The concept of a calcium sensor in transmitter release

Progress in Neurobiology

Volumn 59, Issue 3, 1999, Pages 243-277

  Bennett, M R ^a  

^a Institute for Biomedical Research   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL; SYNAPTOTAGMIN;

HUMAN; MINIATURE ENDPLATE POTENTIAL; NERVE ENDING; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; REVIEW; TECHNIQUE;

ACTION POTENTIALS; ALGORITHMS; ANIMALS; CALCIUM; CALCIUM CHANNELS; ELECTROPHYSIOLOGY; HISTORY, 20TH CENTURY; MUSCLE, SMOOTH; MYOCARDIUM; NEURONS; NEUROTRANSMITTER AGENTS; SODIUM CHANNELS; SODIUM-CALCIUM EXCHANGER; SYNAPSES;

EID: 0032768724     PISSN: 03010082     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0301-0082(99)00004-0     Document Type: Review

References (162)

1. Adrian R.H., Chandler W.K., Hodgkin A.L. Voltage clamp experiments in striated muscle fibres. J. Physiol. 208:1970;607-644.
2. Akaike N., Fishman H.M., Lee K.S., Moore L.E., Brown A.M. The units of calcium conduction in Helix neurones. Nature. 274:1978;379-382.
3. Andreu R., Barrett E.F. Calcium dependence of evoked transmitter release at very low quantal contents at the frog neuromuscular junction. J. Physiol. 308:1980;79-97.
4. Ashley C.C., Ridgway E.B. Simultaneous recording of membrane potential, calcium transient and tension in single muscle fibers. Nature. 219:1968;1168-1169.
5. Ashley C.C., Ridgway E.B. On the relationships between membrane potential, calcium transient and tension in single barnacle muscle fibres. J. Physiol. 209:1970;105-130.
6. Augustine G.J., Charlton M.P., Smith S.J. Calcium entry into voltage-clamped presynaptic terminals of squid. J. Physiol. 367:1985;143-162.
7. Augustine G.J., Charlton M.P., Smith S.J. Calcium entry and transmitter release at voltage-clamped nerve terminals of squid. J. Physiol. 367:1985;163-181.
8. Baker P.F., Hodgkin A.L., Ridgway E.B. Depolarization and calcium entry in squid giant axons. J. Physiol. 218:1971;709-755.
9. Bazbek et al., 1995: AUTHOR: PLEASE SUPPLY REFERENCE.
10. Bennett M.K., Calakos N., Scheller R.H. Syntaxin: a synaptic protein implicated in docking of synaptic vesicles at presynaptic active zones. Science. 257:1992;255-259.
11. Bennett M.K., Garcia-Arraras J.E., Elferink L.A., Peterson K., Fleming A.M., Hazuka C.D., Scheller R.H. The syntaxin family of vesicular transport receptors. Cell. 74:1993;863-873.
12. Bennett M.R. The effect of cations on the electrical properties of the smooth muscle cells of the guinea-pig vas deferens. J. Physiol. 190:1967;465-479.
13. Bennett M.R., Gibson W.G., Robinson J. Probabilistic secretion of quanta and the synaptosecretosome hypothesis: evoked release at active zones of varicosities, boutons and endplates. Biophys. J. 73:1997;1815-1829.
14. Bertram R., Sherman A., Stanley E.F. Single-domain/bound calcium hypothesis of transmitter release and facilitation. J. Neurophysiol. 75:1996;1919-1931.
15. Bezprozvanny I., Scheller R.H., Tsien R.W. Functional impact of syntaxin on gating of N-type and Q-type calcium channels. Nature. 378:1995;623-626.
16. Bommert K., Charlton M.P., DeBello W.M., Chin G.J., Betz H., Augustine G.J. Inhibition of neurotransmitter release by C2-domain peptides implicates synaptotagmin in exocytosis. Nature. 363:1993;163-165.
