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British Journal of Pharmacology logoLink to British Journal of Pharmacology
. 1991 Dec;104(4):1000–1006. doi: 10.1111/j.1476-5381.1991.tb12540.x

Ca2+ channel activation and membrane depolarization mediated by Cl- channels in response to noradrenaline in vascular myocytes.

P Pacaud 1, G Loirand 1, A Baron 1, C Mironneau 1, J Mironneau 1
PMCID: PMC1908818  PMID: 1667281

Abstract

1. The effects of noradrenaline (NA) were studied on vascular smooth muscle cells isolated from rat portal vein. 2. Two types of single-Ca2+ channel currents with conductances of 17 pS and 8 pS were obtained in cell-attached configuration. Bath application of NA increased the open probability of both channels during depolarizing pulses without a change of background membrane conductance. However, NA did not open Ca2+ channels when the membrane patch potential was held at -50 mV, which is about the resting potential in physiological conditions. 3. In the whole-cell configuration, studies of voltage-dependent Ca2+ channel currents showed that the peak conductance curve was not shifted to more negative potentials by NA. 4. Measurements of internal Ca(2+)-concentration ([Ca2+]i) with Indo-1 indicated that NA increased [Ca2+]i at a holding potential of -50 mV and evoked a Ca(2+)-activated Cl- current. These effects were blocked when heparin was included in the pipette solution. 5. A Cl- channel blocker without effect on Ca2+ channels (anthracene-9-carboxylic acid) inhibited the contractions of portal vein strips induced by NA in a manner similar to that produced by a Ca2+ channel inhibitor (isradipine). The NA-induced contraction was completely suppressed in the presence of ryanodine which depletes intracellular Ca2+ stores. 6. The present study suggests that activation of Cl- channels by Ca2+ release produces a membrane depolarization which is a prerequisite for enhanced opening of voltage-dependent Ca2+ channels in response to NA in venous smooth muscle.

