Skip to main content
The Journal of Physiology logoLink to The Journal of Physiology
. 1991;440:143–165. doi: 10.1113/jphysiol.1991.sp018701

ATP activates cationic currents and modulates the calcium current through GTP-binding protein in rabbit portal vein.

Z L Xiong 1, K Kitamura 1, H Kuriyama 1
PMCID: PMC1180145  PMID: 1725181

Abstract

1. Effects of adenosine 5'-triphosphate (ATP) on ionic currents of dispersed smooth muscle cells of the rabbit portal vein were investigated using the voltage-clamp procedure. 2. ATP (greater than or equal to 300 microM) produced transient and maintained inward currents. The former was inactivated within a few seconds, but the latter lasted more than several minutes. The transient but not the maintained current was blocked by pre-treatment with alpha,beta-methylene adenosine 5'-triphosphate (AMP-CPP). The amplitude of the latter was increased by ATP in a concentration-dependent manner. The following investigations were made on the ionic mechanism of the ATP-induced maintained inward current. 3. In 2.5 mM-Ca(2+)-containing tetraethylammonium chloride (TEA-Cl) solution (2.5 mM-Ca(2+)-TEA+ solution), the reversal potential for the ATP-induced inward current was close to the Cl- equilibrium potential, and in 140 mM-Na+ (nominally Ca(2+)-free or 0.3 mM-EGTA-containing) solution, the reversal potential was coincident with the Na+ equilibrium potential. 4. In 2.5 mM-Ca(2+)-TEA+ solution but not in 140 mM-Na+ solution and in physiological salt solution (PSS), niflumic acid (10 microM), a Cl- channel blocker, and Cl(-)-deficient perfusate in the pipette markedly inhibited the ATP-induced inward current. These results imply that in 2.5 mM-Ca(2+)-TEA+ solution the ATP-activated ion channel may admit Ca2+ which then accelerates the Ca(2+)-dependent Cl- current, but in 140 mM-Na+ solution and in PSS this channel may admit only Na+. 5. Intracellular perfusion of guanosine 5'-O-(3-thio triphosphate (GTP gamma S) did not provoke the current, but significantly increased the amplitude of the ATP-induced inward current in 2.5 mM-Ca(2+)-TEA+, 140 mM-Na+ and 2.5 mM-Ba(2+)-containing TEA+ (2.5 mM-Ba(2+)-TEA+) solutions. On the other hand, intracellular perfusion of guanosine 5'-O-(2-thiodiphosphate) (GDP beta S) reduced the amplitude of the ATP-induced inward current in the above solutions. 6. A low concentration of ATP (30 microM) transiently augmented the amplitude of the voltage-dependent Ca2+ current recorded in both 2.5 mM-Ca(2+)-TEA+ solution and PSS, but a high concentration of ATP (3 mM) consistently inhibited the voltage-dependent Ca2+ current in both solutions (4 mM-EGTA in the pipette). Such inhibition was partly prevented by application of 20 mM-EGTA in the pipette.(ABSTRACT TRUNCATED AT 400 WORDS)

Full text

PDF
143

Selected References

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

  1. Benham C. D. ATP-activated channels gate calcium entry in single smooth muscle cells dissociated from rabbit ear artery. J Physiol. 1989 Dec;419:689–701. doi: 10.1113/jphysiol.1989.sp017893. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Benham C. D., Bolton T. B., Byrne N. G., Large W. A. Action of externally applied adenosine triphosphate on single smooth muscle cells dispersed from rabbit ear artery. J Physiol. 1987 Jun;387:473–488. doi: 10.1113/jphysiol.1987.sp016585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Benham C. D., Bolton T. B., Lang R. J. Acetylcholine activates an inward current in single mammalian smooth muscle cells. Nature. 1985 Jul 25;316(6026):345–347. doi: 10.1038/316345a0. [DOI] [PubMed] [Google Scholar]
  4. Benham C. D., Tsien R. W. A novel receptor-operated Ca2+-permeable channel activated by ATP in smooth muscle. Nature. 1987 Jul 16;328(6127):275–278. doi: 10.1038/328275a0. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. 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]
  7. Clapp L. H., Vivaudou M. B., Walsh J. V., Jr, Singer J. J. Acetylcholine increases voltage-activated Ca2+ current in freshly dissociated smooth muscle cells. Proc Natl Acad Sci U S A. 1987 Apr;84(7):2092–2096. doi: 10.1073/pnas.84.7.2092. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Friel D. D. An ATP-sensitive conductance in single smooth muscle cells from the rat vas deferens. J Physiol. 1988 Jul;401:361–380. doi: 10.1113/jphysiol.1988.sp017167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fukushima Y., Hagiwara S. Currents carried by monovalent cations through calcium channels in mouse neoplastic B lymphocytes. J Physiol. 1985 Jan;358:255–284. doi: 10.1113/jphysiol.1985.sp015550. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. Hashimoto T., Hirata M., Itoh T., Kanmura Y., Kuriyama H. Inositol 1,4,5-trisphosphate activates pharmacomechanical coupling in smooth muscle of the rabbit mesenteric artery. J Physiol. 1986 Jan;370:605–618. doi: 10.1113/jphysiol.1986.sp015953. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Honoré E., Martin C., Mironneau C., Mironneau J. An ATP-sensitive conductance in cultured smooth muscle cells from pregnant rat myometrium. Am J Physiol. 1989 Aug;257(2 Pt 1):C297–C305. doi: 10.1152/ajpcell.1989.257.2.C297. [DOI] [PubMed] [Google Scholar]
  13. Iino M., Kobayashi T., Endo M. Use of ryanodine for functional removal of the calcium store in smooth muscle cells of the guinea-pig. Biochem Biophys Res Commun. 1988 Apr 15;152(1):417–422. doi: 10.1016/s0006-291x(88)80730-7. [DOI] [PubMed] [Google Scholar]
  14. Inoue R., Kitamura K., Kuriyama H. Acetylcholine activates single sodium channels in smooth muscle cells. Pflugers Arch. 1987 Sep;410(1-2):69–74. doi: 10.1007/BF00581898. [DOI] [PubMed] [Google Scholar]
  15. Inoue R., Kitamura K., Kuriyama H. Two Ca-dependent K-channels classified by the application of tetraethylammonium distribute to smooth muscle membranes of the rabbit portal vein. Pflugers Arch. 1985 Oct;405(3):173–179. doi: 10.1007/BF00582557. [DOI] [PubMed] [Google Scholar]
  16. Itoh T., Kanmura Y., Kuriyama H. A23187 increases calcium permeability of store sites more than of surface membranes in the rabbit mesenteric artery. J Physiol. 1985 Feb;359:467–484. doi: 10.1113/jphysiol.1985.sp015597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Iwatsuki N. Effects of divalent cations on acetylcholine-evoked membrane potential in the ionophore A23187 treated mouse pancreas. Pflugers Arch. 1984 Dec;402(4):465–472. doi: 10.1007/BF00583949. [DOI] [PubMed] [Google Scholar]
  18. Karashima T., Takata Y. The effects of ATP related compounds on the electrical activity of the rat portal vein. Gen Pharmacol. 1979;10(6):477–487. doi: 10.1016/0306-3623(79)90013-2. [DOI] [PubMed] [Google Scholar]
  19. Kobayashi S., Somlyo A. V., Somlyo A. P. Heparin inhibits the inositol 1,4,5-trisphosphate-dependent, but not the independent, calcium release induced by guanine nucleotide in vascular smooth muscle. Biochem Biophys Res Commun. 1988 Jun 16;153(2):625–631. doi: 10.1016/s0006-291x(88)81141-0. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. Nakazawa K., Matsuki N. Adenosine triphosphate-activated inward current in isolated smooth muscle cells from rat vas deferens. Pflugers Arch. 1987 Aug;409(6):644–646. doi: 10.1007/BF00584668. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. Ohya Y., Kitamura K., Kuriyama H. Cellular calcium regulates outward currents in rabbit intestinal smooth muscle cell. Am J Physiol. 1987 Apr;252(4 Pt 1):C401–C410. doi: 10.1152/ajpcell.1987.252.4.C401. [DOI] [PubMed] [Google Scholar]
  24. Ohya Y., Kitamura K., Kuriyama H. Modulation of ionic currents in smooth muscle balls of the rabbit intestine by intracellularly perfused ATP and cyclic AMP. Pflugers Arch. 1987 May;408(5):465–473. doi: 10.1007/BF00585070. [DOI] [PubMed] [Google Scholar]
  25. Ohya Y., Terada K., Kitamura K., Kuriyama H. Membrane currents recorded from a fragment of rabbit intestinal smooth muscle cell. Am J Physiol. 1986 Sep;251(3 Pt 1):C335–C346. doi: 10.1152/ajpcell.1986.251.3.C335. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. 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]
  28. 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]
  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. Vivaudou M. B., Clapp L. H., Walsh J. V., Jr, Singer J. J. Regulation of one type of Ca2+ current in smooth muscle cells by diacylglycerol and acetylcholine. FASEB J. 1988 Jun;2(9):2497–2504. doi: 10.1096/fasebj.2.9.2453389. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES