal of Cardiovascular Electrophysiology 2010 21 12 1365 1372 2-s2.0-78650153150 10.1111/j.1540-8167.2010.01844.x
22. Schweizer P. A., Duhme N., Thomas D., Becker R., Zehelein J., Draguhn A., Bruehl C., Katus H. A., Koenen M., cAMP sensitivity of HCN pacemaker channels determines basal heart rate but is not critical for autonomic rate control. Circulation: Arrhythmia and Electrophysiology 2010 3 5 542 552 2-s2.0-78049499917 10.1161/CIRCEP.110.949768
23. Duhme N., Schweizer P. A., Thomas D., Becker R., Schroter J., Barends T. R., Schlichting I., Draguhn A., Bruehl C., Katus H. A., Koenen M., Altered HCN4 channel C-linker interaction is associated with familial tachycardia-bradycardia syndrome and atrial fibrillation. European Heart Journal 2013 10.1093/eurheartj/ehs391
24. Robinson R. B., Brink P. R., Cohen I. S., Rosen M. R., I f and the biological pacemaker. Pharmacological Research 2006 53 5 407 415 2-s2.0-33646580107 10.1016/j.phrs.2006.03.007 (Pubitemid 43729049)
25. Siu C.-W., Lieu D. K., Li R. A., HCN-encoded pacemaker channels: from physiology and biophysics to bioengineering. Journal of Membrane Biology 2006 214 3 115 122 2-s2.0-34447306926 10.1007/s00232-006-0881-9 (Pubitemid 47063504)
26. Rosen M. R., Brink P. R., Cohen I. S., Robinson R. B., Biological pacemakers based on If. Medical & Biological Engineering & Computing 2007 45 2 157 166 2-s2.0-33847162057 10.1007/s11517-006-0060-2 (Pubitemid 46291441)
27. Cho H. C., Marbán E., Biological therapies for cardiac arrhythmias: can genes and cells replace drugs and devices? Circulation Research 2010 106 4 674 685 2-s2.0-77949378885 10.1161/CIRCRESAHA.109.212936
28. Rosen M. R., Robinson R. B., Brink P. R., Cohen I. S., The road to biological pacing. Nature Reviews Cardiology 2011 8 11 656 666 2-s2.0-80055025823 10.1038/nrcardio.2011.120
29. Li R., Gene- and cell-based bio-artificial pacemaker: what basic and translational lessons have we learned? Gene Therapy 2012 19 6 588 595
30. 2+ transient, cAMP production and pacemaker frequency of rabbit sinoatrial node cells. Basic Research in Cardiology 2010 105 1 73 87 2-s2.0-72449157040 10.1007/s00395-009-0048-9
31. 2+ cycling. Journal of Molecular and Cellular Cardiology 2013 10.1016/j.yjmcc.2013.04.026
32. Lippiat J. D., Whole-cell recording using the perforated patch clamp technique. Methods in Molecular Biology 2008 491 141 149 2-s2.0-60349087783 10.1007/978-1-59745-526-8-11
33. Yu H., Wu J., Potapova I., Wymore R. T., Holmes B., Zuckerman J., Pan Z., Wang H., Shi W., Robinson R. B., El-Maghrabi M. R., Benjamin W., Dixon J., McKinnon D., Cohen I. S., Wymore R., MinK-related peptide 1: a β subunit for the HCN ion channel subunit family enhances expression and speeds activation. Circulation Research 2001 88 12 E84 E87 2-s2.0-0010244063
34. Decher N., Bundis F., Vajna R., Steinmeyer K., KCNE2 modulates current amplitudes and activation kinetics of HCN4: influence of KCNE family members on HCN4 currents. Pflügers Archiv European Journal of Physiology 2003 446 6 633 640 2-s2.0-0141817695 10.1007/s00424-003-1127-7 (Pubitemid 37214998)
35. Qu J., Kryukova Y., Potapova I. A., Doronin S. V., Larsen M., Krishnamurthy G., Cohen I. S., Robinson R. B., MiRP1 modulates HCN2 channel expression and gating in cardiac myocytes. Journal of Biological Chemistry 2004 279 42 43497 43502 2-s2.0-6344241129 10.1074/jbc.M405018200 (Pubitemid 39390649)
