Skip to main content
The Journal of Physiology logoLink to The Journal of Physiology
. 1976 Feb;255(2):527–561. doi: 10.1113/jphysiol.1976.sp011294

Two components of the calcium current in the egg cell membrane of the tunicate.

H Okamoto, K Takahashi, M Yoshii
PMCID: PMC1309262  PMID: 3645

Abstract

The Ca current of the egg cell membrane of a certain tunicate, Halocynthia roretzi Drasche, was studied by the voltage-clamp technique. 2. The Ca current in the standard artificial sea water (ASW) was produced at the critical membrane potential of -10 mV after inactivating the Na current by conditioning depolarization, -30 to -15 mV. The Ca current was abolished by replacing Ca in ASW with Mg2+ or Mn2+. The Ca current was not significantly influenced by replacing Na in ASW with choline or Cs. 3. The relation of Ca current to the external Ca concentration was a monotonously increasing function, but was not linear. The current tended to saturate above 50 mM-Ca. In 100 mM-Ca ASW, the maximum peak inward current of Ca ranged from 1 to 7 X 10(-9) A. 4. The kinetics of Ca current was accurately analysed because of the small contribution of K outward current and was found to be relatively slow in comparison with the Na current. The peak time and the half-decay time of the maximum Ca current at about 25 mV were about 25 and 100 msec respectively in 100 mM-Ca ASW at 15 degrees C. 5. Addition of 20 mM-Co2+ to 100 mM-Ca ASW reduced Ca current to one fourth and 1 mM-La3+ to 100 mM-Ca ASW abolished the current. 6. Sr and Ba could substitute for Ca in Ca channels. The selectivity ratios for the 'Ca channels's were Ca (1-00):Sr(1-17):Ba(0-71) at a potential level of +40 mV. The Ca current in the egg cell membrane appeared to be essentially the same as the Ca current in the common excitable membranes, such as the crustacean muscle fibre. 7. The polyvalent cations including Ca ion and monovalent H+ ion showed the stabilizing effect upon both Na and Ca currents, by shifting V-I relations along the voltage axis. From the prediction of a theory of the diffuse double layer, the shift in the V-I relation induced by those cations should be directly related to their binding powers to the membrane. Thus, the sequence of the binding powers was inferred as H+ greater than La3+ greater than Co2+ greater than Mn2+ greater than Ca2+ greater than Sr2+ larger than or equal to Ba2+ greater than Mg2+. 9. In Na-free ASW, such as isotonic Ca ASW, Ca current was composed of two components. The one component was the Ca current described in 1 to 6. The other was also dependent upon the external Ca concentration, but showed the more negative critical membrane potential and the faster kinetics. It was concluded that this component should be the Ca current through Na channels. 10. The selectivity among Ca, Sr and Ba for 'Ca' current through 'Na channels' was significantly different from that of 'Ca' current through 'Ca channels', being Ca greater than Sr larger than or equal to Ba = 0.

