Skip to main content
NCBI home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1992 Oct;456:541–556. doi: 10.1113/jphysiol.1992.sp019352

Intracellular cations modulate noradrenaline-stimulated calcium entry into smooth muscle cells of rat portal vein.

P Pacaud 1, G Loirand 1, T B Bolton 1, C Mironneau 1, J Mironneau 1
PMCID: PMC1175697  PMID: 1284081

Abstract

1. The action of noradrenaline (NA, 10 microM) was studied in single patch-clamped smooth muscle cells of rat portal vein where free internal Ca2+ concentration in the cell (Ca2+i) was estimated using the emission from the dye Indo-1. 2. In the presence of 50 microM D600, a blocker of voltage-dependent Ca2+ channels, NA applied to the cell evoked an initial peak in Ca2+i followed by a smaller sustained rise. The initial rise in Ca2+i was associated with the activation of Ca(2+)-dependent Cl- channels. 3. The maintained rise in Ca2+i induced by NA was enhanced by increasing the external Ca2+ concentration and was abolished in Ca(2+)-free solution. The transient rise was resistant to the absence of external Ca2+. 4. Following the transient rise in Ca2+i induced by NA, the mechanisms extruding and/or sequestering cytoplasmic Ca2+ were stimulated. This stimulation was measured during the sustained rise in Cai and was maintained for a few seconds after NA was removed. 5. Unlike the transient rise in Ca2+i, the sustained rise in Ca2+i produced by NA was affected by changing the cell membrane potential. 6. Changing the Na+ gradient showed that the Na(+)-Ca2+ exchange was not involved in the sustained rise in Ca2+i. 7. The sustained increase in Ca2+i produced by NA was modulated by intracellular cations. This phase could be observed with 130 mM Na+ or 130 mM K+ in the pipette solution, but was severely reduced when the only cation in the intracellular solution was Cs+ and abolished with NMDG (N-methyl-D-glucamine) or TEA. However, inclusion of only 10 mM Na+ or 50 mM K+ in the pipette solution was sufficient to obtain a sustained rise in Ca2+i of maximal amplitude, similar to that obtained with 130 mM Na+i or 130 mM K+i during NA application. 8. In portal vein smooth muscle cells, NA induced a two-phase increase in Ca2+i similar to the two phases which have been previously observed upon muscarinic receptor activation by carbachol in intestinal smooth muscle. The transient rise was due to Ca2+ store release whereas the sustained rise was due to an increased Ca2+ entry into the cell down its electrochemical gradient, but not through voltage-dependent Ca2+ channels. The Ca2+ permeability pathway involved in the sustained rise in Ca2+i induced by NA was modulated by the intracellular cations.

