Ca2+ Dependent Evoked Quantal Neurotransmitter Release does Not Necessarily Involve Exocytosis of Synaptic Vesicles

  • Ladislav Tauc
  • Bernard Poulain


There is now evidence that the target for tetanus (TeTx) and botulinum (BoNT) neurotoxins is located intracellularly (Penner et al., 1986; Poulain et al., 1988) and that they block synaptic transmission without interfering with the influx of calcium at the nerve terminal (Dreyer et al., 1983; Molgo et al., 1989). It seems therefore clear that these toxins act on a component of the nerve terminal implicated in the neurotransmitter release mechanism. Furthermore, when the membrane steps of intoxication are bypassed by different techniques (reviewed in Poulain and Molgo, 1992; Niemann, 1991; Dolly, 1992) the toxins appear nearly equipotent in inhibiting release of acetylcholine, mono-amines or neuropeptides in various preparations. Thus, it may be postulated that their target is common to cells or neurons releasing different transmitters. The above conclusion has to be borne in mind when researching the intracellular target of these toxins. The main complication, however, arises from the fact that the transmitter release mechanism is still obscure despite the rather definitive descriptions found in the textbooks and ascribing this role to the exocytosis of synaptic vesicles.


Synaptic Vesicle Transmitter Release Acetylcholine Release Electric Organ Presynaptic Membrane 


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  1. Almers, W., 1990, Exocytosis, Arrau Rev. Physiol 52: 607.CrossRefGoogle Scholar
  2. Almers, W., Breckenridge, L. J., Iwata, A., Lee, A. K., Spruce, A. E. and Tse, F. W., 1991, Millisecond studies of single membrane fusion events, Aoa. N. Ji Acad. Sci 635: 318.CrossRefGoogle Scholar
  3. Almers, W. and Tse, F. W., 1990, Transmitter release from synapses: does a preassembled fusion pore initiate exocytosis, Neuron 4: 813.PubMedCrossRefGoogle Scholar
  4. Anderson, D. C., King, S. C. and Parsons, S. M., 1983, Inhibition of 3H-acetylcholine active transport by tretraphenylborate and other anions, Molecular Pharmacel 24: 55.Google Scholar
  5. Augustine, G. J., Charlton, M. P. and Smith, S. J., 1987, Calcium action in transmitter release, Amu. Rev. Neurosei 10: 633.CrossRefGoogle Scholar
  6. Bahr, B. A. and Parsons, S. M., 1986, Acetycholine transport and drug inhibition kinetics in Torpedo synaptic vesicle, J. Neurochem. 46: 1214.PubMedCrossRefGoogle Scholar
  7. Baux, G., Poulain, B. and Tauc, L., 1986, Quantal analysis of action of hemicholiniuin-3 studied at a central cholinergie synapse of Aplysia. J. Physiol. (Load) 380: 209.Google Scholar
  8. Baux, G., Simonneau, M. and Tauc, L., 1979, Transmitter release: ruthenium red used to demonstrate a possible role of sialic acid containing substrates, J. Physiol. (tond) 291: 161.Google Scholar
  9. Baux, G. and Tauc, L., 1983, Carbachol can be released at a cholinergie ganglionic synapse as a false transmitter, Proc. Nati. Acad Sci. USA 80: 5126.CrossRefGoogle Scholar
  10. Baux, G. and Tauc, L., 1987, Presynaptic actions of curare and atropine on quantal acetylcholine release at a central synapse of Aplysia, J. Physiol (tond) 388: 665.Google Scholar
  11. Betz, W. J. and Bewick, G. S., 1992, Optical analysis of synaptic vesicle recycling at the frog neuromuscular junction, Science 255: 200.PubMedCrossRefGoogle Scholar
  12. Bevan, S., 1976, Subminiature end-plate potentials at contracted neuromuscular junctions, J. Physiol (tond.) 258: 145.Google Scholar
