Skip to main content
PMC home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1985 Apr;361:441–457. doi: 10.1113/jphysiol.1985.sp015654

Calcium-activated potassium channels in isolated presynaptic nerve terminals from rat brain.

D K Bartschat, M P Blaustein
PMCID: PMC1192868  PMID: 2580982

Abstract

86Rb efflux was examined in isolated presynaptic nerve terminals (synaptosomes) from rat brain in a study designed to assess K permeability (PK) changes sensitive to alterations in internal Ca activity. Rb efflux from 86Rb-loaded synaptosomes into nominally Ca-free physiological saline (PSS) containing 5 mM-K was about 0.3-0.4%/s. Raising extracellular K concentration [( K]o), to depolarize the synaptosomes, stimulated the 86Rb efflux. Addition of Ca to the 5 mM-K PSS had no effect, but Ca did further stimulate 86Rb efflux into K-rich solutions. The effect of Ca was graded, with apparent half-maximal activation, KA approximately equal to 0.5 mM-Ca. These data fit the view that, during depolarization, Ca enters the terminals through voltage-regulated Ca channels, and that the rise in intracellular Ca concentration opens certain (Ca-activated) K channels. The Ca-dependent stimulation of 86Rb efflux was greatest during the initial seconds of incubation (component CT), and then declined to a much lower rate (component CS). Much of this change in rate could be attributed to inactivation of voltage-regulated Ca channels and reduced entry of Ca. The Ca-dependent increase in 86Rb efflux was completely inhibited by 100 microM-La. In the presence of Ca, but not in its absence, the Ca ionophore A23187 stimulated 86Rb efflux both in 5 and 100 mM-K PSS. The effect in 100 mM-K was quantitatively greater, perhaps because of the increased outward driving force on Rb in depolarized synaptosomes. When synaptosomes were suspended in media containing the voltage-sensitive fluorescent dye, DiS-C3-(5) (1,1'-dipentyl-2,2'-thiocarbocyanine), the addition of Ca+ A23187 decreased the fluorescence intensity (= synaptosome hyperpolarization) when the media contained 5 mM-K but not 100 mM-K. This implies that in the presence of Ca + A23187, PK was increased, and the membrane potential moved closer to the K equilibrium potential, EK. Quinine sulphate, a blocker of Ca-activated K channels, reduced the Ca-stimulated 86Rb efflux with high affinity (apparent half-maximal inhibition, KI approximately equal to 1 microM). Tetraethylammonium chloride, another agent known to block Ca-activated K channels, was also a relatively potent inhibitor of Ca-stimulated 86Rb efflux (KI approximately equal to 0.2 mM). The K-channel blocker, 4-aminopyridine, partially inhibited Ca-stimulated 86Rb efflux at concentrations below 0.5 mM, but stimulated this efflux at concentrations greater than or equal to 1 mM.(ABSTRACT TRUNCATED AT 400 WORDS)

