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PMID: 7707358 Published · ppublish English Journal Article Review

Neurotransmitter release at fast synapses.

The Journal of membrane biology ·Vol. 142 ·No. 3 ·1994-12-00 ·Pages 267-79

Parnas H, Parnas I

Abstract

As stated at the beginning of this review, the mechanism of neurotransmitter release is not yet known. Keeping this in mind, we shall, nevertheless, attempt to speculate and outline a possible scenario of events as it emerges from the foregoing discussion. At resting membrane potentials, the release machinery is in a blocked state produced by the constant presence in the synaptic cleft of neurotransmitter at low concentrations. At resting potentials, Ca2+ channels are closed, but this is probably not associated with the presence of low levels of neurotransmitter. Upon arrival of the action potential at the nerve terminal, (as suggested by the Ca-voltage hypothesis) two things happen independently: The release machinery is relieved of its block, being activated and readied to trigger release. Concurrently, Ca2+ enters the presynaptic terminal, and together with specific Ca2+ binding proteins, it abolishes the hydration repulsive forces without which the intimate contact between the vesicle and the plasmatic release machinery is not possible. The biophysical meaning of triggering release is at present not known. There are several suggestions, the one most consistent with the arguments of this review being the mechanism discussed and modeled by Nanavati et al. (1992; see also review: Monck & Fernandez, 1992). According to that hypothesis, an activated scaffold of proteins forms a dimple in the plasma membrane upon stimulation. This dimple, which exhibits high tension--perhaps together with Ca(2+)--overcomes the repulsive forces of hydration, permitting the two membranes to "jump" into intimate contact. As a result, a single hemifused bilayer is formed. In this hemifused bilayer, a lipidic fusion pore opens. In the context of the lipidic fusion pore hypothesis, the role of the depolarization-dependent triggering could be to start those manipulations in the plasmatic membrane that result in increased lateral bilayer tension and formation of the dimple. Ca2+ could then, in view of reduced repulsive forces and increased attractive forces, be responsible for the intimate docking of the vesicle at the release site. Under such conditions, hemifusion could take place with the final formation of the lipidic fusion pore. Finally, once the fusion pore opens, discharge of the vesicular content takes place immediately and lasts for up to 50-70 microseconds. To be so fast, discharge must occur by a mechanism other than diffusion, possibly by ion-exchange (R. Khanin, H. Parnas and L. Segel, in preparation).(ABSTRACT TRUNCATED AT 400 WORDS)