36. + in rabbit isolated sinoatrial node cells. Pflügers Archiv European Journal of Physiology 1994 426 1-2 68 74 2-s2.0-0028176852
37. Frace A. M., Maruoka F., Noma A., Control of the hyperpolarization- activated cation current by external anions in rabbit sino-atrial node cells. Journal of Physiology 1992 453 307 318 2-s2.0-0026718207
38. DiFrancesco D., Ferroni A., Mazzanti M., Tromba C., Properties of the hyperpolarizing-activated current (if) in cells isolated from the rabbit sino-atrial node. Journal of Physiology 1986 377 61 88 2-s2.0-0022558583 (Pubitemid 16072722)
39. van Ginneken A. C. G., Giles W., Voltage clamp measurements of the hyperpolarization-activated inward current If in single cells from rabbit sino-atrial node. Journal of Physiology 1991 434 57 83 2-s2.0-0026088929
40. Verkerk A. O., den Ruijter H. M., Bourier J., Boukens B. J., Brouwer I. A., Wilders R., Coronel R., Dietary fish oil reduces pacemaker current and heart rate in rabbit. Heart Rhythm 2009 6 10 1485 1492 2-s2.0-77649275369 10.1016/j.hrthm.2009.07.024
41. + conductance of the hyperpolarization-activated current in rabbit cardiac pacemaker cells. Pflügers Archiv European Journal of Physiology 1992 421 2-3 97 99 2-s2.0-0026873382
42. Yu X., Chen X.-W., Zhou P., Yao L., Liu T., Zhang B., Li Y., Zheng H., Zheng L.-H., Zhang C. X., Bruce I., Ge J.-B., Wang S.-Q., Hu Z.-A., Yu H.-G., Zhou Z., Calcium influx through If channels in rat ventricular myocytes. American Journal of Physiology Cell Physiology 2007 292 3 C1147 C1155 2-s2.0-33947327221 10.1152/ajpcell.00598.2005 (Pubitemid 46440399)
43. Michels G., Brandt M. C., Zagidullin N., Khan I. F., Larbig R., Van Aaken S., Wippermann J., Hoppe U. C., Direct evidence for calcium conductance of hyperpolarization-activated cyclic nucleotide-gated channels and human native If at physiological calcium concentrations. Cardiovascular Research 2008 78 3 466 475 2-s2.0-44449137886 10.1093/cvr/cvn032 (Pubitemid 351769763)
44. Biel M., Wahl-Schott C., Michalakis S., Zong X., Hyperpolarization- activated cation channels: from genes to function. Physiological Reviews 2009 89 3 847 885 2-s2.0-67651030760 10.1152/physrev.00029.2008
45. Männikkö R., Pandey S., Larsson H. P., Elinder F., Hysteresis in the voltage dependence of HCN channels: conversion between two modes affects pacemaker properties. Journal of General Physiology 2005 125 3 305 326 2-s2.0-15244353283 10.1085/jgp.200409130 (Pubitemid 40388311)
46. Azene E. M., Xue T., Marbán E., Tomaselli G. F., Li R. A., Non-equilibrium behavior of HCN channels: insights into the role of HCN channels in native and engineered pacemakers. Cardiovascular Research 2005 67 2 263 273 2-s2.0-21744440389 10.1016/j.cardiores.2005.03.006 (Pubitemid 40943619)
47. Elinder F., Männikkö R., Pandey S., Larsson H. P., Mode shifts in the voltage gating of the mouse and human HCN2 and HCN4 channels. Journal of Physiology 2006 575 2 417 431 2-s2.0-33747760017 10.1113/jphysiol.2006.110437 (Pubitemid 44274737)
48. Bruening-Wright A., Larsson H. P., Slow conformational changes of the voltage sensor during the mode shift in hyperpolarization-activated cyclic-nucleotide-gated channels. Journal of Neuroscience 2007 27 2 270 278 2-s2.0-33846206751 10.1523/JNEUROSCI.3801-06.2007 (Pubitemid 46105999)
49. Xiao Y. F., Chandler N., Dobrzynski H., Richardson E. S., Tenbroek E. M., Wilhelm J. J., Sharma V., Varghese A., Boyett M. R., Iaizzo P. A., Sigg D. C., Hysteresis in human HCN4 channels: a crucial feature potentially affecting sinoatrial node pacemaking. Acta Physiologica Sinica 2010 62 1 1 13
50. Noma A., Morad M., Irisawa H., Does the "pacemaker current" generate the diastolic depolarization in the rabbit SA node cells? Pflügers Archiv European Journal of Physiology 1983 397 3 190 194 2-s2.0-0020519287 (Pubitemid 13093229)
51. DiFrancesco D., The contribution of the "pacemaker" current (if) to generation of spontaneous activity in rabbit sino-atrial node myocytes. Journal of Physiology 1991 434 23 40 2-s2.0-0025977991
52. Vassalle M., The pacemaker current (If) does not play an important role in regulating SA node pacemaker activity. Cardiovascular Research 1995 30 2 310 2-s2.0-13644264904
53. 2+ release sparks atrial pacemaker activity. News in Physiological Sciences 2001 16 3 101 106 2-s2.0-0035379208 (Pubitemid 33570295)
54. DiFrancesco D., Serious workings of the funny current. Progress in Biophysics and Molecular Biology 2006 90 1-3 13 25 2-s2.0-28344440488 10.1016/j.pbiomolbio.2005.05.001 (Pubitemid 41721041)
55. 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. The EMBO Journal 2007 26 21 4423 4432 2-s2.0-35648939866 10.1038/sj.emboj.7601868 (Pubitemid 350036626)
56. Harzheim D., Pfeiffer K. H., Fabritz L., Kremmer E., Buch T., Waisman A., Kirchhof P., Kaupp U. B., Seifert R., Cardiac pacemaker function of HCN4 channels in mice is confined to embryonic development and requires cyclic AMP. The EMBO Journal 2008 27 4 692 703 2-s2.0-39449098523 10.1038/emboj.2008.3 (Pubitemid 351273125)
57. Lakatta E. G., DiFrancesco D., What keeps us ticking: a funny current, a calcium clock, or both? Journal of Molecular and Cellular Cardiology 2009 47 2 157 170 2-s2.0-67649104033 10.1016/j.yjmcc.2009.03.022
58. Verkerk A. O., Wilders R., Relative importance of funny current in human versus rabbit sinoatrial node. Journal of Molecular and Cellular Cardiology 2010 48 4 799 801 2-s2.0-77649273814 10.1016/j.yjmcc.2009.09.020
59. DiFrancesco D., Considerations on the size of currents required for pacemaking. Journal of Molecular and Cellular Cardiology 2010 48 4 802 803 2-s2.0-77649275507 10.1016/j.yjmcc.2009.11.022
60. Maltsev V. A., Lakatta E. G., Funny current provides a relatively modest contribution to spontaneous beating rate regulation of human and rabbit sinoatrial node cells. Journal of Molecular and Cellular Cardiology 2010 48 4 804 806 2-s2.0-77649274318 10.1016/j.yjmcc.2009.12.009
61. DiFrancesco D., Noble D., The funny current has a major pacemaking role in the sinus node. Heart Rhythm 2012 9 2 299 301 2-s2.0-84856167091 10.1016/j.hrthm.2011.09.021
62. Maltsev V. A., Lakatta E. G., The funny current in the context of the coupled-clock pacemaker cell system. Heart Rhythm 2012 9 2 302 307 2-s2.0-84856147119 10.1016/j.hrthm.2011.09.022
63. DiFrancesco D., Noble D., Rebuttal: "The funny current in the context of the coupled clock pacemaker cell system" Heart Rhythm 2012 9 3 457 458 2-s2.0-84857595363 10.1016/j.hrthm.2011.09.023
64. Lakatta E. G., Maltsev V. A., Rebuttal: what If the shoe doesn't fit? "the funny current has a major pacemaking role in the sinus node" Heart Rhythm 2012 9 3 459 460 2-s2.0-84857520262 10.1016/j.hrthm.2011.09.024