Full text

PDF

Selected References

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

  1. Baker P. F., Hodgkin A. L., Ridgway E. B. Depolarization and calcium entry in squid giant axons. J Physiol. 1971 Nov;218(3):709–755. doi: 10.1113/jphysiol.1971.sp009641. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baker P. F., Meves H., Ridgway E. B. Calcium entry in response to maintained depolarization of squid axons. J Physiol. 1973 Jun;231(3):527–548. doi: 10.1113/jphysiol.1973.sp010247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Baker P. F., Meves H., Ridgway E. B. Effects of manganese and other agents on the calcium uptake that follows depolarization of squid axons. J Physiol. 1973 Jun;231(3):511–526. doi: 10.1113/jphysiol.1973.sp010246. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Blaustein M. P., Goldman D. E. The action of certain polyvalent cations on the voltage-clamped lobster axon. J Gen Physiol. 1968 Mar;51(3):279–291. doi: 10.1085/jgp.51.3.279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chandler W. K., Hodgkin A. L., Meves H. The effect of changing the internal solution on sodium inactivation and related phenomena in giant axons. J Physiol. 1965 Oct;180(4):821–836. doi: 10.1113/jphysiol.1965.sp007733. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. D'Arrigo J. S. Possible screening of surface charges on crayfish axons by polyvalent metal ions. J Physiol. 1973 May;231(1):117–128. doi: 10.1113/jphysiol.1973.sp010223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Ebashi S., Endo M. Calcium ion and muscle contraction. Prog Biophys Mol Biol. 1968;18:123–183. doi: 10.1016/0079-6107(68)90023-0. [DOI] [PubMed] [Google Scholar]
  8. Ehrenstein G., Gilbert D. L. Evidence for membrane surface from measurement of potassium kinetics as a function of external divalent cation concentration. Biophys J. 1973 May;13(5):495–497. doi: 10.1016/S0006-3495(73)86002-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. FATT P., GINSBORG B. L. The ionic requirements for the production of action potentials in crustacean muscle fibres. J Physiol. 1958 Aug 6;142(3):516–543. doi: 10.1113/jphysiol.1958.sp006034. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. FRANKENHAEUSER B., HODGKIN A. L. The action of calcium on the electrical properties of squid axons. J Physiol. 1957 Jul 11;137(2):218–244. doi: 10.1113/jphysiol.1957.sp005808. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. GRAHAME D. C. The electrical double layer and the theory of electrocapillarity. Chem Rev. 1947 Dec;41(3):441–501. doi: 10.1021/cr60130a002. [DOI] [PubMed] [Google Scholar]
  12. Gilbert D. L., Ehrenstein G. Effect of divalent cations on potassium conductance of squid axons: determination of surface charge. Biophys J. 1969 Mar;9(3):447–463. doi: 10.1016/S0006-3495(69)86396-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gilbert D. L., Ehrenstein G. Use of a fixed charge model to determine the pK of the negative sites on the external membrane surface. J Gen Physiol. 1970 Jun;55(6):822–825. [PMC free article] [PubMed] [Google Scholar]
  14. HAGIWARA S., NAKA K. I. THE INITIATION OF SPIKE POTENTIAL IN BARNACLE MUSCLE FIBERS UNDER LOW INTRACELLULAR CA++. J Gen Physiol. 1964 Sep;48:141–162. doi: 10.1085/jgp.48.1.141. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. HODGKIN A. L., HUXLEY A. F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol. 1952 Aug;117(4):500–544. doi: 10.1113/jphysiol.1952.sp004764. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. HODGKIN A. L., KEYNES R. D. Movements of labelled calcium in squid giant axons. J Physiol. 1957 Sep 30;138(2):253–281. doi: 10.1113/jphysiol.1957.sp005850. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Hagiwara S., Hayashi H., Takahashi K. Calcium and potassium currents of the membrane of a barnacle muscle fibre in relation to the calcium spike. J Physiol. 1969 Nov;205(1):115–129. doi: 10.1113/jphysiol.1969.sp008955. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hagiwara S., Nakajima S. Differences in Na and Ca spikes as examined by application of tetrodotoxin, procaine, and manganese ions. J Gen Physiol. 1966 Mar;49(4):793–806. doi: 10.1085/jgp.49.4.793. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. 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]