17. Brock J.A., Cunnane T.C., Evans R.J., Ziogas J. Inhibition of transmitter release from sympathetic nerve endings by omega-conotoxin. Clin. exp. Pharmac. Physiol. 16:1989;333-339.
18. Brose N., Petrenko A.G., Sudhof T.C., Jahn R. Synaptotagmin: a calcium sensor on the synaptic vesicle surface. Science. 256:1992;1021-1025.
19. Brown G.L., Feldberg W. The action of potassium on the superior cervical ganglion of the cat. J. Physiol. 86:1936;290-305.
20. Brown G.L., Feldberg W. The acetylcholine metabolism of a sympathetic ganglion. J. Physiol. 88:1936;265-283.
21. Brown A.M., Camerer H., Kunze D.L., Lux H.D. Similarity of unitary Ca2+ currents in three different species. Nature. 299:1982;156-158.
22. Bulbring E., Kuriyama H. Effects of changes in the external sodium and calcium concentrations on spontaneous electrical activity in smooth muscle of guinea-pig taenia coli. J. Physiol. 166:1963;29-58.
23. 2+ channel toxins. Eur. J. Pharmac. 238:1993;383-386.
24. Carbone E., Lux H.D. A low voltage-activated calcium conductance in embryonic chick sensory neurons. Biophys. J. 46:1984;413-418.
25. del Castillo J., Stark L. The effect of calcium ions on the motor end-plate potentials. J. Physiol. 116:1952;507-515.
26. del Castillo J., Katz B. The effect of magnesium on the activity of motor nerve endings. J. Physiol. 124:1954;553-559.
27. del Castillo J., Katz B. Quantal components of the end-plate potential. J. Physiol. 124:1954;560-573.
28. del Castillo J., Katz B. Changes in end-plate activity produced by presynaptic polarization. J. Physiol. 124:1954;586-604.
29. Chad J.E., Eckert R. Calcium domains associated with individual channels can account for anomalous voltage relations of Ca-dependent responses. Biophys. J. 45:1984;993-999.
30. Chapman E.R., Jahn R. Calcium-dependent interaction of the cytoplasmic region of synaptotagmin with membranes. Autonomous function of a single C2-homologous domain. J. biol. Chem. 269:1994;5735-5741.
31. Clasbrummel B., Osswald H., Illes P. Inhibition of noradrenaline release by omega-conotoxin GVIA in the rat tail artery. Br. J. Pharmac. 96:1989;101-110.
32. David P., el Far O., Martin-Moutot N., Poupon M.F., Takahashi M., Seagar M.J. Expression of synaptotagmin and syntaxin associated with N-type calcium channels in small cell lung cancer. FEBS Lett. 326:1993;135-139.
33. 2+-dependent conformational change in synaptotagmin I. J. biol. Chem. 269:1994;28547-28550.
34. De Luca A., Li C.G., Rand M.J., Reid J.J., Thaina P., Wong-Dusting H.K. Effects of omega-conotoxin GVIA on autonomic neuroeffector transmission in various tissues. Br. J. Pharmac. 101:1990;437-447.
35. Dodge F.A. Jr., Rahamimoff R. Co-operative action of calcium ions in transmitter release at the neuromuscular junction. J. Physiol. 193:1967;419-432.
36. Dooley D.J., Lupp A., Hertting G., Osswald H. Omega-conotoxin GVIA and pharmacological modulation of hippocampal noradrenaline release. Eur. J. Pharmac. 148:1988;261-267.
37. Draper M.H., Weidmann S. Cardiac resting and action potentials recorded with an intracellular electrode. J. Physiol. 115:1951;74-94.
38. 2+ channels in mammalian central neurons. Trends NeuroSci. 18:1995;89-98.
39. Elliott, T.R. (1904) On the action of adrenalin. J. Physiol. 31, pp. xx-xxi.
40. Fatt P., Ginsborg B. The ionic requirements of the production of action potentials in crustacean muscle fibre. J. Physiol. 142:1958;516-543.