Full text

PDF
447

Selected References

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

  1. Alger B. E., Nicoll R. A. Epileptiform burst afterhyperolarization: calcium-dependent potassium potential in hippocampal CA1 pyramidal cells. Science. 1980 Dec 5;210(4474):1122–1124. doi: 10.1126/science.7444438. [DOI] [PubMed] [Google Scholar]
  2. Armando-Hardy M., Ellory J. C., Ferreira H. G., Fleminger S., Lew V. L. Inhibition of the calcium-induced increase in the potassium permeability of human red blood cells by quinine. J Physiol. 1975 Aug;250(1):32P–33P. [PubMed] [Google Scholar]
  3. Atwater I., Dawson C. M., Ribalet B., Rojas E. Potassium permeability activated by intracellular calcium ion concentration in the pancreatic beta-cell. J Physiol. 1979 Mar;288:575–588. [PMC free article] [PubMed] [Google Scholar]
  4. Barrett J. N., Magleby K. L., Pallotta B. S. Properties of single calcium-activated potassium channels in cultured rat muscle. J Physiol. 1982 Oct;331:211–230. doi: 10.1113/jphysiol.1982.sp014370. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bartschat D. K., Blaustein M. P. Potassium channels in isolated presynaptic nerve terminals from rat brain. J Physiol. 1985 Apr;361:419–440. doi: 10.1113/jphysiol.1985.sp015653. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Blaustein M. P., Goldring J. M. Membrane potentials in pinched-off presynaptic nerve ternimals monitored with a fluorescent probe: evidence that synaptosomes have potassium diffusion potentials. J Physiol. 1975 Jun;247(3):589–615. doi: 10.1113/jphysiol.1975.sp010949. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Blaustein M. P., McGraw C. F., Somlyo A. V., Schweitzer E. S. How is the cytoplasmic calcium concentration controlled in nerve terminals? J Physiol (Paris) 1980 Sep;76(5):459–470. [PubMed] [Google Scholar]
  8. 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]
  9. Gorman A. L., Woolum J. C., Cornwall M. C. Selectivity of the Ca2+-activated and light-dependent K+ channels for monovalent cations. Biophys J. 1982 Jun;38(3):319–322. doi: 10.1016/S0006-3495(82)84565-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hermann A., Gorman A. L. Effects of 4-aminopyridine on potassium currents in a molluscan neuron. J Gen Physiol. 1981 Jul;78(1):63–86. doi: 10.1085/jgp.78.1.63. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hermann A., Hartung K. Properties of a Ca2+ activated K+ conductance in Helix neurones investigated by intracellular Ca2+ ionophoresis. Pflugers Arch. 1982 May;393(3):248–253. doi: 10.1007/BF00584078. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. Katz B., Miledi R. The role of calcium in neuromuscular facilitation. J Physiol. 1968 Mar;195(2):481–492. doi: 10.1113/jphysiol.1968.sp008469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kirsch G. E., Narahashi T. 3,4-diaminopyridine. A potent new potassium channel blocker. Biophys J. 1978 Jun;22(3):507–512. doi: 10.1016/S0006-3495(78)85503-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kretz R., Shapiro E., Kandel E. R. Post-tetanic potentiation at an identified synapse in Aplysia is correlated with a Ca2+-activated K+ current in the presynaptic neuron: evidence for Ca2+ accumulation. Proc Natl Acad Sci U S A. 1982 Sep;79(17):5430–5434. doi: 10.1073/pnas.79.17.5430. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Krnjević K., Lisiewicz A. Injections of calcium ions into spinal motoneurones. J Physiol. 1972 Sep;225(2):363–390. doi: 10.1113/jphysiol.1972.sp009945. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Krueger B. K., Worley J. F., 3rd, French R. J. Single sodium channels from rat brain incorporated into planar lipid bilayer membranes. Nature. 1983 May 12;303(5913):172–175. doi: 10.1038/303172a0. [DOI] [PubMed] [Google Scholar]
  18. Lew V. L., Muallem S., Seymour C. A. Properties of the Ca2+-activated K+ channel in one-step inside-out vesicles from human red cell membranes. Nature. 1982 Apr 22;296(5859):742–744. doi: 10.1038/296742a0. [DOI] [PubMed] [Google Scholar]
  19. Llinás R., Steinberg I. Z., Walton K. Transmission in the squid giant synapse: a model based on voltage clamp studies. J Physiol (Paris) 1980 Sep;76(5):413–418. [PubMed] [Google Scholar]
  20. Meech R. W. Calcium-dependent potassium activation in nervous tissues. Annu Rev Biophys Bioeng. 1978;7:1–18. doi: 10.1146/annurev.bb.07.060178.000245. [DOI] [PubMed] [Google Scholar]
  21. Meves H., Pichon Y. The effect of internal and external 4-aminopyridine on the potassium currents in intracellularly perfused squid giant axons. J Physiol. 1977 Jun;268(2):511–532. doi: 10.1113/jphysiol.1977.sp011869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Nachshen D. A., Blaustein M. P. Influx of calcium, strontium, and barium in presynaptic nerve endings. J Gen Physiol. 1982 Jun;79(6):1065–1087. doi: 10.1085/jgp.79.6.1065. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Nachshen D. A., Blaustein M. P. Some properties of potassium-stimulated calcium influx in presynaptic nerve endings. J Gen Physiol. 1980 Dec;76(6):709–728. doi: 10.1085/jgp.76.6.709. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Nelson M. T., Roudna M., Bamberg E. Single K+-channel current measurements from brain synaptosomes in lipid bilayers. Am J Physiol. 1983 Jul;245(1):C151–C156. doi: 10.1152/ajpcell.1983.245.1.C151. [DOI] [PubMed] [Google Scholar]
  25. Petersen O. H., Maruyama Y. Calcium-activated potassium channels and their role in secretion. Nature. 1984 Feb 23;307(5953):693–696. doi: 10.1038/307693a0. [DOI] [PubMed] [Google Scholar]
  26. Schwarz W., Passow H. Ca2+-activated K+ channels in erythrocytes and excitable cells. Annu Rev Physiol. 1983;45:359–374. doi: 10.1146/annurev.ph.45.030183.002043. [DOI] [PubMed] [Google Scholar]
  27. Suarez-Kurtz G. The depolarizing afterpotential of crab muscle fibres. A sodium-dependent process mediated by intracellular calcium. J Physiol. 1979 Jan;286:317–329. doi: 10.1113/jphysiol.1979.sp012621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. 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]
  29. Walden J., Speckmann E. J. Effects of quinine on membrane potential and membrane currents in identified neurons of Helix pomatia. Neurosci Lett. 1981 Dec 11;27(2):139–143. doi: 10.1016/0304-3940(81)90258-5. [DOI] [PubMed] [Google Scholar]
  30. Weinreich D. Ionic mechanism of post-tetanic potentiation at the neuromuscular junction of the frog. J Physiol. 1971 Jan;212(2):431–446. doi: 10.1113/jphysiol.1971.sp009333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Younkin S. G. An analysis of the role of calcium in facilitation at the frog neuromuscular junction. J Physiol. 1974 Feb;237(1):1–14. doi: 10.1113/jphysiol.1974.sp010466. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES