Skip to main content
Biophysical Journal logoLink to Biophysical Journal
. 1992 Dec;63(6):1500–1505. doi: 10.1016/S0006-3495(92)81731-9

Ion channels on synaptic vesicle membranes studied by planar lipid bilayer method.

M Sato 1, K Inoue 1, M Kasai 1
PMCID: PMC1262265  PMID: 1283345

Abstract

An anion selective channel and three types of cation selective channels were found in planar lipid bilayers incorporating synaptic vesicles from rat brains. In asymmetric KCl solutions (cis: 300 mM/trans: 150 mM), the anion selective channel showed a single-channel conductance of 94 pS and was inactivated by negative voltages and by 4-acetoamido-4'-isothiocyanostilbene-2,2'-disulfonic acid disodium salt (SITS). In the same solution, single-channel conductances of three types of cation selective channels were 250 pS (Type 1), 248 pS (Type 2), and 213 pS (Type 3), respectively. These channels resembled one another in single-channel conductances but were different in gating behaviors. Type 1 channel, which was most frequently observed, had a remarkable subconducting state (175 pS). Type 2 channel had a flickering state that increased as the potential became more positive, and a long inactive state that increased as the potentials were more negative. Type 3 channel, which was also sensitive to the potentials, had the open-channel probability increased as the potential became more positive.

Full text

PDF
1500

Selected References

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

  1. Augustine G. J., Charlton M. P., Smith S. J. Calcium action in synaptic transmitter release. Annu Rev Neurosci. 1987;10:633–693. doi: 10.1146/annurev.ne.10.030187.003221. [DOI] [PubMed] [Google Scholar]
  2. Breckenridge L. J., Almers W. Currents through the fusion pore that forms during exocytosis of a secretory vesicle. 1987 Aug 27-Sep 2Nature. 328(6133):814–817. doi: 10.1038/328814a0. [DOI] [PubMed] [Google Scholar]
  3. Breckenridge L. J., Almers W. Final steps in exocytosis observed in a cell with giant secretory granules. Proc Natl Acad Sci U S A. 1987 Apr;84(7):1945–1949. doi: 10.1073/pnas.84.7.1945. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cidon S., Sihra T. S. Characterization of a H+-ATPase in rat brain synaptic vesicles. Coupling to L-glutamate transport. J Biol Chem. 1989 May 15;264(14):8281–8288. [PubMed] [Google Scholar]
  5. Disbrow J. K., Gershten M. J., Ruth J. A. Uptake of L-[3H] glutamic acid by crude and purified synaptic vesicles from rat brain. Biochem Biophys Res Commun. 1982 Oct 15;108(3):1221–1227. doi: 10.1016/0006-291x(82)92130-1. [DOI] [PubMed] [Google Scholar]
  6. Farley J., Rudy B. Multiple types of voltage-dependent Ca2+-activated K+ channels of large conductance in rat brain synaptosomal membranes. Biophys J. 1988 Jun;53(6):919–934. doi: 10.1016/S0006-3495(88)83173-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Hell J. W., Maycox P. R., Jahn R. Energy dependence and functional reconstitution of the gamma-aminobutyric acid carrier from synaptic vesicles. J Biol Chem. 1990 Feb 5;265(4):2111–2117. [PubMed] [Google Scholar]
  8. Hell J. W., Maycox P. R., Stadler H., Jahn R. Uptake of GABA by rat brain synaptic vesicles isolated by a new procedure. EMBO J. 1988 Oct;7(10):3023–3029. doi: 10.1002/j.1460-2075.1988.tb03166.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Heuser J. E., Reese T. S. Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J Cell Biol. 1973 May;57(2):315–344. doi: 10.1083/jcb.57.2.315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Huttner W. B., Schiebler W., Greengard P., De Camilli P. Synapsin I (protein I), a nerve terminal-specific phosphoprotein. III. Its association with synaptic vesicles studied in a highly purified synaptic vesicle preparation. J Cell Biol. 1983 May;96(5):1374–1388. doi: 10.1083/jcb.96.5.1374. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kish P. E., Fischer-Bovenkerk C., Ueda T. Active transport of gamma-aminobutyric acid and glycine into synaptic vesicles. Proc Natl Acad Sci U S A. 1989 May;86(10):3877–3881. doi: 10.1073/pnas.86.10.3877. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Maycox P. R., Deckwerth T., Hell J. W., Jahn R. Glutamate uptake by brain synaptic vesicles. Energy dependence of transport and functional reconstitution in proteoliposomes. J Biol Chem. 1988 Oct 25;263(30):15423–15428. [PubMed] [Google Scholar]
  13. Maycox P. R., Hell J. W., Jahn R. Amino acid neurotransmission: spotlight on synaptic vesicles. Trends Neurosci. 1990 Mar;13(3):83–87. doi: 10.1016/0166-2236(90)90178-d. [DOI] [PubMed] [Google Scholar]
  14. Naito S., Ueda T. Adenosine triphosphate-dependent uptake of glutamate into protein I-associated synaptic vesicles. J Biol Chem. 1983 Jan 25;258(2):696–699. [PubMed] [Google Scholar]
  15. Nomura K., Naruse K., Watanabe K., Sokabe M. Aminoglycoside blockade of Ca2(+)-activated K+ channel from rat brain synaptosomal membranes incorporated into planar bilayers. J Membr Biol. 1990 May;115(3):241–251. doi: 10.1007/BF01868639. [DOI] [PubMed] [Google Scholar]
  16. Nomura K., Sokabe M. Anion channels from rat brain synaptosomal membranes incorporated into planar bilayers. J Membr Biol. 1991 Oct;124(1):53–62. doi: 10.1007/BF01871364. [DOI] [PubMed] [Google Scholar]
  17. Rahamimoff R., DeRiemer S. A., Sakmann B., Stadler H., Yakir N. Ion channels in synaptic vesicles from Torpedo electric organ. Proc Natl Acad Sci U S A. 1988 Jul;85(14):5310–5314. doi: 10.1073/pnas.85.14.5310. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Spruce A. E., Breckenridge L. J., Lee A. K., Almers W. Properties of the fusion pore that forms during exocytosis of a mast cell secretory vesicle. Neuron. 1990 May;4(5):643–654. doi: 10.1016/0896-6273(90)90192-i. [DOI] [PubMed] [Google Scholar]
  19. Tanifuji M., Sato M., Wada Y., Anraku Y., Kasai M. Gating behaviors of a voltage-dependent and Ca2+-activated cation channel of yeast vacuolar membrane incorporated into planar lipid bilayer. J Membr Biol. 1988 Nov;106(1):47–55. doi: 10.1007/BF01871766. [DOI] [PubMed] [Google Scholar]
  20. Thomas L., Hartung K., Langosch D., Rehm H., Bamberg E., Franke W. W., Betz H. Identification of synaptophysin as a hexameric channel protein of the synaptic vesicle membrane. Science. 1988 Nov 18;242(4881):1050–1053. doi: 10.1126/science.2461586. [DOI] [PubMed] [Google Scholar]
  21. White M. M., Miller C. A voltage-gated anion channel from the electric organ of Torpedo californica. J Biol Chem. 1979 Oct 25;254(20):10161–10166. [PubMed] [Google Scholar]
  22. Zimmerberg J., Curran M., Cohen F. S., Brodwick M. Simultaneous electrical and optical measurements show that membrane fusion precedes secretory granule swelling during exocytosis of beige mouse mast cells. Proc Natl Acad Sci U S A. 1987 Mar;84(6):1585–1589. doi: 10.1073/pnas.84.6.1585. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES