Cholinergic Synaptic Vesicles

  • H. Zimmermann
Part of the Handbook of Experimental Pharmacology book series (HEP, volume 86)

Abstract

Axon terminals of cholinergic neurons are typically filled with electron-lucent synaptic vesicles. In the central nervous system, the ganglionic synapses and the neuromuscular junction (NMJ) the diameter of these vesicles is in the range of 40–50 nm. In the cholinergic nerve terminals of the electric organs of electric fishes, important as model cholinergic synapses (see Chap. 2), the diameter of electron-lucent vesicles may be greater (58 nm, electric eel; 90 nm, electric rays; for references, see Volknandt and Zimmermann 1986). It is this type of electronlucent synaptic vesicle which is normally referred to as the cholinergic synaptic vesicle. It should be kept in mind however that cholinergic nerve terminals also typically contain a small number of dense-cored synaptic vesicles of a diameter of 80–150nm. Since very little is known about the function and fate of these dense-cored vesicles and since the electric organ of electric rays as the source par excellence of cholinergic vesicles does not contain any, they have been neglected in the study of the biochemistry of cholinergic synaptic transmission.

Keywords

Morphine Retina Polypeptide Bicarbonate Oxalate 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Ágoston DV, Conlon JM (1986) Presence of vasoactive intestinal polypeptide-like immu- noreactivity in the electromotor system of Torpedo marmorata. J Neurochem 47:446–453Google Scholar
  2. Ágoston DV, Kosh, JW, Lisziewicz J, Whittaker VP (1985) Separation of recycling and reserve synaptic vesicles from cholinergic nerve terminals of the myenteric plexus of guinea-pig ileum. J Neurochem 44:299–305PubMedGoogle Scholar
  3. Ágoston DV, Ballmann M, Conlon JM, Dowe GHC, Whittaker VP (1986) Isolation of neuropeptide-containing vesicles from the guinea-pig ileum. J Neurochem 45:398–406Google Scholar
  4. Anderson DC, King SC, Parsons SM (1982) Proton gradient linkage to active uptake of [3H]acetylcholine by Torpedo electric organ synaptic vesicles. Biochemistry 21: 3037–3043PubMedGoogle Scholar
  5. Anderson DC, King SC, Parsons SM (1983 a) Pharmacological characterization of acetylcholine transport system in purified Torpedo electric organ synaptic vesicles. Mol Pharmacol 24:48–54PubMedGoogle Scholar
  6. Anderson DC, King SC, Parsons SM (1983 b) Inhibition of [3H]acetylcholine active transport by tetraphenylborate and other anions. Mol Pharmacol 24:55–59PubMedGoogle Scholar
  7. Anderson DC, Bahr BA, Parsons SM (1986) Stoichiometrics of acetylcholine uptake, release, and drug inhibition in Torpedo synaptic vesicles; heterogeneity in acetylcholine transport and storage. J Neurochem 46:1207–1213PubMedGoogle Scholar
  8. Angel I, Michaelson DM (1981) Determination of Δψ, ΔpH and the proton electrochemical gradient in isolated cholinergic synaptic vesicles. Life Sci 29:411–416PubMedGoogle Scholar
  9. Bahr BA, Parsons SM (1986 a) Acetylcholine transport and drug inhibition in Torpedo synaptic vesicles. J Neurochem 46:1214–1218PubMedGoogle Scholar
  10. Bahr BA, Parons SM (1986 b) Demonstration of a receptor in Torpedo synaptic vesicles for the acetylcholine storage blocker L-trans-2-(4-phenyl[3,4-3H]-piperidino)cyclohex-anol). Proc Natl Acad Sci USA 83:2267–2270PubMedGoogle Scholar
  11. Barker LA, Dowdall MJ, Whittaker VP (1972) Choline metabolism in the cerebral cortex of guinea pig. Biochem J 130:1063–1080PubMedGoogle Scholar
  12. Batteiger DL, Parsons SM (1986) The ATPase of cholinergic synaptic vesicles is associated with sugars. Neurochem Int 8:249–253PubMedGoogle Scholar
  13. Birman S, Israël M, Lesbats B, Morel N (1986) Solubilization and partial purification of a presynaptic membrane protein ensuring calcium-dependent acetylcholine release from proteoliposomes. J Neurochem 47:433–444PubMedGoogle Scholar
  14. Boyne AF (1978) Neurosecretion: integration of recent findings into the vesicle hypothesis. Life Sci 22:2057–2066PubMedGoogle Scholar
  15. Boyne AF, Bohan TP, Williams TH (1974) Effect of calcium-containing fixation solutions on cholinergic synaptic vesicles. J Cell Biol 63:780–785PubMedGoogle Scholar
  16. Breer H, Morris SJ, Whittaker VP (1977) Adenosine triphosphatase activity associated with purified cholinergic synaptic vesicles of Torpedo marmorata. Eur J Biochem 80:313–318PubMedGoogle Scholar
  17. Breer H, Morris SJ, Whittaker VP (1978) A structural model of cholinergic synaptic vesicles from the electric organ of Torpedo marmorata deduced from density measurements at different osmotic pressures. Eur J Biochem 87:453–458PubMedGoogle Scholar
  18. Buckley K, Kelly RB (1985) Identification of a transmembrane glycoprotein specific for secretory vesicles of neural and endocrine cells. J Cell Biol 100:1284–1294PubMedGoogle Scholar
  19. Buckley KM, Schweitzer ES, Miljanich GP, Clift-O’Grady L, Kustner PP, Reichardt LF, Kelly RB (1983) A synaptic vesicle antigen is restricted to the junctional region of the presynaptic plasma membrane. Proc Natl Acad Sci USA 80:7342–7346PubMedGoogle Scholar
  20. Bulenda D, Gratzl M (1985) Matrix-free Ca2+ in isolated chromaffin vesicles. Biochemistry 24:7760–7765PubMedGoogle Scholar
  21. Carlson SS, Kelly RB (1983) A highly antigenic proteoglycan-like component of cholinergic synaptic vesicles. J Biol Chem 258:11082–11091PubMedGoogle Scholar
  22. Carlson SS, Wagner JA, Kelly JS (1978) Purification of synaptic vesicles from elasmo-branch electric organ and the use of biophysical criteria to demonstrate purity. Biochemistry 17:1188–1199PubMedGoogle Scholar
  23. Carlson SS, Caroni P, Kelly RB (1986) A nerve terminal anchorage protein from electric organ. J Cell Biol 103:509–520PubMedGoogle Scholar
  24. Carpenter RS, Parsons SM (1978) Electrogenic behavior of synaptic vesicles from Torpedo californica. J Biol Chem 253:326–329PubMedGoogle Scholar
  25. Carpenter RS, Koenigsberger R, Parsons SM (1980) Passive uptake of acetylcholine and other organic cations by synaptic vesicles from Torpedo electric organ. Biochemistry 19:4373–4379PubMedGoogle Scholar
  26. Carrol PT, Aspry JM (1980) Subcellular origin of cholinergic transmitter release from mouse brain. Science 210:641–642Google Scholar
  27. Carrol PT, Nelson SH (1978) Cholinergic vesicles: ability to empty and refill independently of cytoplasmic acetylcholine. Nature 199:85–86Google Scholar
  28. Ceccarelli B, Hurlbut WP (1980) Vesicle hypothesis of the release of quanta of acetylcholine. Physiol Rev 6:396–441Google Scholar
  29. Ceccarelli B, Hurlbut WP, Mauro A (1973) Turnover of transmitter and synaptic vesicles at the frog neuromuscular junction. J Cell Biol 57:499–524PubMedGoogle Scholar
  30. Ceccarelli B, Grohovaz F, Hurlbut WP, Jezzi N (1979a) Freeze-fracture studies of frog neuromuscular junctions during intense release of neurotransmitter. I. Effects of black widow spider venom and Ca2+-free solutions on the structure of the active zone. J Cell Biol 81:163–177PubMedGoogle Scholar
  31. Ceccarelli B, Grohovaz F, Hurlbut WP, Jezzi N (1979 b) Freeze-fracture studies of frog neuromuscular junctions during intense release of neurotransmitter — II. Effects of electrical stimulation and high potassium. J Cell Biol 81:178–192PubMedGoogle Scholar
  32. Corthay J, Dunant Y, Loctin F (1982) Acetylcholine changes underlying transmission of a single nerve impulse in the presence of 4-aminopyridine in Torpedo. J Physiol (Lond) 325:461–479Google Scholar
  33. Dahlström A, Larsson P-A, Carlson SS, Bööj S (1985) Localization and axonal transport of immunoreactive cholinergic organelles in rat motor neurons — an immunofluorescent study. Neuroscience 14:607–625PubMedGoogle Scholar
  34. Day NC, Wien D, Michaelson DM (1985) Saturable [D-Ala2, D-Leu5]-enkephalin transport into cholinergic synaptics vesicles. FEBS Lett 183:25–28PubMedGoogle Scholar
