Abstract
The presynaptic nerve terminal is of key importance in communication in the nervous system. Its primary role is to release transmitter quanta on the arrival of an appropriate stimulus. The structural basis of these transmitter quanta are the synaptic vesicles that fuse with the surface membrane of the nerve terminal, to release their content of neurotransmitter molecules and other vesicular components. We subdivide the control of quantal release into two major classes: the processes that take place before the fusion of the synaptic vesicle with the surface membrane (the pre-fusion control) and the processes that occur after the fusion of the vesicle (the post-fusion control). The pre-fusion control is the main determinant of transmitter release. It is achieved by a wide variety of cellular components, among them the ion channels. There are reports of several hundred different ion channel molecules at the surface membrane of the nerve terminal, that for convenience can be grouped into eight major categories. They are the voltage-dependent calcium channels, the potassium channels, the calcium-gated potassium channels, the sodium channels, the chloride channels, the non-selective channels, the ligand gated channels and the stretch-activated channels. There are several categories of intracellular channels in the mitochondria, endoplasmic reticulum and the synaptic vesicles. We speculate that the vesicle channels may be of an importance in the post-fusion control of transmitter release.
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- Alnaes E., Rahamimoff R. On the role of mitochondria in transmitter release from motor nerve terminals. J Physiol. 1975 Jun;248(2):285–306. doi: 10.1113/jphysiol.1975.sp010974. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Alvarez de Toledo G., Fernández-Chacón R., Fernández J. M. Release of secretory products during transient vesicle fusion. Nature. 1993 Jun 10;363(6429):554–558. doi: 10.1038/363554a0. [DOI] [PubMed] [Google Scholar]
- Artalejo C. R., Elhamdani A., Palfrey H. C. Secretion: dense-core vesicles can kiss-and-run too. Curr Biol. 1998 Jan 15;8(2):R62–R65. doi: 10.1016/s0960-9822(98)70036-3. [DOI] [PubMed] [Google Scholar]
- Augustine G. J., Charlton M. P. Calcium dependence of presynaptic calcium current and post-synaptic response at the squid giant synapse. J Physiol. 1986 Dec;381:619–640. doi: 10.1113/jphysiol.1986.sp016347. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Augustine G. J., Charlton M. P., Smith S. J. Calcium entry and transmitter release at voltage-clamped nerve terminals of squid. J Physiol. 1985 Oct;367:163–181. doi: 10.1113/jphysiol.1985.sp015819. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Augustine G. J., Charlton M. P., Smith S. J. Calcium entry into voltage-clamped presynaptic terminals of squid. J Physiol. 1985 Oct;367:143–162. doi: 10.1113/jphysiol.1985.sp015818. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bablito J., Jover E., Couraud F. Activation of the voltage-sensitive sodium channel by a beta-scorpion toxin in rat brain nerve-ending particles. J Neurochem. 1986 Jun;46(6):1763–1770. doi: 10.1111/j.1471-4159.1986.tb08494.x. [DOI] [PubMed] [Google Scholar]
- 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]
- Bielefeldt K., Rotter J. L., Jackson M. B. Three potassium channels in rat posterior pituitary nerve terminals. J Physiol. 1992 Dec;458:41–67. doi: 10.1113/jphysiol.1992.sp019405. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Brethes D., Dayanithi G., Letellier L., Nordmann J. J. Depolarization-induced Ca2+ increase in isolated neurosecretory nerve terminals measured with fura-2. Proc Natl Acad Sci U S A. 1987 Mar;84(5):1439–1443. doi: 10.1073/pnas.84.5.1439. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Butkevich A., Ohana O., Meir A., Rahamimoff R. Voltage dependent switch in the activity mode of the K+ channel in presynaptic nerve terminals. Neuroreport. 1997 Jul 28;8(11):2539–2545. doi: 10.1097/00001756-199707280-00024. [DOI] [PubMed] [Google Scholar]
- Cazalis M., Dayanithi G., Nordmann J. J. Hormone release from isolated nerve endings of the rat neurohypophysis. J Physiol. 1987 Sep;390:55–70. doi: 10.1113/jphysiol.1987.sp016686. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ceccarelli B., Grohovaz F., Hurlbut W. P. Freeze-fracture studies of frog neuromuscular junctions during intense release of neurotransmitter. II. Effects of electrical stimulation and high potassium. J Cell Biol. 1979 Apr;81(1):178–192. doi: 10.1083/jcb.81.1.178. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ceccarelli B., Hurlbut W. P. Ca2+-dependent recycling of synaptic vesicles at the frog neuromuscular junction. J Cell Biol. 1980 Oct;87(1):297–303. doi: 10.1083/jcb.87.1.297. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ceccarelli B., Hurlbut W. P., Iezzi N. Effect of alpha-latrotoxin on the frog neuromuscular junction at low temperature. J Physiol. 1988 Aug;402:195–217. doi: 10.1113/jphysiol.1988.sp017200. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ceccarelli B., Hurlbut W. P., Mauro A. Depletion of vesicles from frog neuromuscular junctions by prolonged tetanic stimulation. J Cell Biol. 1972 Jul;54(1):30–38. doi: 10.1083/jcb.54.1.30. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ceccarelli B., Hurlbut W. P., Mauro A. Turnover of transmitter and synaptic vesicles at the frog neuromuscular junction. J Cell Biol. 1973 May;57(2):499–524. doi: 10.1083/jcb.57.2.499. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ceccarelli B., Hurlbut W. P. Vesicle hypothesis of the release of quanta of acetylcholine. Physiol Rev. 1980 Apr;60(2):396–441. doi: 10.1152/physrev.1980.60.2.396. [DOI] [PubMed] [Google Scholar]
- Chen B. M., Grinnell A. D. Integrins and modulation of transmitter release from motor nerve terminals by stretch. Science. 1995 Sep 15;269(5230):1578–1580. doi: 10.1126/science.7667637. [DOI] [PubMed] [Google Scholar]
- Chen B. M., Grinnell A. D. Kinetics, Ca2+ dependence, and biophysical properties of integrin-mediated mechanical modulation of transmitter release from frog motor nerve terminals. J Neurosci. 1997 Feb 1;17(3):904–916. doi: 10.1523/JNEUROSCI.17-03-00904.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chen B. M., Grinnell A. D. Regulation of transmitter release by muscle length in frog motor nerve terminals. Dynamics of the effect and the role of integrin-ECM interactions. Adv Second Messenger Phosphoprotein Res. 1994;29:383–398. [PubMed] [Google Scholar]
- Clark J. M., Brooks M. W. Role of ion channels and intraterminal calcium homeostasis in the action of deltamethrin at presynaptic nerve terminals. Biochem Pharmacol. 1989 Jul 15;38(14):2233–2245. doi: 10.1016/0006-2952(89)90460-7. [DOI] [PubMed] [Google Scholar]
- Coniglio L. M., Hardwick J. C., Parsons R. L. Quantal transmitter release at snake twitch and tonic muscle fibres during prolonged nerve terminal depolarization. J Physiol. 1993 Jul;466:383–403. [PMC free article] [PubMed] [Google Scholar]
- Crespi D., Gobbi M., Mennini T. 5-HT3 serotonin hetero-receptors inhibit [3H]acethylcholine release in rat cortical synaptosomes. Pharmacol Res. 1997 Apr;35(4):351–354. doi: 10.1006/phrs.1997.0143. [DOI] [PubMed] [Google Scholar]
