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. 1992 Oct;456:285–302. doi: 10.1113/jphysiol.1992.sp019337

Stretch-activated anion currents of rabbit cardiac myocytes.

N Hagiwara 1, H Masuda 1, M Shoda 1, H Irisawa 1
PMCID: PMC1175682  PMID: 1284078

Abstract

1. Stretch-activated anion currents were studied in sino-atrial and atrial cells using the whole-cell patch clamp technique. With continuous application of positive pressure (5-15 cmH2O) through the patch clamp electrode, the cell was inflated and the membrane conductance was increased. 2. Voltage clamp steps revealed that the stretch-activated currents had time-independent characteristics. The increase in membrane conductance was reversible on subsequent application of negative pressure to the electrode. 3. The reversal potential of the stretch-activated currents was shifted by 60 mV for a 10-fold change in intracellular Cl- concentration, while it was unaffected by replacement of Na+ in the extracellular solution by N-methyl-D-glucamine. Cell superfusion with Cl(-)-deficient solution (10 mM Cl-) reduced the amplitude of outward current. These findings indicate that the stretch-activated conductance is Cl- selective. 4. The sequence of anion permeability through the stretch-activated conductance was determined to be I-(1.7) > NO3-(1.5) > Br-(1.2) > Cl-(1.0) > and F-(0.6). SCN- appeared to be more permeant than I-. 5. The stretch-activated conductance was reduced by the Cl- channel blockers, 4,4'-dinitrostilbene-2,2'-disulphonic acid disodium salt, 4-acetamido-4'-isothiocyanatostilbene-2,2'-disulphonic acid or anthracene-9-carboxylate (9-AC). Administration of furosemide or bumetanide had no effect. 6. The stretch-activated Cl- current was recorded even though intracellular Ca2+ ions were chelated by including 10 mM EGTA in the pipette solution. Neither the specific peptide inhibitor of cyclic AMP-dependent protein kinase (50 microM), nor the non-selective blocker of protein kinases, H-7 (20 microM), was effective in reducing the stretch-activated Cl- current, suggesting that the stretch-activated Cl- current is a novel type of cardiac Cl- current, which shows a different modulatory mechanism from that of other cardiac Cl- currents.

