Skip to main content
PMC home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1993 Nov;471:563–582. doi: 10.1113/jphysiol.1993.sp019916

Effect of isoprenaline on Ca2+ channel current in single smooth muscle cells isolated from taenia of the guinea-pig caecum.

K Muraki 1, T B Bolton 1, Y Imaizumi 1, M Watanabe 1
PMCID: PMC1143977  PMID: 8120822

Abstract

1. The effects of isoprenaline (Iso) on Ca2+ channel current in enzymatically isolated single cells of the guinea-pig taenia caeci were examined using the standard whole-cell voltage-clamp method. 2. Iso potentiated the voltage-dependent Ca2+ current; the threshold and maximally effective concentration of Iso to increase Ca2+ current were 3-10 nM and 1-3 microM, respectively. The average increase in Ca2+ current produced by 3 microM Iso was 42 +/- 6% (mean +/- S.E.M.) and the response could be obtained repeatedly in the same cell. The concentration-response relationship could be fitted by a binding model with a Hill coefficient of 1 and a dissociation constant of 42 nM. 3. The effect of Iso on Ca2+ current was voltage dependent. Although potentiation of Ca2+ current by Iso was obvious between -30 and +10 mV, it was small or absent around +20 to +30 mV. Iso had little effect on the relationship between inactivation of the Ca2+ current and voltage obtained using a double-pulse protocol. 4. External application of forskolin, an adenylyl cyclase activator, or internal perfusion of cAMP or dibutyryl cAMP from the recording pipette, did not increase Ca2+ current and potentiation of Ca2+ current by Iso was observed repeatedly and was unchanged. 5. Internal perfusion of GTP gamma S or GDP beta S increased or did not affect the Ca2+ current and potentiation of Ca2+ current by Iso was unchanged and could be recorded repeatedly for about 20 min after rupture of the cell membrane. In addition, treatment of cells with the potent protein kinase C inhibitor, chelerythrine, had no effect on Ca2+ current or on potentiation of Ca2+ current by Iso. 6. These results suggest that the Ca2+ current in guinea-pig taenia caeci cells is potentiated by isoprenaline via mechanisms which do not involve either a cAMP pathway, a G-protein pathway or a protein kinase C pathway. The receptor involved appeared to be an atypical adrenoreceptor not blocked by either alpha- or beta-receptor blocking agents.

