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Calcium and Neuromuscular Transmission

  • William Van der Kloot

Abstract

The importance of Ca2+ in the release of ACh at the neuromuscular junction was shown by experiments of such lucid design and clever execution that they became instant classics (summarized by Katz, 1969). The general opinion is that depolarization of the nerve terminal opens a voltage-gated Ca2+ channel, Ca2+ enters the terminal to initiate quantal release which ends when the Ca2+ is sequestered or ejected from the terminal. This clear picture, naturally enough, hides uncertainties and unanswered questions which will be uncovered as the evidence for the Ca2+ hypothesis is described.

Keywords

Schwann Cell Botulinum Toxin Nerve Terminal Neuromuscular Junction Transmitter Release 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Ahkong, Q. F., Fisher, D., Tampion, W., and Lucy, J. A., 1975, Mechanisms of cell fusion, Nature 253: 194.PubMedCrossRefGoogle Scholar
  2. Alnaes, E., & Rahamimoff, R., 1975, On the role of mitochondria in transmitter release from motor nerve terminals, J. Physiol. ( London ) 248: 285.PubMedGoogle Scholar
  3. Alnaes, E., & Rahamimoff, R., 1974, Dual action of Praseodymium (Pr+++) on transmitter release at the frog neuromuscular synapse, Nature 247: 478.PubMedCrossRefGoogle Scholar
  4. Baker, P. F., 1972, Transport and metabolism of calcium ions in nerve, Progr. Biophys. Mot. Biol. 24: 179.Google Scholar
  5. Baker, P. F., 1974, Excitation - secretion coupling, Recent Advances in Physiol. 9: 51.Google Scholar
  6. Baker, P. F., and Crawford, A. C., 1972, Mobility and transport of magnesium in squid giant axons, J. Physiol. ( London ) 227: 855.PubMedGoogle Scholar
  7. Baker, P. F., and Crawford, A. C., 1975, A note on the mechanism by which inhibitors of the sodium pump accelerate spontaneous release of transmitter from motor nerve terminals, J. Physiol. ( London ) 209: 226.Google Scholar
  8. Balnave, R. J., and Gage, P. W., 1977, Facilitation of transmitter secretion from toad motor nerve terminals during brief trains of action potentials, J. Physiol. ( London ) 266: 435.Google Scholar
  9. Balnave, R. J., and Gage, P. W., 1970, Temperature sensitivity of the time course of facilitation of transmitter release, Brain Res. 21: 297.PubMedCrossRefGoogle Scholar
  10. Bass, L., and Moore, W. J., 1966, Electrokinetic mechanism of miniature postsynaptic potentials, Proc. Nat. Acad. Sci. U. S. A. 55: 1214.CrossRefGoogle Scholar
  11. Barrett, E. F., and Stevens, C. F., 1972, The kinetics of transmitter release at the frog neuromuscular junction, J. Physiol. (London) 221\691.Google Scholar
  12. Bennett, M. R., and Florin, T., 1974, A statistical analysis of the release of acetylcholine at newly formed synapses in striated muscle, J. Physiol. ( London ) 238: 93.Google Scholar
  13. Bennett, M. R., Florin, T., and Pettigrew, A. G., 1976, The effect of calcium ions on the binomial statistic parameters that control acetylcholine release at preganglionic nerve terminals, J. Physiol. ( London ) 257: 597.Google Scholar
  14. Birks, R. I., and Cohen, M. W., 1968, The action of sodium pump inhibitors on neuromuscular transmission, Proc. R. Soc. London3 Ser. B 170: 381.CrossRefGoogle Scholar
  15. Birks, R., Katz, B., and Miledi, R., 1960, Physiological and structural changes at the amphibian myoneural junction, in the course of nerve degeneration, J. Physiol. ( London ) 150: 145.Google Scholar
  16. Branisteanu, D. D., Miyamoto, M. D., and Voile, R. L., 1976, Affects of physiologic alterations on binomial transmitter release at magnesium-depressed neuromuscular junctions, J. Physiol. ( London ) 254: 19.Google Scholar