- DUDEL J., KUFFLER S. W. Presynaptic inhibition at the crayfish neuromuscular junction. J Physiol. 1961 Mar;155:543–562. doi: 10.1113/jphysiol.1961.sp006646. [DOI] [PMC free article] [PubMed] [Google Scholar]
- David G., Barrett J. N., Barrett E. F. Evidence that mitochondria buffer physiological Ca2+ loads in lizard motor nerve terminals. J Physiol. 1998 May 15;509(Pt 1):59–65. doi: 10.1111/j.1469-7793.1998.059bo.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Deist M., Repp H., Dreyer F. Sulfonylurea-sensitive K+ channels and their probable role for the membrane potential of mouse motor nerve endings. Pflugers Arch. 1992 Jun;421(2-3):292–294. doi: 10.1007/BF00374843. [DOI] [PubMed] [Google Scholar]
- Edry-Schiller J., Ginsburg S., Rahamimoff R. A bursting potassium channel in isolated cholinergic synaptosomes of Torpedo electric organ. J Physiol. 1991 Aug;439:627–647. doi: 10.1113/jphysiol.1991.sp018685. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Edry-Schiller J., Ginsburg S., Rahamimoff R. A bursting potassium channel in isolated cholinergic synaptosomes of Torpedo electric organ. J Physiol. 1991 Aug;439:627–647. doi: 10.1113/jphysiol.1991.sp018685. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Edry-Schiller J., Rahamimoff R. Activation and inactivation of the bursting potassium channel from fused Torpedo synaptosomes. J Physiol. 1993 Nov;471:659–678. doi: 10.1113/jphysiol.1993.sp019921. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Engblom A. C., Eriksson K. S., Akerman K. E. Glycine and GABAA receptor-mediated chloride fluxes in synaptoneurosomes from different parts of the rat brain. Brain Res. 1996 Mar 11;712(1):74–83. doi: 10.1016/0006-8993(95)01484-5. [DOI] [PubMed] [Google Scholar]
- FATT P., KATZ B. Spontaneous subthreshold activity at motor nerve endings. J Physiol. 1952 May;117(1):109–128. [PMC free article] [PubMed] [Google Scholar]
- Fatatis A., Holtzclaw L., Payza K., Russell J. T. Secretion from rat neurohypophysial nerve terminals (neurosecretosomes) rapidly inactivates despite continued elevation of intracellular Ca2+. Brain Res. 1992 Mar 6;574(1-2):33–41. doi: 10.1016/0006-8993(92)90796-c. [DOI] [PubMed] [Google Scholar]
- Fesce R., Grohovaz F., Hurlbut W. P., Ceccarelli B. Freeze-fracture studies of frog neuromuscular junctions during intense release of neurotransmitter. III. A morphometric analysis of the number and diameter of intramembrane particles. J Cell Biol. 1980 May;85(2):337–345. doi: 10.1083/jcb.85.2.337. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fesce R., Segal J. R., Ceccarelli B., Hurlbut W. P. Effects of black widow spider venom and Ca2+ on quantal secretion at the frog neuromuscular junction. J Gen Physiol. 1986 Jul;88(1):59–81. doi: 10.1085/jgp.88.1.59. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Finger W., Martin C. Presynaptic effect of gamma-aminobutyric acid on the inhibitory nerve and nerve terminals in the crayfish neuromuscular junction. Neurosci Lett. 1989 Feb 13;97(1-2):129–134. doi: 10.1016/0304-3940(89)90151-1. [DOI] [PubMed] [Google Scholar]
- Grunstein M. Histone acetylation in chromatin structure and transcription. Nature. 1997 Sep 25;389(6649):349–352. doi: 10.1038/38664. [DOI] [PubMed] [Google Scholar]
- Haimann C., Meldolesi J., Ceccarelli B. The phorbol ester, 12-O-tetradecanoyl-phorbol-13-acetate, enhances the evoked quanta release of acetylcholine at the frog neuromuscular junction. Pflugers Arch. 1987 Jan;408(1):27–31. doi: 10.1007/BF00581836. [DOI] [PubMed] [Google Scholar]