  13. Birman, S., Israël, M., Lesbats, B. and Morel, N., 1986, Solubilization and partial purification of a presynaptic membrane protein ensuring calcium-dependent acetylcholine release from proteoliposomes, J. Neurochem. 47: 433.PubMedCrossRefGoogle Scholar
  14. Cabeza, R. and Collier, B., 1988, Acetylcholine mobilization in a sympathetic ganglion in the presence and absence of 2-(4-phenylpiperidino)cyclohexanol (AH5183), J. Neurochem. 50: 112.PubMedCrossRefGoogle Scholar
  15. Ceccarelli, B. and Hurlbut, W. P., 1980, Vesicle hypothesis of the release of quanta of acetylcholine, Physiol. Rev. 60: 396.PubMedGoogle Scholar
  16. Ceccarelli, B., Hurlbut, W. P. and Mauro, A., 1973, Turnover of transmitter and synaptic vesicles at the frog neuromuscular junctions. J. Cell Biol. 57: 499.PubMedCrossRefGoogle Scholar
  17. Ceccarelli, B., Valtorta, F. and Hurlbut, W., 1988, New evidence supporting the vesicle hypothesis for quantal secretion at the neuromuscular junction, In: “Cellular and Molecular Basis of Synaptic Transmission” H. Zimmermann, ed., NATO ASI Series 21: 51.CrossRefGoogle Scholar
  18. Collier, B., 1969, The preferential release of newly synthetized transmitter by a sympathetic ganglion, J. Physiol. (tond.) 205: 341.Google Scholar
  19. Cooper, J. R. and Meyer, E. M., 1984, Possible mechanisms involved in the release and modulation of release of neuroactive agents, Neurochem Int 6: 419.PubMedCrossRefGoogle Scholar
  20. Corthay, J., Dunant, Y. and Loctin, F., 1982, Acetylcholine changes underlying transmission of a single nerve impulse in the presence of 4-aminopyridine in Torpedo, J. Physiol (tond) 325: 461.Google Scholar
  21. Couteaux, R. and Pécot-Dechavassine, M., 1973, Données ultrastructurales et cytochimiques sur le mécanisme de la libération de l’acétylcholine dans la transmission synaptique, Arch. Ital. Biel. 3: 231.Google Scholar
  22. De Camilli, P., Benfenati, F., Valtorta, F. and Greengard, P., 1990, The synapsins, Anna Rev. Cell Biol. 6: 433.CrossRefGoogle Scholar
  23. De Camilli, P. and Jahn, R., 1990, Patway to regulated exocytosis in neurons, Anna Rev. Physiol. 52: 625.CrossRefGoogle Scholar
  24. Del Castillo, J. and Katz, B., 1957, La base “quantale” de la transmission neuromusculaire, In: “Microphysiologie comparée des éléments excitables” Colloq. Int. C.N.R.S. A. Fessard, ed. Paris 67: 245.Google Scholar
  25. De Robertis, E. D. P., Pellegrino de Iraldi, A., Rodriguez de Lores Arnais, G. and Salganicoff, L., 1962, Cholinergic and non-cholinergic nerve endings in rat brain I. Isolation and subcellular distribution of acetylcholine and acetylcholinesterase, J. Neunochem. 9: 23.CrossRefGoogle Scholar
  26. Dolly, J. O., 1992, Peptide toxins that alter neurotransmitter release, In: “Handbook of Experimental Pharmacology”, H. Herkin and F. Hucho, eds., Springer, Berlin.Google Scholar
  27. Dreyer, F., Mallart, A. and Brigant, J. L., 1983, Botulinum A and tetanus toxin do not affect presynaptic membrane currents in mammalian motor nerve endings, BMA, Research 270: 373.Google Scholar
  28. Dunant, Y., 1986, On the mechanism of acetylcholine release, Progress in Neurobloi 26: 55.CrossRefGoogle Scholar
  29. Dunant, Y., Esquerda, J. E., Loctin, F., Marsal, J. and Müller, D., 1987, Botulinum toxin inhibits quantal acetylcholine release and energy metabolism in the Torpedo electric organ, J. Physiol (tond) 385: 677.Google Scholar
  30. Dunant, Y., Gautron, J., Israël, M., Lesbats, B. and Manaranche, R., 1974, Evolution de la décharge de l’organe électrique de la Torpille et variations simultanées de l’acétylcholine au cours de la stimulation, J. Neuzachem 23. 635.CrossRefGoogle Scholar