  35. De Robertis E, Rodriguez de Lores Arnaiz G, Salganicoff L, Pellegrino de Iraldi A, Zieher LM (1963) Isolation of synaptic vesicles and structural organization of the acetylcholine system within brain nerve endings. J Neurochem 10:225–235Google Scholar
  36. Deutsch JW, Kelly RB (1981) The lipids of synaptic vesicles: relevance to the mechanisms of membrane fusion. Biochemistry 20:378–385PubMedGoogle Scholar
  37. Diebler, MF, Lazereg S (1985) Mg-ATPase and Torpedo cholinergic synaptic vesicles. J Neurochem 44:1633–1641PubMedGoogle Scholar
  38. Diebler MF, Morot-Gaudry (1981) Acetylcholine incorporation by cholinergic synaptic vesicles from Torpedo marmorata. J Neurochem 37:467–475PubMedGoogle Scholar
  39. Dowdall MJ, Barker LA, Whittaker VP (1972) Choline metabolism in the cerebral cortex of guinea pigs. Phosphorylcholine and lipid choline. Biochem J 130:1081–1094PubMedGoogle Scholar
  40. Dowdall MJ, Boyne AF, Whittaker VP (1974) Adenosine triphosphate, a constituent of cholinergic synaptic vesicles. Biochem J 140:1–12PubMedGoogle Scholar
  41. Dowe GHC, Kilbinger H, Whittaker VP (1980) Isolation of cholinergic synaptic vesicles from the myenteric plexus of guinea-pig small intestine. J Neurochem 35:993–1003PubMedGoogle Scholar
  42. Dunant Y, Gautron J, Israël M, Lesbats B, Manaranche R (1972) Les compartiments d’acétylcholine de l’organe électrique de la Torpille et leurs modifications par la stimulation. J Neurochem 19:1987–2002PubMedGoogle Scholar
  43. Dunant Y, Jones GJ, Loctin F (1982) Acetylcholine measured at short time intervals during transmission of nerve impulses in the electric organ of Torpedo. J Physiol (Lond) 325:441–460Google Scholar
  44. Edwards C, Doležal V, Tuček S, Zemková H, Yyskočil F (1985) Is an acetylcholine transport system responsible for nonquantal release of acetylcholine at the rodent myoneural junction? Proc Natl Acad Sci USA 82:3514–3518PubMedGoogle Scholar
  45. Füldner HH, Stadler H (1982) 31P-NMR analysis of synaptic vesicles. Status of ATP and internal pH. Eur J Biochem 121:519–524PubMedGoogle Scholar
  46. Garcia-Segura LM, Muller D, Dunant Y (1986) Increase in the number of presynaptic large intramembrane particles during synaptic transmission at the Torpedo nerve-electro- plaque junction. Neuroscience 19:63–79PubMedGoogle Scholar
  47. Giompres PE, Luqmani YA (1980) Cholinergic synaptic vesicles isolated from Torpedo marmorata: demonstration of acetylcholine and choline uptake in an in vitro system. Neuroscience 5:1041–1052PubMedGoogle Scholar
  48. Giompres PE, Whittaker VP (1984) Differences in the osmotic fragility of recycling and reserve synaptic vesicles from the cholinergic electromotor nerve terminals of Torpedo and their possible significance for vesicle recycling. Biochem Biophys Acta 770: 166–170PubMedGoogle Scholar
  49. Giompres PE, Morris SJ, Whittaker VP (1981 a) The water spaces in cholinergic synaptic vesicles from Torpedo measured by changes in density induced by permeant substances. Neuroscience 6:757–763PubMedGoogle Scholar
  50. Giompres PE, Zimmermann H, Whittaker VP (1981 b) Purification of small dense vesicles from stimulated Torpedo electric tissue by glass bead chromatography. Neuroscience 6:765–774PubMedGoogle Scholar
  51. Giompres PE, Zimmermann H, Whittaker VP (1981 c) Changes in the biochemical and biophysical parameters of cholinergic synaptic vesicles on transmitter release and during a subsequent period of rest. Neuroscience 6:775–785PubMedGoogle Scholar
  52. Grondai EJM, Zimmermann H (1986) Ectonucleotidase activities associated with cholinergic synaptosomes isolated from Torpedo electric organ. J Neurochem 47:871–881Google Scholar
  53. Häggblad J, Heilbronn E (1987) Externally applied ATP causes inosital triphosphate accumulation in cultured myotubes. Neurosci Lett 74:199–204PubMedGoogle Scholar
  54. Harlos P, Lee DA, Stadler H (1984) Characterization of a Mg2+-ATPase and a proton pump in cholinergic synaptic vesicles from the electric organ of Torpedo marmorata. Eur J Biochem 144:441–446PubMedGoogle Scholar