- Hayashi J. H., Stuart A. E. Currents in the presynaptic terminal arbors of barnacle photoreceptors. Vis Neurosci. 1993 Mar-Apr;10(2):261–270. doi: 10.1017/s0952523800003667. [DOI] [PubMed] [Google Scholar]
- Henkel A. W., Almers W. Fast steps in exocytosis and endocytosis studied by capacitance measurements in endocrine cells. Curr Opin Neurobiol. 1996 Jun;6(3):350–357. doi: 10.1016/s0959-4388(96)80119-x. [DOI] [PubMed] [Google Scholar]
- 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]
- Heuser J. E., Reese T. S. Structural changes after transmitter release at the frog neuromuscular junction. J Cell Biol. 1981 Mar;88(3):564–580. doi: 10.1083/jcb.88.3.564. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Heuser J. E. Review of electron microscopic evidence favouring vesicle exocytosis as the structural basis for quantal release during synaptic transmission. Q J Exp Physiol. 1989 Dec;74(7):1051–1069. doi: 10.1113/expphysiol.1989.sp003333. [DOI] [PubMed] [Google Scholar]
- Hurlbut W. P., Iezzi N., Fesce R., Ceccarelli B. Correlation between quantal secretion and vesicle loss at the frog neuromuscular junction. J Physiol. 1990 Jun;425:501–526. doi: 10.1113/jphysiol.1990.sp018115. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hussy N. Calcium-activated chloride channels in cultured embryonic Xenopus spinal neurons. J Neurophysiol. 1992 Dec;68(6):2042–2050. doi: 10.1152/jn.1992.68.6.2042. [DOI] [PubMed] [Google Scholar]
- Ingber D. E. Tensegrity: the architectural basis of cellular mechanotransduction. Annu Rev Physiol. 1997;59:575–599. doi: 10.1146/annurev.physiol.59.1.575. [DOI] [PubMed] [Google Scholar]
- Inoue I., Nagase H., Kishi K., Higuti T. ATP-sensitive K+ channel in the mitochondrial inner membrane. Nature. 1991 Jul 18;352(6332):244–247. doi: 10.1038/352244a0. [DOI] [PubMed] [Google Scholar]
- Issa N. P., Hudspeth A. J. Clustering of Ca2+ channels and Ca(2+)-activated K+ channels at fluorescently labeled presynaptic active zones of hair cells. Proc Natl Acad Sci U S A. 1994 Aug 2;91(16):7578–7582. doi: 10.1073/pnas.91.16.7578. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jackson M. B., Konnerth A., Augustine G. J. Action potential broadening and frequency-dependent facilitation of calcium signals in pituitary nerve terminals. Proc Natl Acad Sci U S A. 1991 Jan 15;88(2):380–384. doi: 10.1073/pnas.88.2.380. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jackson M. B., Zhang S. J. Action potential propagation and propagation block by GABA in rat posterior pituitary nerve terminals. J Physiol. 1995 Mar 15;483(Pt 3):597–611. doi: 10.1113/jphysiol.1995.sp020609. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Katz B. Bayliss-Starling memorial lecture (1985). Reminiscences of a physiologist, 50 years after. J Physiol. 1986 Jan;370:1–12. doi: 10.1113/jphysiol.1986.sp015918. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Katz B., Miledi R. Release of acetylcholine from a nerve terminal by electric pulses of variable strength and duration. Nature. 1965 Sep 4;207(5001):1097–1098. doi: 10.1038/2071097a0. [DOI] [PubMed] [Google Scholar]
- Kelly M. L., Woodbury D. J. Ion channels from synaptic vesicle membrane fragments reconstituted into lipid bilayers. Biophys J. 1996 Jun;70(6):2593–2599. doi: 10.1016/S0006-3495(96)79830-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kiene M. L., Stadler H. Synaptic vesicles in electromotoneurones. I. Axonal transport, site of transmitter uptake and processing of a core proteoglycan during maturation. EMBO J. 1987 Aug;6(8):2209–2215. doi: 10.1002/j.1460-2075.1987.tb02492.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Kuhn D. M., Volknandt W., Stadler H., Zimmermann H. Cholinergic vesicle specific proteoglycan: stability in isolated vesicles and in synaptosomes during induced transmitter release. J Neurochem. 1988 Jan;50(1):11–16. doi: 10.1111/j.1471-4159.1988.tb13223.x. [DOI] [PubMed] [Google Scholar]
- Lee C. J., Dayanithi G., Nordmann J. J., Lemos J. R. Possible role during exocytosis of a Ca(2+)-activated channel in neurohypophysial granules. Neuron. 1992 Feb;8(2):335–342. doi: 10.1016/0896-6273(92)90299-s. [DOI] [PubMed] [Google Scholar]
- Lee K., Dixon A. K., Rowe I. C., Ashford M. L., Richardson P. J. Direct demonstration of sulphonylurea-sensitive KATP channels on nerve terminals of the rat motor cortex. Br J Pharmacol. 1995 Jun;115(3):385–387. doi: 10.1111/j.1476-5381.1995.tb16344.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lee K., Dixon A. K., Rowe I. C., Ashford M. L., Richardson P. J. The high-affinity sulphonylurea receptor regulates KATP channels in nerve terminals of the rat motor cortex. J Neurochem. 1996 Jun;66(6):2562–2571. doi: 10.1046/j.1471-4159.1996.66062562.x. [DOI] [PubMed] [Google Scholar]
- Legendre P., Tixier-Vidal A., Brigant J. L., Vincent J. D. Electrophysiology and ultrastructure of mouse hypothalamic neurons in culture: a correlative analysis during development. Brain Res. 1988 Oct 1;471(2):273–285. doi: 10.1016/0165-3806(88)90105-8. [DOI] [PubMed] [Google Scholar]
- Lemos J. R., Nordmann J. J., Cooke I. M., Stuenkel E. L. Single channels and ionic currents in peptidergic nerve terminals. 1986 Jan 30-Feb 5Nature. 319(6052):410–412. doi: 10.1038/319410a0. [DOI] [PubMed] [Google Scholar]
- Lemos J. R., Nordmann J. J. Ionic channels and hormone release from peptidergic nerve terminals. J Exp Biol. 1986 Sep;124:53–72. doi: 10.1242/jeb.124.1.53. [DOI] [PubMed] [Google Scholar]
- Lukasiewicz P. D. GABAC receptors in the vertebrate retina. Mol Neurobiol. 1996 Jun;12(3):181–194. doi: 10.1007/BF02755587. [DOI] [PubMed] [Google Scholar]
- Mason W. T., Dyball R. E. Single ion channel activity in peptidergic nerve terminals of the isolated rat neurohypophysis related to stimulation of neural stalk axons. Brain Res. 1986 Sep 24;383(1-2):279–286. doi: 10.1016/0006-8993(86)90026-0. [DOI] [PubMed] [Google Scholar]
- Maura G., Andrioli G. C., Cavazzani P., Raiteri M. 5-Hydroxytryptamine3 receptors sited on cholinergic axon terminals of human cerebral cortex mediate inhibition of acetylcholine release. J Neurochem. 1992 Jun;58(6):2334–2337. doi: 10.1111/j.1471-4159.1992.tb10983.x. [DOI] [PubMed] [Google Scholar]
- McGehee D. S., Role L. W. Presynaptic ionotropic receptors. Curr Opin Neurobiol. 1996 Jun;6(3):342–349. doi: 10.1016/s0959-4388(96)80118-8. [DOI] [PubMed] [Google Scholar]
- Meir A., Rahamimoff R. A voltage-dependent and calcium-permeable ion channel in fused presynaptic terminals of Torpedo. J Neurophysiol. 1996 May;75(5):1858–1870. doi: 10.1152/jn.1996.75.5.1858. [DOI] [PubMed] [Google Scholar]
- Melamed-Book N., Rahamimoff R. The revival of the role of the mitochondrion in regulation of transmitter release. J Physiol. 1998 May 15;509(Pt 1):2–2. doi: 10.1111/j.1469-7793.1998.002bo.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Meldolesi J., Ceccarelli B. Exocytosis and membrane recycling. Philos Trans R Soc Lond B Biol Sci. 1981 Dec 18;296(1080):55–65. doi: 10.1098/rstb.1981.0171. [DOI] [PubMed] [Google Scholar]
- Motin L., Bennett M. R. Effect of P2-purinoceptor antagonists on glutamatergic transmission in the rat hippocampus. Br J Pharmacol. 1995 Aug;115(7):1276–1280. doi: 10.1111/j.1476-5381.1995.tb15036.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nanavati C., Fernandez J. M. The secretory granule matrix: a fast-acting smart polymer. Science. 1993 Feb 12;259(5097):963–965. doi: 10.1126/science.8438154. [DOI] [PubMed] [Google Scholar]