41. Fatt P., Katz B. Spontaneous subthreshold activity at motor nerve endings. J. Physiol. 117:1952;109-128.
42. Fatt P., Katz B. The effect of sodium ions on neuromuscular transmission. J. Physiol. 118:1952;73-87.
43. Fatt P., Katz B. The effect of inhibitory nerve impulses on a crustacean muscle fibre. J. Physiol. 121:1953;374-389.
44. Feng T.P. Studies on the neuromuscular junction. XVIII. The local potentials around N-M junctions induced by single and multiple volleys. Chin. J. Physiol. 15:1940;367-404.
45. Feng T.P., Li T.H. Studies on the neuromuscular junction. XXIII. A new aspect of the phenomena of eserine potentiation and post-tetanic facilitation in mammalian muscle. Chin. J. Physiol. 16:1941;37-50.
46. Fenwick E.M., Marty A., Neher E. A patch-clamp study of bovine chromaffin cells and of their sensitivity to acetylcholine. J. Physiol. 331:1982;577-597.
47. Fenwick E.M., Marty A., Neher E. Sodium and calcium channels in bovine chromaffin cells. J. Physiol. 331:1982;599-635.
48. Fox A.P., Nowycky M.C., Tsien R.W. Single-channel recordings of three types of calcium channels in chick sensory neurones. J. Physiol. 394:1987;173-200.
49. Fukuda M., Moreira J.E., Lewis F.M., Sugimori M., Niinobe M., Mikoshiba K., Llinas R. Role of the C2B domain of synaptotagmin in vesicular release and recycling as determined by specific antibody injection into the squid giant synapse preterminal. Proc. natl Acad. Sci. USA. 92:1995;10708-10712.
50. Furukawa T., Sasaoka T., Hosoya Y. Effects of tetrodotoxin on the neuromuscular junction. Jap. J. Physiol. 9:1959;143-152.
51. Geduldig D., Gruener R. Voltage clamp of the Aplysia giant neurone: early sodium and calcium currents. J. Physiol. 211:1970;217-244.
52. Geppert M., Archer B.T., Sudhof T.C. Synaptotagmin II. A novel differentially distributed form of synaptotagmin. J. biol. Chem. 266:1991;13548-13552.
53. Geppert M., Goda Y., Hammer R.E., Li C., Rosahl T.W., Stevens C.F., Sudhof T.C. Synaptotagmin I: a major Ca2+ sensor for transmitter release at a central synapse. Cell. 79:1994;717-727.
54. Goda Y., Stevens C.F. Two components of transmitter release at a central synapse. Proc. natn Acad. Sci. USA. 91:1994;12942-12946.
55. Gonzalez Burgos G.R., Biali F.I., Cherksey B.D., Sugimori M., Llinas R.R., Uchitel O.D. Different calcium channels mediate transmitter release evoked by transient or sustained depolarization at mammalian sympathetic ganglia. Neuroscience. 64:1995;117-123.
56. 2+. J. Gen. Physiol. 48:1964;141-162.
57. Hamill O.P., Marty A., Neher E., Sakmann B., Sigworth F.J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pfluger's Arch.-Eur. J. Physiol. 391:1981;85-100.
58. Harvey A.M., MacIntosh F.C. Calcium and synaptic transmission in a sympathetic ganglion. J. Physiol. 97:1940;408-416.
59. Heidelberger R., Heinemann C., Neher E., Matthews G. Calcium dependence of the rate of exocytosis in a synaptic terminal. Nature. 371:1994;513-515.
60. Hilbush B.S., Morgan J.I. A third synaptotagmin gene, Syt3, in the mouse. Proc. natn Acad. Sci. USA. 91:1994;8195-8199.
61. Hodgkin A.L., Huxley A.F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. 117:1952;500-544.
62. Hodgkin A.L., Keynes R.D. Movements of labelled calcium in squid giant axons. J. Physiol. 138:1957;253-281.
63. Hoffman B.F., Suckling E.E. Effect of several cations on transmembrane potentials of cardiac muscle. Am. J. Physiol. 186:1956;317-324.