  55. Heuser JE, Reese TS (1973) Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog junction. J Cell Biol 57:315–344PubMedGoogle Scholar
  56. Heuser JE, Reese TS, Dennis MJ, Jan Y, Jan L, Evans L (1979) Synaptic vesicle exocytosis captured by quick freezing and correlated with quantal transmitter release. J Cell Biol 81:275–300PubMedGoogle Scholar
  57. Hooper JE, Kelly RB (1984 a) Calcium-dependent calmodulin binding to cholinergic synaptic vesicles. J Biol Chem 259:141–147PubMedGoogle Scholar
  58. Hooper JE, Kelly RB (1984b) Calmodulin is tightly associated with synaptic vesicles independent of calcium. J Biol Chem 259:148–153PubMedGoogle Scholar
  59. Hooper JE, Carlson SS, Kelly RB (1980) Antibodies to synaptic vesicles purified from Narcine electric organ bind a sub-class of mammalian nerve terminals. J Cell Biol 87:104–113PubMedGoogle Scholar
  60. Israël M, Manaranche R (1985) The release of acetylcholine: from a cellular towards a molecular mechanism. Biol Cell 55:1–14PubMedGoogle Scholar
  61. Israël M, Gautron J, Lesbats B (1970) Fractionnement de l’organe éléctrique de la Torpille: localisation subcellulaire de l’acetylcholine. J Neurochem 17:1441–1450PubMedGoogle Scholar
  62. Israël M, Dunant Y, Manaranche R (1979) The present status of the vesicular hypothesis. Prog Neurobiol 13:237–275PubMedGoogle Scholar
  63. Israël M, Manaranche R, Marsal J, Meunier FM, Morel N, Frachon P, Lesbats B (1980) ATP-dependent calcium uptake by cholinergic synaptic vesicles isolated from Torpedo electric organ. J Membr Biol 54:115–126PubMedGoogle Scholar
  64. Israël M, Lesbats B, Morel N, Manaranche R, Gulik-Krzywicki T, Dedieu JC (1984) Reconstitution of a functional synaptosomal membrane possessing the protein constituents involved in acetylcholine translocation. Proc Natl Acad Sci USA 81:277–281PubMedGoogle Scholar
  65. Jones RT, Walker JH, Stadler H, Whittaker VP (1982) Immunohistochemical localization of a synaptic vesicle antigen in a cholinergic neuron under conditions of stimulation and rest. Cell Tissue Res 223:117–126PubMedGoogle Scholar
  66. Kelly RB, Hooper JE (1982) Cholinergic vesicles. In: Poisner AM, Trifaró JM (eds) The secretory granule. Elsevier, Amsterdam, pp 81–119Google Scholar
  67. Kelly RB, Deutsch JW, Carlson SS, Wagner JA (1979) Biochemistry of neurotransmitter release. Annu Rev Neurosci 2:399–446PubMedGoogle Scholar
  68. Kiene M-L, Stadler H (1987) Synaptic vesicles in electromotoneurones. I. Axonal transport, site of transmitter uptake and processing of a core proteoglycan during maturation. EMBO J 6:2209–2215PubMedGoogle Scholar
  69. Knight DE, Scrutton MC (1986) Gaining access to the cytosol: the technique and some applications of electropermeabilization. Biochem J 234:497–506PubMedGoogle Scholar
  70. Kobos RK, Rechnitz GA (1976) Acetylcholine-ATP binding by direct membrane electrode measurement. Biochem Biophys Res Commun 71:762–767PubMedGoogle Scholar
  71. Koenigsberger R, Parsons SM (1980) Bicarbonate and magnesium ion-ATP dependent stimulation of acetylcholine uptake by Torpedo electric organ synaptic vesicles. Biochem Biophys Res Commun 94:305–312PubMedGoogle Scholar
  72. Ledeen RW, Sbaschnig-Agler M, Aquino DA, Diebler MF, Lazereg S, Parsons SM (1987) Ganglioside transport and function in the nervous system. Evidence for gangliosides in synaptics vesicles. In: Tuček S (ed) Metabolism and development of the nervous system. Academia, Praha, pp 106–112Google Scholar
  73. Lundberg JM, Fried G, Fahrenkrugh J, Holmstedt B, Hökfelt T, Lagercrantz H, Lundgren G, Ånggård A (1981) Subcellular fractionation of cat submandibular gland: comparative studies on the distribution of acetylcholine and vasoactive intestinal polypeptide (VIP). Neuroscience 6:1001–1010PubMedGoogle Scholar
  74. Luqmani YA (1981) Nucleotide uptake by isolated cholinergic synaptic vesicles: evidence for an ATP carrier. Neuroscience 6:1011–1021PubMedGoogle Scholar
