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. 1991 Nov;443:25–44. doi: 10.1113/jphysiol.1991.sp018820

The effect of permeant ions on single calcium channel activation in mouse neuroblastoma cells: ion-channel interaction.

Y M Shuba 1, V I Teslenko 1, A N Savchenko 1, N H Pogorelaya 1
PMCID: PMC1179828  PMID: 1668337

Abstract

1. Single low-threshold inactivating (LTI or T-type) Ca2+ channels of undifferentiated neuroblastoma cells (clone N1E-115) were investigated using the patch-clamp technique. 2. Single-channel conductance, gi, for Ca2+, Sr2+ or Ba2+ as a permeant cation was similar (7.2 pS). Mean channel open time, tau op, was also practically independent of the divalent ion species; it decreased from 0.7 to 0.3 ms between -40 and 0 mV. 3. Modification of the calcium channel selectivity by lowering the external Ca2+ concentration to 10(-8) M produced an increase in gi for Na+ and Li+ ions and a shift of potential-dependent characteristics in the hyperpolarizing direction. Voltage sensitivity and absolute values of tau op were also changed. These changes were dependent on both permeant monovalent ion type and concentration. 4. At high [Na+]o, tau op was almost potential independent (congruent to 0.3 ms). Decrease in [Na+]o and substitution of Li+ for Na+ increased tau op and the steepness of its potential dependency. 5. The divalent and monovalent cations that were tested had much smaller effect on the mean intraburst shut time, tau cl(f), which was nearly independent of membrane potential (congruent to 0.6 ms). By contrast, mean burst duration was strongly potential dependent and noticeably affected by permeant ion type. 6. All kinetic changes were analysed in terms of a four-state sequential model for channel activation. According to this model the channel enters the open state through three closed states. Transitions between closed states can be formally related to the transmembrane movement of two charged gating particles (m2 process). The interaction between ion flux and a sterical region of the Ca2+ channel selectivity filter may, depending on ion transfer rate and ionic radius, lead to a local increase of the dielectric constant, resulting in redistribution of the electric field and changes in potential dependency of tau op.

