Skip to main content
PMC home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1993 Apr;463:565–583. doi: 10.1113/jphysiol.1993.sp019611

Inhibitory effects of histamine and bradykinin on calcium current in smooth muscle cells isolated from guinea-pig ileum.

D J Beech 1
PMCID: PMC1175360  PMID: 8246198

Abstract

1. Single smooth muscle cells were isolated from the longitudinal muscle layer of the guinea-pig ileum and within 10 h Ca(2+)-currents (ICa) were recorded using the whole-cell patch clamp technique. 2. Histamine (10 microMs) and bradykinin (BK, 1 microM) suppressed ICa; the effect had two phases: a rapid and transient suppression of ICa followed by a sustained suppression. Acetylcholine and substance P appeared to have similar effects but these were not investigated in detail. 3. The effects of histamine and BK on ICa were established by high intracellular concentrations of the Ca2+ buffer EGTA (30 mM) or 1,2-bis(O-aminophenoxy)ethane-N,N,N',N'-tetraacetic acid (BAPTA) (5 mM) in the absence of Ca2+ added to the pipette solution. When [Ca2+]i was strongly buffered to 125 or 190 nM by BAPTA-Ca2+ mixtures in the pipette the transient suppression of ICa was blocked but the sustained effect still occurred. This indicated that the transient effect was caused by a rise in [Ca2+]i. The sustained effect, in contrast, did not seem to be caused by a rise in [Ca2+]i but did show Ca2+ dependence because it did not occur if [Ca2+]i was abnormally low. 4. Application of caffeine (10 mM) to deplete stored Ca2+ or intracellular heparin (1 mM) to block the action of D-myo-inositol 1,4,5-trisphosphate (IP3) to release stored Ca2+ prevented the transient but not the sustained suppression of ICa. Heparin also blocked the transient Ca(2+)-activated K+ current in response to histamine or BK. Both transient and sustained suppressions of Ca2+ channel activity were observed in the absence of extracellular Ca2+ when current was carried mostly by Na+ ions. 5. Intracellular guanosine 5'-O-(3-thiotriphosphate) (GTP-gamma-S; 10 or 100 microM) induced a gradual decline of ICa upon which transient decreases of current were superimposed. Histamine caused a larger than normal inhibition of ICa and no recovery occurred on wash-out. Intracellular guanosine 5'-O-(2-thiodiphosphate) (GDP-beta-S; 1 mM) abolished the effects of histamine and BK on ICa.(ABSTRACT TRUNCATED AT 400 WORDS)