65. Wilders R., Computer modelling of the sinoatrial node. Medical & Biological Engineering & Computing 2007 45 2 189 207 2-s2.0-33847170518 10.1007/s11517-006-0127-0 (Pubitemid 46291444)
66. 2+ clocks and sarcolemmal voltage clocks confers robust and flexible pacemaker function in a novel pacemaker cell model. American Journal of Physiology Heart and Circulatory Physiology 2009 296 3 H594 H615 2-s2.0-64049083007 10.1152/ajpheart.01118.2008
67. Severi S., Fantini M., Charawi L. A., DiFrancesco D., An updated computational model of rabbit sinoatrial action potential to investigate the mechanisms of heart rate modulation. Journal of Physiology 2012 590, Part 18 4483 4499
68. Verkerk A. O., Wilders R., Coronel R., Ravesloot J. H., Verheijck E. E., Ionic remodeling of sinoatrial node cells by heart failure. Circulation 2003 108 6 760 766 2-s2.0-0042162977 10.1161/01.CIR.0000083719.51661.B9 (Pubitemid 36999264)
69. Yanagihara K., Irisawa H., Inward current activated during hyperpolarization in the rabbit sinoatrial node cell. Pflügers Archiv European Journal of Physiology 1980 385 1 11 19 2-s2.0-0018837655 (Pubitemid 10102676)
70. DiFrancesco D., Noble D., Jacklet J. W., Current If and its contribution to cardiac pacemaking. Neuronal and Cellular Oscillators 1989 New York, NY, USA Marcel Dekker 31 57
71. 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. Journal of Physiology 1994 477 3 423 435 2-s2.0-0028358212 (Pubitemid 24211326)
72. DiFrancesco D., Characterization of the pace-maker current kinetics in calf Purkinje fibres. Journal of Physiology 1984 348 341 367 2-s2.0-0021287356
73. Hodgkin A. L., Huxley A. F., A quantitative description of membrane current and its application to conduction and excitation in nerve. The Journal of Physiology 1952 117 4 500 544 2-s2.0-35649001607
74. Dokos S., Celler B., Lovell N., Ion currents underlying sinoatrial node pacemaker activity: a new single cell mathematical model. Journal of Theoretical Biology 1996 181 3 245 272 2-s2.0-0030573669 10.1006/jtbi.1996.0129 (Pubitemid 26315750)
75. Zhang H., Holden A. V., Kodama I., Honjo H., Lei M., Varghese T., Boyett M. R., Mathematical models of action potentials in the periphery and center of the rabbit sinoatrial node. American Journal of Physiology Heart and Circulatory Physiology 2000 279 1 H397 H421 2-s2.0-0033858925 (Pubitemid 30616684)
76. Demir S. S., Clark J. W., Murphey C. R., Giles W. R., A mathematical model of a rabbit sinoatrial node cell. American Journal of Physiology 1994 266 3 C832 C852 2-s2.0-0028204386
77. Kurata Y., Hisatome I., Imanishi S., Shibamoto T., Dynamical description of sinoatrial node pacemaking: improved mathematical model for primary pacemaker cell. American Journal of Physiology Heart and Circulatory Physiology 2002 283 5 H2074 H2101 2-s2.0-0036838501 (Pubitemid 35217043)
78. Sarai N., Matsuoka S., Kuratomi S., Ono K., Noma A., Role of individual ionic current systems in the SA node hypothesized by a model study. Japanese Journal of Physiology 2003 53 2 125 134 2-s2.0-0042196441 10.2170/jjphysiol.53. 125 (Pubitemid 36950538)
79. Matsuoka S., Sarai N., Kuratomi S., Ono K., Noma A., Role of individual ionic current systems in ventricular cells hypothesized by a model study. Japanese Journal of Physiology 2003 53 2 105 123 2-s2.0-0041742200 10.2170/jjphysiol.53.105 (Pubitemid 36950537)