64. Holman M.E. Membrane potentials recorded with high-resistance micro-electrodes; and the effects of changes in ionic environment on the electrical and mechanical activity of the smooth muscle of the taenia coli of the guinea pig. J. Physiol. 141:1958;464-488.
65. Ireland D., Davies P., McLachlan E.M. Voltage-activated Ca2+ channels mediating acetylcholine release in mammalian sympathetic ganglia. Proc. Aust. Neurosci. Soc. 8:1997;70.
66. Johnson E.A., Lieberman M. Heart: excitation and contraction. A. Rev. Physiol. 33:1971;479-532.
67. Junge D. Multi-ionic action potentials in molluscan giant neurones. Nature. 215:1967;546-548.
68. Katz B. The Fenn Lecture - Neural transmitter release: from quantal secretion to exocytosis and beyond. J. Neurocytol. 25:1996;677-686.
69. Katz B., Kuffler S.W. The effect of calcium on the neuro-muscular junction. J. Neurophysiol. 7:1942;17-26.
70. Katz B., Miledi R. The timing of calcium action during neuromuscular transmission. J. Physiol. 189:1967;535-544.
71. Katz B., Miledi R. A study of synaptic transmission in the absence of nerve impulses. J. Physiol. 192:1967;407-436.
72. Katz B., Miledi R. Modification of transmitter release by electrical interference with motor nerve endings. Proc. R. Soc. Lond. - Series B: Biol. Sci. 167:1967;1-7.
73. Katz B., Miledi R. Tetrodotoxin and neuromuscular transmission. Proc. R. Soc. Lond. - Series B: Biol. Sci. 167:1967;8-22.
74. Katz B., Miledi R. The release of acetylcholine from nerve endings by graded electric pulses. Proc. R. Soc. Lond. - Series B: Biol. Sci. 167:1967;23-38.
75. Katz B., Miledi R. Tetrodotoxin-resistant electric activity in presynaptic terminals. J. Physiol. 203:1969;459-487.
76. Katz B., Miledi R. Further study of the role of calcium in synaptic transmission. J. Physiol. 207:1970;789-801.
77. Keenan M.J., Niedergerke R. Intracellular sodium concentration and resting sodium fluxes of the frog heart ventricle. J. Physiol. 188:1967;235-260.
78. Kerr L.M., Yoshikami D. A venom peptide with a novel presynaptic blocking action. Nature. 308:1984;282-284.
79. Koh D.S., Hille B. Modulation by neurotransmitters of catecholamine secretion from sympathetic ganglion neurons detected by amperometry. Proc. natn Acad. Sci. USA. 94:1997;1506-1511.
80. Kostyuk P.G., Krishtal O.A. Effects of calcium and calcium-chelating agents on the inward and outward current in the membrane of mollusc neurones. J. Physiol. 270:1977;569-580.
81. Kostyuk P.G., Krishtal O.A., Pidoplichko V.I. Asymmetrical displacement currents in nerve cell membrane and effect of internal fluoride. Nature. 267:1977;70-72.
82. Kostyuk P.G., Krishtal O.A., Shakhovalov Yu.A. Separation of calcium and sodium currents in the somatic membrane of mollusc neurones. J. Physiol. 270:1977;545-568.
83. Krishtal, O.A. and Pidoplichko, V.I. (1975) Intracellular perfusion of Helix neurones. Neirofiziologiya 7, 327-329 (Neurophysiology, Engl. Trans. 7, 258-259).
84. Krishtal, O.A. and Pidoplichko, V.I. (1975) Intracellular perfusion of Helix neurones. Neirofiziologiya 7, 327-329 (Neurophysiology, Engl. Trans. 7, 258-259).
85. Kuriyama H. Effect of calcium and magnesium on neuromuscular transmission in the hypogastric nerve-vas deferens preparation of the guinea pig. J. Physiol. 175:1964;211-230.
86. Lee K.S., Akaike N., Brown A.M. Trypsin inhibits the action of tetrodotoxin on neurones. Nature. 265:1977;751-753.
87. Leveque C., Hoshino T., David P., Shoji-Kasai Y., Leys K., Omori A., Lang B., el Far O., Sato K., Martin-Moutot N., Newsom-Davis J., Takahashi M., Seagar M.J. The synaptic vesicle protein synaptotagmin associates with calcium channels and is a putative Lambert-Eaton myasthenic syndrome antigen. Proc. natl Acad. Sci. U.S.A. 89:1992;3625-3629.
88. 2+ sensors for the fast and slow components of neurotransmitter release. J. biol. Chem. 270:1995;24898-24902.
89. 2+)-dependent and -independent activities of neural and non-neural synaptotagmins. Nature. 375:1995;594-599.
90. Lin Y.Q., Brain K.L., Nichol K.A., Morgan J.J., Bennett M.R. Vesicle-associated proteins and calcium in nerve terminals of chick ciliary ganglia during development of facilitation. J. Physiol. 497:1996;639-656.
91. 2+)-dependent manner. Trends NeuroSci. 18:1995;177-183.
92. Littleton J.T., Stern M., Schulze K., Perin M., Bellen H.J. Mutational analysis of Drosophila synaptotagmin demonstrates its essential role in Ca(2+)-activated neurotransmitter release. Cell. 74:1993;1125-1134.
93. Littleton J.T., Stern M., Perin M., Bellen H.J. Calcium dependence of neurotransmitter release and rate of spontaneous vesicle fusions are altered in Drosophila synaptotagmin mutants. Proc. natl Acad. Sci. USA. 91:1994;10888-10892.
94. Llinas R., Blinks J.R., Nicholson C. Calcium transient in presynaptic terminal of squid giant synapse: detection with aequorin. Science. 176:1972;1127-1129.
95. Llinas R., Steinberg I.Z., Walton K. Relationship between presynaptic calcium current and postsynaptic potential in squid giant synapse. Biophys. J. 33:1981;323-351.
96. Llinas R., Sugimori M., Lin J.W., Cherksey B. Blocking and isolation of a calcium channel from neurons in mammals and cephalopods utilizing a toxin fraction (FTX) from funnel-web spider poison. Proc. natl Acad. Sci. USA. 86:1989;1689-1693.
97. Llinas R., Sugimori M., Silver R.B. Presynaptic calcium concentration microdomains and transmitter release. J. Physiol. Paris. 86:1992;135-138.
98. Llinas R., Sugimori M., Silver R.B. Microdomains of high calcium concentration in a presynaptic terminal. Science. 256:1992;677-679.
99. 2+ channels in the mammalian central nervous system. Trends NeuroSci. 15:1992;351-355.
100. Llinas R.R., Sugimori M., Silver R.B. Localization of calcium concentration microdomains at the active zone in the squid giant synapse. Adv. Second Messenger Phosphoprotein Res. 29:1994;133-137.
101. Locke F.S. Notiz uber den Einfluss physiologischer Kochsalzlosung auf die elektrische Erregbarkeit von Muskel und Nerv. Zbl. Physiol. 8:1894;166-167.
102. Lorente de No R. On the effect of certain quaternary ammonium ions upon frog nerve. J. Cell. Comp. Physiol. 33(suppl.):1949;1-231.
103. Luebke J.I., Dunlap K., Turner T.J. Multiple calcium channel types control glutamatergic synaptic transmission in the hippocampus. Neuron. 11:1993;895-902.
104. Lux H.D., Nagy K. Single channel Ca2+ currents in Helix pomatia neurons. Pfluger's Arch. - Eur. J. Physiol. 391:1981;252-254.
105. Mann P.J.G., Tennenbaum M., Quastel J.H. Acetylcholine metabolism in the central nervous system. The effects of potassium and other cations on acetylcholine liberation. Biochem. J. 33:1939;822-835.
106. Martin-Moutot N., Charvin N., Leveque C., Sato K., Nishiki T., Kozaki S., Takahashi M., Seagar M. Interaction of SNARE complexes with P/Q-type calcium channels in rat cerebellar synaptosomes. J. biol. Chem. 271:1996;6567-6570.
107. Matthew W.D., Tsavaler L., Reichardt L.F. Identification of a synaptic vesicle-specific membrane protein with a wide distribution in neuronal and neurosecretory tissue. J. Cell Biol. 91:1981;257-269.
108. Mikami A., Imoto K., Tanabe T., Niidome T., Mori Y., Takeshima H., Narumiya S., Numa S. Primary structure and functional expression of the cardiac dihydropyridine-sensitive calcium channel. Nature. 340:1989;230-233.
109. Mikoshiba K., Fukuda M., Moreira J.E., Lewis F.M., Sugimori M., Niinobe M., Llinas R. Role of the C2A domain of synaptotagmin in transmitter release as determined by specific antibody injection into the squid giant synapse preterminal. Proc. natl Acad. Sci. USA. 92:1995;10703-10707.
110. Miledi R. Transmitter release induced by injection of calcium ions into nerve terminals. Proc. R. Soc. Lond. - Series B: Biol. Sci. 183:1973;421-425.
111. Mintz I.M., Adams M.E., Bean B.P. P-type calcium channels in rat central and peripheral neurones. Neuron. 9:1992;85-95.
112. Mintz I.M., Venema V.J., Swiderek K.M., Lee T.D., Bean B.P., Adams M.E. P-type calcium channels blocked by the spider toxin omega-Aga-IVA. Nature. 355:1992;827-829.
113. Mizuta M., Inagaki N., Nemoto Y., Matsukura S., Takahashi M., Seino S. Synaptotagmin III is a novel isoform of rat synaptotagmin expressed in endocrine and neuronal cells. J. biol. Chem. 269:1994;11675-11678.
114. Mochida S., Saisu H., Kobayashi H., Abe T. Impairment of syntaxin by botulinum neurotoxin C1 or antibodies inhibits acetylcholine release but not Ca2+ channel activity. Neuroscience. 65:1995;905-915.
115. Mori Y., Friedrich T., Kim M.S., Mikami A., Nakai J., Ruth P., Bosse E., Hofmann F., Flockerzi V., Furuichi T., Mikoshiba K., Imoto K., Tanabe T., Numa S. Primary structure and functional expression from complementary DNA of a brain calcium channel. Nature. 350:1991;398-402.
116. Narahashi T., Deguchi T., Urakawa N., Ohkubo Y. Stabilization and rectification of muscle fiber membrane by tetrodotoxin. Am. J. Physiol. 198:1960;934-938.
117. Neher E., Sakmann B. Single-channel currents recorded from membrane of denervated frog muscle fibres. Nature. 260:1976;799-802.
118. Neher E., Sakmann B., Steinbach J.H. The extracellular patch clamp: a method for resolving currents through individual open channels in biological membranes. Pfluger's Arch. - Eur. J. Physiol. 375:1978;219-228.
119. Nilius B., Hess P., Lansman J.B., Tsien R.W. A novel type of cardiac calcium channel in ventricular cells. Nature. 316:1985;443-446.
120. Nonet M.L., Grundahl K., Meyer B.J., Rand J.B. Synaptic function is impaired but not eliminated in C. elegans mutants lacking synaptotagmin. Cell. 73:1993;1291-1305.
121. Nonomura Y., Hotta Y., Ohashi H. Tetrodotoxin and manganese ions: effects on electrical activity and tension in taenia coli of guinea pig. Science. 152:1966;97-99.
122. Nowycky M.C., Fox A.P., Tsien R.W. Three types of neuronal calcium with different calcium agonist sensitivity. Nature. 316:1985;440-443.
123. Nowycky M.C., Fox A.P., Tsien R.W. Long-opening mode of gating of neuronal calcium channels and its promotion by the dihydropyridine calcium agonist Bay K 8644. Proc. natl Acad. Sci. USA. 82:1985;2178-2182.
