Skip to main content
NCBI home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1983 Sep;342:309–325. doi: 10.1113/jphysiol.1983.sp014852

A transient calcium-dependent chloride current in the immature Xenopus oocyte.

M E Barish
PMCID: PMC1193960  PMID: 6313909

Abstract

Ionic currents were studied in immature full-grown Xenopus oocytes using the two-micro-electrode voltage-clamp technique. Recordings of total membrane current showed a transient outward peak during depolarizations from the approximate resting voltage (-70 or -80 mV) to voltages more positive than -20 mV. The current-voltage relation for peak outward current was U-shaped, with a maximum at about 0 mV. Replacement of external Cl with methanesulphonate reversed this transient outward current to a transient inward current. Current relaxations recorded after the membrane potential was stepped to different voltages at the time of the peak showed a component that inverted at about -25 to -30 mV. This value was close to ECl as determined by measurement of the intracellular Cl ion concentration. The reversal potential for these current relaxations changed with the external Cl concentration as predicted by the Nernst relation. Replacement of external Ca with Mg, Sr or Ba, or addition of low concentrations of Ni in the presence of Ca, eliminated the transient outward current. Increasing the external Ca concentration increased the amplitude of the transient outward current without affecting the amplitude of the steady-state current. It was concluded that the outward peak in records of total membrane current represented the contribution of a transient outward current carried by Cl ions which was dependent on the entry of external Ca. It will be noted as ICl(Ca). Decay of ICl(Ca) could be described at the normal Ca concentration by a single exponential function whose time constant showed a shallow U-shaped voltage dependence. ICl(Ca) was maximally activatable by depolarizations from a holding potential of about -100 mV, but could not be activated by depolarizations from -40 mV. The amplitude of ICl(Ca) showed a large temperature dependence as compared to the steady-state current, suggesting complex control of its activation.