  31. Dunant, Y., Jones, G. J. and Loctin, F., 1982, Acetylcholine measured at short time intervals during transmission of nerve impulses in the electric organ of Torpedo, J. Physiol. (tond) 325: 441.Google Scholar
  32. Dunant, Y. and Müller, D., 1986, Quantal release of acetylcholine evoked by focal depolarization at the Torpedo nerve-electroplaque junction, I. Physiol (Lond.) 379: 461.Google Scholar
  33. Eder-Colli, L., Briand, P. A., Pellegrinelli, N. and Dunant, Y., 1989, A monoclonal antibody raised against plasma membrane of cholinergic nerve terminals of the Torpedo inhibits choline acetyltransferase activity and acetylcholine release, J. Neurochem. 53: 1419.PubMedCrossRefGoogle Scholar
  34. Edwards, C., Dolezal, V, Tucek, S., Zemkova, H. and Vyskocil, F., 1985, Is an acetylcholine transport system responsible for nonquantal release of acetylcholine at the rodent myoneural junction?, Proc. Natl. Acad. Sci USA 82: 3514.PubMedCrossRefGoogle Scholar
  35. Erxleben, C. and Kriebel, M. E., 1988, Subunit composition of the spontaneous miniature end-plate currents at the mouse neuromuscular junction, J. Physiol (Lond) 400: 659.Google Scholar
  36. Estrella, D., Green, K. L., Prior, C., Dempster, J., Halliwell, R. F., Jacobs, R. S., Parsons, S. M., Parsons, R. L. and Marshall, I. G., 1988, A further study of the neuromuscular effects of vesamicol (AH5I83) and of its enantiomer specificity, Br. J Pharmacol 93: 759.PubMedCrossRefGoogle Scholar
  37. Faber, D. S. and Korn, H., 1985, Binary mode of transmitter release at central synapses, T.LN.S. 5: 157.Google Scholar
  38. Fesce, R., Segal, J. R., Ceccarelli, B. and Hurlbut, W. P., 1986, Effects of black widow spider venom and Cat on quantal secretion at the frog neuromuscular junction, J. Gen. Physiol 88: 59.PubMedCrossRefGoogle Scholar
  39. Flechter, P. and Forrester, T., 1975, The effect of curare on the release of acetylcholine from mammalian nerve terminals and an estimate of the quantum content, J. Physiol (Load.) 251: 131.Google Scholar
  40. Fossier, P., Baux, G., Poulain, B and Tauc, L., 1990, Receptor-mediated presynaptic facilitation of quantal release of acetylcholine induced by pralidoxime in Aplysia, Ccli Molccular Ncurobiol 10: 383.Google Scholar
  41. Fossier, P., Baux, G., Trudeau, L. E. and Taw, L., 1992, Involvement of Cat’ uptake by a reticulum-like store in the control of transmitter release, Neuroscience,in press.Google Scholar
  42. Giompres, P. E. and Luqmani, Y A., 1980, Cholinergie vesicle isolated from Toipeilo Inamorata demonstration of acetylcholine and choline uptake in an in vitro system, Ncuro sciences 5: 1041.Google Scholar
  43. Gracz, L. M., Wang, W. C. and Parsons, S. M., 1988, Cholinergic synaptic vesicle heterogeneity: Evidence for regulation of acetylcholine transport, Biochemistry 27: 5268.PubMedCrossRefGoogle Scholar
  44. Gray, E. G., 1976, Problems of understanding the substructure of synapses, In: “Progress in Brain Research. Perspectives in brain research”, M.A. Corner and D.F. Swaab, Eds., Elsevier, Amsterdam 45: 207.Google Scholar
  45. Grinnell, A. D., Gundersen, C. B., Meriney, S. D. and Young, S. H., 1989, Direct measurement of ACh release from exposed frog nerve terminals: constraints on interpretation of non-quantal release, J Physiol (Lond) 419: 225.Google Scholar
  46. Heuser, J. E., 1989, Review of electron microscopic evidence favouring vesicle exocytosis as the structural basis for quantal release during synaptic transmission, Quaterly J Exp. Physiol 74: 1051.Google Scholar
  47. Heuser, J. E. and Reese, T. S., 1981, Structural changes after transmitter release at the frog neuromuscular junction, J CellBiol. 88: 564.CrossRefGoogle Scholar
  48. Heuser, J. E., Reese, T. S. and Landis, D. M. D., 1974, Functional changes in frog neuromuscular junction studied with freeze fracture, J. Neurocytol 3: 109.PubMedCrossRefGoogle Scholar
  49. Hubbard, J. I. and Schmidt, R. F., 1963, An electrophysiological investigation of mammalian motor nerve terminals, J. Physiol (Land.) 166: 145.Google Scholar
  50. Hurlbut, W. P., 1989, The correlation between vesicle loss and quantal secretion at the neuromuscular junction, Cell Biol Int. Reports 13: 1053.CrossRefGoogle Scholar
  51. Israel, M., Dunant, Y. and Manaranche, R., 1979, The present status of the vesicular hypothesis, Progress in Neurobiology 13: 237.PubMedCrossRefGoogle Scholar
  52. Israël, M., Lesbat, B., Manaranche, R. and Morel, N., 1983, Acetylcholine release from proteoliposomes equipped with synaptosomal membrane constituents, Biocbim. Biophys. Acts 728: 438.CrossRefGoogle Scholar
  53. Israel, M. and Lesbats, B., 1981, Continuous determination by a chemiluminescent method of acetylcholine release and compartmentation in Torpedo electric organ synaptosomes, J. Neurochem. 37: 1475.PubMedCrossRefGoogle Scholar
  54. Israel, M., Lesbats, B., Morel, N., Manaranche, R. and Le Gal la Salle, G., 1988, Is the acetylcholine releasing protein mediatophore present in rat brain?, FBBS Letters 233: 421.CrossRefGoogle Scholar
  55. Israel, M. and Manaranche, R., 1985, The release of acetylcholine: from a cellular towards a molecular mechanism, Biol. Cell. 55: 1.PubMedCrossRefGoogle Scholar
  56. Israel, M., Manaranche, R., Marsal, J., Meunier, F. M., Morel, N., Frachon, P. and Lesbats, B., 1980, ATP-dependent calcium uptake by cholinergic synaptic vesicles isolated from Torpedo electric organ, J Membrane Biol. 54: 115.CrossRefGoogle Scholar
  57. Israel, M., Manaranche, R., Morel, N., Dedieu, J. C., Gulik-Krzywicki, T. and Lesbats, B., 1981, Redistribution of intramembrane particles in conditions of acetylcholine release by cholinergie synaptosomes, J. Ultrastruct Res. 75: 162.PubMedCrossRefGoogle Scholar
  58. Israel, M. and Morel, N., 1990, Mediatophore: a nerve terminal membrane protein supporting the final step of the actetylcholine release process, In: “Progress in Brain Research”, S.M. Aquilonius and P.G. Gillerg, eds., 84: 101.Google Scholar
  59. Katz, B., 1969, “The Release of Neural Substances” Liverpool University Press, Liverpool.Google Scholar
  60. Katz, B. and Miledi, R., 1977, Transmitter leakage from motor nerve endings, Proc. R. Soc. Land. Ser. B 196: 59.CrossRefGoogle Scholar
  61. Katz, B. and Miledi, R., 1979, Estimates of quantal content during “chemical potentiation” of transmitter release, Five. R. Soc. Land. Sec 205: 369.Google Scholar
  62. Kelly, R. B., 1991, Secretory granule and synaptic vesicle formation, Cell Bibl 3: 654.Google Scholar
  63. Knaus, P., Marquez-Pouey, B., Scherer, H. and Betz, H., 1990, Synaptoporin, a novel putative channel protein of synaptic vesicles, Neuron 5: 453.PubMedCrossRefGoogle Scholar
  64. Korn, H. and Faber, D. S., 1991, Quantal analysis and synaptic efficacy in the CNS, T.IN.S. 14: 439.Google Scholar
  65. Kriebel, M. E., 1978, Small mode miniature end plate potentials are increased and evoked in fatigued preparations and in high Mg2+ saline, Brain Research 148: 381.PubMedCrossRefGoogle Scholar
  66. Kriebel, M. E. and Gross, C. E., 1974, Multimodal distribution of frog miniature endplate potentials in adult, denervated and tadpole leg muscle, J Gen. Physiol. 64: 85.PubMedCrossRefGoogle Scholar
  67. Kriebel, M. E., LLados, F. and Carlson, C. G., 1980, Effect of the Ca2+ ionophore X-537A at heat challenge on the distribution of mouse MEPP amplitude histograms, J. Physiol. (Paris) 76: 435.Google Scholar
  68. Kriebel, M. E., Llados, F. and Matteson, D. R., 1976, Spontaneous subminiature endplate potentials in mouse diaphragm muscle: evidence for synchronous release, J. Physiol. (Lond) 262: 553.Google Scholar
  69. Kriebel, M. E., Vautrin, J. and Holsapple, J., 1990, Transmitter release: prepackaging and random mechanism or dynamic and deterministic process, Brain Res Rev. 15: 167.PubMedCrossRefGoogle Scholar
  70. Kuffler, S. W. and Yoshikami, D., 1975, The number of transmitter molecules in a quantum: an estimate from ionophoretic application of acetylcholine at the neuromuscular synapse, J. Physiol. (fond.) 251: 465.Google Scholar
  71. Landmesser, L. and Pilar, G., 1972, The onset and development of transmission in the chick ciliary ganglion, J. Physiol. (Load) 222: 691.Google Scholar
  72. Large, W. A. and Rang, H. P., 1978, Factors affecting the rate of incorporation of a false transmitter into mammalian nerve terminals, J. Physiol (Lond) 285: 1.Google Scholar
  73. Lin, J. W., Sugimori, M., Llinas, R. R., McGuinness, T. L. and Greengard, P., 1990, Effect of Synapsin I and Ca2+/Calmodulin dependent protein kinase II on spontaneous neurotransmitter release in the squid giant synapse, Pro. Natl. Acad. Sci USA 87: 8257.CrossRefGoogle Scholar
  74. Llinas, R. R., 1977, Calcium and transmitter release in squid synapse, Soc. Neurosci 2: 139.Google Scholar
  75. Llinas, R. R., 1991, Depolarization release coupling: an overview, Ana. N Y. Acad Sci 635: 3.CrossRefGoogle Scholar
  76. Lunas, R. R. and Heuser, J. E., 1978, Depolarization-release coupling system in neurons, Res. Program Bull. 15: 557.Google Scholar
  77. Lunas, R., Sugimori, M. and Silver, R. B., 1992, Mierodomains of high calcium concentration in a presynaptic terminal, Science 256: 677.CrossRefGoogle Scholar
  78. Marchbanks, R. M., 1979, Role of storage vesicles in synaptic transmission, Soc Exp. Biol. Symp. XXXIL Secretory mechanisms; Hopkins and Duncan, eds.,:251.Google Scholar
  79. Marchbanks, R. M. and Israel, M., 1972, The heterogeneity of bound acetylcholine and synaptic vesicles, Biochein. J. 129: 1049.Google Scholar
  80. Marsal, J., Solona, C., Rabasseda, X., Blasi, J. and Casanova, A., 1987, Depolarization-induced release of ATP from cholinergic synaptosomes is not blocked by botulinum toxin type A, Neurochein. Iat. 10: 295.Google Scholar
  81. Marshall, I. G. and Parsons, S. M., 1987, The vesicular acetylcholine transport system, T.LN.S. 10: 174.Google Scholar
  82. Matteoli, M. and De Camilli, P., 1991, Molecular mechanisms in neurotransmitter release, Corr. Opinion Neurobiol 1: 91.CrossRefGoogle Scholar
  83. Maycox, P. R., Hell, J. W. and Jahn, R., 1990, Amino acid neurotransmission: spotlight on synaptic vesicles, T.IN.S. 13: 83.Google Scholar
  84. Melega, W. P. and Howard, B. D., 1984, Biochemical evidence that vesicles are the source of the acetylcholine released from stimulated PC 12 cells, Proc. Natl. Acad. Sci. USA 81: 6535.PubMedCrossRefGoogle Scholar
  85. Meunier, F. M., Israel, M. and Lesbats, B., 1975, Release of ATP from stimulated nerve electroplaque junctions, Nature 257: 407.PubMedCrossRefGoogle Scholar
