Skip to main content
PMC home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1993 Nov;471:87–105. doi: 10.1113/jphysiol.1993.sp019892

Evidence for multiple open states of the Ca2+ channels in smooth muscle cells isolated from the guinea-pig detrusor.

S Nakayama 1, A F Brading 1
PMCID: PMC1143953  PMID: 8120836

Abstract

1. Whole-cell voltage clamp techniques were used to examine the properties of voltage-dependent Ca2+ channel currents in single smooth muscle cells enzymatically dissociated from guinea-pig urinary bladder. Potassium currents were blocked with intracellular Cs+. A holding potential of -60 mV was normally applied. 2. When the membrane potential was returned to the holding potential after a depolarizing step, tail currents were seen after depolarizations to positive potentials, and the size of the tail current increased with increasing positivity of the preceding depolarization. 3. After depolarization to +80 mV (a potential at which little inward current flowed through the Ca2+ channels) tail currents on returning to the holding potential increased in size as the duration of the depolarization was increased. 4. Investigation of the mechanism mediating the tail currents showed that they were not flowing through non-selective cation channels, and had no contribution from Ca(2+)-activated Cl- channels or Na(+)-Ca2+ exchange. 5. The tail currents and the inward currents evoked by a simple depolarizing test potential were equally decreased by nifedipine in a dose-dependent manner. This suggests that L-type Ca2+ channels are responsible for both of the two types of inward currents. The inward currents were also inhibited in a similar manner when caffeine was applied. 6. Although the tail currents evoked on stepping from +80 mV to a holding potential of -60 mV increased in size with the duration of the conditioning potential, the total membrane Ca2+ conductance did not increase, since the inward currents evoked on stepping to +20 mV (a potential at which the Ca2+ channels are still fully activated) did not change with time. 7. The amplitude of the inward current evoked by a simple depolarizing test potential was similar to that evoked on stepping to the same test potential after preconditioning at +80 mV, if the test potential was higher than +20 mV. However, following repolarization to the holding potential, the amplitude of the subsequent tail current was larger and the deactivation time constant longer, after the conditioning depolarization. These results suggest that the voltage-dependent Ca2+ channels have at least two open states with different time constants, the tail current being the result of a long open channel state induced by large depolarizations. 8. When variable repolarizing potentials were applied after n +80 mV depolarization (5 s), the current-voltage relationship of the tail current was nearly linear between -60 and +30 mV. The deactivation was faster when a larger repolarization step was applied.(ABSTRACT TRUNCATED AT 400 WORDS)