  17. Blioch, Z. L., Glagoleva, I. M., Liberman, E. A., and Nenashev, V. A., 1968, A study of the mechanism of quantal transmitter release at a chemical synapse, J. Physiol. ( London ) 199: 11.Google Scholar
  18. Bowen, J. M., 1972, Effects of rare earths and yttrium on striated muscle and the neuromuscular junction, Can. J. Physiol. Pharmacol. 50: 603.PubMedCrossRefGoogle Scholar
  19. Bracho, H., and Orkand, R. K., 1970, Effect of calcium on excitatory neuromuscular transmission in the crayfish, J. Physiol. ( London ) 206: 61.Google Scholar
  20. Bray, D., 1977, Actin and myosin in neurones: a first review, Biochimie 59: 1.PubMedCrossRefGoogle Scholar
  21. Brinley, Jr., F. J., Scarpa, A., and Tiffert, T., 1977, The concentration of ionized magnesium in barnacle muscle fibres, J. Physiol. ( London ) 266: 545.Google Scholar
  22. Carlen, P. I., Kosower, E. M., and Werman, R., 1976, The thiol- oxidizing agent diamide increases transmitter release by de-creasing calcium requirements for neuromuscular transmission in the frog, Brain Res. 11: 257.CrossRefGoogle Scholar
  23. del Castillo, J., and Stark, L., 1952, The effect of calcium on the motor end-plate potentials, J. Physiol. ( London ) 116: 507.Google Scholar
  24. del Castillo, J., and Katz, B., 1954a, Changes in end-plate activity produced by pre-synaptic polarization, J. Physiol. ( London ) 124: 586.Google Scholar
  25. del Castillo, J., and Katz, B., 1954b, The membrane change produced by the neuromuscular transmitter, J. Physiol. ( London ) 125: 546.Google Scholar
  26. Cohen, I., and Van der Kloot, W., 1976, The effects of pH changes on the frequency of miniature end-plate potentials at the frog neuromuscular junction, J. Physiol. ( London ) 262: 401.Google Scholar
  27. Cooke, J. D., and Quastel, D. M. J., 1973a, Transmitter release by mammalian motor nerve terminals in response to focal polarization, J. Physiol. ( London ) 228: 377.Google Scholar
  28. Cooke, J. D., and Quastel, D. M. J., 1973b, Cumulative and persistent effects of nerve terminal depolarization on transmitter release, J. Physiol. ( London ) 228: 407.Google Scholar
  29. Cooke, J. D., and Quastel, D. M. J., 1973c, The specific effect of potassium on transmitter release by motor nerve terminals and its inhibition by calcium, J. Physiol. ( London ) 228: 435.Google Scholar
  30. Cooke, J. D., Okamoto, K., and Quastel, D. M. J., 1973, The role of calcium in depolarization-secretion coupling at the motor nerve terminal, J. Physiol. ( London ) 228: 459.Google Scholar
  31. Crawford, A. C., 1974, The dependence of evoked transmitter release on external calcium ions at very low mean quantal contents, J. Physiol. ( London ) 240: 255.Google Scholar
  32. Crawford, A. C., 1975, Lithium ions and the release of transmitter at the frog neuromuscular junction, J. Physiol. ( London ) 246: 109.Google Scholar
  33. Cull-Candy, S. G., Lundh, H., and Thesleff, S., 1976, Effects of botulinum toxin on neuromuscular transmission in the rat, J. Physiol. ( London ) 260: 177.Google Scholar
  34. Dennis, M. J., and Miledi, R., 1974, Electrically induced release of acetylcholine from denervated Schwann cells, J. Physiol. ( London ) 237: 431.Google Scholar
  35. Devore, D. I., and Nastuk, W. L., 1975, Effects of !calcium iono- phoref X-537A on frog skeletal muscle, Nature 253: 644.PubMedCrossRefGoogle Scholar
  36. Dodge, F. A., Jr., and Rahamimoff, R., 1967, Cooperative action of calcium ions in transmitter release at the neuromuscular junction, J. Physiol. ( London ) 193: 419.Google Scholar
  37. Dodge, F. A., Jr., Miledi, R., and Rahamimoff, R., 1969, Strontium and quantal release of transmitter at the neuromuscular junction, J. Physiol. ( London ) 200: 267.Google Scholar