Full text

PDF
565

Selected References

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

  1. BULBRING E., KURIYAMA H. Effects of changes in ionic environment on the action of acetylcholine and adrenaline on the smooth muscle cells of guinea-pig taenia coli. J Physiol. 1963 Apr;166:59–74. doi: 10.1113/jphysiol.1963.sp007090. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. BURNSTOCK G. The effects of acetylcholine on membrane potential, spike frequency, conduction velocity and excitability in the taenia coli of the guinea-pig. J Physiol. 1958 Aug 29;143(1):165–182. doi: 10.1113/jphysiol.1958.sp006051. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bauer V., Ito Y. Effect of potassium channel blocking agents on the actions of phenylephrine in rabbit taenia caeci. Gen Physiol Biophys. 1991 Apr;10(2):111–124. [PubMed] [Google Scholar]
  4. Bean B. P., Nowycky M. C., Tsien R. W. Beta-adrenergic modulation of calcium channels in frog ventricular heart cells. 1984 Jan 26-Feb 1Nature. 307(5949):371–375. doi: 10.1038/307371a0. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Benham C. D., Bolton T. B. Spontaneous transient outward currents in single visceral and vascular smooth muscle cells of the rabbit. J Physiol. 1986 Dec;381:385–406. doi: 10.1113/jphysiol.1986.sp016333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. 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]
  8. 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]
  9. Bolton T. B. The depolarizing action of acetylcholine or carbachol in intestinal smooth muscle. J Physiol. 1972 Feb;220(3):647–671. doi: 10.1113/jphysiol.1972.sp009728. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Boutjdir M., Méry P. F., Hanf R., Shrier A., Fischmeister R. High affinity forskolin inhibition of L-type Ca2+ current in cardiac cells. Mol Pharmacol. 1990 Dec;38(6):758–765. [PubMed] [Google Scholar]
  11. Bülbring E., Tomita T. Catecholamine action on smooth muscle. Pharmacol Rev. 1987 Mar;39(1):49–96. [PubMed] [Google Scholar]
  12. Bülbring E., Tomita T. Increase of membrane conductance by adrenaline in the smooth muscle of guinea-pig taenia coli. Proc R Soc Lond B Biol Sci. 1969 Mar 11;172(1027):89–102. doi: 10.1098/rspb.1969.0013. [DOI] [PubMed] [Google Scholar]
  13. Bülbring E., Tomita T. The effect of catecholamines on the membrane resistance and spike generation in the smooth muscle of guinea-pig taenia coli. J Physiol. 1968 Feb;194(2):74–6P. [PubMed] [Google Scholar]
  14. Cavalié A., Allen T. J., Trautwein W. Role of the GTP-binding protein Gs in the beta-adrenergic modulation of cardiac Ca channels. Pflugers Arch. 1991 Nov;419(5):433–443. doi: 10.1007/BF00370785. [DOI] [PubMed] [Google Scholar]
  15. Droogmans G., Declerck I., Casteels R. Effect of adrenergic agonists on Ca2+-channel currents in single vascular smooth muscle cells. Pflugers Arch. 1987 Jun;409(1-2):7–12. doi: 10.1007/BF00584744. [DOI] [PubMed] [Google Scholar]
  16. Fukumitsu T., Hayashi H., Tokuno H., Tomita T. Increase in calcium channel current by beta-adrenoceptor agonists in single smooth muscle cells isolated from porcine coronary artery. Br J Pharmacol. 1990 Jul;100(3):593–599. doi: 10.1111/j.1476-5381.1990.tb15852.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Gilman A. G. G proteins: transducers of receptor-generated signals. Annu Rev Biochem. 1987;56:615–649. doi: 10.1146/annurev.bi.56.070187.003151. [DOI] [PubMed] [Google Scholar]
  18. Goto K., Kasuya Y., Matsuki N., Takuwa Y., Kurihara H., Ishikawa T., Kimura S., Yanagisawa M., Masaki T. Endothelin activates the dihydropyridine-sensitive, voltage-dependent Ca2+ channel in vascular smooth muscle. Proc Natl Acad Sci U S A. 1989 May;86(10):3915–3918. doi: 10.1073/pnas.86.10.3915. [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. Hartzell H. C., Fischmeister R. Effect of forskolin and acetylcholine on calcium current in single isolated cardiac myocytes. Mol Pharmacol. 1987 Nov;32(5):639–645. [PubMed] [Google Scholar]
  21. Hartzell H. C., Méry P. F., Fischmeister R., Szabo G. Sympathetic regulation of cardiac calcium current is due exclusively to cAMP-dependent phosphorylation. Nature. 1991 Jun 13;351(6327):573–576. doi: 10.1038/351573a0. [DOI] [PubMed] [Google Scholar]
  22. Herbert J. M., Augereau J. M., Gleye J., Maffrand J. P. Chelerythrine is a potent and specific inhibitor of protein kinase C. Biochem Biophys Res Commun. 1990 Nov 15;172(3):993–999. doi: 10.1016/0006-291x(90)91544-3. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. Kameyama M., Hescheler J., Hofmann F., Trautwein W. Modulation of Ca current during the phosphorylation cycle in the guinea pig heart. Pflugers Arch. 1986 Aug;407(2):123–128. doi: 10.1007/BF00580662. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. 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]
  27. Koch W. J., Ellinor P. T., Schwartz A. cDNA cloning of a dihydropyridine-sensitive calcium channel from rat aorta. Evidence for the existence of alternatively spliced forms. J Biol Chem. 1990 Oct 15;265(29):17786–17791. [PubMed] [Google Scholar]
  28. 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]
  29. Marks T. N., Dubyak G. R., Jones S. W. Calcium currents in the A7r5 smooth muscle-derived cell line. Pflugers Arch. 1990 Dec;417(4):433–439. doi: 10.1007/BF00370664. [DOI] [PubMed] [Google Scholar]
