Skip to main content
SpringerLink
Log in

Neuromuscular transmission in Ca2+-free extracellular solution

  • Reviews
  • Published:
Biochemistry (Moscow) Supplement Series A: Membrane and Cell Biology Aims and scope

Abstract

The review brings together the data on neuromuscular transmission upon substitution of different alkaline earth metals for Ca2+ ions. It is known that due to the low selectivity of calcium channels and their ability to conduct other divalent cations, a considerable presynaptic current carried by strontium or barium may develop, which under certain conditions may lead to the neuromuscular transmission. The review illustrates how the equimolar substitution of external Ca2+ by other polyvalent cations affects the parameters of nonquantum, spontaneous, and induced quantum exocytosis of the neuromediator, as well as endocytosis and the activities of acetylcholinesterase and postsynaptic receptors. The effects of the modulators of synaptic transmission under these conditions are also considered.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Huxley A.F., Stampfli R. 1951. Effect of potassium and sodium on resting and action potentials of single myelinated nerve fibers. J. Physiol. 112 (3–4), 496–508.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Katz B. 1962. The transmission of impulses from nerve to muscle and the subcellular unit of synaptic action (The Croonian Lecture). Proc. R. Soc. B. 155, 455–477.

    Article  Google Scholar 

  3. Fatt P., Katz B. 1953. The electrical properties of crustacean muscle fibres J. Physiol. 120, 171–204.

    Article  CAS  Google Scholar 

  4. Fatt P., Ginsborg B.L. 1958. The ionic requirements for the production of action potentials in crustacean muscle fibres. J. Physiol. 142 (3), 516–543.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Okamoto H., Takahashi K., Yoshii M. 1976. Membrane currents of the tunicate egg under the voltageclamp condition. J. Physiol. 254 (3), 607–638.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Hagiwara S., Byerly L. 1981. Calcium channel. Ann. Rev. Neurosci. 4, 69–125.

    Article  CAS  PubMed  Google Scholar 

  7. Trautwein W., McDonald T.F., Tripathi O. 1975. Calcium conductance and tension in mammalian ventricular muscle. Pflügers Arch. 354 (1), 55–74.

    Article  CAS  PubMed  Google Scholar 

  8. Reuter H., Scholz H. 1977. A study of the ion selectivity and the kinetic properties of the calcium dependent slow inward current in mammalian cardiac muscle. J. Physiol. 264 (1), 17–47.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Isenberg G., Klöckner U. 1982. Calcium currents of isolated bovine ventricular myocytes are fast and of large amplitude. Pflügers Arch. 395 (1), 30–41.

    Article  CAS  PubMed  Google Scholar 

  10. Sánchez J.A., Stefani E. 1978. Inward calcium current in twitch muscle fibres of the frog. J. Physiol. 283, 197–209.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Sánchez J.A, Stefani E. 1983. Kinetic properties of calcium channels of twitch muscle fibres of the frog. J. Physiol. 337, 1–17.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Donaldson P.L., Beam K.G. 1983. Calcium currents in a fast-twitch skeletal muscle of the rat. J. Gen. Physiol. 82 (4), 449–468.

    Article  CAS  PubMed  Google Scholar 

  13. Okamoto H., Takahashi K., Yamashita N. 1977. Ionic currents through the membrane of the mammalian oocyte and their comparison with those in the tunicate and sea urchin. J. Physiol. 267 (2), 465–495.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Ohmori H. 1984. Studies of ionic currents in the isolated vestibular hair cell of the chick. J. Physiol. 350, 561–581.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Fatt P., Katz B. 1952. Some problems of neuro-muscular transmission. Cold. Spring. Harb. Symp. Quant. Biol. 17, 275–280.

    Article  CAS  PubMed  Google Scholar 

  16. Kostyuk P.G. 1986. Kal’tsiy i kletochnaya provodimost' (Calcium and cellular conductance), Moscow: Nauka.

    Google Scholar 

  17. Grishin S.N. 2010. Kal’tsiyevy tok (Calcium current), Kazan: Izd. Kazanskogo gosudarstvennogo tekhnicheskogo universiteta.