  38. Elmqvist, D., and Feldman, D. S., 1965, Effects of sodium pump inhibitors on spontaneous acetylcholine release at the neuro-muscular junction, J. Physiol. ( London ) 181: 498.Google Scholar
  39. Gage, P. W., and Quastel, D. M. J., 1966, Competition between sodium and calcium ions in transmitter release at a mammalian neuromuscular junction, J. Physiol. ( London ) 185: 95.Google Scholar
  40. Glagoleva, I. M., Liberman, Y. A., and Khashayev, Z., 1970, Effect of uncoupling agents of oxidation phosphorylation on the release of acetylcholine from nerve endings, Biophysics (USSR) 15: 76.Google Scholar
  41. Hall, J. E., and Simon, S. A., 1976, A simple model for calcium induced exocytosis, Biochim. Biophys. Acta 436: 613.PubMedCrossRefGoogle Scholar
  42. Heuser, J., and Miledi, R., 1971, Effect of lanthanum ions on function and structure of frog neuromuscular junction, Proc. R. Soc. London Ser. B 179: 247.CrossRefGoogle Scholar
  43. Heuser, J., Katz, B., and Miledi, R., 1971, Structural and functional changes of frog neuromuscular junction in high calcium solutions, Proc. R. Soc. London Ser. B 178: 407.CrossRefGoogle Scholar
  44. Hubbard, J. I., 1963, Repetitive stimulation at the mammalian neuromuscular junction and the mobilisation of transmitter, J. Physiol. ( London ) 169: 641.Google Scholar
  45. Hubbard, J. I., and Loyning, Y., 1966, The effects of hypoxia on neuromuscular transmission in a mammalian preparation, J. Physiol. ( London ) 185: 205.Google Scholar
  46. Hubbard, J. J., Jones, S. F., and Landau, E. M., 1968, On the mechanism by which calcium and magnesium affect the release of transmitter by nerve impulses, J. Physiol. ( London ) 196: 75.Google Scholar
  47. Hurlbut, W. P., Longenecker, H. B., and Mauro, A., 1971, Effects of calcium and magnesium on the frequency of end-plate potentials during prolonged tetanization, J. Physiol. ( London ) 219: 17.Google Scholar
  48. Ito, Y., and Miledi, R., 1977, The effect of calcium-ionophores on acetylcholine release from Schwann cells, Proc. R. Soc. London, Ser. B 196: 51.CrossRefGoogle Scholar
  49. Jan, L. Y., and Jan, Y. N., 1976, Properties of the larval neuro-muscular junction in Drosophila melanogaster, J. Physiol. ( London ) 262: 189.Google Scholar
  50. Jansson, S. E., Heinonen, E., Heinanen, V., Gripenberg, J., Tolppanen, E. M., and Salmi, T., 1976, On the effect of the ionophore X-537A on neuromuscular transmission in the rat, Life Sci. 18: 1359.PubMedCrossRefGoogle Scholar
  51. Jenkinson, D. H., 1957, The nature of the antagonism between calcium and magnesium ions at the neuromuscular junction, J. Physiol. ( London ) 138: 434.Google Scholar
  52. Johnson, E. W., and Wernig, A., 1971, The binomial nature of transmitter release at the crayfish neuromuscular junction, J. Physiol. ( London ) 218: 757.Google Scholar
  53. Kajimoto, N., and Pirpekar, S. M., 1972, Effects of manganese and lanthanum on spontaneous release of acetylcholine at frog motor nerve terminals, Nature (New Biol.) 235: 29.Google Scholar
  54. Katz, B., 1969, “The release of neural transmitter substances,” Charles C. Thomas, Springfield, 60 pp.Google Scholar
  55. Katz, B., and Miledi, R., 1965a, The effect of calcium on acetylcholine release from motor nerve terminals, Proa. R. Soo. London, Ser. B 161: 496.CrossRefGoogle Scholar
  56. Katz, B., and Miledi, R., 1965b, Release of acetylcholine from a nerve terminal by electric pulses of variable strength and duration, Nature 207: 1097.PubMedCrossRefGoogle Scholar
  57. Katz, B., and Miledi, R., 1967a, The release of acetylcholine from nerve endings by graded electric pulses, Proc. R. Soo. London3 Ser. B 167: 23.CrossRefGoogle Scholar