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Selected References

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

  1. Almers W., Neher E. The Ca signal from fura-2 loaded mast cells depends strongly on the method of dye-loading. FEBS Lett. 1985 Nov 11;192(1):13–18. doi: 10.1016/0014-5793(85)80033-8. [DOI] [PubMed] [Google Scholar]
  2. Benham C. D., Tsien R. W. Noradrenaline modulation of calcium channels in single smooth muscle cells from rabbit ear artery. J Physiol. 1988 Oct;404:767–784. doi: 10.1113/jphysiol.1988.sp017318. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Benham C. D. Voltage-gated and agonist-mediated rises in intracellular Ca2+ in rat clonal pituitary cells (GH3) held under voltage clamp. J Physiol. 1989 Aug;415:143–158. doi: 10.1113/jphysiol.1989.sp017716. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bolton T. B. Mechanisms of action of transmitters and other substances on smooth muscle. Physiol Rev. 1979 Jul;59(3):606–718. doi: 10.1152/physrev.1979.59.3.606. [DOI] [PubMed] [Google Scholar]
  5. Boton R., Dascal N., Gillo B., Lass Y. Two calcium-activated chloride conductances in Xenopus laevis oocytes permeabilized with the ionophore A23187. J Physiol. 1989 Jan;408:511–534. doi: 10.1113/jphysiol.1989.sp017473. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Byrne N. G., Large W. A. Mechanism of action of alpha-adrenoceptor activation in single cells freshly dissociated from the rabbit portal vein. Br J Pharmacol. 1988 Jun;94(2):475–482. doi: 10.1111/j.1476-5381.1988.tb11550.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Byrne N. G., Large W. A. Membrane ionic mechanisms activated by noradrenaline in cells isolated from the rabbit portal vein. J Physiol. 1988 Oct;404:557–573. doi: 10.1113/jphysiol.1988.sp017306. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bülbring E., Tomita T. Catecholamine action on smooth muscle. Pharmacol Rev. 1987 Mar;39(1):49–96. [PubMed] [Google Scholar]
  9. Dacquet C., Mironneau C., Mironneau J. Effects of calcium entry blockers on calcium-dependent contractions of rat portal vein. Br J Pharmacol. 1987 Sep;92(1):203–211. doi: 10.1111/j.1476-5381.1987.tb11313.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fox A. P., Nowycky M. C., Tsien R. W. Kinetic and pharmacological properties distinguishing three types of calcium currents in chick sensory neurones. J Physiol. 1987 Dec;394:149–172. doi: 10.1113/jphysiol.1987.sp016864. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ghosh T. K., Eis P. S., Mullaney J. M., Ebert C. L., Gill D. L. Competitive, reversible, and potent antagonism of inositol 1,4,5-trisphosphate-activated calcium release by heparin. J Biol Chem. 1988 Aug 15;263(23):11075–11079. [PubMed] [Google Scholar]
  12. Grynkiewicz G., Poenie M., Tsien R. Y. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem. 1985 Mar 25;260(6):3440–3450. [PubMed] [Google Scholar]
  13. 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]
  14. Inoue R., Isenberg G. Effect of membrane potential on acetylcholine-induced inward current in guinea-pig ileum. J Physiol. 1990 May;424:57–71. doi: 10.1113/jphysiol.1990.sp018055. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Inoue R., Isenberg G. Intracellular calcium ions modulate acetylcholine-induced inward current in guinea-pig ileum. J Physiol. 1990 May;424:73–92. doi: 10.1113/jphysiol.1990.sp018056. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Inoue Y., Oike M., Nakao K., Kitamura K., Kuriyama H. Endothelin augments unitary calcium channel currents on the smooth muscle cell membrane of guinea-pig portal vein. J Physiol. 1990 Apr;423:171–191. doi: 10.1113/jphysiol.1990.sp018017. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Klöckner U., Isenberg G. Endothelin depolarizes myocytes from porcine coronary and human mesenteric arteries through a Ca-activated chloride current. Pflugers Arch. 1991 Mar;418(1-2):168–175. doi: 10.1007/BF00370467. [DOI] [PubMed] [Google Scholar]
  18. Komori S., Bolton T. B. Calcium release induced by inositol 1,4,5-trisphosphate in single rabbit intestinal smooth muscle cells. J Physiol. 1991 Feb;433:495–517. doi: 10.1113/jphysiol.1991.sp018440. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Komori S., Bolton T. B. Role of G-proteins in muscarinic receptor inward and outward currents in rabbit jejunal smooth muscle. J Physiol. 1990 Aug;427:395–419. doi: 10.1113/jphysiol.1990.sp018178. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Loirand G., Mironneau C., Mironneau J., Pacaud P. Two types of calcium currents in single smooth muscle cells from rat portal vein. J Physiol. 1989 May;412:333–349. doi: 10.1113/jphysiol.1989.sp017619. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Loirand G., Pacaud P., Mironneau C., Mironneau J. Evidence for two distinct calcium channels in rat vascular smooth muscle cells in short-term primary culture. Pflugers Arch. 1986 Nov;407(5):566–568. doi: 10.1007/BF00657519. [DOI] [PubMed] [Google Scholar]
  22. Loirand G., Pacaud P., Mironneau C., Mironneau J. GTP-binding proteins mediate noradrenaline effects on calcium and chloride currents in rat portal vein myocytes. J Physiol. 1990 Sep;428:517–529. doi: 10.1113/jphysiol.1990.sp018225. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Markwardt F., Franke T., Albitz R., Nilius B. Effects of thrombin on single calcium channels in frog ventricular cells. Pflugers Arch. 1990 Feb;415(5):547–553. doi: 10.1007/BF02583505. [DOI] [PubMed] [Google Scholar]
  24. Mironneau J., Gargouil Y. M. Action of indapamide on excitation-contraction coupling in vascular smooth muscle. Eur J Pharmacol. 1979 Jul 15;57(1):57–67. doi: 10.1016/0014-2999(79)90103-1. [DOI] [PubMed] [Google Scholar]
  25. Nanjo T. Effects of noradrenaline and acetylcholine on electro-mechanical properties of the guinea-pig portal vein. Br J Pharmacol. 1984 Mar;81(3):427–440. doi: 10.1111/j.1476-5381.1984.tb10095.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Nelson M. T., Patlak J. B., Worley J. F., Standen N. B. Calcium channels, potassium channels, and voltage dependence of arterial smooth muscle tone. Am J Physiol. 1990 Jul;259(1 Pt 1):C3–18. doi: 10.1152/ajpcell.1990.259.1.C3. [DOI] [PubMed] [Google Scholar]
  27. Nelson M. T., Standen N. B., Brayden J. E., Worley J. F., 3rd Noradrenaline contracts arteries by activating voltage-dependent calcium channels. Nature. 1988 Nov 24;336(6197):382–385. doi: 10.1038/336382a0. [DOI] [PubMed] [Google Scholar]
  28. Pacaud P., Loirand G., Mironneau C., Mironneau J. Noradrenaline activates a calcium-activated chloride conductance and increases the voltage-dependent calcium current in cultured single cells of rat portal vein. Br J Pharmacol. 1989 May;97(1):139–146. doi: 10.1111/j.1476-5381.1989.tb11934.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Rousseau E., Smith J. S., Meissner G. Ryanodine modifies conductance and gating behavior of single Ca2+ release channel. Am J Physiol. 1987 Sep;253(3 Pt 1):C364–C368. doi: 10.1152/ajpcell.1987.253.3.C364. [DOI] [PubMed] [Google Scholar]
  30. Sakai T., Terada K., Kitamura K., Kuriyama H. Ryanodine inhibits the Ca-dependent K current after depletion of Ca stored in smooth muscle cells of the rabbit ileal longitudinal muscle. Br J Pharmacol. 1988 Dec;95(4):1089–1100. doi: 10.1111/j.1476-5381.1988.tb11743.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Suzuki H. Effects of endogenous and exogenous noradrenaline on the smooth muscle of guinea-pig mesenteric vein. J Physiol. 1981 Dec;321:495–512. doi: 10.1113/jphysiol.1981.sp013999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Takata Y. Regional differences in electrical and mechanical properties of guinea-pig mesenteric vessels. Jpn J Physiol. 1980;30(5):709–728. doi: 10.2170/jjphysiol.30.709. [DOI] [PubMed] [Google Scholar]
  33. Tsien R. W., Bean B. P., Hess P., Lansman J. B., Nilius B., Nowycky M. C. Mechanisms of calcium channel modulation by beta-adrenergic agents and dihydropyridine calcium agonists. J Mol Cell Cardiol. 1986 Jul;18(7):691–710. doi: 10.1016/s0022-2828(86)80941-5. [DOI] [PubMed] [Google Scholar]
  34. Van Helden D. F. An alpha-adrenoceptor-mediated chloride conductance in mesenteric veins of the guinea-pig. J Physiol. 1988 Jul;401:489–501. doi: 10.1113/jphysiol.1988.sp017174. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Yamamoto Y., Hotta K. Mechanisms involved in contraction of smooth muscles of the rat portal vein as induced by sodium depletion. Jpn J Physiol. 1985;35(5):717–727. doi: 10.2170/jjphysiol.35.717. [DOI] [PubMed] [Google Scholar]

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