80. Wilders R., Jongsma H. J., van Ginneken A. C. G., Pacemaker activity of the rabbit sinoatrial node. A comparison of mathematical models. Biophysical Journal 1991 60 5 1202 1216 2-s2.0-0025830164
81. Liu Z.-W., Zou A.-R., Demir S. S., Clark J. W., Nathan R. D., Characterization of a hyperpolarization-activated inward current in cultured pacemaker cells from the sinoatrial node. Journal of Molecular and Cellular Cardiology 1996 28 12 2523 2535 2-s2.0-0030469469 10.1006/jmcc.1996.0244 (Pubitemid 27023039)
82. Honjo H., Boyett M. R., Kodama I., Toyama J., Correlation between electrical activity and the size of rabbit sino-atrial node cells. Journal of Physiology 1996 496 3 795 808 2-s2.0-0029962743 (Pubitemid 26387862)
83. Noble D., DiFrancesco D., Denyer J. C., Jacklet J. W., Ionic mechanisms in normal and abnormal cardiac pacemaker activity. Neuronal and Cellular Oscillators 1989 New York, NY, USA Marcel Dekker 59 85
84. 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. Journal of Physiology 2003 549 2 347 359 2-s2.0-0037834607 (Pubitemid 36701749)
85. Barbuti A., Baruscotti M., DiFrancesco D., The pacemaker current: from basics to the clinics. Journal of Cardiovascular Electrophysiology 2007 18 3 342 347 2-s2.0-33846950337 10.1111/j.1540-8167.2006.00736.x
86. DiFrancesco D., Noble D., Boumann L. N., Jongsma H. J., Implications of the reinterpretation of iK2 for the modelling of the electrical activity of the pacemaker tissues in the heart. Cardiac Rate and Rhythm: Physiological, Morphological and Developmental Aspects 1982 The Hague, The Netherlands Martinus Nijhoff 93 128
87. 2+ and hyperpolarization-activated currents to autonomie agonists in the rabbit sino-atrial node. Journal of Physiology 1996 491 2 347 355 2-s2.0-0029944490
88. Dokos S., Celler B. G., Lovell N. H., Vagal control of sinoatrial rhythm: a mathematical model. Journal of Theoretical Biology 1996 182 1 21 44 2-s2.0-0030573811 10.1006/jtbi.1996.0141 (Pubitemid 26358721)
89. Demir S. S., Clark J. W., Giles W. R., Parasympathetic modulation of sinoatrial node pacemaker activity in rabbit heart: a unifying model. American Journal of Physiology 1999 276 6 H2221 H2244 2-s2.0-0033001517 (Pubitemid 29323511)
90. Zhang H., Holden A. V., Noble D., Boyett M. R., Analysis of the chronotropic effect of acetylcholine on sinoatrial node cells. Journal of Cardiovascular Electrophysiology 2002 13 5 465 474 2-s2.0-0036257813 (Pubitemid 34494267)
91. Maltsev V. A., Lakatta E. G., A novel quantitative explanation for the autonomic modulation of cardiac pacemaker cell automaticity via a dynamic system of sarcolemmal and intracellular proteins. American Journal of Physiology Heart and Circulatory Physiology 2010 298 6 H2010 H2023 2-s2.0-77952609567 10.1152/ajpheart.00783.2009
92. Zhang H., Butters T., Adeniran I., Higham J., Holden A. V., Boyett M. R., Hancox J. C., Modeling the chronotropic effect of isoprenaline on rabbit sinoatrial node. Frontiers in Physiology 2012 3 241
93. DiFrancesco D., Dual allosteric modulation of pacemaker (f) channels by cAMP and voltage in rabbit SA node. Journal of Physiology 1999 515 2 367 376 2-s2.0-0033104823
94. Zaza A., Micheletti M., Brioschi A., Rocchetti M., Ionic currents during sustained pacemaker activity in rabbit sino-atrial myocytes. Journal of Physiology 1997 505 3 677 688 2-s2.0-0031574245 10.1111/j.1469-7793.1997.677ba.x (Pubitemid 28022368)