Full text

PDF
309

Selected References

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

  1. Baud C., Kado R. T., Marcher K. Sodium channels induced by depolarization of the Xenopus laevis oocyte. Proc Natl Acad Sci U S A. 1982 May;79(10):3188–3192. doi: 10.1073/pnas.79.10.3188. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Brehm P., Eckert R. Calcium entry leads to inactivation of calcium channel in Paramecium. Science. 1978 Dec 15;202(4373):1203–1206. doi: 10.1126/science.103199. [DOI] [PubMed] [Google Scholar]
  3. Byerly L., Hagiwara S. Calcium currents in internally perfused nerve cell bodies of Limnea stagnalis. J Physiol. 1982 Jan;322:503–528. doi: 10.1113/jphysiol.1982.sp014052. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Colquhoun D., Neher E., Reuter H., Stevens C. F. Inward current channels activated by intracellular Ca in cultured cardiac cells. Nature. 1981 Dec 24;294(5843):752–754. doi: 10.1038/294752a0. [DOI] [PubMed] [Google Scholar]
  5. Connor J. A., Stevens C. F. Voltage clamp studies of a transient outward membrane current in gastropod neural somata. J Physiol. 1971 Feb;213(1):21–30. doi: 10.1113/jphysiol.1971.sp009365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cross N. L., Elinson R. P. A fast block to polyspermy in frogs mediated by changes in the membrane potential. Dev Biol. 1980 Mar;75(1):187–198. doi: 10.1016/0012-1606(80)90154-2. [DOI] [PubMed] [Google Scholar]
  7. Cross N. L. Initiation of the activation potential by an increase in intracellular calcium in eggs of the frog, Rana pipiens. Dev Biol. 1981 Jul 30;85(2):380–384. doi: 10.1016/0012-1606(81)90269-4. [DOI] [PubMed] [Google Scholar]
  8. Cuthbertson K. S., Whittingham D. G., Cobbold P. H. Free Ca2+ increases in exponential phases during mouse oocyte activation. Nature. 1981 Dec 24;294(5843):754–757. doi: 10.1038/294754a0. [DOI] [PubMed] [Google Scholar]
  9. Dascal N., Landau E. M. Types of muscarinic response in Xenopus oocytes. Life Sci. 1980 Oct 13;27(15):1423–1428. doi: 10.1016/0024-3205(80)90407-5. [DOI] [PubMed] [Google Scholar]
  10. Dick D. A., McLaughlin S. G. The activities and concentrations of sodium and potassium in toad oocytes. J Physiol. 1969 Nov;205(1):61–78. doi: 10.1113/jphysiol.1969.sp008951. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dumont J. N. Oogenesis in Xenopus laevis (Daudin). I. Stages of oocyte development in laboratory maintained animals. J Morphol. 1972 Feb;136(2):153–179. doi: 10.1002/jmor.1051360203. [DOI] [PubMed] [Google Scholar]
  12. Fox A. P. Voltage-dependent inactivation of a calcium channel. Proc Natl Acad Sci U S A. 1981 Feb;78(2):953–956. doi: 10.1073/pnas.78.2.953. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gorman A. L., Hermann A. Internal effects of divalent cations on potassium permeability in molluscan neurones. J Physiol. 1979 Nov;296:393–410. doi: 10.1113/jphysiol.1979.sp013012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gorman A. L., Thomas M. V. Intracellular calcium accumulation during depolarization in a molluscan neurone. J Physiol. 1980 Nov;308:259–285. doi: 10.1113/jphysiol.1980.sp013471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Grey R. D., Bastiani M. J., Webb D. J., Schertel E. R. An electrical block is required to prevent polyspermy in eggs fertilized by natural mating of Xenopus laevis. Dev Biol. 1982 Feb;89(2):475–484. doi: 10.1016/0012-1606(82)90335-9. [DOI] [PubMed] [Google Scholar]
  16. HAGIWARA S., KUSANO K., SAITO N. Membrane changes of Onchidium nerve cell in potassium-rich media. J Physiol. 1961 Mar;155:470–489. doi: 10.1113/jphysiol.1961.sp006640. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hagiwara S., Byerly L. Calcium channel. Annu Rev Neurosci. 1981;4:69–125. doi: 10.1146/annurev.ne.04.030181.000441. [DOI] [PubMed] [Google Scholar]
  18. Hagiwara S., Fukuda J., Eaton D. C. Membrane currents carried by Ca, Sr, and Ba in barnacle muscle fiber during voltage clamp. J Gen Physiol. 1974 May;63(5):564–578. doi: 10.1085/jgp.63.5.564. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hagiwara S., Jaffe L. A. Electrical properties of egg cell membranes. Annu Rev Biophys Bioeng. 1979;8:385–416. doi: 10.1146/annurev.bb.08.060179.002125. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. Hagiwara S., Ozawa S., Sand O. Voltage clamp analysis of two inward current mechanisms in the egg cell membrane of a starfish. J Gen Physiol. 1975 May;65(5):617–644. doi: 10.1085/jgp.65.5.617. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hagiwara S., Takahashi K. Surface density of calcium ions and calcium spikes in the barnacle muscle fiber membrane. J Gen Physiol. 1967 Jan;50(3):583–601. doi: 10.1085/jgp.50.3.583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Hermann A., Gorman A. L. Blockade of voltage-dependent and Ca2+-dependent K+ current components by internal Ba2+ in molluscan pacemaker neurons. Experientia. 1979 Feb 15;35(2):229–231. doi: 10.1007/BF01920633. [DOI] [PubMed] [Google Scholar]