124. O'Connor V.M., Shamotienko O., Grishin E., Betz H. On the structure of the 'synaptosecretosome'. Evidence for a neurexin/synaptotagmin/syntaxin/calcium channel complex. FEBS Lett. 326:1993;255-260.
125. Olivera B.M., Miljanich G.P., Ramachandran J., Adams M.E. Calcium channel diversity and neurotransmitter release: the omega-conotoxins and omega-agatoxins. A. Rev. Biochem. 63:1994;823-867.
126. Perin M.S., Fried V.A., Mignery G.A., Jahn R., Sudhof T.C. Phospholipid binding by a synaptic vesicle protein homologous to the regulatory region of protein kinase C. Nature. 345:1990;260-263.
127. Perin M.S., Brose N., Jahn R., Sudhof T.C. Domain structure of synaptotagmin (p65). J. biol. Chem. 266:1991;623-629.
128. Protti D.A., Sanchez V.A., Cherksey B.D., Sugimori M., Llinas R., Uchitel O.D. Mammalian neuromuscular transmission blocked by funnel web toxin. Ann. N.Y. Acad. Sci. 681:1993;405-407.
129. Regehr W.G., Mintz I.M. Participation of multiple calcium channel types in transmission at single climbing fiber to Purkinje cell synapses. Neuron. 12:1994;605-613.
130. Reid C.A., Clements J.A., Bekkers J.M. Nonuniform distribution of calcium channel subtypes on presynaptic terminals of excitatory synapses in hippocampal cultures. J. Neurosci. 17:1997;2738-2745.
131. Reuter H. The dependence of slow inward current in Purkinje fibres on the extracellular calcium-concentration. J. Physiol. 192:1967;479-492.
132. Reuter H. Divalent cations as charge carriers in excitable membranes. Butler J.A.V., Noble D. Progress in Biophysics and Molecular Biology. vol. 26:1973;1-43 Pergamon, Oxford.
133. Reuter H., Scholz H. On the influence of the extracellular calcium concentration on membrane potential and contraction of isolated heart preparations during graded depolarization. Pfluger's Arch. ges. Physiol. 300:1968;87-107.
134. Reuter H., Stevens C.F., Tsien R.W., Yellen G. Properties of single calcium channels in cardiac cell culture. Nature. 297:1982;501-504.
135. Robinson I.M., Yamada M., Carrion-Vazquez M., Lennon V.A., Fernandez J.M. Specialized release zones in chromaffin cells examined with pulsed-laser imaging. Cell Calcium. 20:1996;181-201.
136. Sano K., Enomoto K., Maeno T. Effects of synthetic omega-conotoxin, a new type Ca2+ antagonist, on frog and mouse neuromuscular transmission. Eur. J. Pharmac. 141:1987;235-241.
137. Scholz H. Differences in contractural character of ventricular and atrial preparations from homeotherm hearts. Pfluger's Arch. - Eur. J. Physiol. 312:1969;63-81.
138. Scholz H., Reuter H. Elektrophysiologische Versuche zur Wirkung von Tetrodotoxin am Herzen[transti](Electrophysiological studies of the action of tetrodotoxin on the heart). Naunyn-Schmiedberg's Arch. Pharmac. exp. Pathol. 263:1969;248.
139. Sheng Z.H., Rettig J., Takahashi M., Catterall W.A. Identification of a syntaxin-binding site on N-type calcium channels. Neuron. 13:1994;1303-1313.
140. Shimomura O., Johnson F.H., Saiga Y. Extraction, purification and properties of aequorin, a bioluminescent protein from the luminous hydromedusan, Aequorea. J. Cell. Comp. Physiol. 59:1962;223-239.
141. Sigworth F.J., Neher E. Single Na+ channel currents observed in cultured rat muscle cells. Nature. 287:1980;447-449.
142. Simon S.M., Llinas R.R. Compartmentalization of the submembrane calcium activity during calcium influx and its significance in transmitter release. Biophys. J. 48:1985;485-498.