    Google Scholar 

  18. Ohno-Shosaku T., Sawada S., Hirata K., Yamamoto C. 1994. A comparison between potencies of external calcium, strontium and barium to support GABAergic synaptic transmission in rat cultured hippocampal neurons. Neurosci. Res. 20 (3), 223–229.

    Article  CAS  PubMed  Google Scholar 

  19. Helmholtz H. 1853. Ueber einige Gesetze der Vertheilung elektrischer Ströme in körperlichen Leitern mit Anwendung auf die thierisch-elektrischen Versuche. Annalen der Physik und Chemie. 165 (6), 211–233.

    Article  Google Scholar 

  20. Gouy M. 1910. Sur la constitution de la charge électrique à la surface d’un électrolyte J. Phys. Theor. Appl. 9, 457–468.

    Article  CAS  Google Scholar 

  21. Chapman D.L. 1913. A contribution to the theory of electrocapillarity. Philosophi

    Google Scholar 

  22. Stern O. 1924. The theory of the electrolytic double layer. Z. Elektrochem. Angew. Phys. Chem. 30, 508–526.

    CAS  Google Scholar 

  23. Kostyuk P.G. 1999. Low-voltage activated calcium channels: Achievements and problems. Neuroscience. 92 (4), 1157–1163.

    Article  CAS  PubMed  Google Scholar 

  24. Hille B. 1968. Charges and potentials at the nerve surface. Divalent ions and pH. J. Gen. Physiol. 51 (2), 221–236.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Hille B., Woodhull A.M., Shapiro B.I. 1975. Negative surface charge near sodium channels of nerve: Divalent ions, monovalent ions, and pH. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 270 (908), 301–318.

    Article  CAS  PubMed  Google Scholar 

  26. Blaustein M.P., Goldman D.E. 1968. The action of certain polyvalent cations on the voltage-clamped lobster axon. J. Gen. Physiol. 51 (3), 279–291.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Doroshenko P.A., Kostyuk P.G., Tsyndarenko A.Ya. 1978. Allocation of potassium and calcium channels in neuronal cell soma membrane. Neirofiziologiya (Rus.). 10, 645–653.

    CAS  Google Scholar 

  28. Tang L., Gamal El-Din T.M., Payandeh J., Martinez G.Q., Heard T.M., Scheuer T., Zheng N., Catterall W.A. 2014. Structural basis for Ca2+ selectivity of a voltage-gated calcium channel. Nature. 505 (7481), 56–61.

    Article  PubMed  CAS  Google Scholar 

  29. Neumaier F., Dibué-Adjei M., Hescheler J., Schneider T. 2015. Voltage-gated calcium channels: Determinants of channel function and modulation by inorganic cations. Prog. Neurobiol. pii: S0301-0082(15)00024-6.

    Google Scholar 

  30. Hagiwara S. 1973. Ca2+ spike. Adv. Biophys. 4, 71–102.

    CAS  PubMed  Google Scholar 

  31. Akaike N., Lee K.S., Brown A.M. 1978. The calcium current of Helix neuron. J. Gen. Physiol. 71 (5), 509–531.

    Article  CAS  PubMed  Google Scholar 

  32. Baleev A.E. 1979. Selectivity of the soma membrane calcium ion channel of Helix pomatia to calcium, strontium and barium ions. Neirofiziologiya (Rus.). 11 (4), 371–374.

    Google Scholar 

  33. Zhuravleva S.O., Kostyuk P.G., Shuba Y.M. 1999. Divalent cation selectivity of the subtypes of low voltage-activated Ca2+ channels in thalamic neurons. Neuroreport. 10 (3), 651–657.

    Article  CAS  PubMed  Google Scholar 

  34. Kostyuk P.G., Doroshenko P.A. 1990. Modulation of calcium channel function in nerve cell membrane. Gen. Physiol. Biophys. 9 (5), 433–443.

