Skip to main content
NCBI home page
The Journal of General Physiology logoLink to The Journal of General Physiology
. 1982 Jun 1;79(6):1065–1087. doi: 10.1085/jgp.79.6.1065

Influx of calcium, strontium, and barium in presynaptic nerve endings

PMCID: PMC2216453  PMID: 6286843

Abstract

Depolarization-induced (potassium-stimulated) influx of 45Ca, 85Sr, and 133Ba was measured in synaptosomes prepared from rat brain. There are two phases of divalent cation entry, "fast" and "slow;" each phase is mediated by channels with distinctive characteristics. The fast channels inactivate (within 1 s) and are blocked by low concentrations (less than 1 micro M) of La. The slow channels do not inactivate (within 10 s), and are blocked by high concentrations (greater than 50 micro M) of La. Divalent cation influx through both channels saturates with increasing concentrations of permeant divalent cation; in addition, each permeant divalent cation species competitively blocks the influx of other permeant species. These results are consistent with the presence of "binding sites" for divalent cations in the fast and slow channels. The Ca:Sr:Ba permeability ratio, determined by measuring the influx of all three species in triple-label experiments, was 6:3:2 for the fast channel and 6:3:1 for the slow channel. A simple model for ion selectivity, based on the presence of a binding site in the channel, could account well for slow and, to some extent, for fast, channel selectivity data.

Full Text

The Full Text of this article is available as a PDF (1.2 MB).

Selected References

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

  1. Adams D. J., Gage P. W. Divalent ion currents and the delayed potassium conductance in an Aplysia neurone. J Physiol. 1980 Jul;304:297–313. doi: 10.1113/jphysiol.1980.sp013325. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Akaike N., Fishman H. M., Lee K. S., Moore L. E., Brown A. M. The units of calcium conduction in Helix neurones. Nature. 1978 Jul 27;274(5669):379–382. doi: 10.1038/274379a0. [DOI] [PubMed] [Google Scholar]
  3. Blaustein M. P. Effects of potassium, veratridine, and scorpion venom on calcium accumulation and transmitter release by nerve terminals in vitro. J Physiol. 1975 Jun;247(3):617–655. doi: 10.1113/jphysiol.1975.sp010950. [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. 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]
  6. Blaustein M. P., Oborn C. J. The influence of sodium on calcium fluxes in pinched-off nerve terminals in vitro. J Physiol. 1975 Jun;247(3):657–686. doi: 10.1113/jphysiol.1975.sp010951. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. 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]
  8. Diamond J. M., Wright E. M. Biological membranes: the physical basis of ion and nonelectrolyte selectivity. Annu Rev Physiol. 1969;31:581–646. doi: 10.1146/annurev.ph.31.030169.003053. [DOI] [PubMed] [Google Scholar]
  9. Dodge F. A., Jr, Miledi R., Rahamimoff R. Strontium and quantal release of transmitter at the neuromuscular junction. J Physiol. 1969 Jan;200(1):267–283. doi: 10.1113/jphysiol.1969.sp008692. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. 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]
  12. 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]
  13. Hagiwara S. Ca-dependent action potential. Membranes. 1975;3:359–381. [PubMed] [Google Scholar]
  14. 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]
  15. Hajós F. An improved method for the preparation of synaptosomal fractions in high purity. Brain Res. 1975 Aug 15;93(3):485–489. doi: 10.1016/0006-8993(75)90186-9. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. Hille B., Woodhull A. M., Shapiro B. I. Negative surface charge near sodium channels of nerve: divalent ions, monovalent ions, and pH. Philos Trans R Soc Lond B Biol Sci. 1975 Jun 10;270(908):301–318. doi: 10.1098/rstb.1975.0011. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Krueger B. K., Ratzlaff R. W., Strichartz G. R., Blaustein M. P. Saxitoxin binding to synaptosomes, membranes, and solubilized binding sites from rat brain. J Membr Biol. 1979 Nov 30;50(3-4):287–310. doi: 10.1007/BF01868894. [DOI] [PubMed] [Google Scholar]
  20. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  21. Lehninger A. L. Mitochondria and calcium ion transport. Biochem J. 1970 Sep;119(2):129–138. doi: 10.1042/bj1190129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Madden K. S., Van der Kloot W. Surface charges and the effects of calcium on the frequency of miniature end-plate potentials at the frog neuromuscular junction. J Physiol. 1978 Mar;276:227–232. doi: 10.1113/jphysiol.1978.sp012230. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. McLachlan E. M. The effects of strontium and barium ions at synapses in sympathetic ganglia. J Physiol. 1977 May;267(2):497–518. doi: 10.1113/jphysiol.1977.sp011823. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. Muller R. U., Finkelstein A. The electrostatic basis of Mg++ inhibition of transmitter release. Proc Natl Acad Sci U S A. 1974 Mar;71(3):923–926. doi: 10.1073/pnas.71.3.923. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Nachshen D. A., Blaustein M. P. Regulation of nerve terminal calcium channel selectivity by a weak acid site. Biophys J. 1979 May;26(2):329–334. doi: 10.1016/S0006-3495(79)85253-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]
  28. Okamoto H., Takahashi K., Yamashita N. Ionic currents through the membrane of the mammalian oocyte and their comparison with those in the tunicate and sea urchin. J Physiol. 1977 May;267(2):465–495. doi: 10.1113/jphysiol.1977.sp011822. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Ramos S., Grollman E. F., Lazo P. S., Dyer S. A., Habig W. H., Hardegree M. C., Kaback H. R., Kohn L. D. Effect of tetanus toxin on the accumulation of the permeant lipophilic cation tetraphenylphosphonium by guinea pig brain synaptosomes. Proc Natl Acad Sci U S A. 1979 Oct;76(10):4783–4787. doi: 10.1073/pnas.76.10.4783. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. 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]
  31. Silinsky E. M. On the role of barium in supporting the asynchronous release of acetylcholine quanta by motor nerve impulses. J Physiol. 1978 Jan;274:157–171. doi: 10.1113/jphysiol.1978.sp012141. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. 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]
  33. 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]

Articles from The Journal of General Physiology are provided here courtesy of The Rockefeller University Press

RESOURCES