143. Simon S.M., Sugimori M., Llinas R. Modelling of submembranous calcium-concentration changes and their relation to rate of presynaptic transmitter release in the squid giant synapse. Biophys. J. 45:1984;264a.
144. Smith A.B., Cunnane T.C. Omega-conotoxin GVIA-resistant neurotransmitter release in postganglionic sympathetic nerve terminals. Neuroscience. 70:1996;817-824.
145. 2+ channels: diversity of form and function. Curr. Opin. Neurobiol. 2:1992;247-253.
146. Snutch T.P., Leonard J.P., Gilbert M.M., Lester H.A., Davidson N. Rat brain expresses a heterogeneous family of calcium channels. Proc. natl Acad. Sci. USA. 87:1990;3391-3395.
147. Standen N.B. Voltage-clamp studies of the calcium inward current in an identified snail neurone: comparison with the sodium inward current. J. Physiol. 249:1975;253-268.
148. Sudhof T.C. The synaptic vesicle cycle: a cascade of protein-protein interactions. Nature. 375:1995;645-653.
149. Sudhof T.C., Rizo J. Synaptotagmins: C2-domain proteins that regulate membrane traffic. Neuron. 17:1996;379-388.
150. Takahashi T., Momiyama A. Different types of calcium channels mediate central synaptic transmission. Nature. 366:1993;156-158.
151. Trifaro J.M., Fournier S., Novas M.L. The p65 protein is a calmodulin-binding protein present in several types of secretory vesicles. Neuroscience. 29:1989;1-8.
152. Turner T.J., Dunlap K. Pharmacological characterization of presynaptic calcium channels using subsecond biochemical measurements of synaptosomal neurosecretion. Neuropharmacology. 34:1995;1469-1478.
153. Ullrich B., Li C., Zhang J.Z., McMahon H., Anderson R.G., Geppert M., Sudhof T.C. Functional properties of multiple synaptotagmins in brain. Neuron. 13:1994;1281-1291.
154. Waterman S.A. Role of N-, P- and Q-type voltage-gated calcium channels in transmitter release from sympathetic neurones in the mouse isolated vas deferens. Br. J. Pharmac. 120:1997;393-398.
155. Wessler I., Dooley D.J., Werhand J., Schlemmer F. Differential effects of calcium channel antagonists (omega-conotoxin GVIA, nifedipine, verapamil) on the electrically-evoked release of [3H]acetylcholine from the myenteric plexus, phrenic nerve and neocortex of rats. Naunyn-Schmiedberg's Arch. Pharmac. 341:1990;288-294.
156. Wheeler D.B., Randall A., Tsien R.W. Roles of N-type and Q-type Ca2+ channels in supporting hippocampal synaptic transmission. Science. 264:1994;107-111.
157. Wheeler D.B., Sather W.A., Randall A., Tsien R.W. Distinctive properties of a neuronal calcium channel and its contribution to excitatory synaptic transmission in the central nervous system. Adv. Second Messenger Phosphoprotein Res. 29:1994;155-171.
158. Williams M.E., Feldman D.H., McCue A.F., Brenner R., Velicelebi G., Ellis S.B., Harpold M.M. Structure and functional expression of alpha 1, alpha 2, and beta subunits of a novel human neuronal calcium channel subtype. Neuron. 8:1992;71-84.
159. Woodward J.J., Rezazadeh S.M., Leslie S.W. Differential sensitivity of synaptosomal calcium entry and endogenous dopamine release to omega-conotoxin. Brain Res. 475:1988;141-145.
160. Wright C.E., Angus J.A. Effects of N-, P- and Q-type neuronal calcium channel antagonists on mammalian peripheral neurotransmission. Br. J. Pharmac. 119:1996;49-56.
161. 2+ channels and their possible counterparts in mammalian CNS neurons. Neuropharmacology. 32:1993;1075-1088.
162. Zucker R.S., Fogelson A.L. Relationship between transmitter release and presynaptic calcium influx when calcium enters through discrete channels. Proc. natl Acad. Sci. USA. 83:1986;3032-3036.