Full text

PDF
541

Selected References

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

  1. Aaronson P. I., Benham C. D. Alterations in [Ca2+]i mediated by sodium-calcium exchange in smooth muscle cells isolated from the guinea-pig ureter. J Physiol. 1989 Sep;416:1–18. doi: 10.1113/jphysiol.1989.sp017745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Aickin C. C., Brading A. F., Burdyga T. V. Evidence for sodium-calcium exchange in the guinea-pig ureter. J Physiol. 1984 Feb;347:411–430. doi: 10.1113/jphysiol.1984.sp015073. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Aickin C. C. Investigation of factors affecting the intracellular sodium activity in the smooth muscle of guinea-pig ureter. J Physiol. 1987 Apr;385:483–505. doi: 10.1113/jphysiol.1987.sp016503. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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]
  5. 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]
  6. 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]
  7. Berridge M. J. Inositol trisphosphate and diacylglycerol: two interacting second messengers. Annu Rev Biochem. 1987;56:159–193. doi: 10.1146/annurev.bi.56.070187.001111. [DOI] [PubMed] [Google Scholar]
  8. Berridge M. J., Irvine R. F. Inositol trisphosphate, a novel second messenger in cellular signal transduction. Nature. 1984 Nov 22;312(5992):315–321. doi: 10.1038/312315a0. [DOI] [PubMed] [Google Scholar]
  9. Bird G. S., Rossier M. F., Hughes A. R., Shears S. B., Armstrong D. L., Putney J. W., Jr Activation of Ca2+ entry into acinar cells by a non-phosphorylatable inositol trisphosphate. Nature. 1991 Jul 11;352(6331):162–165. doi: 10.1038/352162a0. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Dipolo R., Bezanilla F., Caputo C., Rojas H. Voltage dependence of the Na/Ca exchange in voltage-clamped, dialyzed squid axons. Na-dependent Ca efflux. J Gen Physiol. 1985 Oct;86(4):457–478. doi: 10.1085/jgp.86.4.457. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Furukawa K., Tawada Y., Shigekawa M. Regulation of the plasma membrane Ca2+ pump by cyclic nucleotides in cultured vascular smooth muscle cells. J Biol Chem. 1988 Jun 15;263(17):8058–8065. [PubMed] [Google Scholar]
  13. 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]
  14. 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]
  15. Huang C. L., Takenawa T., Ives H. E. Platelet-derived growth factor-mediated Ca2+ entry is blocked by antibodies to phosphatidylinositol 4,5-bisphosphate but does not involve heparin-sensitive inositol 1,4,5-trisphosphate receptors. J Biol Chem. 1991 Mar 5;266(7):4045–4048. [PubMed] [Google Scholar]
  16. Irvine R. F., Moor R. M. Micro-injection of inositol 1,3,4,5-tetrakisphosphate activates sea urchin eggs by a mechanism dependent on external Ca2+. Biochem J. 1986 Dec 15;240(3):917–920. doi: 10.1042/bj2400917. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Jacob R. Agonist-stimulated divalent cation entry into single cultured human umbilical vein endothelial cells. J Physiol. 1990 Feb;421:55–77. doi: 10.1113/jphysiol.1990.sp017933. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Llano I., Marty A., Tanguy J. Dependence of intracellular effects of GTP gamma S and inositoltrisphosphate on cell membrane potential and on external Ca ions. Pflugers Arch. 1987 Aug;409(4-5):499–506. doi: 10.1007/BF00583807. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. Ma T. S., Bose D. Sodium in smooth muscle relaxation. Am J Physiol. 1977 Jan;232(1):C59–C66. doi: 10.1152/ajpcell.1977.232.1.C59. [DOI] [PubMed] [Google Scholar]
  21. Manolopoulos V. G., Pipili-Synetos E., Den Hertog A., Nelemans A. Inositol phosphates formed in rat aorta after alpha 1-adrenoceptor stimulation are inhibited by forskolin. Eur J Pharmacol. 1991 May 25;207(1):29–36. doi: 10.1016/s0922-4106(05)80034-3. [DOI] [PubMed] [Google Scholar]
  22. Matlib M. A., Schwartz A., Yamori Y. A Na+-Ca2+ exchange process in isolated sarcolemmal membranes of mesenteric arteries from WKY and SHR rats. Am J Physiol. 1985 Jul;249(1 Pt 1):C166–C172. doi: 10.1152/ajpcell.1985.249.1.C166. [DOI] [PubMed] [Google Scholar]
  23. Matthews G., Neher E., Penner R. Second messenger-activated calcium influx in rat peritoneal mast cells. J Physiol. 1989 Nov;418:105–130. doi: 10.1113/jphysiol.1989.sp017830. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Mayer M. L., Westbrook G. L. Permeation and block of N-methyl-D-aspartic acid receptor channels by divalent cations in mouse cultured central neurones. J Physiol. 1987 Dec;394:501–527. doi: 10.1113/jphysiol.1987.sp016883. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Morel N., Godfraind T. Na-Ca exchange in heart and smooth muscle microsomes. Arch Int Pharmacodyn Ther. 1982 Aug;258(2):319–321. [PubMed] [Google Scholar]
  26. Morris A. P., Gallacher D. V., Irvine R. F., Petersen O. H. Synergism of inositol trisphosphate and tetrakisphosphate in activating Ca2+-dependent K+ channels. Nature. 1987 Dec 17;330(6149):653–655. doi: 10.1038/330653a0. [DOI] [PubMed] [Google Scholar]
  27. Muallem S., Schoeffield M. S., Fimmel C. J., Pandol S. J. Agonist-sensitive calcium pool in the pancreatic acinar cell. II. Characterization of reloading. Am J Physiol. 1988 Aug;255(2 Pt 1):G229–G235. doi: 10.1152/ajpgi.1988.255.2.G229. [DOI] [PubMed] [Google Scholar]
  28. Nabel E. G., Berk B. C., Brock T. A., Smith T. W. Na+-Ca2+ exchange in cultured vascular smooth muscle cells. Circ Res. 1988 Mar;62(3):486–493. doi: 10.1161/01.res.62.3.486. [DOI] [PubMed] [Google Scholar]
  29. Pacaud P., Bolton T. B. Relation between muscarinic receptor cationic current and internal calcium in guinea-pig jejunal smooth muscle cells. J Physiol. 1991 Sep;441:477–499. doi: 10.1113/jphysiol.1991.sp018763. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Pacaud P., Loirand G., Baron A., Mironneau C., Mironneau J. Ca2+ channel activation and membrane depolarization mediated by Cl- channels in response to noradrenaline in vascular myocytes. Br J Pharmacol. 1991 Dec;104(4):1000–1006. doi: 10.1111/j.1476-5381.1991.tb12540.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Pacaud P., Loirand G., Lavie J. L., Mironneau C., Mironneau J. Calcium-activated chloride current in rat vascular smooth muscle cells in short-term primary culture. Pflugers Arch. 1989 Apr;413(6):629–636. doi: 10.1007/BF00581813. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. Penner R., Matthews G., Neher E. Regulation of calcium influx by second messengers in rat mast cells. Nature. 1988 Aug 11;334(6182):499–504. doi: 10.1038/334499a0. [DOI] [PubMed] [Google Scholar]
  34. Putney J. W., Jr A model for receptor-regulated calcium entry. Cell Calcium. 1986 Feb;7(1):1–12. doi: 10.1016/0143-4160(86)90026-6. [DOI] [PubMed] [Google Scholar]
  35. Putney J. W., Jr Biphasic modulation of potassium release in rat parotid gland by carbachol and phenylephrine. J Pharmacol Exp Ther. 1976 Aug;198(2):375–384. [PubMed] [Google Scholar]
  36. Putney J. W., Jr, Takemura H., Hughes A. R., Horstman D. A., Thastrup O. How do inositol phosphates regulate calcium signaling? FASEB J. 1989 Jun;3(8):1899–1905. doi: 10.1096/fasebj.3.8.2542110. [DOI] [PubMed] [Google Scholar]
  37. Sage S. O., Merritt J. E., Hallam T. J., Rink T. J. Receptor-mediated calcium entry in fura-2-loaded human platelets stimulated with ADP and thrombin. Dual-wavelengths studies with Mn2+. Biochem J. 1989 Mar 15;258(3):923–926. doi: 10.1042/bj2580923. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Sage S. O., Rink T. J. The kinetics of changes in intracellular calcium concentration in fura-2-loaded human platelets. J Biol Chem. 1987 Dec 5;262(34):16364–16369. [PubMed] [Google Scholar]
  39. von Tscharner V., Prod'hom B., Baggiolini M., Reuter H. Ion channels in human neutrophils activated by a rise in free cytosolic calcium concentration. 1986 Nov 27-Dec 3Nature. 324(6095):369–372. doi: 10.1038/324369a0. [DOI] [PubMed] [Google Scholar]

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

RESOURCES