- Nichols R. A., Mollard P. Direct observation of serotonin 5-HT3 receptor-induced increases in calcium levels in individual brain nerve terminals. J Neurochem. 1996 Aug;67(2):581–592. doi: 10.1046/j.1471-4159.1996.67020581.x. [DOI] [PubMed] [Google Scholar]
- Okada T., Horiguchi H., Tachibana M. Ca(2+)-dependent Cl- current at the presynaptic terminals of goldfish retinal bipolar cells. Neurosci Res. 1995 Oct;23(3):297–303. doi: 10.1016/0168-0102(95)00955-8. [DOI] [PubMed] [Google Scholar]
- Ouyang Y., Martone M. E., Deerinck T. J., Airey J. A., Sutko J. L., Ellisman M. H. Differential distribution and subcellular localization of ryanodine receptor isoforms in the chicken cerebellum during development. Brain Res. 1997 Nov 14;775(1-2):52–62. doi: 10.1016/s0006-8993(97)00840-8. [DOI] [PubMed] [Google Scholar]
- Palfrey H. C., Artalejo C. R. Vesicle recycling revisited: rapid endocytosis may be the first step. Neuroscience. 1998 Apr;83(4):969–989. doi: 10.1016/s0306-4522(97)00453-3. [DOI] [PubMed] [Google Scholar]
- Pozzan T., Rizzuto R., Volpe P., Meldolesi J. Molecular and cellular physiology of intracellular calcium stores. Physiol Rev. 1994 Jul;74(3):595–636. doi: 10.1152/physrev.1994.74.3.595. [DOI] [PubMed] [Google Scholar]
- Rahamimoff R., DeRiemer S. A., Ginsburg S., Kaiserman I., Sakmann B., Shapira R., Stadler H., Yakir N. Ionic channels in synaptic vesicles: are they involved in transmitter release? Q J Exp Physiol. 1989 Dec;74(7):1019–1031. doi: 10.1113/expphysiol.1989.sp003330. [DOI] [PubMed] [Google Scholar]
- Rahamimoff R., DeRiemer S. A., Ginsburg S., Kaiserman I., Sakmann B., Stadler H., Yakir N. Ionic channels and proteins in synaptic vesicles: facts and speculations. J Basic Clin Physiol Pharmacol. 1990 Jan-Dec;1(1-4):7–17. doi: 10.1515/jbcpp.1990.1.1-4.7. [DOI] [PubMed] [Google Scholar]
- Rahamimoff R., Edry-Schiller J., Ginsburg S. A long closed state of the synaptosomal bursting potassium channel confers a statistical memory. J Neurophysiol. 1992 Dec;68(6):2260–2263. doi: 10.1152/jn.1992.68.6.2260. [DOI] [PubMed] [Google Scholar]
- Rahamimoff R., Edry-Schiller J., Rubin-Fraenkel M., Butkevich A., Ginsburg S. Oscillations in the activity of a potassium channel at the presynaptic nerve terminal. J Neurophysiol. 1995 Jun;73(6):2448–2458. doi: 10.1152/jn.1995.73.6.2448. [DOI] [PubMed] [Google Scholar]
- Rahamimoff R., Fernandez J. M. Pre- and postfusion regulation of transmitter release. Neuron. 1997 Jan;18(1):17–27. doi: 10.1016/s0896-6273(01)80043-x. [DOI] [PubMed] [Google Scholar]
- Reyes M., Stanton P. K. Induction of hippocampal long-term depression requires release of Ca2+ from separate presynaptic and postsynaptic intracellular stores. J Neurosci. 1996 Oct 1;16(19):5951–5960. doi: 10.1523/JNEUROSCI.16-19-05951.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rizzuto R., Brini M., Bastianutto C., Marsault R., Pozzan T. Photoprotein-mediated measurement of calcium ion concentration in mitochondria of living cells. Methods Enzymol. 1995;260:417–428. doi: 10.1016/0076-6879(95)60155-4. [DOI] [PubMed] [Google Scholar]
- Roberts W. M., Jacobs R. A., Hudspeth A. J. Colocalization of ion channels involved in frequency selectivity and synaptic transmission at presynaptic active zones of hair cells. J Neurosci. 1990 Nov;10(11):3664–3684. doi: 10.1523/JNEUROSCI.10-11-03664.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Roberts W. M. Localization of calcium signals by a mobile calcium buffer in frog saccular hair cells. J Neurosci. 1994 May;14(5 Pt 2):3246–3262. doi: 10.1523/JNEUROSCI.14-05-03246.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Robitaille R., Adler E. M., Charlton M. P. Calcium channels and calcium-gated potassium channels at the frog neuromuscular junction. J Physiol Paris. 1993;87(1):15–24. doi: 10.1016/0928-4257(93)90020-t. [DOI] [PubMed] [Google Scholar]