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Selected References

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

  1. Almers W., McCleskey E. W., Palade P. T. A non-selective cation conductance in frog muscle membrane blocked by micromolar external calcium ions. J Physiol. 1984 Aug;353:565–583. doi: 10.1113/jphysiol.1984.sp015351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Ashcroft F. M., Stanfield P. R. Calcium dependence of the inactivation of calcium currents in skeletal muscle fibers of an insect. Science. 1981 Jul 10;213(4504):224–226. doi: 10.1126/science.213.4504.224. [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. Blatz A. L., Magleby K. L. Correcting single channel data for missed events. Biophys J. 1986 May;49(5):967–980. doi: 10.1016/S0006-3495(86)83725-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bossu J. L., Feltz A., Thomann J. M. Depolarization elicits two distinct calcium currents in vertebrate sensory neurones. Pflugers Arch. 1985 Apr;403(4):360–368. doi: 10.1007/BF00589247. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. Brown A. M., Tsuda Y., Wilson D. L. A description of activation and conduction in calcium channels based on tail and turn-on current measurements in the snail. J Physiol. 1983 Nov;344:549–583. doi: 10.1113/jphysiol.1983.sp014956. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. Carbone E., Lux H. D. A low voltage-activated, fully inactivating Ca channel in vertebrate sensory neurones. Nature. 1984 Aug 9;310(5977):501–502. doi: 10.1038/310501a0. [DOI] [PubMed] [Google Scholar]
  10. Carbone E., Lux H. D. Kinetics and selectivity of a low-voltage-activated calcium current in chick and rat sensory neurones. J Physiol. 1987 May;386:547–570. doi: 10.1113/jphysiol.1987.sp016551. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Carbone E., Lux H. D. Single low-voltage-activated calcium channels in chick and rat sensory neurones. J Physiol. 1987 May;386:571–601. doi: 10.1113/jphysiol.1987.sp016552. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Cavalié A., Ochi R., Pelzer D., Trautwein W. Elementary currents through Ca2+ channels in guinea pig myocytes. Pflugers Arch. 1983 Sep;398(4):284–297. doi: 10.1007/BF00657238. [DOI] [PubMed] [Google Scholar]
  13. Chad J. E., Eckert R. An enzymatic mechanism for calcium current inactivation in dialysed Helix neurones. J Physiol. 1986 Sep;378:31–51. doi: 10.1113/jphysiol.1986.sp016206. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Droogmans G., Nilius B. Kinetic properties of the cardiac T-type calcium channel in the guinea-pig. J Physiol. 1989 Dec;419:627–650. doi: 10.1113/jphysiol.1989.sp017890. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Durroux T., Gallo-Payet N., Payet M. D. Three components of the calcium current in cultured glomerulosa cells from rat adrenal gland. J Physiol. 1988 Oct;404:713–729. doi: 10.1113/jphysiol.1988.sp017315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Eckert R., Tillotson D. L. Calcium-mediated inactivation of the calcium conductance in caesium-loaded giant neurones of Aplysia californica. J Physiol. 1981 May;314:265–280. doi: 10.1113/jphysiol.1981.sp013706. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. 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]
  19. 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]
  20. Fox A. P., Nowycky M. C., Tsien R. W. Kinetic and pharmacological properties distinguishing three types of calcium currents in chick sensory neurones. J Physiol. 1987 Dec;394:149–172. doi: 10.1113/jphysiol.1987.sp016864. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Fox A. P., Nowycky M. C., Tsien R. W. Single-channel recordings of three types of calcium channels in chick sensory neurones. J Physiol. 1987 Dec;394:173–200. doi: 10.1113/jphysiol.1987.sp016865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Ganitkevich VYa, Shuba M. F., Smirnov S. V. Calcium-dependent inactivation of potential-dependent calcium inward current in an isolated guinea-pig smooth muscle cell. J Physiol. 1987 Nov;392:431–449. doi: 10.1113/jphysiol.1987.sp016789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. 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]
  26. 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]
  27. Hille B. Ionic selectivity of Na and K channels of nerve membranes. Membranes. 1975;3:255–323. [PubMed] [Google Scholar]
  28. Honig B. H., Hubbell W. L., Flewelling R. F. Electrostatic interactions in membranes and proteins. Annu Rev Biophys Biophys Chem. 1986;15:163–193. doi: 10.1146/annurev.bb.15.060186.001115. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. Kostyuk P. G., Shirokov R. E. Deactivation kinetics of different components of calcium inward current in the membrane of mice sensory neurones. J Physiol. 1989 Feb;409:343–355. doi: 10.1113/jphysiol.1989.sp017501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Kostyuk P. G., Shuba YaM, Savchenko A. N. Three types of calcium channels in the membrane of mouse sensory neurons. Pflugers Arch. 1988 Jun;411(6):661–669. doi: 10.1007/BF00580863. [DOI] [PubMed] [Google Scholar]
  32. Kostyuk P. G., Shuba YaM, Teslenko V. I. Activation kinetics of single high-threshold calcium channels in the membrane of sensory neurons from mouse embryos. J Membr Biol. 1989 Aug;110(1):29–38. doi: 10.1007/BF01870990. [DOI] [PubMed] [Google Scholar]
  33. Kostyuk P., Akaike N., Osipchuk Y. u., Savchenko A., Shuba Y. a. Gating and permeation of different types of Ca channels. Ann N Y Acad Sci. 1989;560:63–79. doi: 10.1111/j.1749-6632.1989.tb24081.x. [DOI] [PubMed] [Google Scholar]
  34. Läuger P. Ionic channels with conformational substates. Biophys J. 1985 May;47(5):581–590. doi: 10.1016/S0006-3495(85)83954-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Magleby K. L., Pallotta B. S. Burst kinetics of single calcium-activated potassium channels in cultured rat muscle. J Physiol. 1983 Nov;344:605–623. doi: 10.1113/jphysiol.1983.sp014958. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Matteson D. R., Armstrong C. M. Properties of two types of calcium channels in clonal pituitary cells. J Gen Physiol. 1986 Jan;87(1):161–182. doi: 10.1085/jgp.87.1.161. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. McCleskey E. W., Almers W. The Ca channel in skeletal muscle is a large pore. Proc Natl Acad Sci U S A. 1985 Oct;82(20):7149–7153. doi: 10.1073/pnas.82.20.7149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. McDonald T. F., Cavalié A., Trautwein W., Pelzer D. Voltage-dependent properties of macroscopic and elementary calcium channel currents in guinea pig ventricular myocytes. Pflugers Arch. 1986 May;406(5):437–448. doi: 10.1007/BF00583365. [DOI] [PubMed] [Google Scholar]
  39. Miller C. Genetic manipulation of ion channels: a new approach to structure and mechanism. Neuron. 1989 Mar;2(3):1195–1205. doi: 10.1016/0896-6273(89)90304-8. [DOI] [PubMed] [Google Scholar]
  40. 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]
  41. 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]
  42. Nelson M. T. Interactions of divalent cations with single calcium channels from rat brain synaptosomes. J Gen Physiol. 1986 Feb;87(2):201–222. doi: 10.1085/jgp.87.2.201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Nowycky M. C., Fox A. P., Tsien R. W. Three types of neuronal calcium channel with different calcium agonist sensitivity. Nature. 1985 Aug 1;316(6027):440–443. doi: 10.1038/316440a0. [DOI] [PubMed] [Google Scholar]
  44. 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]
  45. Saimi Y., Kung C. Are ions involved in the gating of calcium channels? Science. 1982 Oct 8;218(4568):153–156. doi: 10.1126/science.6289432. [DOI] [PubMed] [Google Scholar]
  46. 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]
  47. Tsien R. W., Hess P., McCleskey E. W., Rosenberg R. L. Calcium channels: mechanisms of selectivity, permeation, and block. Annu Rev Biophys Biophys Chem. 1987;16:265–290. doi: 10.1146/annurev.bb.16.060187.001405. [DOI] [PubMed] [Google Scholar]

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