  30. McCarron J. G., McGeown J. G., Reardon S., Ikebe M., Fay F. S., Walsh J. V., Jr Calcium-dependent enhancement of calcium current in smooth muscle by calmodulin-dependent protein kinase II. Nature. 1992 May 7;357(6373):74–77. doi: 10.1038/357074a0. [DOI] [PubMed] [Google Scholar]
  31. Nakazawa K., Saito H., Matsuki N. Effects of calcitonin gene-related peptide (CGRP) on Ca(2+)-channel current of isolated smooth muscle cells from rat vas deferens. Naunyn Schmiedebergs Arch Pharmacol. 1992 Nov;346(5):515–522. doi: 10.1007/BF00169006. [DOI] [PubMed] [Google Scholar]
  32. Nilius B., Hess P., Lansman J. B., Tsien R. W. A novel type of cardiac calcium channel in ventricular cells. Nature. 1985 Aug 1;316(6027):443–446. doi: 10.1038/316443a0. [DOI] [PubMed] [Google Scholar]
  33. Nishimura J., Moreland S., Ahn H. Y., Kawase T., Moreland R. S., van Breemen C. Endothelin increases myofilament Ca2+ sensitivity in alpha-toxin-permeabilized rabbit mesenteric artery. Circ Res. 1992 Oct;71(4):951–959. doi: 10.1161/01.res.71.4.951. [DOI] [PubMed] [Google Scholar]
  34. 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]
  35. Ohya Y., Sperelakis N. Involvement of a GTP-binding protein in stimulating action of angiotensin II on calcium channels in vascular smooth muscle cells. Circ Res. 1991 Mar;68(3):763–771. doi: 10.1161/01.res.68.3.763. [DOI] [PubMed] [Google Scholar]
  36. Oike M., Kitamura K., Kuriyama H. Histamine H3-receptor activation augments voltage-dependent Ca2+ current via GTP hydrolysis in rabbit saphenous artery. J Physiol. 1992 Mar;448:133–152. doi: 10.1113/jphysiol.1992.sp019033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. 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]
  38. Quist E., Powell P., Vasan R. Guanylnucleotide specificity for muscarinic receptor inhibitory coupling to cardiac adenylate cyclase. Mol Pharmacol. 1992 Jan;41(1):177–184. [PubMed] [Google Scholar]
  39. Rusko J., Bauer V. Calcium and the activation of the alpha 1-adrenoceptors in the guinea-pig taenia caeci. Br J Pharmacol. 1988 Jun;94(2):557–565. doi: 10.1111/j.1476-5381.1988.tb11561.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Rusko J., Bolton T. B., Aaronson P., Bauer V. Effects of phenylephrine in single isolated smooth muscle cells of rabbit and guinea pig taenia caeci. Eur J Pharmacol. 1990 Aug 10;184(2-3):325–328. doi: 10.1016/0014-2999(90)90626-h. [DOI] [PubMed] [Google Scholar]
  41. Scamps F., Rybin V., Puceat M., Tkachuk V., Vassort G. A Gs protein couples P2-purinergic stimulation to cardiac Ca channels without cyclic AMP production. J Gen Physiol. 1992 Oct;100(4):675–701. doi: 10.1085/jgp.100.4.675. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Shimada T., Somlyo A. P. Modulation of voltage-dependent Ca channel current by arachidonic acid and other long-chain fatty acids in rabbit intestinal smooth muscle. J Gen Physiol. 1992 Jul;100(1):27–44. doi: 10.1085/jgp.100.1.27. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Tiaho F., Nargeot J., Richard S. Voltage-dependent regulation of L-type cardiac Ca channels by isoproterenol. Pflugers Arch. 1991 Dec;419(6):596–602. doi: 10.1007/BF00370301. [DOI] [PubMed] [Google Scholar]
  44. Tokuno H., Tomita T. Collagenase eliminates the electrical responses of smooth muscle to catecholamines. Eur J Pharmacol. 1987 Sep 2;141(1):131–133. doi: 10.1016/0014-2999(87)90419-5. [DOI] [PubMed] [Google Scholar]
  45. Tomasic M., Boyle J. P., Worley J. F., 3rd, Kotlikoff M. I. Contractile agonists activate voltage-dependent calcium channels in airway smooth muscle cells. Am J Physiol. 1992 Jul;263(1 Pt 1):C106–C113. doi: 10.1152/ajpcell.1992.263.1.C106. [DOI] [PubMed] [Google Scholar]
  46. Usuki T., Obara K., Someya T., Ozaki H., Karaki H., Fusetani N., Yabu H. Calyculin A increases voltage-dependent inward current in smooth muscle cells isolated from guinea pig taenia coli. Experientia. 1991 Sep 15;47(9):939–941. doi: 10.1007/BF01929886. [DOI] [PubMed] [Google Scholar]
  47. Welling A., Felbel J., Peper K., Hofmann F. Hormonal regulation of calcium current in freshly isolated airway smooth muscle cells. Am J Physiol. 1992 Mar;262(3 Pt 1):L351–L359. doi: 10.1152/ajplung.1992.262.3.L351. [DOI] [PubMed] [Google Scholar]
  48. Worley J. F., Quayle J. M., Standen N. B., Nelson M. T. Regulation of single calcium channels in cerebral arteries by voltage, serotonin, and dihydropyridines. Am J Physiol. 1991 Dec;261(6 Pt 2):H1951–H1960. doi: 10.1152/ajpheart.1991.261.6.H1951. [DOI] [PubMed] [Google Scholar]
  49. Yatani A., Brown A. M. Rapid beta-adrenergic modulation of cardiac calcium channel currents by a fast G protein pathway. Science. 1989 Jul 7;245(4913):71–74. doi: 10.1126/science.2544999. [DOI] [PubMed] [Google Scholar]
  50. Yatani A., Imoto Y., Codina J., Hamilton S. L., Brown A. M., Birnbaumer L. The stimulatory G protein of adenylyl cyclase, Gs, also stimulates dihydropyridine-sensitive Ca2+ channels. Evidence for direct regulation independent of phosphorylation by cAMP-dependent protein kinase or stimulation by a dihydropyridine agonist. J Biol Chem. 1988 Jul 15;263(20):9887–9895. [PubMed] [Google Scholar]
  51. Yoshino M., Someya T., Nishio A., Yazawa K., Usuki T., Yabu H. Multiple types of voltage-dependent Ca channels in mammalian intestinal smooth muscle cells. Pflugers Arch. 1989 Aug;414(4):401–409. doi: 10.1007/BF00585049. [DOI] [PubMed] [Google Scholar]

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

RESOURCES