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. 1988 Nov;54(5):885–895. doi: 10.1016/S0006-3495(88)83025-X

Gating and permeation properties of two types of calcium channels in neuroblastoma cells.

M Yoshii 1, A Tsunoo 1, T Narahashi 1
PMCID: PMC1330397  PMID: 2853978

Abstract

The gating and permeation properties of two types of calcium channels were studied in the neuroblastoma cell line N1E-115. Calcium channel currents as carried by Ba2+ (50 mM) were recorded using the whole-cell variation of the patch electrode voltage-clamp technique. The two types of calcium channels showed similar membrane potential dependence with respect to the steady-state activation and inactivation gating properties. However, the properties of the long-lasting type II channels were shifted approximately 30 mV in the depolarizing direction compared with those of the transient type I channels. Activation of type I channels developed with a sigmoidal time course which was described by m2 kinetics, whereas the activation of type II channels was described by a single exponential function. Tail current upon repolarization followed an exponential decay in either type of calcium channels. In comparison to type I channels, the activation process of type II channels was shifted approximately 30 mV in the positive direction, while the deactivation process showed a 60 mV shift in the positive direction. The rate constants of activation obtained from the activation and deactivation processes indicated that under comparable membrane potential conditions, type II channels close 2.4 times faster than type I channels upon repolarization. When external 50 mM Ba2+ was replaced with Ca2+ or Sr2+ on the equimolar basis, the amplitudes of transient and long-lasting currents were altered without a significant change in their time courses. The ion permeability ratios determined from the maximum amplitude of the inward current were as follows: Ba2+ (1.0) = Sr2+ (1.0) greater than Ca2+ (0.7) for type I channels, and Ba2+ (1.0) greater than Sr2+ (0.7) greater than Ca2+ (0.3) for type II channels. Replacement of Ba2+ with Ca2+ caused a 10-12 mV positive shift in the current-voltage relation for type II channels. However, the shift for type I channels was much less. This suggests that negative surface charges are present around type II channels. After correction for the surface charge effect on the ion permeation, there was no significant difference between the permeability ratios of these cations for the two channel types. It was concluded that the two types of calcium channels have many common properties in their gating and permeation mechanisms despite their differential voltage sensitivity and ion selectivity.