Full text

PDF
87

Selected References

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

  1. Aaronson P. I., Bolton T. B., Lang R. J., MacKenzie I. Calcium currents in single isolated smooth muscle cells from the rabbit ear artery in normal-calcium and high-barium solutions. J Physiol. 1988 Nov;405:57–75. doi: 10.1113/jphysiol.1988.sp017321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Amédée T., Large W. A., Wang Q. Characteristics of chloride currents activated by noradrenaline in rabbit ear artery cells. J Physiol. 1990 Sep;428:501–516. doi: 10.1113/jphysiol.1990.sp018224. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bean B. P. Classes of calcium channels in vertebrate cells. Annu Rev Physiol. 1989;51:367–384. doi: 10.1146/annurev.ph.51.030189.002055. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Creed K. E. Effects of ions and drugs on the smooth muscle cell membrane of the guinea-pig urinary bladder. Pflugers Arch. 1971;326(2):127–141. doi: 10.1007/BF00586905. [DOI] [PubMed] [Google Scholar]
  6. Endo M. Calcium release from the sarcoplasmic reticulum. Physiol Rev. 1977 Jan;57(1):71–108. doi: 10.1152/physrev.1977.57.1.71. [DOI] [PubMed] [Google Scholar]
  7. Evans M. G., Marty A. Calcium-dependent chloride currents in isolated cells from rat lacrimal glands. J Physiol. 1986 Sep;378:437–460. doi: 10.1113/jphysiol.1986.sp016229. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. Ganitkevich V Y. a., Isenberg G. Depolarization-mediated intracellular calcium transients in isolated smooth muscle cells of guinea-pig urinary bladder. J Physiol. 1991 Apr;435:187–205. doi: 10.1113/jphysiol.1991.sp018505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hagiwara S., Ohmori H. Studies of calcium channels in rat clonal pituitary cells with patch electrode voltage clamp. J Physiol. 1982 Oct;331:231–252. doi: 10.1113/jphysiol.1982.sp014371. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hess P., Lansman J. B., Tsien R. W. Calcium channel selectivity for divalent and monovalent cations. Voltage and concentration dependence of single channel current in ventricular heart cells. J Gen Physiol. 1986 Sep;88(3):293–319. doi: 10.1085/jgp.88.3.293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hoshi T., Smith S. J. Large depolarization induces long openings of voltage-dependent calcium channels in adrenal chromaffin cells. J Neurosci. 1987 Feb;7(2):571–580. doi: 10.1523/JNEUROSCI.07-02-00571.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hughes A. D., Hering S., Bolton T. B. The action of caffeine on inward barium current through voltage-dependent calcium channels in single rabbit ear artery cells. Pflugers Arch. 1990 Jun;416(4):462–466. doi: 10.1007/BF00370755. [DOI] [PubMed] [Google Scholar]
  14. Inoue R., Brading A. F. The properties of the ATP-induced depolarization and current in single cells isolated from the guinea-pig urinary bladder. Br J Pharmacol. 1990 Jul;100(3):619–625. doi: 10.1111/j.1476-5381.1990.tb15856.x. [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. Klöckner U., Isenberg G. Calcium currents of cesium loaded isolated smooth muscle cells (urinary bladder of the guinea pig). Pflugers Arch. 1985 Dec;405(4):340–348. doi: 10.1007/BF00595686. [DOI] [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. Lang R. J. The whole-cell Ca2+ channel current in single smooth muscle cells of the guinea-pig ureter. J Physiol. 1990 Apr;423:453–473. doi: 10.1113/jphysiol.1990.sp018033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Lansman J. B., Hess P., Tsien R. W. Blockade of current through single calcium channels by Cd2+, Mg2+, and Ca2+. Voltage and concentration dependence of calcium entry into the pore. J Gen Physiol. 1986 Sep;88(3):321–347. doi: 10.1085/jgp.88.3.321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Loirand G., Pacaud P., Baron A., Mironneau C., Mironneau J. Large conductance calcium-activated non-selective cation channel in smooth muscle cells isolated from rat portal vein. J Physiol. 1991 Jun;437:461–475. doi: 10.1113/jphysiol.1991.sp018606. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Marks T. N., Jones S. W. Calcium currents in the A7r5 smooth muscle-derived cell line. An allosteric model for calcium channel activation and dihydropyridine agonist action. J Gen Physiol. 1992 Mar;99(3):367–390. doi: 10.1085/jgp.99.3.367. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Martin C., Dacquet C., Mironneau C., Mironneau J. Caffeine-induced inhibition of calcium channel current in cultured smooth cells from pregnant rat myometrium. Br J Pharmacol. 1989 Oct;98(2):493–498. doi: 10.1111/j.1476-5381.1989.tb12622.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Matsuda J. J., Volk K. A., Shibata E. F. Calcium currents in isolated rabbit coronary arterial smooth muscle myocytes. J Physiol. 1990 Aug;427:657–680. doi: 10.1113/jphysiol.1990.sp018192. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Nakayama S., Brading A. F. Inactivation of the voltage-dependent Ca2+ channel current in smooth muscle cells isolated from the guinea-pig detrusor. J Physiol. 1993 Nov;471:107–127. doi: 10.1113/jphysiol.1993.sp019893. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. 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]
  26. Pelzer D., Pelzer S., McDonald T. F. Properties and regulation of calcium channels in muscle cells. Rev Physiol Biochem Pharmacol. 1990;114:107–207. doi: 10.1007/BFb0031019. [DOI] [PubMed] [Google Scholar]
  27. Pietrobon D., Hess P. Novel mechanism of voltage-dependent gating in L-type calcium channels. Nature. 1990 Aug 16;346(6285):651–655. doi: 10.1038/346651a0. [DOI] [PubMed] [Google Scholar]

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

RESOURCES