  86. Michaelson, D. M., Avissar, S., Ophir, I., Pinchasi, I., Angel, I., Kloog, Y. and Sokolovsky, M., 1980, On the regulation of acetylcholine release: a study utilizing Torpedo synaptosomes and synaptic vesicles, J. Physiol(Lond.) 76: 505.Google Scholar
  87. Michaelson, D. M. and Burstein, M., 1985, Biochemical evidence that acetylcholine release from cholinergie nerve terminals is mostly vesicular, FEBS Lett. 188: 389.PubMedCrossRefGoogle Scholar
  88. Miledi, R., Molenaar, P. C. and Polak, R. L., 1980, The effect of lanthanum ions on acetylcholine in frog muscle, J. Physiol (fond) 309: 199.Google Scholar
  89. Miledi, R., Molenaar, P. C. and Polak, R. L., 1982, Free and bound acetylcholine in frog muscle, J Physiol (Conti) 333: 189.Google Scholar
  90. Miledi, R., Molenaar, P. C. and Polak, R. L., 1983, Electrophysiological and chemical determination of acetylcholine release at the frog neuromuscular junction, J Physiol. (Load) 334: 245.Google Scholar
  91. Molgo, J., Siegel, L. S., Tabti, N. and Thesleff, S., 1989, A study of synchronization of quantal transmitter release from mammalian motor endings by the use of botulinal toxins type A and D, J. Physiol. (Load) 411: 195.Google Scholar
  92. Morel, N., Israel, M. and Manaranche, R., 1978, Determination of ACh concentration in Torpedo synaptosomes, J. Neurochen 30: 1553.CrossRefGoogle Scholar
  93. Morel, N. and Meunier, F. M., 1981, Simultaneous release of acetylcholine and ATP from stimulated cholinergie synaptosomes, J. Neurochem. 36: 1766.PubMedCrossRefGoogle Scholar
  94. Morot Gaudry-Talarmain, Y.,Diebler, M. F. and O’Regan, S,1989, Compared effects of two vesicular acetylcholine uptake blockers AH5183 and cetiedil on cholinergic functions in Torpedo synaptosomes: acetylcholine synthesis choline transport vesicular uptake and evoked acetylcholine release, J Neurochem. 52: 822.Google Scholar
  95. Müller, D. and Dunant, Y., 1985, Subminiature electroplaque potentials are present in Torpedo electric organ, Experientia 41: 824.Google Scholar
  96. Müller, D., Garcia-Segura, L. M., Parducz, A. and Dunant, Y., 1987, Brief occurence of a population of presynaptic intramembrane particles coincides with transmission of a nerve impulse, Proc. Natl. Acad. Sci USA 84: 590.PubMedCrossRefGoogle Scholar
  97. Neher, E. and Marty, A., 1982, Discrete changes of cell membrane capacitance observed under conditions of enhanced secretion in bovine adrenal chromaffm cells, Proc. Natl. Acad Sci USA 79: 6712.PubMedCrossRefGoogle Scholar
  98. Nicholls, D. G., 1989, Release of glutamate, aspartate, and -aminobutyric acid from isolated nerve terminals, J. Neurochem. 52: 331.PubMedCrossRefGoogle Scholar
  99. Niemann, H., 1991, Molecular biology of clostridial toxins, In: “Sourcebook of Bacterial Protein Toxin”, Alouf J. and Freer J., eds., Academic Press, Lond.Google Scholar
  100. Penner, R., Neher, E. and Dreyer, F., 1986, Intracellularly injected tetanus toxin inhibits exocytosis in bovine adrenal chromaffm cells, Nature 324: 76.PubMedCrossRefGoogle Scholar
  101. Potter, L. T., 1970, Synthesis, storage and release of 14C-acetylcholine in isolated rat diaphragm muscles,. J Physiol. (Load) 206: 145.Google Scholar
  102. Poulain, B, Baux, G. and Tauc, L., 1986, Presynaptic transmitter content controls the number of quanta released at a neuro-neuronal cholinergic synapse, Proc. Nati. Acad Sci USA 83: 170.CrossRefGoogle Scholar
  103. Poulain, B, Fossier, P., Baux, G. and Tauc, L., 1987, Hemicholinium-3 facilitates the release of acetylcholine by acting on presynaptic nicotinic receptors at a central synapse in Aplysia, Brain Res. 435: 63.PubMedCrossRefGoogle Scholar
  104. Poulain, B and Molgo, J., 1992, Botulinal neurotoxins. Methods used in the study of their mode of action on neuro-transmitter release, In: “Methods in Neurosciences”, P. M. Conn, ed., Academic Press, San Diego.Google Scholar
  105. Poulain, B, Tauc, L., Maisey, E. A., Wadsworth, J. D. F., Mohan, P. M. and Dolly, J. O., 1988, Neurotransmitter release is blocked intracellularly by botulinum neurotoxin, and this requires uptake of both toxin polypeptides by a process mediated by the larger chain, Proc. Natl. Acad. Sci USA 85: 4090.PubMedCrossRefGoogle Scholar
  106. Simonneau, M., Tauc, L. and Baux, G., 1980, Quantal release of acetylcholine examined by current fluctuation analysis at an identified neuro-neuronal synapse of Aplysia, Proc. Natl. Acad. Sci USA 77: 1661.PubMedCrossRefGoogle Scholar
  107. Tauc, L., 1977, Transmitter release at cholinergic synapses, In: “Synapses”, G.A. Cottrell and P.N.R. Usherwood, eds., Blackie, Glasgow.Google Scholar
  108. Tauc, L., 1979, Are vesicles necessary for release of acetylcholine at cholinergie synapses ?, Biochem-Pharmacol. 27: 3493.CrossRefGoogle Scholar
  109. Tauc, L., 1982, Nonvesicular release of neurotransmitter, Physiol Rev. 62: 857.PubMedGoogle Scholar
  110. Tauc, L. and Baux, G., 1980, Libération du transmetteur synaptique: examen critique de la theorie vésiculaire, In: “La transmission neuromusculaire. Les médiateurs et le milieu intérieur”, Colloque Claude Bernard, Masson Paris.Google Scholar
  111. Tauc, L. and Baux, G., 1982, Are there intracellular acetylcholine receptors in the cholinergic synaptic nerve terminals?, J. Physiol (Paris) 78: 366.Google Scholar
  112. Tauc, L. and Baux, G., 1985, Mechanism of acetylcholine release at neuro-neuronal synapses, In: “Nonvesicular transport”, S.S.Rothman and J.J.L. Ho, eds., Willey and Sons, New York.Google Scholar
  113. Tauc, L., Hoffmann, A., Tsuji, S., Hinzen, D. H. and Faille, L., 1974, Transmission abolished on a cholinergie synapse after injection of acetylcholinesterase into the pre-synaptic neurone, Nature 250: 496.PubMedCrossRefGoogle Scholar
  114. Taue, L. and Poulain, B., 1991, The non-vesicular hypothesis of quantal release of neurotransmitters, In: “Presynaptic Regulation of Neurotransmitter Release: A Handbook”, M. Hanani and J. Feigenbaum, eds., Freund Publishing House Lond.Google Scholar
  115. Tauc, L. and Poulain, B., 1991, Vesigate hypothesis of neurotransmitter release explains the formation of quanta by a non-vesicular mechanism, Physiol Res. 40: 279.PubMedGoogle Scholar
  116. Thesleff, S., 1986, Different kinds of acetylcholine release from the motor nerve, Int. Rev. Neurobiol. 28:59.PubMedCrossRefGoogle Scholar
  117. Thomas, L., Hartung, K., Langosch, D., Rehm, H., Bamberg, E., Francke, W. W. and Betz, H., 1988, Identification of synaptophysin as a hexameric channel protein of the synaptic vesicle membrane, Science 242:1050.CrossRefGoogle Scholar
  118. Torri-Tarelli, F., Grohovaz, F., Fesce, R. and Ceccarelli, B., 1985, Temporal coincidence between synaptic vesicle fusion and quantal secretion of acetylcholine, J. Cell Biol. 101: 1386.PubMedCrossRefGoogle Scholar
  119. Tremblay, J. P., Laurie, R. E. and Colonnier, M., 1983, Is the MEPP duc to the release of one vesicle or to simultaneous release of several vesicles at one active zone?, Brain Res Rev. 6: 299.CrossRefGoogle Scholar
  120. Tucek, S., 1985, Regulation of acetylcholine synthesis in the brain, J. Neurochcm. 44: 11.CrossRefGoogle Scholar