- Robitaille R., Garcia M. L., Kaczorowski G. J., Charlton M. P. Functional colocalization of calcium and calcium-gated potassium channels in control of transmitter release. Neuron. 1993 Oct;11(4):645–655. doi: 10.1016/0896-6273(93)90076-4. [DOI] [PubMed] [Google Scholar]
- Rosenboom H., Lindau M. Exo-endocytosis and closing of the fission pore during endocytosis in single pituitary nerve terminals internally perfused with high calcium concentrations. Proc Natl Acad Sci U S A. 1994 Jun 7;91(12):5267–5271. doi: 10.1073/pnas.91.12.5267. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rudomin P. Presynaptic inhibition of muscle spindle and tendon organ afferents in the mammalian spinal cord. Trends Neurosci. 1990 Dec;13(12):499–505. doi: 10.1016/0166-2236(90)90084-n. [DOI] [PubMed] [Google Scholar]
- Ryan T. A., Reuter H., Wendland B., Schweizer F. E., Tsien R. W., Smith S. J. The kinetics of synaptic vesicle recycling measured at single presynaptic boutons. Neuron. 1993 Oct;11(4):713–724. doi: 10.1016/0896-6273(93)90081-2. [DOI] [PubMed] [Google Scholar]
- Ryan T. A., Smith S. J., Reuter H. The timing of synaptic vesicle endocytosis. Proc Natl Acad Sci U S A. 1996 May 28;93(11):5567–5571. doi: 10.1073/pnas.93.11.5567. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sackin H. Stretch-activated ion channels. Kidney Int. 1995 Oct;48(4):1134–1147. doi: 10.1038/ki.1995.397. [DOI] [PubMed] [Google Scholar]
- Salzberg B. M., Obaid A. L., Senseman D. M., Gainer H. Optical recording of action potentials from vertebrate nerve terminals using potentiometric probes provides evidence for sodium and calcium components. Nature. 1983 Nov 3;306(5938):36–40. doi: 10.1038/306036a0. [DOI] [PubMed] [Google Scholar]
- Sorgato M. C., Keller B. U., Stühmer W. Patch-clamping of the inner mitochondrial membrane reveals a voltage-dependent ion channel. Nature. 1987 Dec 3;330(6147):498–500. doi: 10.1038/330498a0. [DOI] [PubMed] [Google Scholar]
- Sorgato M. C., Moran O., De Pinto V., Keller B. U., Stuehmer W. Further investigation on the high-conductance ion channel of the inner membrane of mitochondria. J Bioenerg Biomembr. 1989 Aug;21(4):485–496. doi: 10.1007/BF00762520. [DOI] [PubMed] [Google Scholar]
- Stadler H., Dowe G. H. Identification of a heparan sulphate-containing proteoglycan as a specific core component of cholinergic synaptic vesicles from Torpedo marmorata. EMBO J. 1982;1(11):1381–1384. doi: 10.1002/j.1460-2075.1982.tb01326.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stadler H., Kiene M. L. Synaptic vesicles in electromotoneurones. II. Heterogeneity of populations is expressed in uptake properties; exocytosis and insertion of a core proteoglycan into the extracellular matrix. EMBO J. 1987 Aug;6(8):2217–2221. doi: 10.1002/j.1460-2075.1987.tb02493.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stanford I. M., Lacey M. G. Electrophysiological investigation of adenosine trisphosphate-sensitive potassium channels in the rat substantia nigra pars reticulata. Neuroscience. 1996 Sep;74(2):499–509. doi: 10.1016/0306-4522(96)00151-0. [DOI] [PubMed] [Google Scholar]
- Storrie B., Desjardins M. The biogenesis of lysosomes: is it a kiss and run, continuous fusion and fission process? Bioessays. 1996 Nov;18(11):895–903. doi: 10.1002/bies.950181108. [DOI] [PubMed] [Google Scholar]
- Stuenkel E. L., Ruben P., Cooke I. M., Lemos J. R. Sodium-activated cation channels in peptidergic nerve terminals. Brain Res. 1990 May 28;517(1-2):35–43. doi: 10.1016/0006-8993(90)91004-z. [DOI] [PubMed] [Google Scholar]
- Sun X. P., Stanley E. F. An ATP-activated, ligand-gated ion channel on a cholinergic presynaptic nerve terminal. Proc Natl Acad Sci U S A. 1996 Mar 5;93(5):1859–1863. doi: 10.1073/pnas.93.5.1859. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Takata Y., Shimada F., Kato H. Possible involvement of ATP-sensitive K+ channels in the inhibition of rat central adrenergic neurotransmission under hypoxia. Jpn J Pharmacol. 1993 Jul;62(3):279–287. doi: 10.1254/jjp.62.279. [DOI] [PubMed] [Google Scholar]
- Tareilus E., Hanke W., Breer H. Identification of a cationic channel in synaptosomal membranes. Eur Biophys J. 1990;19(2):79–86. doi: 10.1007/BF00185090. [DOI] [PubMed] [Google Scholar]
- 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]
- Torri-Tarelli F., Grohovaz F., Fesce R., Ceccarelli B. Temporal coincidence between synaptic vesicle fusion and quantal secretion of acetylcholine. J Cell Biol. 1985 Oct;101(4):1386–1399. doi: 10.1083/jcb.101.4.1386. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Torri-Tarelli F., Haimann C., Ceccarelli B. Coated vesicles and pits during enhanced quantal release of acetylcholine at the neuromuscular junction. J Neurocytol. 1987 Apr;16(2):205–214. doi: 10.1007/BF01795304. [DOI] [PubMed] [Google Scholar]
- Uvnäs B., Aborg C. H. Cation exchange--a common mechanism in the storage and release of biogenic amines stored in granules (vesicles)? I. Comparative studies on the uptake of sodium and biogenic amines by the weak cation (carboxyl) exchangers Amberlite IRC-50 and Sephadex C-50 and by biogenic (granule-enriched) materials in vitro. Acta Physiol Scand. 1983 Nov;119(3):225–234. doi: 10.1111/j.1748-1716.1983.tb07332.x. [DOI] [PubMed] [Google Scholar]
- Valtorta F., Fesce R., Grohovaz F., Haimann C., Hurlbut W. P., Iezzi N., Torri Tarelli F., Villa A., Ceccarelli B. Neurotransmitter release and synaptic vesicle recycling. Neuroscience. 1990;35(3):477–489. doi: 10.1016/0306-4522(90)90323-v. [DOI] [PubMed] [Google Scholar]
- Wahl P., Elster L., Schousboe A. Identification and function of glycine receptors in cultured cerebellar granule cells. J Neurochem. 1994 Jun;62(6):2457–2463. doi: 10.1046/j.1471-4159.1994.62062457.x. [DOI] [PubMed] [Google Scholar]
- Watts A. E., Hicks G. A., Henderson G. Putative pre- and postsynaptic ATP-sensitive potassium channels in the rat substantia nigra in vitro. J Neurosci. 1995 Apr;15(4):3065–3074. doi: 10.1523/JNEUROSCI.15-04-03065.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Woodbury D. J. Evaluation of the evidence for ion channels in synaptic vesicles. Mol Membr Biol. 1995 Apr-Jun;12(2):165–171. doi: 10.3109/09687689509027504. [DOI] [PubMed] [Google Scholar]
- Yakir N., Rahamimoff R. The non-specific ion channel in Torpedo ocellata fused synaptic vesicles. J Physiol. 1995 Jun 15;485(Pt 3):683–697. doi: 10.1113/jphysiol.1995.sp020762. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ye G. L., Leung C. K., Yung W. H. Pre-synaptic effect of the ATP-sensitive potassium channel opener diazoxide on rat substantia nigra pars reticulata neurons. Brain Res. 1997 Apr 4;753(1):1–7. doi: 10.1016/s0006-8993(96)01473-4. [DOI] [PubMed] [Google Scholar]
- Zhang S. J., Jackson M. B. GABA-activated chloride channels in secretory nerve endings. Science. 1993 Jan 22;259(5094):531–534. doi: 10.1126/science.8380942. [DOI] [PubMed] [Google Scholar]