  75. Luqmani YA, Sudlow G, Whittaker VP (1980) Homocholine and acetylcholine: false transmitters in the cholinergic electromotor system of Torpedo. Neuroscience 5:153–160PubMedGoogle Scholar
  76. Macintosh FC (1980) The role of vesicles in cholinergic systems. In Brzin M, Sket D, Bachelard H (eds) Synaptic constituents in health and disease. Mladinska, Lubljana; Pergamon, Oxford, pp 11–50Google Scholar
  77. Macintosh FC, Collier B (1976) Neurochemistry of cholinergic nerve terminals. In: Zamis E (ed) Neuromuscular junction. Springer, Berlin Heidelberg New York, pp 99–228 (Handbook of experimental pharmacology, vol 42)Google Scholar
  78. Marshall IG, Parsons SM (1987) The vesicular acetylcholine transport system. Trends Neurosci 10:174–177Google Scholar
  79. Matthew WD, Tsavaler L, Reichardt LF (1981) Identification of a synaptic vesicle-specific membrane protein with a wide distribution in neuronal and neurosecretory tissue. J Cell Biol 91:257–269PubMedGoogle Scholar
  80. Meldolesi J, Borgese N, de Camilli P, Ceccarelli B (1978) Cytoplasmic membranes and the secretory process. In: Poste G, Nicolson GL (eds) Membrane fusion. Elsevier/North-Holland, Amsterdam, pp 509–627 (Cell surface reviews, vol. 5)Google Scholar
  81. Melega WP, Howard BD (1981) Choline and acetylcholine metabolism in PC12 secretory cells. Biochemistry 20:4477–4483PubMedGoogle Scholar
  82. Michaelson DM, Angel I (1980) Determination of Δ pH in cholinergic synaptic vesicles: its effect on storage and release of acetylcholine. Life Sci 27:39–44PubMedGoogle Scholar
  83. Michaelson DM, Angel I (1981) Saturable acetylcholine transport into purified cholinergic vesicles. Proc Natl Acad Sci USA 78:2048–2052PubMedGoogle Scholar
  84. Michaelson DM, Ophir I (1980) Sideness of (calcium, magnesium) adenosine triphosphatase of purified Torpedo synaptic vesicles. J Neurochem 34:1483–1490PubMedGoogle Scholar
  85. Michaelson DM, Wien-Naor D (1987) Enkephalin uptake into cholinergic synaptic vesicles and nerve terminals. Ann NY Acad Sci 493:234–251PubMedGoogle Scholar
  86. Michaelson DM, Ophir I, Angel I (1980) ATP-stimulated Ca2+ transport into cholinergic Torpedo synaptic vesicles. J Neurochem 35:116–124PubMedGoogle Scholar
  87. Michaelson DM, McDowall C, Sarne Y (1984) The Torpedo electric organ is a model for opiate regulation of acetylcholine release. Brain Res 305:173–176PubMedGoogle Scholar
  88. Michaelson DM, Licht R, Burstein M (1987) The effects of the vesicular uptake blocker AH5183 on evoked and spontaneous release of acetylcholine from cholinergic nerve terminals. In: Dowdall MJ, Hawthorne JN (eds) Cellular and molecular basis of cholinergic function. Horwood, Chichester, pp 316–322Google Scholar
  89. Miledi R, Molenaar PC, Polak RL (1982) Free and bound acetylcholine in frog muscle. J Physiol (Lond) 333:189–199Google Scholar
  90. Molenaar PC, Polak RL (1973) Newly formed acetylcholine in synaptic vesicles in brain tissue. Brain Res 62:537–542PubMedGoogle Scholar
  91. Molenaar PC, Nickolson VJ, Polak RL (1973) Preferential release of newly synthetized [3H]acetylcholine from rat cerebral cortex slices in vitro. Br J Pharmacol 47:97–108PubMedGoogle Scholar
  92. Morel N, Meunier FR (1981) Simultaneous release of acetylcholine and ATP from stimulated cholinergic synaptosomes. J Neurochem 36:1766–1773PubMedGoogle Scholar
  93. Morris SJ (1973) Removal of residual amounts of acetylcholinesterase and membrane contamination from synaptic vesicles isolated from the electric organ of Torpedo. J Neurochem 21:713–715PubMedGoogle Scholar
  94. Morris SJ (1980) The structure and stoichiometry of electric ray synaptic vesicles. Neuroscience 5:1509–1516PubMedGoogle Scholar
  95. Nagy A, Baker RR, Morris SJ, Whittaker VP (1976) The preparation and characterization of synaptic vesicles of high purity. Brain Res 109:285–309PubMedGoogle Scholar
  96. Ohsawa K, Dowe GHC, Morris SJ, Whittaker VP (1979) The lipid and protein content of cholinergic synaptic vesicles from the electric organ of Torpedo marmorata purified to constant composition: implications for vesicle structure. Brain Res 161:447–457PubMedGoogle Scholar
  97. Osborne NN, Beale R, Nicholas D, Stadler H, Walker JH, Jones RT, Whittaker VP (1982) An antiserum to cholinergic synaptic vesicles from Torpedo recognizes nerve terminals in retinas from a variety of species. Cell Mol Neurobiol 2:157–163Google Scholar
  98. Parsons SM, Koenigsberger R (1980) Specific stimulated uptake of acetylcholine by Torpedo electric organ synaptic vesicles. Proc Natl Acad Sci USA 77:6234–6238PubMedGoogle Scholar
  99. Parsons SM, Carpenter RS, Koenigsberger R, Rothlein JE (1982) Transport in the cholinergic synaptic vesicle. Fed Proc 41:2765–2768Google Scholar
  100. Reichardt LF, Kelly RB (1983) A molecular description of nerve terminal function. Annu Rev Biochem 52:871–926PubMedGoogle Scholar
  101. Rephaeli A, Parsons SM (1982) Calmodulin stimulation of 45Ca2+ transport and protein phosphorylation in cholinergic synaptic vesicles. Proc Natl Acad Sci USA 79:5783–5787PubMedGoogle Scholar
  102. Rothlein JE, Parsons SM (1979) Specificity of association of a Ca2+/Mg2+ ATPase with cholinergic synaptic vesicles from Torpedo electric organ. Biochem Biophys Res Commun 88:1069–1079PubMedGoogle Scholar
  103. Rothlein JE, Parsons SM (1980) Bicarbonate stimulation of the Ca2+/Mg2+ ATPase of Torpedo electric organ synaptic vesicles. Biochem Biophys Res Commun 95: 1869–1874PubMedGoogle Scholar
  104. Rothlein JE, Parsons SM (1982) Origin of the bicarbonate stimulation of Torpedo electric organ synaptic vesicle ATPase. J Neurochem 39:1660–1668PubMedGoogle Scholar
  105. Salehomoghaddam SH, Collier B (1976) The relationship between acetylcholine release from brain slices and the acetylcholine content of subcellular fractions prepared from brain. J Neurochem 27:71–76Google Scholar
  106. Schmidt R, Zimmermann H, Whittaker VP (1980) Metal ion content of cholinergic vesicles isolated from the electric organ of Torpedo effect of stimulation induced transmitter release. Neuroscience 5:625–638PubMedGoogle Scholar
  107. Schweitzer E (1987) Coordinated release of ATP and ACh from cholinergic synaptosomes and its inhibition by calmodulin antagonists. J Neurosci 7:2948–2956PubMedGoogle Scholar
  108. Sheridan MN, Whittaker VP, Israël M (1966) The subcellular fractionation of the electric organ of Torpedo. Z Zellforsch 74:291–307Google Scholar
  109. Stadler H, Dowe GHC (1982) Identification of a heparan sulfate-containing proteoglycan as a specific core component of cholinergic synaptic vesicles from Torpedo marmorata. EMBO J 1:1381–1384PubMedGoogle Scholar
  110. Stadler H, Fenwick EM (1983) Cholinergic synaptic vesicles from Torpedo marmorata contain an atractyloside-binding protein related to the mitochondrial ADP/ATP carrier. Eur J Biochem 136:377–382PubMedGoogle Scholar
  111. Stadler H, Füldner HH (1980) Proton NMR detection of acetylcholine status in synaptic vesicles. Nature 286:293–294PubMedGoogle Scholar
  112. Stadler H, Kiene M-L (1987) 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 6:2217–2221PubMedGoogle Scholar
  113. Stadler H, Tashiro T (1979) Isolation of synaptosomal plasma membranes from cholinergic nerve terminals and a comparison of their proteins with those of synaptic vesicles. Eur J Biochem 101:171–178PubMedGoogle Scholar
  114. Stadler H, Tsukita K (1984) Synaptic vesicles contain an ATP-dependent proton pump and show ‘knob-like’ protrusions on their surface. EMBO J 3:3333–3337PubMedGoogle Scholar
  115. Suszkiw JB (1980) Kinetics of acetylcholine recovery in Torpedo electromotor synapses depleted of synaptic vesicles. Neuroscience 5:1341–1349PubMedGoogle Scholar
  116. Suszkiw JB, Manalis RS (1987) Acetylcholine mobilization: effects of vesicular ACh uptake blocker, AH5183, on ACh release in rat brain synaptosomes, Torpedo electroplax and frog neuromuscular junction. In: Dowdall MJ, Hawthorne JN (eds) Cellular and molecular basis of cholinergic function. Horwood, Chichester, pp 323–332Google Scholar
  117. Suszkiw JB, Zimmermann H, Whittaker VP (1978) Vesicular storage and release of acetylcholine in Torpedo elecroplaque synapses. J Neurochem 30:1269–1280PubMedGoogle Scholar
  118. Tashiro T, Stadler H (1978) Chemical composition of cholinergic synaptic vesicles from Torpedo marmorata based on improved purification. Eur J Biochem 90:479–487PubMedGoogle Scholar
  119. Toll T, Howard BD (1980) Evidence that an ATPase and a protonmotive force function in the transport of acetylcholine into storage vesicles. J Biol Chem 255:1787–1789PubMedGoogle Scholar
  120. Torri-Tarelli F, Grohovaz F, Fesce R, Ceccarelli B (1985) Temporal coincidence between synaptic vesicle fusion and quantal secretion of acetylcholine. J Cell Biol 101: 1386–1399PubMedGoogle Scholar
  121. Tuček S (1978) Acetylcholine synthesis in neurones. Chapman and Hall, LondonGoogle Scholar
  122. Volknandt W, 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 47:1449–1462PubMedGoogle Scholar
  123. Volknandt W, Naito S, Ueda T, Zimmermann H (1987) Synapsin I is associated with cholinergic nerve terminals in the electric organs of Torpedo, Electrophorus and Malapterurus and copurifies with Torpedo synaptic vesicles. J Neurochem 49:342–347PubMedGoogle Scholar
  124. Von Wedel R, Carlson SS, Kelly RB (1981) Transfer of synaptic vesicle antigens to the presynaptic plasma membrane during exocytosis. Proc Natl Acad Sci USA 78:1014–1018Google Scholar
  125. Wagner JA, Kelly RB (1979) Topological organization of proteins in an intracellular secretory organelle: the synaptic vesicle. Proc Natl Acad Sci USA 76:4126–4130PubMedGoogle Scholar
  126. Wagner JA, Carlson SS, Kelly RB (1978) Chemical and physical characterization of cholinergic synaptic vesicles. Biochemistry 17:1199–1206PubMedGoogle Scholar
  127. Walker JH, Jones RT, Obrocki J, Richardson GP, Stadler H (1982) Presynaptic plasma membranes and synaptic vesicles of cholinergic nerve endlings demonstrated by means of specific antisera. Cell Tissue Res 223:101–116PubMedGoogle Scholar
  128. Walker JH, Obrocki J, Südhoff TC (1983 a) Calelectrin, a calcium-dependent membrane- binding protein associated with secretory granules in Torpedo cholinergic electromotor nerve endings and rat adrenal medulla. J Neurochem 41:139–145PubMedGoogle Scholar
  129. Walker JH, Obrocki J, Zimmermann CW (1983 b) Identification of a proteoglycan antigen characteristic of cholinergic synaptic vesicles. J Neurochem 41:209–216PubMedGoogle Scholar
  130. Walker JH, Stadler H, Witzemann VL (1984) Calmodulin binding proteins of the cholinergic electromotor synapse: synaptosomes, synaptic vesicles, receptor-enriched membranes, and cytoskeleton. J Neurochem 42:314–320PubMedGoogle Scholar
  131. Walker JH, Kristjansson GI, Stadler H (1986) Identification of a synaptic vesicle antigen (M1 86000) conserved between Torpedo and rat. J Neurochem 46:875–881PubMedGoogle Scholar
  132. Weiler M, Roed IS, Whittaker VP (1982) The kinetics of acetylcholine turnover in a resting cholinergic nerve terminal and the magnitude of the cytoplasmic compartment. J Neurochem 38:1187–1191PubMedGoogle Scholar
  133. Whittaker VP (1984 a) The structure and function of cholinergic synaptic vesicles. Biochem Soc Transact 12:561–575Google Scholar
  134. Whittaker VP (1984 b) The synaptic vesicle. In: Lajtha A (ed) Structural elements of the nervous system. Plenum, New York, pp 41–69 (Handbook of Neurochemistry, 2nd edn, vol 7)Google Scholar
  135. Whittaker VP, Sheridan MN (1965) The morphology and acetylcholine content of cerebral cortical synaptic vesicles. J Neurochem 12:363–372PubMedGoogle Scholar
  136. Whittaker VP, Stadler G (1980) The structure and function of cholinergic synaptic vesicles. In: Bradshaw RA, Schneider DM (eds) Proteins of the nervous system, 2nd edn. Raven, New York, pp 231–255Google Scholar
  137. Whittaker VP, Michaelson IA, Kirkland RJA (1963) The separation of synaptic vesicles from disrupted nerve ending particles. Biochem Pharmacol 12:300–302PubMedGoogle Scholar