  121. Unsworth, C. D. and Johson, R. G., 1990, Acetylcholine and ATP are coreleased from the electromotor nerve terminals of Narcine brasiliensis by an exocytotic mechanism, Froc. Natl. Acad Sci USA 87: 553.CrossRefGoogle Scholar
  122. Uvniis, B., 1985, Is exocytosis an initial or fmal event in the release of biogenic amines?, In: “Nonvesicular transport”, S.S. Rothman and J.J.L. Ho eds., Willey and Sons, New York.Google Scholar
  123. Valtorta, F., Fesce, R., Grohovaz, F., Haimann, C., Hurlbut, W. P., Iezzi, N, Torri Tarelli, F., Villa, A. and Ceccarelli, B., 1990, Neurotransmitter release and synaptic recycling, Neuroscience 35: 477.PubMedCrossRefGoogle Scholar
  124. Van der Kloot, W., 1988, Acetylcholine quanta are released from vesicles by exocytosis (and why some think not), Neuroscience 24: 1.PubMedCrossRefGoogle Scholar
  125. Van der Kloot, W., 1991, The regulation of quantal size, Progre sinNeurobiol. 36: 93.CrossRefGoogle Scholar
  126. Vautrin, J. and Membrini, J., 1981, Caractéristiques du potentiel unitaire de plaque motrice de la grenouille, J. Physiol. (Pan) 77: 999.Google Scholar
  127. Vizi, E. S., 1984, Critique. Physiological role of cytoplasmic and non-synaptic release of transmitter, Neurochem. hit. 6: 435.Google Scholar
  128. Volknandt, W. and Zimmermann, H., 1986, Acetylcholine, ATP, and proteoglycan are common to synaptic vesicles isolated from the electric organs of electric eel and electric catfish as well as from rat diaphragm, J. Neurochem. 47: 1449.PubMedCrossRefGoogle Scholar
  129. Wellhöner, H. H., 1992, Tetanus and botulinum Neurotoxins, In: “Handbook of Experimental Pharmacology”, H. Herkin and F. Hucho, eds., Springer, Berlin.Google Scholar
  130. Wernig, A. and Stirner, H., 1977, Quantum amplitude distributions points to functional unity of the synaptic `active zone’, Nature 268: 820.CrossRefGoogle Scholar
  131. White, T. D., Potter, P. and Wonnacott, S., 1980, Depolarization induced release of ATP from cortical synaptosomes is not associated with acetylcholine release, J. Neurochem. 34: 1109.PubMedCrossRefGoogle Scholar
  132. Whittaker, V. P., 1986, The storage and release of acetylcholine, T.LP.S. 7: 312.Google Scholar
  133. Whittaker, V. P., Essman, W. B. and Dowe, G. H. C., 1972, The isolation of pure cholinergic synaptic vesicles from the electric organs of elasmobranch fish of the family Torpinidae, Biochem. J. 128: 833.PubMedGoogle Scholar
  134. Whittaker, V. P., Michaelson, I. A. and Kirkland, R. J. A., 1963, The separation of synaptic vesicles from disrupted nerve ending particles, synaptosomes, Blochem. Pharmacol. 12: 300.CrossRefGoogle Scholar
  135. Young, S. H. and Chow, L, 1987, Quantal release of transmitter is not associated with channel opening on the neuronal membrane, Science 238: 1712.PubMedCrossRefGoogle Scholar
  136. Zimmerberg, J., Curran, M. and Cohen, F. S., 1991, A lipid/protein complex hypothesis for exocytotic fusion pore formation, Ann. N. Y. Acad. Sci 635: 307.PubMedCrossRefGoogle Scholar
  137. Zimmermann, H., 1982, Biochemistry of the isolated cholinergic vesicles, In: “Neurotransmitter vesicles”, R.L. Klein, H. Lagercrantz and H. Zimmermann, eds., Academic Press, New York.Google Scholar
  138. Zimmermann, H., 1988, Cholinergie synaptic vesicles, In: “The cholinergie synapse”, V.P. Whittaker ed., Springer-Verlag, Berlin.Google Scholar

Copyright information

© Springer Science+Business Media New York 1993

Authors and Affiliations

  • Ladislav Tauc
    • 1
  • Bernard Poulain
    • 1
  1. 1.Laboratoire de Neurobiologie Cellulaire et MoléculaireC.N.R.S.Gif-sur-Yvette CedexFrance

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