The Korean Journal of Physiology and Pharmacology

The Korean Society of Pharmacology (대한약리학회)
권호 표지

Role of Stretch-Activated Channels in Stretch-Induced Changes of Electrical Activity in Rat Atrial Myocytes

  • Youm, Jae-Boum (Department of Physiology, Cheju National University College of Medicine) ;
  • Jo, Su-Hyun (Department of Physiology, Cheju National University College of Medicine) ;
  • Leem, Chae-Hun (Department of Physiology and the Institute for Calcium Research, University of Ulsan College of Medicine) ;
  • Ho, Won-Kyung (Department of Physiology and Biophysics, Seoul National University College of Medicine) ;
  • Earm, Yung E. (Department of Physiology and Biophysics, Seoul National University College of Medicine)
  • Published : 2004.02.21
Download PDF
⟨ Previous Next ⟩

Abstract

We developed a cardiac cell model to explain the phenomenon of mechano-electric feedback (MEF), based on the experimental data with rat atrial myocytes. It incorporated the activity of ion channels, pumps, exchangers, and changes of intracellular ion concentration. Changes in membrane excitability and $Ca^{2+}$ transients could then be calculated. In the model, the major ion channels responsible for the stretch-induced changes in electrical activity were the stretch-activated channels (SACs). The relationship between the extent of stretch and activation of SACs was formulated based on the experimental findings. Then, the effects of mechanical stretch on the electrical activity were reproduced. The shape of the action potential (AP) was significantly changed by stretch in the model simulation. The duration was decreased at initial fast phase of repolarization (AP duration at 20% repolarization level from 3.7 to 2.5 ms) and increased at late slow phase of repolarization (AP duration at 90% repolarization level from 62 to 178 ms). The resting potential was depolarized from -75 to -61 mV. This mathematical model of SACs may quantitatively predict changes in cardiomyocytes by mechanical stretch.

Keywords

References

  1. Allen DG, Kurihara S. The effects of muscle length on intracellular calcium transients in mammalian cardiac muscle. J Physiol 327: 79－94, 1982 https://doi.org/10.1113/jphysiol.1982.sp014221
  2. Belus A, White E. Streptomycin and intracellular calcium modulate the response of single guinea-pig ventricular myocytes to axial stretch. J Physiol 546: 501－509, 2003 https://doi.org/10.1113/jphysiol.2002.027573
  3. Boland J, Troquet J. Intracellular action potential changes induced in both ventricles of the rat by an acute right ventricular pressure overload. Cardiovasc Res 14: 735－740, 1980 https://doi.org/10.1093/cvr/14.12.735
  4. Boyle WA, Nerbonne JM. Two functionally distinct 4-aminopyridine- sensitive outward K+ currents in rat atrial myocytes. J Gen Physiol 100: 1041－1067, 1992 https://doi.org/10.1085/jgp.100.6.1041
  5. Brady AJ. Mechanical properties of isolated cardiac myocytes. Physiol Rev 71: 413－428, 1991 https://doi.org/10.1152/physrev.1991.71.2.413
  6. Bustamante JO, Ruknudin A, Sachs F. Stretch-activated channels in heart cells: relevance to cardiac hypertrophy. J Cardiovasc Pharmacol 17: S110－S113, 1991 https://doi.org/10.1097/00005344-199117002-00024
  7. Calaghan SC, Belus A, White E. Do stretch-induced changes in intracellular calcium modify the electrical activity of cardiac muscle? Prog Biophys Mol Biol 82: 81－95, 2003 https://doi.org/10.1016/S0079-6107(03)00007-5
  8. Cazorla O, Pascarel C, Brette F, Le Guennec JY. Modulation of ions channels and membrane receptors activities by mechanical interventions in cardiomyocytes: possible mechanisms for mechanosensitivity. Prog Biophys Mol Biol 71: 29－58, 1999 https://doi.org/10.1016/S0079-6107(98)00036-4
  9. Craelius W. Stretch-activation of rat cardiac myocytes. Exp Physiol 78: 411－423, 1993 https://doi.org/10.1113/expphysiol.1993.sp003695
  10. Dean JW, Lab MJ. Arrhythmia in heart failure: role of mechanically induced changes in electrophysiology. Lancet 1: 1309－ 1312, 1989
  11. Franz MR, Burkhoff D, Yue DT, Sagawa K. Mechanically induced action potential changes and arrhythmia in isolated and in situ canine hearts. Cardiovasc Res 23: 213－223, 1989 https://doi.org/10.1093/cvr/23.3.213
  12. Franz MR, Cima R, Wang D, Profitt D, Kurz R. Electrophysiological effects of myocardial stretch and mechanical determinants of stretch-activated arrhythmias. Circulation 86: 968－978, 1992 Erratum in: Circulation 86: 1663, 1992
  13. Gannier F, White E, Garnier, Le Guennec JY. A possible mechanism for large stretch-induced increase in $[Ca^{2+}]_i$ in isolated guinea-pig ventricular myocytes. Cardiovasc Res 32: 158－167, 1996
  14. Gannier F, White E, Lacampagne A, Garnier D, Le Guennec JY. Streptomycin reverses a large stretch induced increases in $[Ca^{2+}]_i$ in isolated guinea pig ventricular myocytes. Cardiovasc Res 28: 1193－1198, 1994 https://doi.org/10.1093/cvr/28.8.1193
  15. Hagiwara N, Irisawa H, Kasanuki H, Hosoda S. Background current in sino-atrial node cells of the rabbit heart. J Physiol 448: 53－72, 1992 https://doi.org/10.1113/jphysiol.1992.sp019029
  16. Hansen DE. Mechanoelectrical feedback effects of altering preload, afterload, and ventricular shortening. Am J Physiol 264: H423－ H432, 1993
  17. Hansen DE, Craig CS, Hondeghem LM. Stretch-induced arrhythmias in the isolated canine ventricle. Evidence for the importance of mechanoelectrical feedback. Circulation 81: 1094－1105, 1990 https://doi.org/10.1161/01.CIR.81.3.1094
  18. Hongo K, White E, Le Guennec JY, Orchard CH. Changes in $[Ca^{2+}]_i$, $[Na^+]_i$ and $Ca^{2+}$ current in isolated rat ventricular myocytes following an increase in cell length. J Physiol 491: 609－619, 1996 https://doi.org/10.1113/jphysiol.1996.sp021243
  19. Hoyer J, Distler A, Haase W, Gogelein H. Ca2$^+$ influx through stretch-activated cation channels activates maxi K$^+$ channels in porcine endocardial endothelium. Proc Natl Acad Sci USA 91: 2367－2371, 1994. https://doi.org/10.1073/pnas.91.6.2367
  20. Isenberg G, Borschke B, Rueckschloss U. Ca2$^+$ transients of cardiomyocytes from senescent mice peak late and decay slowly. Cell Calcium 34: 271－280, 2003 https://doi.org/10.1016/S0143-4160(03)00121-0
  21. Kamkin A, Kiseleva I, Isenberg G. Stretch-activated currents in ventricular myocytes: amplitude and arrhythmogenic effects increase with hypertrophy. Cardiovasc Res 48: 409-420, 2000 https://doi.org/10.1016/S0008-6363(00)00208-X
  22. Kamkin A, Kiseleva I, Isenberg G. Ion selectivity of stretchactivated cation currents in mouse ventricular myocytes. Pflugers Arch 446: 220－231, 2003 https://doi.org/10.1007/s00424-003-1018-y
  23. Kohl P, Ravens U. Cardiac mechano-electric feedback: past, present, and prospect. Prog Biophys Mol Biol 82: 3－9, 2003 https://doi.org/10.1016/S0079-6107(03)00022-1
  24. Lab MJ. Mechanically dependent changes in action potentials recorded from the intact frog ventricle. Circ Res 42: 519-528, 1978 https://doi.org/10.1161/01.RES.42.4.519
  25. Lab MJ. Mechanoelectric feedback (transduction) in heart: concepts and implications. Cardiovasc Res 32: 3－14, 1996 https://doi.org/10.1016/S0008-6363(96)00088-0
  26. Li GR, Feng JL, Wang ZG, Nattel S. Transmembrane chloride currents in human atrial myocytes. Am J Physiol 270: C500－ C507, 1996 https://doi.org/10.1152/ajpcell.1996.270.2.C500
  27. Matsuoka S, Sarai N, Kuratomi S, Ono K, Noma A. Role of individual ionic current systems in ventricular cells hypothesized by a model study. Jpn J Physiol 53: 105－123, 2003 https://doi.org/10.2170/jjphysiol.53.105
  28. Parmley WW, Chuck L. Length-dependent changes in myocardial contractile state. Am J Physiol 224: 1195－1199, 1973
  29. Riemer TL, Tung L. Stretch-induced excitation and action potential changes of single cardiac cells. Prog Biophys Mol Biol 82: 97－ 110, 2003 https://doi.org/10.1016/S0079-6107(03)00008-7
  30. Sachs F. Mechanical transduction in biological systems. Crit Rev Biomed Eng 16: 141－169, 1988
  31. Sakai R, Hagiwara N, Kasanuki H, Hosoda S. Chloride conductance in human atrial cells. J Mol Cell Cardiol 27: 2403-2408, 1995 https://doi.org/10.1016/S0022-2828(95)92199-0
  32. 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. Jpn J Physiol 53: 125－134, 2003 https://doi.org/10.2170/jjphysiol.53.125
  33. Sasaki N, Mitsuiye T, Noma A. Effects of mechanical stretch on membrane currents of single ventricular myocytes of guinea-pig heart. Jpn J Physiol 42: 957－970, 1992 https://doi.org/10.2170/jjphysiol.42.957
  34. Tavi P, Han C, Weckstrom M. Mechanisms of stretch-induced changes in $[Ca^{2+}]_i$ in rat atrial myocytes: role of increased troponin C affinity and stretch-activated ion channels. Circ Res 83: 1165－77, 1998 https://doi.org/10.1161/01.RES.83.11.1165
  35. Tseng GN. Cell swelling increases membrane conductance of canine cardiac cells: evidence for a volume-sensitive Cl channel. Am J Physiol 262: C1056－1068, 1992 https://doi.org/10.1152/ajpcell.1992.262.4.C1056
  36. Tucci PFJ, Bregagnollo EA, Spadaro J, Cicogna AC, Ribeiro MCL. Length dependence of activation studied in the isovolumic blood-perfused dog heart. Circ Res 55: 59－66, 1984 https://doi.org/10.1161/01.RES.55.1.59
  37. Tung L, Zou S. Influence of stretch on excitation threshold of single frog ventricular cells. Exp Physiol 80: 221－235, 1995 https://doi.org/10.1113/expphysiol.1995.sp003842
  38. Ubl J, Murer H, Kolb HA. Hypotonic shock evokes opening of Ca2$^+$- activated K channels in opossum kidney cells. Pflugers Arch 412: 551－553, 1988 https://doi.org/10.1007/BF00582547
  39. White E, Le Guennec JY, Nigretto JM, Gannier F, Argibay JA, Garnier D. The effects of increasing cell length on auxotonic contractions; membrane potential and intracellular calcium transients in single guinea-pig ventricular myocytes. Exp Physiol 78: 65－78, 1993 https://doi.org/10.1113/expphysiol.1993.sp003671
  40. Youm JB, Ho WK, Earm YE. Permeability characteristics of monovalent cations in atrial myocytes of the rat heart. Exp Physiol 85: 143－150, 2000 https://doi.org/10.1017/S0958067000019515
  41. Zeng T, Bett GCL, Sachs F. Stretch-activated whole cell currents in adult rat cardiac myocytes. Am J Physiol 278: H548－H557, 2000
  42. Zhang YH, Youm JB, Sung HK, Lee SH, Ryu SY, Ho WK, Earm YE. Stretch-activated and background non-selective cation channels in rat atrial myocytes. J Physiol 523: 607－619, 2000 https://doi.org/10.1111/j.1469-7793.2000.00607.x