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. 1990 Jun;425:579–598. doi: 10.1113/jphysiol.1990.sp018119

Chloride-sensitive nature of the adrenaline-induced current in guinea-pig cardiac myocytes.

S Matsuoka 1, T Ehara 1, A Noma 1
PMCID: PMC1189864  PMID: 1698979

Abstract

1. Ionic selectivity of an adrenaline-induced current was investigated in single guinea-pig ventricular cells by recording whole-cell currents using the patch clamp technique combined with internal perfusion. Other ionic currents and exchange currents known in ventricular cells were suppressed by appropriate inhibitors and the adrenaline-induced current was defined as a difference between currents obtained in the presence and absence of adrenaline. 2. The adrenaline-induced current was time independent and its I-V relation showed saturation of the inward current in the negative voltage range. 3. The reversal potential was approximately -20 mV with 140 mM-NaCl external solution and Cs(+)-rich internal solution containing 51 mM-Cl-. Replacing Na+ with various monovalent and divalent cations (Li+, K+, Rb+, Cs+, Ca2+, Sr2+ and Ba2+) produced no appreciable change in the reversal potential. 4. Varying the external Cl- concentration ([Cl-]o) in exchange for aspartate or benzenesulphonate greatly changed the reversal potential. The relationship between the reversal potential and log[Cl-]o indicated a slope of 59.5 or 53.6 mV per tenfold change in [Cl-]o in the presence of 51 or 102 mM-Cl- in the internal solution, respectively. 5. Anion substitutions did not appreciably affect the I-V relation before application of adrenaline, suggesting that the cell membrane had a low Cl- conductance in the control state. 6. 4.4'-Dinitrostilbene-2-2'-disulphonic acid (DNDS: 1-10 mM), a specific inhibitor of membrane chloride permeability, depressed the adrenaline-induced current without changing the reversal potential. 7. The results suggest strongly that the adrenaline-induced current is carried mainly by Cl-. However, the development of this current appears to depend also on external cations, since the magnitude of the adrenaline response varied depending on the external cations species, with no response in Tris-HCl or TEA-Cl solution. The external cations may facilitate the adrenaline response with a sequence of efficacy of Na+ greater than K+, Rb+ greater than Cs+, Li+, divalent cations.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bahinski A., Nairn A. C., Greengard P., Gadsby D. C. Chloride conductance regulated by cyclic AMP-dependent protein kinase in cardiac myocytes. Nature. 1989 Aug 31;340(6236):718–721. doi: 10.1038/340718a0. [DOI] [PubMed] [Google Scholar]
  2. Baker P. F., McNaughton P. A. Kinetics and energetics of calcium efflux from intact squid giant axons. J Physiol. 1976 Jul;259(1):103–144. doi: 10.1113/jphysiol.1976.sp011457. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Boyden P. A., Cranefield P. F., Gadsby D. C. Noradrenaline hyperpolarizes cells of the canine coronary sinus by increasing their permeability to potassium ions. J Physiol. 1983 Jun;339:185–206. doi: 10.1113/jphysiol.1983.sp014711. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bretag A. H. Muscle chloride channels. Physiol Rev. 1987 Apr;67(2):618–724. doi: 10.1152/physrev.1987.67.2.618. [DOI] [PubMed] [Google Scholar]
  5. Bridges R. J., Worrell R. T., Frizzell R. A., Benos D. J. Stilbene disulfonate blockade of colonic secretory Cl- channels in planar lipid bilayers. Am J Physiol. 1989 Apr;256(4 Pt 1):C902–C912. doi: 10.1152/ajpcell.1989.256.4.C902. [DOI] [PubMed] [Google Scholar]
  6. CARMELIET E. E. Chloride ions and the membrane potential of Purkinje fibres. J Physiol. 1961 Apr;156:375–388. doi: 10.1113/jphysiol.1961.sp006682. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Colquhoun D., Neher E., Reuter H., Stevens C. F. Inward current channels activated by intracellular Ca in cultured cardiac cells. Nature. 1981 Dec 24;294(5843):752–754. doi: 10.1038/294752a0. [DOI] [PubMed] [Google Scholar]
  8. Coronado R., Latorre R. Detection of K+ and Cl-channels from calf cardiac sarcolemma in planar lipid bilayer membranes. Nature. 1982 Aug 26;298(5877):849–852. doi: 10.1038/298849a0. [DOI] [PubMed] [Google Scholar]
  9. DiFrancesco D., Ferroni A., Visentin S. Barium-induced blockade of the inward rectifier in calf Purkinje fibres. Pflugers Arch. 1984 Dec;402(4):446–453. doi: 10.1007/BF00583946. [DOI] [PubMed] [Google Scholar]
  10. Egan T. M., Noble D., Noble S. J., Powell T., Twist V. W. An isoprenaline activated sodium-dependent inward current in ventricular myocytes. Nature. 1987 Aug 13;328(6131):634–637. doi: 10.1038/328634a0. [DOI] [PubMed] [Google Scholar]