  24. Katz B., Miledi R. A study of synaptic transmission in the absence of nerve impulses. J Physiol. 1967 Sep;192(2):407–436. doi: 10.1113/jphysiol.1967.sp008307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Katz B., Miledi R. Suppression of transmitter release at the neuromuscular junction. Proc R Soc Lond B Biol Sci. 1977 Apr;196(1125):465–469. doi: 10.1098/rspb.1977.0051. [DOI] [PubMed] [Google Scholar]
  26. Kusano K., Miledi R., Stinnakre J. Acetylcholine receptors in the oocyte membrane. Nature. 1977 Dec 22;270(5639):739–741. doi: 10.1038/270739a0. [DOI] [PubMed] [Google Scholar]
  27. Kusano K., Miledi R., Stinnakre J. Cholinergic and catecholaminergic receptors in the Xenopus oocyte membrane. J Physiol. 1982 Jul;328:143–170. doi: 10.1113/jphysiol.1982.sp014257. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Lotan I., Dascal N., Cohen S., Lass Y. Adenosine-induced slow ionic currents in the Xenopus oocyte. Nature. 1982 Aug 5;298(5874):572–574. doi: 10.1038/298572a0. [DOI] [PubMed] [Google Scholar]
  29. MAENO T. Electrical characteristics and activation potential of Bufo eggs. J Gen Physiol. 1959 Sep;43:139–157. doi: 10.1085/jgp.43.1.139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Masui Y. Relative roles of the pituitary, follicle cells, and progesterone in the induction of oocyte maturation in Rana pipiens. J Exp Zool. 1967 Dec;166(3):365–375. doi: 10.1002/jez.1401660309. [DOI] [PubMed] [Google Scholar]
  31. Meech R. W., Standen N. B. Potassium activation in Helix aspersa neurones under voltage clamp: a component mediated by calcium influx. J Physiol. 1975 Jul;249(2):211–239. doi: 10.1113/jphysiol.1975.sp011012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Miledi R. A calcium-dependent transient outward current in Xenopus laevis oocytes. Proc R Soc Lond B Biol Sci. 1982 Jul 22;215(1201):491–497. doi: 10.1098/rspb.1982.0056. [DOI] [PubMed] [Google Scholar]
  33. Neher E. Two fast transient current components during voltage clamp on snail neurons. J Gen Physiol. 1971 Jul;58(1):36–53. doi: 10.1085/jgp.58.1.36. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Ohmori H., Yoshii M. Surface potential reflected in both gating and permeation mechanisms of sodium and calcium channels of the tunicate egg cell membrane. J Physiol. 1977 May;267(2):429–463. doi: 10.1113/jphysiol.1977.sp011821. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Palmer L. G., Century T. J., Civan M. M. Activity coefficients of intracellular Na+ and K+ during development of frog oocytes. J Membr Biol. 1978 Apr 20;40(1):25–38. doi: 10.1007/BF01909737. [DOI] [PubMed] [Google Scholar]
  36. Ridgway E. B., Gilkey J. C., Jaffe L. F. Free calcium increases explosively in activating medaka eggs. Proc Natl Acad Sci U S A. 1977 Feb;74(2):623–627. doi: 10.1073/pnas.74.2.623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Robinson K. R. Electrical currents through full-grown and maturing Xenopus oocytes. Proc Natl Acad Sci U S A. 1979 Feb;76(2):837–841. doi: 10.1073/pnas.76.2.837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Schlichter L. C., Elinson R. P. Electrical responses of immature and mature Rana pipiens oocytes to sperm and other activating stimuli. Dev Biol. 1981 Apr 15;83(1):33–41. doi: 10.1016/s0012-1606(81)80005-x. [DOI] [PubMed] [Google Scholar]
  39. Sharp A. P., Thomas R. C. The effects of chloride substitution on intracellular pH in crab muscle. J Physiol. 1981 Mar;312:71–80. doi: 10.1113/jphysiol.1981.sp013616. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Siegelbaum S. A., Tsien R. W. Calcium-activated transient outward current in calf cardiac Purkinje fibres. J Physiol. 1980 Feb;299:485–506. doi: 10.1113/jphysiol.1980.sp013138. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Steinhardt R., Zucker R., Schatten G. Intracellular calcium release at fertilization in the sea urchin egg. Dev Biol. 1977 Jul 1;58(1):185–196. doi: 10.1016/0012-1606(77)90084-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Thompson S. H. Three pharmacologically distinct potassium channels in molluscan neurones. J Physiol. 1977 Feb;265(2):465–488. doi: 10.1113/jphysiol.1977.sp011725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Tillotson D. Inactivation of Ca conductance dependent on entry of Ca ions in molluscan neurons. Proc Natl Acad Sci U S A. 1979 Mar;76(3):1497–1500. doi: 10.1073/pnas.76.3.1497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. WERMAN R., GRUNDFEST H. Graded and all-or-none electrogenesis in arthropod muscle. II. The effects of alkali-earth and onium ions on lobster muscle fibers. J Gen Physiol. 1961 May;44:997–1027. doi: 10.1085/jgp.44.5.997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Yellen G. Single Ca2+-activated nonselective cation channels in neuroblastoma. Nature. 1982 Mar 25;296(5855):357–359. doi: 10.1038/296357a0. [DOI] [PubMed] [Google Scholar]
  46. de Laat S. W., Buwalda R. J., Habets A. M. Intracellular ionic distribution, cell membrane permeability and membrane potential of the Xenopus egg during first cleavage. Exp Cell Res. 1974 Nov;89(1):1–14. doi: 10.1016/0014-4827(74)90180-3. [DOI] [PubMed] [Google Scholar]

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

RESOURCES