MeSH Terms
Animals Calcium/metabolism Calcium Channels/physiology Exocytosis/physiology Kinetics Neurotransmitter Agents/metabolism Synapses/metabolism Synaptic Vesicles/metabolism,physiology Temperature
Chemicals
Calcium Channels Neurotransmitter Agents Calcium
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Parnas H
Department of Neurobiology, Hebrew University, Jerusalem, Israel.
Parnas I
References (63)
63 references, click to expand
  1. Mechanism of acetylcholine release: possible involvement of presynaptic muscarinic receptors in regulation of acetylcholine release and protein phosphorylation.
    Proc Natl Acad Sci U S A. 1979 Dec;76(12):6336-40 PMID: 293724
  2. A dual effect of calcium ions on neuromuscular facilitation.
    J Physiol. 1968 Mar;195(2):471-80 PMID: 4296698
  3. Neurotransmitter release: development of a theory for total release based on kinetics.
    J Theor Biol. 1989 Jan 23;136(2):151-70 PMID: 2570884
  4. Neurotransmitter release and its facilitation in crayfish. II. Duration of facilitation and removal processes of calcium from the terminal.
    Pflugers Arch. 1982 May;393(3):232-6 PMID: 6124930
  5. On the contribution of mathematical models to the understanding of neurotransmitter release.
    Int Rev Neurobiol. 1990;32:1-50 PMID: 1981883
  6. Bisquaternary pyridinium oximes as presynaptic agonists and postsynaptic antagonists of muscarinic receptors.
    J Neurochem. 1986 Mar;46(3):767-72 PMID: 3950607
  7. The magnitude and significance of Ca2+ domains for release of neurotransmitter.
    Bull Math Biol. 1994 Nov;56(6):1095-119 PMID: 7833845
  8. Neurotransmitter release and its facilitation in crayfish. VIII. Modulation of release by hyperpolarizing pulses.
    Pflugers Arch. 1986 Feb;406(2):131-7 PMID: 2870467
  9. Presynaptic calcium diffusion from various arrays of single channels. Implications for transmitter release and synaptic facilitation.
    Biophys J. 1985 Dec;48(6):1003-17 PMID: 2418887
  10. Calcium ions, active zones and synaptic transmitter release.
    Trends Neurosci. 1988 Oct;11(10):458-64 PMID: 2469165
  11. Amperometric monitoring of chemical secretions from individual pancreatic beta-cells.
    Anal Chem. 1993 Jul 15;65(14):1882-7 PMID: 8368536
  12. Multiple calcium-dependent processes related to secretion in bovine chromaffin cells.
    Neuron. 1993 Jan;10(1):21-30 PMID: 8427700
  13. Mechanisms of membrane fusion.
    Annu Rev Biophys Biomol Struct. 1993;22:433-66 PMID: 8347997
  14. Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction.
    J Cell Biol. 1973 May;57(2):315-44 PMID: 4348786
  15. Three types of Ca2+ channel trigger secretion with different efficacies in chromaffin cells.
    Nature. 1994 Jan 6;367(6458):72-6 PMID: 8107778
  16. Effect of Ca2+ diffusion on the time course of neurotransmitter release.
    Biophys J. 1989 May;55(5):859-74 PMID: 2566336
  17. Sodium and calcium channels in bovine chromaffin cells.
    J Physiol. 1982 Oct;331:599-635 PMID: 6296372
  18. Excitatory amino acids depress synaptic currents in neonate rat sympathetic preganglionic neurons.
    J Neurophysiol. 1993 Jun;69(6):2030-8 PMID: 7688799
  19. Inhibition of pertussis toxin catalyzed ADP-ribosylation of G-proteins by membrane depolarization in rat brain synaptoneurosomes.
    Neurosci Lett. 1991 May 13;126(1):87-90 PMID: 1907726
  20. Release of secretory products during transient vesicle fusion.
    Nature. 1993 Jun 10;363(6429):554-8 PMID: 8505984
  21. Cation exchange--a common mechanism in the storage and release of biogenic amines stored in granules (vesicles)? III. A possible role of sodium ions in non-exocytotic fractional release of neurotransmitters.
    Acta Physiol Scand. 1984 Jan;120(1):99-107 PMID: 6144242
  22. Kinetic analysis of secretion from permeabilized adrenal chromaffin cells reveals distinct components.
    J Biol Chem. 1992 Aug 15;267(23):16219-25 PMID: 1644807
  23. Properties of a presynaptic metabotropic glutamate receptor in rat neostriatal slices.
    J Neurophysiol. 1993 Apr;69(4):1236-44 PMID: 8388042
  24. Cation exchanger properties of isolated rat peritoneal mast cell granules.
    Acta Physiol Scand. 1985 Sep;125(1):25-31 PMID: 2413721
  25. Time course of transmitter release calculated from simulations of a calcium diffusion model.
    Biophys J. 1992 Mar;61(3):671-82 PMID: 1354503
  26. Control of quantal transmitter release at frog's motor nerve terminals. II. Modulation by de- or hyperpolarizing pulses.
    Pflugers Arch. 1984 Nov;402(3):235-43 PMID: 6151643
  27. Cation exchange--a common mechanism in the storage and release of biogenic amines stored in granules (vesicles)? II. Comparative studies on sodium-induced release of biogenic amines from the synthetic weak cation-exchangers Amberlite IRC-50 and duolite CS-100 and from biogenic (granule-enriched) materials.
    Acta Physiol Scand. 1984 Jan;120(1):87-97 PMID: 6720329
  28. Calcium dependence of evoked transmitter release at very low quantal contents at the frog neuromuscular junction.
    J Physiol. 1980 Nov;308:79-97 PMID: 6112267
  29. Neurotransmitter release and its facilitation in crayfish muscle. VI. Release determined by both, intracellular calcium concentration and depolarization of the nerve terminal.
    Pflugers Arch. 1983 Sep;399(1):1-10 PMID: 6139784
  30. Proton NMR detection of acetylcholine status in synaptic vesicles.
    Nature. 1980 Jul 17;286(5770):293-4 PMID: 6250057
  31. Calcium action in synaptic transmitter release.
    Annu Rev Neurosci. 1987;10:633-93 PMID: 2436546
  32. Techniques and concepts in exocytosis: focus on mast cells.
    Biochim Biophys Acta. 1991 Dec 12;1071(4):429-71 PMID: 1751542
  33. Effects of intra-axonal injection of Ca2+ buffers on evoked release and on facilitation in the crayfish neuromuscular junction.
    Neurosci Lett. 1991 Apr 29;125(2):215-8 PMID: 1908959
  34. Agonist-induced localized Ca2+ spikes directly triggering exocytotic secretion in exocrine pancreas.
    EMBO J. 1993 Aug;12(8):3017-22 PMID: 8344243
  35. Transmission by presynaptic spike-like depolarization in the squid giant synapse.
    Proc Natl Acad Sci U S A. 1982 Apr;79(7):2415-9 PMID: 6954549
  36. Release kinetics as a tool to describe drug effects on neurotransmitter release.
    J Theor Biol. 1990 May 22;144(2):225-48 PMID: 1973749
  37. Differential release of amino acids, neuropeptides, and catecholamines from isolated nerve terminals.
    Neuron. 1991 Apr;6(4):517-24 PMID: 2015091
  38. Delay in vesicle fusion revealed by electrochemical monitoring of single secretory events in adrenal chromaffin cells.
    Nature. 1992 Mar 5;356(6364):60-3 PMID: 1538782
  39. Quantal secretion of catecholamines measured from individual bovine adrenal medullary cells permeabilized with digitonin.
    J Biol Chem. 1992 Sep 15;267(26):18329-35 PMID: 1526972
  40. Mimicry and mechanism in phospholipid models of membrane fusion.
    Annu Rev Physiol. 1986;48:201-12 PMID: 3518615
  41. Single calcium channels and acetylcholine release at a presynaptic nerve terminal.
    Neuron. 1993 Dec;11(6):1007-11 PMID: 8274272
  42. The exocytotic fusion pore.
    J Cell Biol. 1992 Dec;119(6):1395-404 PMID: 1469040
  43. The role of calcium in neuromuscular facilitation.
    J Physiol. 1968 Mar;195(2):481-92 PMID: 4296699
  44. Control of quantal transmitter release at frog's motor nerve terminals. I. Dependence on amplitude and duration of depolarization.
    Pflugers Arch. 1984 Nov;402(3):225-34 PMID: 6151642
  45. Neurotransmitter release and its facilitation in crayfish. VII. Another voltage dependent process beside Ca entry controls the time course of phasic release.
    Pflugers Arch. 1986 Feb;406(2):121-30 PMID: 2421235
  46. Membrane depolarization evokes neurotransmitter release in the absence of calcium entry.
    Nature. 1989 Nov 23;342(6248):433-5 PMID: 2573839
  47. Phasic secretion of acetylcholine at a mammalian neuromuscular junction.
    J Physiol. 1980 Jun;303:299-314 PMID: 6253620
  48. Cytosolic Ca2+, exocytosis, and endocytosis in single melanotrophs of the rat pituitary.
    Neuron. 1990 Nov;5(5):723-33 PMID: 2223095
  49. The exocytotic fusion pore modeled as a lipidic pore.
    Biophys J. 1992 Oct;63(4):1118-32 PMID: 1420930
  50. Control of exocytosis in adrenal chromaffin cells.
    Biochim Biophys Acta. 1991 Jul 22;1071(2):174-202 PMID: 1649638
  51. Three types of neuronal calcium channel with different calcium agonist sensitivity.
    Nature. 1985 Aug 1-7;316(6027):440-3 PMID: 2410796
  52. Diffusion cannot govern the discharge of neurotransmitter in fast synapses.
    Biophys J. 1994 Sep;67(3):966-72 PMID: 7811953
  53. Neurotransmitter release and its facilitation in crayfish. I. Saturation kinetics of release, and of entry and removal of calcium.
    Pflugers Arch. 1982 Mar;393(1):1-14 PMID: 6123979
  54. THE MEASUREMENT OF SYNAPTIC DELAY, AND THE TIME COURSE OF ACETYLCHOLINE RELEASE AT THE NEUROMUSCULAR JUNCTION.
    Proc R Soc Lond B Biol Sci. 1965 Feb 16;161:483-95 PMID: 14278409
  55. A new method for determining co-operativity in neurotransmitter release.
    J Theor Biol. 1986 Apr 21;119(4):481-99 PMID: 2875222
  56. Physical force considerations in model and biological membranes.
    Can J Biochem Cell Biol. 1984 Aug;62(8):752-9 PMID: 6498591
  57. Blockage of synaptic release by brief hyperpolarizing pulses in the neuromuscular junction of the crayfish.
    J Physiol. 1990 Nov;430:119-33 PMID: 1707963
  58. GTP gamma S stimulates exocytosis in patch-clamped rat melanotrophs.
    Neuron. 1993 Jul;11(1):165-72 PMID: 8338664
  59. Compartmentalization of the submembrane calcium activity during calcium influx and its significance in transmitter release.
    Biophys J. 1985 Sep;48(3):485-98 PMID: 2412607
  60. Proteins of synaptic vesicles involved in exocytosis and membrane recycling.
    Neuron. 1991 May;6(5):665-77 PMID: 1673848
  61. Quantal transmitter secretion from myocytes loaded with acetylcholine.
    Nature. 1992 Oct 22;359(6397):733-6 PMID: 1436036
  62. Neurotransmitter release: facilitation and three-dimensional diffusion of intracellular calcium.
    Bull Math Biol. 1992 Sep;54(5):875-94 PMID: 1353391
  63. Calcium levels measured in a presynaptic neurone of Aplysia under conditions that modulate transmitter release.
    J Physiol. 1986 Jun;375:625-42 PMID: 2432228
Article Info
Journal
The Journal of membrane biology
Abbr.
J Membr Biol
ISSN
0022-2631
Published
1994-12-00
Pages
267-79
Language
English
Region
United States
NLM ID
0211301
Subset
IM
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