  138. Whittaker VP, Michaelson IA, Kirkland RJA (1964) The separation of synaptic vesicles from nerve-ending particles (‘synaptosomes’). Biochem J 90:293–303PubMedGoogle Scholar
  139. Whittaker VP, Essman WB, Dowe GHC (1972) The isolation of pure cholinergic synaptic vesicles from the electric organs of elasmobranch fish of the family Torpedinidae. Biochem J 128:833–846PubMedGoogle Scholar
  140. Wilson WS, Schulz RA, Cooper JT (1973) The isolation of cholinergic synaptic vesicles from bovine superior cervical ganglion and estimation of their acetylcholine content. J Neurochem 20:659–667PubMedGoogle Scholar
  141. Zechel K, Stadler H (1982) Identification of actin in highly purified synaptic vesicles from the electric organ of Torpedo marmorata. J Neurochem 39:788–795PubMedGoogle Scholar
  142. Zhu PC, Thureson-Klein Å, Klein RL (1986) Exocytosis from large dense cored vesicles outside the active synaptic zones of terminals within the trigeminal subnucleus caudalis: a possible mechanism for neuropeptide release. Neuroscience 19:43–54PubMedGoogle Scholar
  143. Zimmermann H (1978) Turnover of adenine nucleotides in cholinergic synaptic vesicles of the Torpedo electric organ. Neuroscience 3:827–836PubMedGoogle Scholar
  144. Zimmermann H (1979) Vesicle recycling and transmitter release. Neuroscience 4: 1773–1804PubMedGoogle Scholar
  145. Zimmermann H (1981) Mechanism(s) of secretion of chemical neurotransmitters: chairman’s overview: In: Stjärne L, Hedquist P, Lagercrantz H, Wennmalm Å (eds) Chemical neurotransmission 75 years. Academic, New York, pp 179–185Google Scholar
  146. Zimmermann H (1982 a) Isolation of cholinergic nerve vesicles. In: Klein RL, Lagercrantz H, Zimmermann H (eds) Neurotransmitter vesicles. Academic, New York, pp 241–269Google Scholar
  147. Zimmermann H (1982b) Biochemistry of the isolated cholinergic vesicles. In: Klein RL, Lagercrantz H, Zimmermann H (eds) Neurotransmitter vesicles. Academic, New York, pp 271–304Google Scholar
  148. Zimmermann H (1982c) Insights into the functional role of cholinergic vesicles. In: Klein RL, Lagercrantz H, Zimmermann H (eds) Neurotransmitter vesicles. Academic, New York, pp 305–359Google Scholar
  149. Zimmermann H, Bokor JT (1979) ATP recycles independently of ACh in cholinergic synaptic vesicles. Neurosci Lett 13:319–324PubMedGoogle Scholar
  150. Zimmermann H, Denston CR (1977 a) Recycling of synaptic vesicles in the cholinergic synapses of the Torpedo electric organ during induced transmitter release. Neuroscience 2:695–714Google Scholar
  151. Zimmermann H, Denston CR (1977 b) Separation of synaptic vesicles of different functional states from the cholinergic synapses of the Torpedo electric organ. Neuroscience 2:715–730PubMedGoogle Scholar
  152. Zimmermann H, Dowdall MJ (1977) Vesicular storage and release of a cholinergic false transmitter (acetylpyrrolcholine) in the Torpedo electric organ. Neuroscience 2:731–739PubMedGoogle Scholar
  153. Zimmermann H, Whittaker VP (1974 a) Effect of electrical stimulation on the yield and composition of synaptic vesicles from the cholinergic synapses of the electric organ of Torpedo: a combined biochemical, electrophysiological and morphological study. J Neurochem 22:435–450PubMedGoogle Scholar
  154. Zimmermann H, Whittaker VP (1974 b) Different recovery rates of the electro- physiological, biochemical and morphological parameters in the cholinergic synapses of the Torpedo electric organ after stimulation. J Neurochem 22:1109–1114PubMedGoogle Scholar
  155. Zimmermann H, Stadler H, Whittaker VP (1981) Structure and function of cholinergic synaptic vesicles. In: Stjärne L, Hedquist P, Lagercrantz H, Wennmalm A (eds) Chemical neurotransmission 75 years. Academic, New York, pp 91–111Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1988

Authors and Affiliations

  • H. Zimmermann

There are no affiliations available

Personalised recommendations