  11. Egan T. M., Noble D., Noble S. J., Powell T., Twist V. W., Yamaoka K. On the mechanism of isoprenaline- and forskolin-induced depolarization of single guinea-pig ventricular myocytes. J Physiol. 1988 Jun;400:299–320. doi: 10.1113/jphysiol.1988.sp017121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Ehara T., Matsuoka S., Noma A. Measurement of reversal potential of Na+-Ca2+ exchange current in single guinea-pig ventricular cells. J Physiol. 1989 Mar;410:227–249. doi: 10.1113/jphysiol.1989.sp017530. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Ehara T., Noma A., Ono K. Calcium-activated non-selective cation channel in ventricular cells isolated from adult guinea-pig hearts. J Physiol. 1988 Sep;403:117–133. doi: 10.1113/jphysiol.1988.sp017242. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Ehara T. Rectifier properties of canine papillary muscle. Jpn J Physiol. 1971 Feb;21(1):49–69. doi: 10.2170/jjphysiol.21.49. [DOI] [PubMed] [Google Scholar]
  15. Fabiato A., Fabiato F. Calculator programs for computing the composition of the solutions containing multiple metals and ligands used for experiments in skinned muscle cells. J Physiol (Paris) 1979;75(5):463–505. [PubMed] [Google Scholar]
  16. Frizzell R. A., Rechkemmer G., Shoemaker R. L. Altered regulation of airway epithelial cell chloride channels in cystic fibrosis. Science. 1986 Aug 1;233(4763):558–560. doi: 10.1126/science.2425436. [DOI] [PubMed] [Google Scholar]
  17. Gadsby D. C. Beta-adrenoceptor agonists increase membrane K+ conductance in cardiac Purkinje fibres. Nature. 1983 Dec 15;306(5944):691–693. doi: 10.1038/306691a0. [DOI] [PubMed] [Google Scholar]
  18. HODGKIN A. L., KATZ B. The effect of sodium ions on the electrical activity of giant axon of the squid. J Physiol. 1949 Mar 1;108(1):37–77. doi: 10.1113/jphysiol.1949.sp004310. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. HUTTER O. F., NOBLE D. Anion conductance of cardiac muscle. J Physiol. 1961 Jul;157:335–350. doi: 10.1113/jphysiol.1961.sp006726. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hamill O. P., Marty A., Neher E., Sakmann B., Sigworth F. J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981 Aug;391(2):85–100. doi: 10.1007/BF00656997. [DOI] [PubMed] [Google Scholar]
  21. Harvey R. D., Hume J. R. Autonomic regulation of a chloride current in heart. Science. 1989 May 26;244(4907):983–985. doi: 10.1126/science.2543073. [DOI] [PubMed] [Google Scholar]
  22. Hoffman F. L. Regarding remarks of Dr. Rodney Yoell as printed on page 447 of the June, 1935, issue of California and Western Medicine: A letter from Frederick L. Hoffman, LL.D. Cal West Med. 1935 Jul;43(1):102–102. [PMC free article] [PubMed] [Google Scholar]
  23. Imoto Y., Ehara T., Matsuura H. Voltage- and time-dependent block of iK1 underlying Ba2+-induced ventricular automaticity. Am J Physiol. 1987 Feb;252(2 Pt 2):H325–H333. doi: 10.1152/ajpheart.1987.252.2.H325. [DOI] [PubMed] [Google Scholar]
  24. Isenberg G., Klockner U. Calcium tolerant ventricular myocytes prepared by preincubation in a "KB medium". Pflugers Arch. 1982 Oct;395(1):6–18. doi: 10.1007/BF00584963. [DOI] [PubMed] [Google Scholar]
  25. Kimura J., Noma A., Irisawa H. Na-Ca exchange current in mammalian heart cells. Nature. 1986 Feb 13;319(6054):596–597. doi: 10.1038/319596a0. [DOI] [PubMed] [Google Scholar]
  26. Matsuoka S., Noma A., Powell T. Li+ inhibition of membrane current responses to epinephrine in guinea-pig ventricular cells. Pflugers Arch. 1989 Dec;415(3):384–386. doi: 10.1007/BF00370892. [DOI] [PubMed] [Google Scholar]
  27. Powell T., Terrar D. A., Twist V. W. Electrical properties of individual cells isolated from adult rat ventricular myocardium. J Physiol. 1980 May;302:131–153. doi: 10.1113/jphysiol.1980.sp013234. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Sanguinetti M. C., Kass R. S. Voltage-dependent block of calcium channel current in the calf cardiac Purkinje fiber by dihydropyridine calcium channel antagonists. Circ Res. 1984 Sep;55(3):336–348. doi: 10.1161/01.res.55.3.336. [DOI] [PubMed] [Google Scholar]
  29. Soejima M., Noma A. Mode of regulation of the ACh-sensitive K-channel by the muscarinic receptor in rabbit atrial cells. Pflugers Arch. 1984 Apr;400(4):424–431. doi: 10.1007/BF00587544. [DOI] [PubMed] [Google Scholar]
  30. Terada K., Kitamura K., Kuriyama H. Blocking actions of Ca2+ antagonists on the Ca2+ channels in the smooth muscle cell membrane of rabbit small intestine. Pflugers Arch. 1987 May;408(6):552–557. doi: 10.1007/BF00581155. [DOI] [PubMed] [Google Scholar]
  31. Welsh M. J. An apical-membrane chloride channel in human tracheal epithelium. Science. 1986 Jun 27;232(4758):1648–1650. doi: 10.1126/science.2424085. [DOI] [PubMed] [Google Scholar]

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