    CAS  PubMed  Google Scholar 

  35. Akaike N. 1983. Physiology and pharmacology of calcium channel. Nihon. Seirigaku Zasshi. 45 (6), 261–278.

    CAS  PubMed  Google Scholar 

  36. Nachshen D.A. 1984. Selectivity of the Ca binding site in synaptosome Ca channels. Inhibition of Ca influx by multivalent metal cations. J. Gen. Physiol. 83 (6), 941–967.

    Article  CAS  PubMed  Google Scholar 

  37. Wilson D.L., Morimoto K., Tsuda Y., Brown A.M. 1983. Interaction between calcium ions and surface charge as it relates to calcium currents. J. Membr. Biol. 72 (1–2), 117–130.

    Article  CAS  PubMed  Google Scholar 

  38. Bal R., Janahmadi M., Green G.G., Sanders D.J. 2000. Effect of calcium and calcium channel blockers on transient outward current of F76 and D1 neuronal soma membranes in the subesophageal ganglia of Helix aspersa. J. Membr. Biol. 173 (3), 179–185.

    Article  CAS  PubMed  Google Scholar 

  39. Cota G., Stefani E. 1984. Saturation of calcium channels and surface charge effects in skeletal muscle fibres of the frog. J. Physiol. 351, 135–154.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Katz B., Miledi R. 1969. Tetrodotoxin-resistant electric activity in presynaptic terminals. J. Physiol. 203 (2), 459–487.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Nachshen D.A., Blaustein M.P. 1982. Influx of calcium, strontium, and barium in presynaptic nerve endings. J. Gen. Physiol. 79 (6), 1065–1087.

    Article  CAS  PubMed  Google Scholar 

  42. Lux H.D., Nagy K. 1981. Single channel Ca2+ currents in Helix pomatia neurons. Pflügers Arch. 391 (3), 252–254.

    Article  CAS  PubMed  Google Scholar 

  43. DiPolo R., Caputo C., Bezanilla F. 1983. Voltagedependent calcium channel in the squid axon. Proc. Natl. Acad. Sci. USA. 80 (6), 1743–1745.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Tillotson D. 1979. Inactivation of Ca conductance dependent on entry of Ca ions in molluscan neurons. Proc. Natl. Acad. Sci. USA. 76 (3), 1497–1500.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Brehm P., Eckert R., Tillotson D. 1980. Calciummediated inactivation of calcium current in Paramecium. J. Physiol. 306, 193–203.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Eckert R., Tillotson D.L. 1981. Calcium-mediated inactivation of the calcium conductance in caesiumloaded giant neurones of Aplysia californica. J. Physiol. 314, 265–280.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Brown A.M., Morimoto K., Tsuda Y., Wilson D.L. 1981. Calcium current-dependent and voltage-dependent inactivation of calcium channels in Helix aspersa. J. Physiol. 320, 193–218.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Grishin S.N. 2014. Transmembrane calcium current: Mechanism, registration procedures, Ca2+-mediated modulators of synaptic transmission. Biochem. (Mosc.) Suppl. Series A. 8 (3), 213–224.

    Article  Google Scholar 

  49. Mukhamedyarov M.A., Grishin S.N., Zefirov A.L., Palotas A. 2006. Evidences for calcium-dependent inactivation of calcium current at the frog motor nerve terminal. Brain Res. Bull. 69, 652–655.

    Article  CAS  PubMed  Google Scholar 

  50. Silinsky E.M., Solsona C.S. 1992. Calcium currents at motor nerve endings: Absence of effects of adenosine receptor agonists in the frog. J. Physiol. 457, 315–328.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Silinsky E.M., Watanabe M., Redman R.S., Qiu R., Hirsh J.K., Hunt J.M., Solsona C.S., Alford S., Mac-Donald R.C. 1995. Neurotransmitter release evoked by nerve impulses without Ca2+ entry through Ca2+ channels in frog motor nerve endings. J. Physiol. 482 (Pt 3), 511–520.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Silinsky E.M. 2000. Antagonism of calcium currents and neurotransmitter release by barium ions at frog motor nerve endings. Br. J. Pharmacol. 129 (2), 360–366.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Nicholls J.G., Martin A.R., Wallace B.G., Fuchs P.A. 2001. From neuron to brain. Sinauer Associates, Inc.