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Selected References

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

  1. Bader C. R., Bertrand D., Schlichter R. Calcium-activated chloride current in cultured sensory and parasympathetic quail neurones. J Physiol. 1987 Dec;394:125–148. doi: 10.1113/jphysiol.1987.sp016863. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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]
  3. 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]
  4. 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]
  5. Cooper K. E., Tang J. M., Rae J. L., Eisenberg R. S. A cation channel in frog lens epithelia responsive to pressure and calcium. J Membr Biol. 1986;93(3):259–269. doi: 10.1007/BF01871180. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. Denyer J. C., Brown H. F. Rabbit sino-atrial node cells: isolation and electrophysiological properties. J Physiol. 1990 Sep;428:405–424. doi: 10.1113/jphysiol.1990.sp018219. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Diamond J. M., Wright E. M. Biological membranes: the physical basis of ion and nonelectrolyte selectivity. Annu Rev Physiol. 1969;31:581–646. doi: 10.1146/annurev.ph.31.030169.003053. [DOI] [PubMed] [Google Scholar]
  9. Dudel J., Peper K., Rüdel R., Trautwein W. The dynamic chloride component of membrane current in Purkinje fibers. Pflugers Arch Gesamte Physiol Menschen Tiere. 1967;295(3):197–212. doi: 10.1007/BF01844100. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Ehara T., Ishihara K. Anion channels activated by adrenaline in cardiac myocytes. Nature. 1990 Sep 20;347(6290):284–286. doi: 10.1038/347284a0. [DOI] [PubMed] [Google Scholar]
  12. Evans M. G., Marty A., Tan Y. P., Trautmann A. Blockage of Ca-activated Cl conductance by furosemide in rat lacrimal glands. Pflugers Arch. 1986 Jan;406(1):65–68. doi: 10.1007/BF00582955. [DOI] [PubMed] [Google Scholar]
  13. Guharay F., Sachs F. Mechanotransducer ion channels in chick skeletal muscle: the effects of extracellular pH. J Physiol. 1985 Jun;363:119–134. doi: 10.1113/jphysiol.1985.sp015699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Guharay F., Sachs F. Stretch-activated single ion channel currents in tissue-cultured embryonic chick skeletal muscle. J Physiol. 1984 Jul;352:685–701. doi: 10.1113/jphysiol.1984.sp015317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. HUTTER O. F., PADSHA S. M. Effect of nitrate and other anions on the membrane resistance of frog skeletal muscle. J Physiol. 1959 Apr 23;146(1):117–132. doi: 10.1113/jphysiol.1959.sp006182. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hagiwara N., Irisawa H., Kameyama M. Contribution of two types of calcium currents to the pacemaker potentials of rabbit sino-atrial node cells. J Physiol. 1988 Jan;395:233–253. doi: 10.1113/jphysiol.1988.sp016916. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hagiwara N., Irisawa H., Kasanuki H., Hosoda S. Background current in sino-atrial node cells of the rabbit heart. J Physiol. 1992 Mar;448:53–72. doi: 10.1113/jphysiol.1992.sp019029. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. 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]
  20. Harvey R. D., Clark C. D., Hume J. R. Chloride current in mammalian cardiac myocytes. Novel mechanism for autonomic regulation of action potential duration and resting membrane potential. J Gen Physiol. 1990 Jun;95(6):1077–1102. doi: 10.1085/jgp.95.6.1077. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Hidaka H., Inagaki M., Kawamoto S., Sasaki Y. Isoquinolinesulfonamides, novel and potent inhibitors of cyclic nucleotide dependent protein kinase and protein kinase C. Biochemistry. 1984 Oct 9;23(21):5036–5041. doi: 10.1021/bi00316a032. [DOI] [PubMed] [Google Scholar]
  22. Hoffmann E. K. Anion transport systems in the plasma membrane of vertebrate cells. Biochim Biophys Acta. 1986 Jun 12;864(1):1–31. doi: 10.1016/0304-4157(86)90014-6. [DOI] [PubMed] [Google Scholar]
  23. Hoffmann E. K., Lambert I. H., Simonsen L. O. Separate, Ca2+-activated K+ and Cl- transport pathways in Ehrlich ascites tumor cells. J Membr Biol. 1986;91(3):227–244. doi: 10.1007/BF01868816. [DOI] [PubMed] [Google Scholar]
  24. Hudson R. L., Schultz S. G. Sodium-coupled glycine uptake by Ehrlich ascites tumor cells results in an increase in cell volume and plasma membrane channel activities. Proc Natl Acad Sci U S A. 1988 Jan;85(1):279–283. doi: 10.1073/pnas.85.1.279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. 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]
  26. Kameyama M., Hofmann F., Trautwein W. On the mechanism of beta-adrenergic regulation of the Ca channel in the guinea-pig heart. Pflugers Arch. 1985 Oct;405(3):285–293. doi: 10.1007/BF00582573. [DOI] [PubMed] [Google Scholar]
  27. Martinac B., Buechner M., Delcour A. H., Adler J., Kung C. Pressure-sensitive ion channel in Escherichia coli. Proc Natl Acad Sci U S A. 1987 Apr;84(8):2297–2301. doi: 10.1073/pnas.84.8.2297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Matsuoka S., Ehara T., Noma A. Chloride-sensitive nature of the adrenaline-induced current in guinea-pig cardiac myocytes. J Physiol. 1990 Jun;425:579–598. doi: 10.1113/jphysiol.1990.sp018119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. McCann J. D., Li M., Welsh M. J. Identification and regulation of whole-cell chloride currents in airway epithelium. J Gen Physiol. 1989 Dec;94(6):1015–1036. doi: 10.1085/jgp.94.6.1015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. McCann J. D., Welsh M. J. Regulation of Cl- and K+ channels in airway epithelium. Annu Rev Physiol. 1990;52:115–135. doi: 10.1146/annurev.ph.52.030190.000555. [DOI] [PubMed] [Google Scholar]
  31. Morris C. E. Mechanosensitive ion channels. J Membr Biol. 1990 Feb;113(2):93–107. doi: 10.1007/BF01872883. [DOI] [PubMed] [Google Scholar]
  32. Sachs F. Baroreceptor mechanisms at the cellular level. Fed Proc. 1987 Jan;46(1):12–16. [PubMed] [Google Scholar]
  33. Seyama I. Characteristics of the anion channel in the sino-atrial node cell of the rabbit. J Physiol. 1979 Sep;294:447–460. doi: 10.1113/jphysiol.1979.sp012940. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Ubl J., Murer H., Kolb H. A. Hypotonic shock evokes opening of Ca2+-activated K channels in opossum kidney cells. Pflugers Arch. 1988 Oct;412(5):551–553. doi: 10.1007/BF00582547. [DOI] [PubMed] [Google Scholar]
  35. Wright E. M., Diamond J. M. Anion selectivity in biological systems. Physiol Rev. 1977 Jan;57(1):109–156. doi: 10.1152/physrev.1977.57.1.109. [DOI] [PubMed] [Google Scholar]
  36. Yazawa K., Kameyama M. Mechanism of receptor-mediated modulation of the delayed outward potassium current in guinea-pig ventricular myocytes. J Physiol. 1990 Feb;421:135–150. doi: 10.1113/jphysiol.1990.sp017937. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Zygmunt A. C., Gibbons W. R. Calcium-activated chloride current in rabbit ventricular myocytes. Circ Res. 1991 Feb;68(2):424–437. doi: 10.1161/01.res.68.2.424. [DOI] [PubMed] [Google Scholar]

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