  58. Katz, B., and Miledi, R., 1967b, The timing of calcium action during neuromuscular transmission, J. Physiol. ( London ) 189: 535.Google Scholar
  59. Katz, B., and Miledi, R., 1968, The role of calcium in neuro-muscular facilitation, J. Physiol. ( London ) 195: 481.Google Scholar
  60. Katz, B., and Miledi, R., 1969, Spontaneous and evoked activity of motor nerve endings in calcium Ringer, J. Physiol. ( London ) 203: 689.Google Scholar
  61. Katz, B., and Miledi, R., 1977, Transmitter leakage from motor nerve endings, Proc. R. Soo. London, Ser. B 196: 59.CrossRefGoogle Scholar
  62. Katz, N., and Edwards, C., 1973, Effects of metabolic inhibitors on spontaneous and evoked transmitter release from frog nerve terminals, J. gen. Physiol. 61: 259.Google Scholar
  63. Kelly, J. S., 1965, Antagonism between Na+ and Ca2+ at the neuromuscular junction, Nature 205: 296.PubMedCrossRefGoogle Scholar
  64. Kita, H., and Van der Kloot, W., 1971, The effects of changing the osmolarity of the Ringer on acetylcholine release at the frog neuromuscular junction, Life Sei. 10: 1423.CrossRefGoogle Scholar
  65. Kita, H., and Van der Kloot, W., 1973, The quantitative relation between extracellular calcium and acetylcholine release at the frog neuromuscular junction, Brain Res. 49: 205.PubMedCrossRefGoogle Scholar
  66. Kita, H., and Van der Kloot, W., 1973, Action of Co and Ni at the frog neuromuscular junction, Nature (New Biol.) 245: 52.CrossRefGoogle Scholar
  67. Kita, H., and Van der Kloot, W., 1974, Calcium ionophore X-537A increases spontaneous and phasic quantal release of acetylcholine at frog neuromuscular junction, Nature 250: 658.PubMedCrossRefGoogle Scholar
  68. Kita, H., and Van der Kloot, W., 1976, Effects of the ionophore X-537A on acetylcholine release at the frog neuromuscular junction, J. Physiol. ( London ) 259: 177.Google Scholar
  69. Kita, H., and Van der Kloot, W., 1977, Time course and magnitude of effects of changes in tonicity on acetylcholine release at frog neuromuscular junction, J. Neurophysiol. 40: 212.PubMedGoogle Scholar
  70. Kita, H., Madden, K, and Van der Kloot, W., 1976, Effects of the “Calcium ionophore” A-23187 on transmitter release at the frog neuromuscular junction, Life Sei. 17: 1837.CrossRefGoogle Scholar
  71. Krnjevic, K., Puil, E., and Werman, R., 1976, Intracellular Mg2+ increases neuronal excitability, Can. J. Physiol. Pharmacol. 54: 73.PubMedCrossRefGoogle Scholar
  72. Locke, F. S., 1894, Notiz über den Einfluss physiologischer Kochsalzlosung auf die elektrische Erregbarkeit von Muskel and Nerv., Zentralbl. Physiol. 8: 166.Google Scholar
  73. Mallart, A., and Martin, A. R., 1967, An analysis of facilitation of transmitter release at the neuromuscular junction of the frog, J. Physiol. ( London ) 193: 679.Google Scholar
  74. Manalis, R. S., and Cooper, G. P., 1973, Presynaptic and post-synaptic effects of lead at the frog neuromuscular junction, Nature 243: 354.PubMedCrossRefGoogle Scholar
  75. Manalis, R. S., and Cooper, G. P., 1975, Evoked transmitter released increased by inorganic mercury at frog neuromuscular junction, Nature 257: 690.PubMedCrossRefGoogle Scholar
  76. Matthews, G., and Wickelgren, W. O., 1977, On the effect of calcium on the frequency of miniature end-plate potentials at the frog neuromuscular junction, J. Physiol. ( London ) 266: 91.Google Scholar
  77. Meech, R. W., and Thomas, R. C., 1977, The effect of calcium injection on the intracellular sodium and pH of snail neurones, J. Physiol. ( London ) 265: 867.Google Scholar
  78. Meiri, U., and Rahamimoff, R., 1972, Neuromuscular transmission: inhibition by manganese ions, Science 176: 308.PubMedCrossRefGoogle Scholar
  79. Meiri, U., and Rahamimoff, R., 1971, Activation of transmitter release by strontium and calcium ions at the neuromuscular junction, J. Physiol. ( London ) 215: 709.Google Scholar
  80. Muller, R. U., and Finkelstein, A., 1974, The electrostatic basis of Mg++ inhibition of transmitter release, Proc. Nat. Acad. Sci. U. S. A. 71: 923.CrossRefGoogle Scholar
  81. Noble, D., 1975, “The initiation of the heart beat”, Clarendon Press, Oxford, 150 pp.Google Scholar
  82. Papahadjopoulos, D., Poste, G., Schaeffer, B. E., and Vail, W. J., 1974, Membrane fusion and molecular segregation in phospholipid vesicles, Biochim. Biophys. Acta 352: 10.PubMedCrossRefGoogle Scholar
  83. Poste, G., and Allison, A. C., 1973, Membrane fusion, Biochim. Biophys. Acta 300: 421.PubMedGoogle Scholar
  84. Potter, L. T., 1969, Synthesis, storage and release of (lt+C) acetyl-choline in isolated rat diaphragm muscles, J. Physiol. ( London ) 206: 145.Google Scholar
  85. Rahamimoff, R., 1968, A dual effect of calcium ions on neuromuscular facilitation, J. Physiol. ( London ) 195: 471.Google Scholar
  86. Rahamimoff, R., and Alnaes, E., 1973, Inhibitory action of Ruthenium red on neuromuscular transmission, Proc. Nat. Acad. Sci. U. S. A. 70: 3613.CrossRefGoogle Scholar
  87. Rahamimoff, R., and Yaari, Y., 1973, Delayed release of transmitter at the frog neuromuscular junction, J. Physiol. ( London ) 228: 241.Google Scholar
  88. Rees, D., 1974, The effect of metabolic inhibitors on the cockroach nerve-muscle synapse, J. Exp. Biol. 61: 331.PubMedGoogle Scholar
  89. Remler, M. P., 1973, A semiquantitative theory of synaptic vesicle movements, Biophys. J. 13: 104.PubMedCrossRefGoogle Scholar
  90. Rosenthal, J., 1969, Post-tetanic potentiation at the neuromuscular junction of the frog, J. Physiol. ( London ) 203: 121.Google Scholar
  91. Schober, R., Nitsch, C., and Rinne, U., Calcium-induced displacement of membrane-associated particles upon aggregation of chromaffin granules, Science 195: 495.Google Scholar
  92. Spertell, R. B., 1976, A theoretical inquiry into the role of phospholipids in membrane fusion, J. Theor. Biol. 60: 197.PubMedCrossRefGoogle Scholar
  93. Stratham, H. E.,and Duncan, C. J., 1976, The action of ionophores at the frog neuromuscular junction, Life Soi. 17: 1401.Google Scholar
  94. Van der Kloot, W., 1977, Quantal acetylcholine release: vesicles or gated channels?, Gen. Pharmacol. 8: 21.PubMedCrossRefGoogle Scholar
  95. Van der Kloot, W., and Kita, H., 1973, The possible role of fixed membrane surface charges in acetylcholine release at the frog neuromuscular junction, J. Memb. Biol. 14: 365.CrossRefGoogle Scholar
  96. Van der Kloot, W., and Kita, H., 1975, The effects of the “calcium- antagonist” verapamil on muscle action potentials in the frog and crayfish and on neuromuscular transmission in the crayfish, Comp. Bioehem. Physiol. 50C: 121.Google Scholar
  97. Van der Kloot, W., Kita, H., and Kita, K., 1975, Action of the “calcium-antagonist”, prenylamine, on skeletal muscle, the myoneural junction, and the adrenal of the frog, Gen. Pharmacol. 6: 63.CrossRefGoogle Scholar
  98. Weakly, J. N., 1973, The action of Cobalt ions on neuromuscular transmission in the frog, J. Physiol. ( London ) 234: 597.Google Scholar
  99. Younkin, S. G., 1974, An analysis of the role of calcium in facilitation at the frog neuromuscular junction, J. Physiol. ( London ) 237: 1.Google Scholar
  100. Zucker, R. S., 1973, Changes in the statistics of transmitter release during facilitation, J. Physiol. ( London ) 229: 787.Google Scholar

Copyright information

© Plenum Press, New York 1978

Authors and Affiliations

  • William Van der Kloot
    • 1
  1. 1.Department of Physiology and Biophysics Health Sciences CenterSUNYStony BrookUSA

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