    Google Scholar 

  54. Kostyuk P.G. 1990. Calcium channels in cellular membranes. J. Mol. Neurosci. 2 (3), 123–141.

    Article  CAS  PubMed  Google Scholar 

  55. Katz B., Miledi R. 1977. Transmitter leakage from motor nerve endings. Proc. R. Soc. Lond. B. Biol. Sci. 196 (1122), 59–72.

    Article  CAS  PubMed  Google Scholar 

  56. Vyskocil F., Illes P. 1977. Non-quantal release of transmitter at mouse neuromuscular junction and its dependence on the activity of Na+-K+ ATPase. Pflüg. Arch. 370, 295–297.

    Article  CAS  Google Scholar 

  57. Vyskocil F., Malomouzh A.I., Nikolsky E.E. 2009. Nonquantal acetylcholine release at the neuromuscular junction. Physiol. Res. 58 (6), 763–784.

    CAS  PubMed  Google Scholar 

  58. Vyskocil F., Nikolsky E., Edwards C. 1983. An analysis of the mechanisms underlying the non-quantal release of acetylcholine at the mouse neuromuscular junction. Neuroscience. 9 (2), 429–435.

    Article  CAS  PubMed  Google Scholar 

  59. Malomuzh A.I., Nikol’sky E.E. 2010. Nonquantum release of acetylcholine in mammalian neuromuscular synapse: Dependence on extracellular concentrations of magnesium and calcium ions. Dokl. Akad. Nauk (Rus.). 430 (2), 277–280.

    Google Scholar 

  60. Fatt P., Katz B. 1952. Spontaneous subthreshold activity at motor nerve endings. J. Physiol. 117 (1), 109–128.

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Del Castillo J., Katz B. 1954. The effect of magnesium on the activity of motor nerve endings. J. Physiol. 124 (3), 553–559.

    Article  PubMed Central  Google Scholar 

  62. Blioch Z.L., Glagoleva I.M., Liberman E.A., Nenashev V.A. 1968. A study of the mechanism of quantal transmitter release at a chemical synapse. J. Physiol. 199 (1), 11–35.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Liley A.W. 1956. The effects of presynaptic polarization on the spontaneous activity at the mammalian neuromuscular junction. J. Physiol. 134 (2), 427–443.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Hubbard J.I. 1961. The effect of calcium and magnesium on the spontaneous release of transmitter from mammalian motor nerve endings. J. Physiol. 159, 507–517.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Elmqvist D., Feldman D.S. 1965. Calcium dependence of spontaneous acetylcholine release at mammalian motor nerve terminals. J. Physiol. 181 (3), 487–497.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Anwyl R., Kelly T., Sweeney F. 1982. Alterations of spontaneous quantal transmitter release at the mammalian neuromuscular junction induced by divalent and trivalent ions. Brain. Res. 246 (1), 127–132.

    Article  CAS  PubMed  Google Scholar 

  67. Curtis M.J., Quastel D.M., Saint D.A. 1986. Lanthanum as a surrogate for calcium in transmitter release at mouse motor nerve terminals. J. Physiol. 373, 243–260.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Silinsky E.M. 1977. An estimate of the equilibrium dissociation constant for calcium as an antagonist of evoked acetylcholine release: implications for excitation-secretion coupling. Br. J. Pharmacol. 61 (4), 691–693.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Mellow A.M., Phillips T.E., Silinsky E.M. 1978. On the conductance pathway traversed by strontium in mediating the asynchronous release of acetylcholine by motor nerve impulses. Br. J. Pharmacol. 63 (2), 229–232.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Zengel J.E., Magleby K.L. 1981. Changes in miniature endplate potential frequency during repetitive nerve stimulation in the presence of Ca2+, Ba2+, and Sr2+ at the frog neuromuscular junction. J. Gen. Physiol. 77 (5), 503–529.