  22. Hille B. Charges and potentials at the nerve surface. Divalent ions and pH. J Gen Physiol. 1968 Feb;51(2):221–236. doi: 10.1085/jgp.51.2.221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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]
  24. Katz B., Miledi R. Tetrodotoxin-resistant electric activity in presynaptic terminals. J Physiol. 1969 Aug;203(2):459–487. doi: 10.1113/jphysiol.1969.sp008875. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Katz B., Miledi R. The effect of prolonged depolarization on synaptic transfer in the stellate ganglion of the squid. J Physiol. 1971 Jul;216(2):503–512. doi: 10.1113/jphysiol.1971.sp009537. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Keynes R. D., Rojas E., Taylor R. E., Vergara J. Calcium and potassium systems of a giant barnacle muscle fibre under membrane potential control. J Physiol. 1973 Mar;229(2):409–455. doi: 10.1113/jphysiol.1973.sp010146. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. McLaughlin S. G., Szabo G., Eisenman G. Divalent ions and the surface potential of charged phospholipid membranes. J Gen Physiol. 1971 Dec;58(6):667–687. doi: 10.1085/jgp.58.6.667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Meves H., Vogel W. Calcium inward currents in internally perfused giant axons. J Physiol. 1973 Nov;235(1):225–265. doi: 10.1113/jphysiol.1973.sp010386. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Miyazaki S. I., Takahashi K., Tsuda K. Electrical excitability in the egg cell membrane of the tunicate. J Physiol. 1974 Apr;238(1):37–54. doi: 10.1113/jphysiol.1974.sp010509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Miyazaki S., Takahashi K., Tsuda K. Calcium and sodium contributions to regenerative responses in the embryonic excitable cell membrane. Science. 1972 Jun 30;176(4042):1441–1443. doi: 10.1126/science.176.4042.1441. [DOI] [PubMed] [Google Scholar]
  31. Muller R. U., Finkelstein A. The effect of surface charge on the voltage-dependent conductance induced in thin lipid membranes by monazomycin. J Gen Physiol. 1972 Sep;60(3):285–306. doi: 10.1085/jgp.60.3.285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Okamoto H., Takahashi K., Yoshii M. Membrane currents of the tunicate egg under the voltage-clamp condition. J Physiol. 1976 Jan;254(3):607–638. doi: 10.1113/jphysiol.1976.sp011249. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Reuter H. Divalent cations as charge carriers in excitable membranes. Prog Biophys Mol Biol. 1973;26:1–43. doi: 10.1016/0079-6107(73)90016-3. [DOI] [PubMed] [Google Scholar]
  34. Steinhardt R. A., Epel D. Activation of sea-urchin eggs by a calcium ionophore. Proc Natl Acad Sci U S A. 1974 May;71(5):1915–1919. doi: 10.1073/pnas.71.5.1915. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Steinhardt R. A., Epel D., Carroll E. J., Jr, Yanagimachi R. Is calcium ionophore a universal activator for unfertilised eggs? Nature. 1974 Nov 1;252(5478):41–43. doi: 10.1038/252041a0. [DOI] [PubMed] [Google Scholar]
  36. Tasaki I., Lerman L., Watanabe A. Analysis of excitation process in squid giant axons under bi-ionic conditions. Am J Physiol. 1969 Jan;216(1):130–138. doi: 10.1152/ajplegacy.1969.216.1.130. [DOI] [PubMed] [Google Scholar]
  37. Tasaki I., Watanabe A., Lerman L. Role of divalent cations in excitation of squid giant axons. Am J Physiol. 1967 Dec;213(6):1465–1474. doi: 10.1152/ajplegacy.1967.213.6.1465. [DOI] [PubMed] [Google Scholar]
  38. Tasaki I., Watanabe A., Singer I. Excitability of squid giant axons in the absence of univalent cations in the external medium. Proc Natl Acad Sci U S A. 1966 Oct;56(4):1116–1122. doi: 10.1073/pnas.56.4.1116. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. 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]
  40. Watanabe A., Tasaki I., Lerman L. Bi-ionic action potentials in squid giant axons internally perfused with sodium saltssalts. Proc Natl Acad Sci U S A. 1967 Dec;58(6):2246–2252. doi: 10.1073/pnas.58.6.2246. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Watanabe A., Tasaki I., Singer I., Lerman L. Effects of tetrodotoxin on excitability of squid giant axons in sodium-free media. Science. 1967 Jan 6;155(3758):95–97. doi: 10.1126/science.155.3758.95. [DOI] [PubMed] [Google Scholar]

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

RESOURCES