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Selected References

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  1. Akaike N., Lee K. S., Brown A. M. The calcium current of Helix neuron. J Gen Physiol. 1978 May;71(5):509–531. doi: 10.1085/jgp.71.5.509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Armstrong C. M., Matteson D. R. Two distinct populations of calcium channels in a clonal line of pituitary cells. Science. 1985 Jan 4;227(4682):65–67. doi: 10.1126/science.2578071. [DOI] [PubMed] [Google Scholar]
  3. Bean B. P. Two kinds of calcium channels in canine atrial cells. Differences in kinetics, selectivity, and pharmacology. J Gen Physiol. 1985 Jul;86(1):1–30. doi: 10.1085/jgp.86.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brown A. M., Lux H. D., Wilson D. L. Activation and inactivation of single calcium channels in snail neurons. J Gen Physiol. 1984 May;83(5):751–769. doi: 10.1085/jgp.83.5.751. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Brown A. M., Morimoto K., Tsuda Y., wilson D. L. Calcium current-dependent and voltage-dependent inactivation of calcium channels in Helix aspersa. J Physiol. 1981 Nov;320:193–218. doi: 10.1113/jphysiol.1981.sp013944. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Byerly L., Chase P. B., Stimers J. R. Calcium current activation kinetics in neurones of the snail Lymnaea stagnalis. J Physiol. 1984 Mar;348:187–207. doi: 10.1113/jphysiol.1984.sp015105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. 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]
  8. 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]
  9. Fedulova S. A., Kostyuk P. G., Veselovsky N. S. Two types of calcium channels in the somatic membrane of new-born rat dorsal root ganglion neurones. J Physiol. 1985 Feb;359:431–446. doi: 10.1113/jphysiol.1985.sp015594. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fenwick E. M., Marty A., Neher E. Sodium and calcium channels in bovine chromaffin cells. J Physiol. 1982 Oct;331:599–635. doi: 10.1113/jphysiol.1982.sp014394. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fishman M. C., Spector I. Potassium current suppression by quinidine reveals additional calcium currents in neuroblastoma cells. Proc Natl Acad Sci U S A. 1981 Aug;78(8):5245–5249. doi: 10.1073/pnas.78.8.5245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Fukushima Y., Hagiwara S. Voltage-gated Ca2+ channel in mouse myeloma cells. Proc Natl Acad Sci U S A. 1983 Apr;80(8):2240–2242. doi: 10.1073/pnas.80.8.2240. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Goldman D. E. POTENTIAL, IMPEDANCE, AND RECTIFICATION IN MEMBRANES. J Gen Physiol. 1943 Sep 20;27(1):37–60. doi: 10.1085/jgp.27.1.37. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. HODGKIN A. L., KATZ B. The effect of sodium ions on the electrical activity of giant axon of the squid. J Physiol. 1949 Mar 1;108(1):37–77. doi: 10.1113/jphysiol.1949.sp004310. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  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 single calcium channel currents in rat clonal pituitary cells. J Physiol. 1983 Mar;336:649–661. doi: 10.1113/jphysiol.1983.sp014603. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. Hille B. The selective inhibition of delayed potassium currents in nerve by tetraethylammonium ion. J Gen Physiol. 1967 May;50(5):1287–1302. doi: 10.1085/jgp.50.5.1287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Hirano T., Takahashi K. Comparison of properties of calcium channels between the differentiated 1-cell embryo and the egg cell of ascidians. J Physiol. 1984 Feb;347:327–344. doi: 10.1113/jphysiol.1984.sp015068. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kimhi Y., Palfrey C., Spector I., Barak Y., Littauer U. Z. Maturation of neuroblastoma cells in the presence of dimethylsulfoxide. Proc Natl Acad Sci U S A. 1976 Feb;73(2):462–466. doi: 10.1073/pnas.73.2.462. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kostyuk P. G., Krishtal O. A., Shakhovalov Y. A. Separation of sodium and calcium currents in the somatic membrane of mollusc neurones. J Physiol. 1977 Sep;270(3):545–568. doi: 10.1113/jphysiol.1977.sp011968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. McLaughlin S. G., Szabo G., Eisenman G., Ciani S. M. Surface charge and the conductance of phospholipid membranes. Proc Natl Acad Sci U S A. 1970 Nov;67(3):1268–1275. doi: 10.1073/pnas.67.3.1268. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Moolenaar W. H., Spector I. Ionic currents in cultured mouse neuroblastoma cells under voltage-clamp conditions. J Physiol. 1978 May;278:265–286. doi: 10.1113/jphysiol.1978.sp012303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. NARAHASHI T., MOORE J. W., SCOTT W. R. TETRODOTOXIN BLOCKAGE OF SODIUM CONDUCTANCE INCREASE IN LOBSTER GIANT AXONS. J Gen Physiol. 1964 May;47:965–974. doi: 10.1085/jgp.47.5.965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Narahashi T., Tsunoo A., Yoshii M. Characterization of two types of calcium channels in mouse neuroblastoma cells. J Physiol. 1987 Feb;383:231–249. doi: 10.1113/jphysiol.1987.sp016406. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. 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]
  31. Okamoto H., Takahashi K., Yoshii M. Two components of the calcium current in the egg cell membrane of the tunicate. J Physiol. 1976 Feb;255(2):527–561. doi: 10.1113/jphysiol.1976.sp011294. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Quandt F. N., Narahashi T. Isolation and kinetic analysis of inward currents in neuroblastoma cells. Neuroscience. 1984 Sep;13(1):249–262. doi: 10.1016/0306-4522(84)90275-6. [DOI] [PubMed] [Google Scholar]
  33. Reuter H., Stevens C. F., Tsien R. W., Yellen G. Properties of single calcium channels in cardiac cell culture. Nature. 1982 Jun 10;297(5866):501–504. doi: 10.1038/297501a0. [DOI] [PubMed] [Google Scholar]
  34. Tsien R. W. Calcium channels in excitable cell membranes. Annu Rev Physiol. 1983;45:341–358. doi: 10.1146/annurev.ph.45.030183.002013. [DOI] [PubMed] [Google Scholar]
  35. Tsunoo A., Yoshii M., Narahashi T. Block of calcium channels by enkephalin and somatostatin in neuroblastoma-glioma hybrid NG108-15 cells. Proc Natl Acad Sci U S A. 1986 Dec;83(24):9832–9836. doi: 10.1073/pnas.83.24.9832. [DOI] [PMC free article] [PubMed] [Google Scholar]

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