Full text

PDF
569

Selected References

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

  1. Anwyl R. Modulation of vertebrate neuronal calcium channels by transmitters. Brain Res Brain Res Rev. 1991 Sep-Dec;16(3):265–281. doi: 10.1016/0165-0173(91)90010-6. [DOI] [PubMed] [Google Scholar]
  2. Baraban J. M., Gould R. J., Peroutka S. J., Snyder S. H. Phorbol ester effects on neurotransmission: interaction with neurotransmitters and calcium in smooth muscle. Proc Natl Acad Sci U S A. 1985 Jan;82(2):604–607. doi: 10.1073/pnas.82.2.604. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Beech D. J., Bernheim L., Mathie A., Hille B. Intracellular Ca2+ buffers disrupt muscarinic suppression of Ca2+ current and M current in rat sympathetic neurons. Proc Natl Acad Sci U S A. 1991 Jan 15;88(2):652–656. doi: 10.1073/pnas.88.2.652. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Best L., Brooks K. J., Bolton T. B. Relationship between stimulated inositol lipid hydrolysis and contractility in guinea-pig visceral longitudinal smooth muscle. Biochem Pharmacol. 1985 Jul 1;34(13):2297–2301. doi: 10.1016/0006-2952(85)90785-3. [DOI] [PubMed] [Google Scholar]
  5. Birnbaumer L., Abramowitz J., Brown A. M. Receptor-effector coupling by G proteins. Biochim Biophys Acta. 1990 May 7;1031(2):163–224. doi: 10.1016/0304-4157(90)90007-y. [DOI] [PubMed] [Google Scholar]
  6. Bolton T. B., Clark J. P., Kitamura K., Lang R. J. Evidence that histamine and carbachol may open the same ion channels in longitudinal smooth muscle of guinea-pig ileum. J Physiol. 1981 Nov;320:363–379. doi: 10.1113/jphysiol.1981.sp013955. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. DAY M., VANE J. R. An analysis of the direct and indirect actions of drugs on the isolated guinea-pig ileum. Br J Pharmacol Chemother. 1963 Feb;20:150–170. doi: 10.1111/j.1476-5381.1963.tb01306.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Declerck I., Himpens B., Droogmans G., Casteels R. The alpha 1-agonist phenylephrine inhibits voltage-gated Ca2(+)-channels in vascular smooth muscle cells of rabbit ear artery. Pflugers Arch. 1990 Sep;417(1):117–119. doi: 10.1007/BF00370780. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Eckert R., Chad J. E. Inactivation of Ca channels. Prog Biophys Mol Biol. 1984;44(3):215–267. doi: 10.1016/0079-6107(84)90009-9. [DOI] [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. Hall D. W., Bonta I. L. The biphasic response of the isolated guinea-pig ileum by bradykinin. Eur J Pharmacol. 1973 Feb;21(2):147–154. doi: 10.1016/0014-2999(73)90219-7. [DOI] [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. Himpens B., Droogmans G., Casteels R. Carbachol-induced nonspecific desensitization in guinea-pig ileum. Naunyn Schmiedebergs Arch Pharmacol. 1991 Jun;343(6):580–587. doi: 10.1007/BF00184288. [DOI] [PubMed] [Google Scholar]
  15. Holzer P., Lippe I. T. Substance P can contract the longitudinal muscle of the guinea-pig small intestine by releasing intracellular calcium. Br J Pharmacol. 1984 May;82(1):259–267. doi: 10.1111/j.1476-5381.1984.tb16466.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Horio S., Shima M., Ueda H., Ishida Y. Temperature-dependence of desensitization induced by acetylcholine and histamine in guinea-pig ileal longitudinal muscle. Br J Pharmacol. 1990 Jul;100(3):636–640. doi: 10.1111/j.1476-5381.1990.tb15859.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Horn R., Marty A. Muscarinic activation of ionic currents measured by a new whole-cell recording method. J Gen Physiol. 1988 Aug;92(2):145–159. doi: 10.1085/jgp.92.2.145. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Imaizumi Y., Takeda M., Muraki K., Watanabe M. Mechanisms of NE-induced reduction of Ca current in single smooth muscle cells from guinea pig vas deferens. Am J Physiol. 1991 Jan;260(1 Pt 1):C17–C25. doi: 10.1152/ajpcell.1991.260.1.C17. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. Jafferji S. S., Michell R. H. Stimulation of phosphatidylinositol turnover by histamine, 5-hydroxytryptamine and adrenaline in the longitudinal smooth muscle of guinea pig ileum. Biochem Pharmacol. 1976 Jun 15;25(12):1429–1430. doi: 10.1016/0006-2952(76)90115-5. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. Komori S., Bolton T. B. Inositol trisphosphate releases stored calcium to block voltage-dependent calcium channels in single smooth muscle cells. Pflugers Arch. 1991 Jun;418(5):437–441. doi: 10.1007/BF00497770. [DOI] [PubMed] [Google Scholar]
  23. Komori S., Kawai M., Takewaki T., Ohashi H. GTP-binding protein involvement in membrane currents evoked by carbachol and histamine in guinea-pig ileal muscle. J Physiol. 1992 May;450:105–126. doi: 10.1113/jphysiol.1992.sp019118. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kramer R. H., Kaczmarek L. K., Levitan E. S. Neuropeptide inhibition of voltage-gated calcium channels mediated by mobilization of intracellular calcium. Neuron. 1991 Apr;6(4):557–563. doi: 10.1016/0896-6273(91)90058-8. [DOI] [PubMed] [Google Scholar]
  25. Mitsui M., Karaki H. Dual effects of carbachol on cytosolic Ca2+ and contraction in intestinal smooth muscle. Am J Physiol. 1990 May;258(5 Pt 1):C787–C793. doi: 10.1152/ajpcell.1990.258.5.C787. [DOI] [PubMed] [Google Scholar]
  26. Murphy T. H., Worley P. F., Baraban J. M. L-type voltage-sensitive calcium channels mediate synaptic activation of immediate early genes. Neuron. 1991 Oct;7(4):625–635. doi: 10.1016/0896-6273(91)90375-a. [DOI] [PubMed] [Google Scholar]
  27. Ohya Y., Kitamura K., Kuriyama H. Regulation of calcium current by intracellular calcium in smooth muscle cells of rabbit portal vein. Circ Res. 1988 Feb;62(2):375–383. doi: 10.1161/01.res.62.2.375. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. Pacaud P., Loirand G., Mironneau C., Mironneau J. Opposing effects of noradrenaline on the two classes of voltage-dependent calcium channels of single vascular smooth muscle cells in short-term primary culture. Pflugers Arch. 1987 Nov;410(4-5):557–559. doi: 10.1007/BF00586539. [DOI] [PubMed] [Google Scholar]
  30. Ransom R. W., Goodman C. B., Young G. S. Bradykinin stimulation of phosphoinositide hydrolysis in guinea-pig ileum longitudinal muscle. Br J Pharmacol. 1992 Apr;105(4):919–924. doi: 10.1111/j.1476-5381.1992.tb09078.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Schneider P., Hopp H. H., Isenberg G. Ca2+ influx through ATP-gated channels increments [Ca2+]i and inactivates ICa in myocytes from guinea-pig urinary bladder. J Physiol. 1991;440:479–496. doi: 10.1113/jphysiol.1991.sp018720. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Tsien R. Y. New calcium indicators and buffers with high selectivity against magnesium and protons: design, synthesis, and properties of prototype structures. Biochemistry. 1980 May 27;19(11):2396–2404. doi: 10.1021/bi00552a018. [DOI] [PubMed] [Google Scholar]
  33. Wang R., Karpinski E., Pang P. K. Parathyroid hormone selectively inhibits L-type calcium channels in single vascular smooth muscle cells of the rat. J Physiol. 1991 Sep;441:325–346. doi: 10.1113/jphysiol.1991.sp018754. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Xiong Z. L., Kitamura K., Kuriyama H. ATP activates cationic currents and modulates the calcium current through GTP-binding protein in rabbit portal vein. J Physiol. 1991;440:143–165. doi: 10.1113/jphysiol.1991.sp018701. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Zholos A. V., Baidan L. V., Shuba M. F. The inhibitory action of caffeine on calcium currents in isolated intestinal smooth muscle cells. Pflugers Arch. 1991 Oct;419(3-4):267–273. doi: 10.1007/BF00371106. [DOI] [PubMed] [Google Scholar]

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

RESOURCES