    Article  CAS  PubMed  Google Scholar 

  71. Mellow A.M., Perry B.D., Silinsky E.M. 1982. Effects of calcium and strontium in the process of acetylcholine release from motor nerve endings. J. Physiol. 328, 547–562.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Searl T.J., Silinsky E.M. 2002. Evidence for two distinct processes in the final stages of neurotransmitter release as detected by binomial analysis in calcium and strontium solutions. J. Physiol. 539 (Pt 3), 693–705.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Searl T.J., Silinsky E.M. 2008. Mechanisms of neuromodulation as dissected using Sr2+ at motor nerve endings. J. Neurophysiol. 99 (6), 2779–2788.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Fatt P., Katz B. 1950. Membrane potentials at the motor end-plate. J. Physiol. 111, 46–47.

    Article  Google Scholar 

  75. Grishin S.N., Ziganshin A.U. 2015. Synaptic organization of tonic motor units in vertebrates. Biochem.( Moscow) Suppl. Series A: Membr. Cell Biol. 9 (1), 13–20.

    Article  Google Scholar 

  76. Del Castillo J., Engbaek L. 1954. The nature of the neuromuscular block produced by magnesium. J. Physiol. 124 (2), 370–384.

    Article  PubMed Central  Google Scholar 

  77. Weakly J.N. 1973. The action of cobalt ions on neuromuscular transmission in the frog. J. Physiol. 234 (3), 597–612.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Miledi R. 1966. Strontium as a substitute for calcium in the process of transmitter release at the neuromuscular junction. Nature. 212 (5067), 1233–1234.

    Article  CAS  PubMed  Google Scholar 

  79. Mukhamedyarov M.A., Grishin, S.N., Zefirov A.L., Palotas A. 2009. The mechanisms of multi-component paired-pulse facilitation of neurotransmitter release at the frog neuromuscular junction. Pflügers Arch. 458 (3), 563–570.

    Article  CAS  PubMed  Google Scholar 

  80. Bain A.I., Quastel D.M. 1992. Quantal transmitter release mediated by strontium at the mouse motor nerve terminal. J. Physiol. 450, 63–87.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Bukharaeva E.A., Samigullin D.V., Nikolsky E.E., Magazanik L.G. 2007. Modulation of the kinetics of evoked quantal release at mouse neuromuscular junctions by calcium and strontium. J. Neurochem. 100 (4), 939–949.

    Article  CAS  PubMed  Google Scholar 

  82. Hubbard J.I. 1973. Microphysiology of vertebrate neuromuscular transmission. Physiol. Rev. 53 (3), 674–723.

    CAS  PubMed  Google Scholar 

  83. Silinsky E.M. 1977. Can barium support the release of acetylcholine by nerve impulses? Br. J. Pharmacol. 59 (1), 215–217.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Magura I.S. 1977. Long-lasting inward current in snail neurons in barium solutions in voltage-clamp conditions. J. Membr. Biol. 35 (3), 239–256.

    Article  CAS  PubMed  Google Scholar 

  85. Eccles J.C. 1963. The physiology of synapses. Springer–Verlag Berlin Gottingen.

    Google Scholar 

  86. Abdrakhmanov M.M., Petrov A.M., Grigoryev P.N., Zefirov A.L. 2013. Depolarization-induced calciumindependent synaptic vesicle exo-and endocytosis at frog motor nerve terminals. Acta Naturae. 5 (4), 77–82.

    CAS  PubMed  PubMed Central  Google Scholar 

  87. Neves G., Neef A., Lagnado L. 2001. The actions of barium and strontium on exocytosis in the synaptic terminal of goldfish bipolar cells. J. Physiol. 535, 809–824.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Conner S.D., Schmid S.L. 2002. Identification of an adaptor-associated kinase, AAK1, as a regulator of clathrin-mediated endocytosis. J. Cell. Biol. 156 (5), 921–929.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Zefirov AL, Grigor’ev PN. 2010. Sensitivity of intracellular calcium-binding sites for exo-and endocytosis of synaptic vesicles to Sr, Ba, and Mg ions. Neurosci. Behav. Physiol. 40 (4), 389–396.

    Article  CAS  PubMed  Google Scholar 

  90. Chapman E.R. 2008. How does synaptotagmin trigger neurotransmitter release? Annu. Rev. Biochem. 77, 615–641.

    Article  CAS  PubMed  Google Scholar 

  91. Zakharov A.V., Petrov A.M., Kotov N.V., Zefirov A.L. 2012. Experimental and model studies of the mechanism of recycling of synaptic vesicles. Biofizika (Rus.). 57 (4), 670–682.

    CAS  Google Scholar 

  92. Takei K., Haucke V., Slepnev V., Farsad K., Salazar M., Chen H., De Camilli P. 1998. Generation of coated intermediates of clathrin-mediated endocytosis on protein-free liposomes. Cell. 94 (1), 131–141.

    Article  CAS  PubMed  Google Scholar 

  93. Loewenstein W.R., Molins D. 1958. Cholinesterase in a receptor. Science. 128 (3334), 1284.

    Article  CAS  PubMed  Google Scholar 

  94. Schallreuter K.U., Gibbons N.C., Elwary S.M., Parkin S.M., Wood J.M. 2007. Calcium-activated butyrylcholinesterase in human skin protects acetylcholinesterase against suicide inhibition by neurotoxic organophosphates. Biochem. Biophys. Res. Commun. 355 (4), 1069–1074.

    Article  CAS  PubMed  Google Scholar 

  95. Hofer P., Fringeli U.P., Hopff W.H. 1984. Activation of acetylcholinesterase by monovalent (Na+, K+) and divalent (Ca2+, Mg2+) cations. Biochemistry. 23 (12), 2730–2734.

    Article  CAS  PubMed  Google Scholar 

  96. Bradley R.J. 1986. Calcium or magnesium concentration affects the severity of organophosphate-induced neuromuscular block. Eur. J. Pharmacol. 127 (3), 275–278.

    Article  CAS  PubMed  Google Scholar 

  97. Wins P., Schoffeniels E., Foidart J.M. 1970. Inhibition of membrane-bound acetylcholinesterase by d-tubocurarine and its reversal by bivalent cations. Life Sci. 9 (5), 259–267.

    Article  CAS  PubMed  Google Scholar 

  98. Pohanka M. 2014. Copper, aluminum, iron and calcium inhibit human acetylcholinesterase in vitro. Environ. Toxicol. Pharmacol. 37 (1), 455–459.

    Article  CAS  PubMed  Google Scholar 

  99. Dodge F.A., Miledi R., Rahamimoff R. 1969. Strontium and quantal release of transmitter at the neuromuscular junction. J. Physiol. 200 (1), 267–283.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Magazanik L.G., Vyskocil F. 1970. Dependence of acetylcholine desensitization on the membrane potential of frog muscle fibre and on the ionic changes in the medium. J. Physiol. 210 (3), 507–518.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Misler S., Falke L.C. 1987. Dependence on multivalent cations of quantal release of transmitter induced by black widow spider venom. Am. J. Physiol. 253 (3 Pt 1), 469–476.

    Google Scholar 

  102. Molgó J., Lemeignan M., Guerrero S. 1982. Facilitatory effects of 4-aminopyridine on strontium-mediated evoked and delayed transmitter release from motor nerve terminals. Eur. J. Pharmacol. 84 (1–2), 1–7.

    Article  PubMed  Google Scholar 

  103. Burnstock G., Arnett T.R., Orriss I.R. 2013. Purinergic signalling in the musculoskeletal system. Purinergic Signal. 9 (4), 541–572.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Ziganshin A.U., Kamaliev R.R., Grishin S.N., Ziganshin B.A., Burnstock G. 2009. Interaction of hydrocortisone with ATP and adenosine on nerve-mediated contractions of frog skeletal muscle. Eur. J. Pharmacol. 607, 54–59.

    Article  CAS  PubMed  Google Scholar 

  105. Kim Y.V., Bobkov Y.V., Kolesnikov S.S. 2000. Adenosine triphosphate mobilizes cytosolic calcium and modulates ionic currents in mouse taste receptor cells. Neurosci. Lett. 290 (3):165–168.

    Article  CAS  PubMed  Google Scholar 

  106. Grishin S.N., Ziganshin A.U. 2013. Modulatory role of purines in neuromuscular transmission. Biochem. (Mosc.). 7 (3), 183–191.

    Google Scholar 

  107. Tsentsevitsky A.N., Khaziyev E.F., Bukharayeva E.A. 2015. Are the effects of ATP on the quantal secretion of neurotransmitter are associated with the activity of calcium channels of nerve ending? In: Prikladnaya electrodinamika, fotonika i zhivye sistemy (Applied electrodynamics, photonics, and living systems), 2015. Kazan: Novoye znaniye, p. 239–240.

    Google Scholar 

  108. Yatani A., Wilson D.L., Brown A.M. 1983. Recovery of Ca currents from inactivation: The roles of Ca influx, membrane potential, and cellular metabolism. Cell Mol. Neurobiol. 3 (4), 381–395.

    Article  CAS  PubMed  Google Scholar 

  109. Silinsky E.M. 1984. On the mechanism by which adenosine receptor activation inhibits the release of acetylcholine from motor nerve endings. J. Physiol. 346, 243–256.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Kostyuk P.G., Doroshenko P.A. 1990. Modulation of calcium channel function in nerve cell membrane. Gen. Physiol. Biophys. 9 (5), 433–443.

    CAS  PubMed  Google Scholar 

  111. Zefirov A.L., Abdrakhmanov M.M., Mukhamedyarov M.A., Grigoryev P.N. 2006. The role of extracellular calcium in exo-and endocytosis of synaptic vesicles at the frog motor nerve terminals. Neuroscience. 143 (4), 905–910.

    Article  CAS  PubMed  Google Scholar 

  112. Mukhitov A.R., Nikolsky E.E. 2014. The effect of electric stimulation of various frequencies and durations on microtubules in frog motor axon terminals. Dokl. Biol. Sci. 459 (1), 334–337.

    Article  CAS  PubMed  Google Scholar 

  113. Cousin M.A., Robinson P.J. 2000. Ca2+ influx inhibits dynamin and arrests synaptic vesicle endocytosis at the active zone. J. Neurosci. 20 (3), 949–957.

    CAS  PubMed  Google Scholar 

  114. Takei K., Slepnev V.I., De Camilli P. 2001. Interactions of dynamin and amphiphysin with liposomes. Methods Enzymol. 329, 478–486.

    Article  CAS  PubMed  Google Scholar 

  115. Zefirov A.L., Mukhamedzyanov R.D., Cheranov S.Yu., Abdrakhmanov M.M., Grigoryev P.N., Minlebayev M.G. 2002. Secretion of neurotransmitter in the neuromuscular synapse of frog after long-term exposure to calciumfree solutions. Ross. Fiziologichesky Zh. im. I.M. Sechenova (Rus.). 88 (2), 191–204.

    CAS  Google Scholar 

  116. Süudhof T.C. 2008. Neurotransmitter release. Handb. Exp. Pharmacol. 184, 1–21.

    Article  PubMed  Google Scholar 

  117. Fukuda M., Kojima T., Mikoshiba K. 1997. Regulation by bivalent cations of phospholipid binding to the C2A domain of synaptotagmin III. Biochem. J. 323 (Pt 2), 421–425.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Sudhof T.C. 2004. The synaptic vesicle cycle. Annu. Rev. Neurosci. 27, 509–547.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Medical and Biological Physics with Computer Science and Medical Equipment, Kazan State Medical University, ul. Butlerova 49, Kazan, 420012, Russia

    S. N. Grishin

  2. Research Institute of Applied Electrodynamics, Photonics and Living Systems, Kazan National Research Technical University, ul. K. Marksa 31/7, Kazan, 420111, Russia

    S. N. Grishin

Authors
  1. S. N. Grishin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to S. N. Grishin.

Additional information

Original Russian Text © S.N. Grishin, 2016, published in Biologicheskie Membrany, 2016, Vol. 33, No. 2, pp. 87–97.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Grishin, S.N. Neuromuscular transmission in Ca2+-free extracellular solution. Biochem. Moscow Suppl. Ser. A 10, 99–108 (2016). https://doi.org/10.1134/S1990747816010050

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1990747816010050

Keywords

Search

Navigation