Skip to main content
NCBI home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1988 Nov;405:169–185. doi: 10.1113/jphysiol.1988.sp017327

Adenosine 5'-triphosphate activates acetylcholine receptor channels in cultured Xenopus myotomal muscle cells.

Y Igusa 1
PMCID: PMC1190970  PMID: 2475606

Abstract

1. Single-channel currents activated by extracellular adenosine 5'-triphosphate (ATP-induced currents) were recorded in cultured muscle cells of Xenopus laevis using the cell-attached patch clamp technique. 2. The amplitude histogram of the ATP-induced currents had two distinct peaks, corresponding to 60 pS (high-conductance (gamma) channels currents) and 41 pS (low-gamma channel currents). The peak values of the currents were unaltered during 1-6 days in culture. 3. The mean open time of the two types of ATP-induced currents was 0.93 ms for high-gamma and 0.86 ms for low-gamma channel currents at 50 mV hyperpolarization. The reversal potential of the ATP-induced current, estimated from the I-V relationship, ranged between -5 and -15 mV. 4. The open-state probability of currents induced by 10 microM-ATP decreased in the presence of 20 microM-d-tubocurarine. 5. The frequency of ATP-induced current events depended upon the ATP concentration. The current events were first detected at 0.1 microM-ATP and occurred with increasing frequency up to 10 microM-ATP. At concentrations higher than 10 microM, the frequency of current events decreased. 6. When acetylcholine (ACh, 0.1 nM) was applied together with various concentrations of ATP, the frequency of current events increased 2- to 3-fold at the ATP concentration range between 0.1 and 10 microM. At higher concentrations of ATP the frequency decreased again. When ACh (0.1 nM) was applied without ATP, current events were rarely observed. 7. Two types of ATP-induced currents were also observed with adenylylimido 5'-diphosphate (AMP-PNP) at one-hundred micromolar concentrations. Neither AMP (adenosine 5'-monophosphate) nor ADP (adenosine 5'-diphosphate) (1-500 microM) induced channel events. 8. It is concluded that the nicotinic ACh receptor channels in cultured Xenopus skeletal muscle cells are opened by micromolar concentrations of exogenous ATP. The possible physiological significance is discussed.

Full text

PDF
169

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adams P. R., Sakmann B. Decamethonium both opens and blocks endplate channels. Proc Natl Acad Sci U S A. 1978 Jun;75(6):2994–2998. doi: 10.1073/pnas.75.6.2994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Akasu T., Hirai K., Koketsu K. Increase of acetylcholine-receptor sensitivity by adenosine triphosphate: a novel action of ATP on ACh-sensitivity. Br J Pharmacol. 1981 Oct;74(2):505–507. doi: 10.1111/j.1476-5381.1981.tb09997.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Anderson C. R., Stevens C. F. Voltage clamp analysis of acetylcholine produced end-plate current fluctuations at frog neuromuscular junction. J Physiol. 1973 Dec;235(3):655–691. doi: 10.1113/jphysiol.1973.sp010410. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Anderson M. J., Cohen M. W., Zorychta E. Effects of innervation on the distribution of acetylcholine receptors on cultured muscle cells. J Physiol. 1977 Jul;268(3):731–756. doi: 10.1113/jphysiol.1977.sp011879. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Brehm P., Kidokoro Y., Moody-Corbett F. Acetylcholine receptor channel properties during development of Xenopus muscle cells in culture. J Physiol. 1984 Dec;357:203–217. doi: 10.1113/jphysiol.1984.sp015497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brehm P., Kullberg R., Moody-Corbett F. Properties of non-junctional acetylcholine receptor channels on innervated muscle of Xenopus laevis. J Physiol. 1984 May;350:631–648. doi: 10.1113/jphysiol.1984.sp015222. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Castel M., Gainer H., Dellmann H. D. Neuronal secretory systems. Int Rev Cytol. 1984;88:303–459. doi: 10.1016/s0074-7696(08)62760-6. [DOI] [PubMed] [Google Scholar]
  8. Colquhoun D., Dreyer F., Sheridan R. E. The actions of tubocurarine at the frog neuromuscular junction. J Physiol. 1979 Aug;293:247–284. doi: 10.1113/jphysiol.1979.sp012888. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dowdall M. J., Boyne A. F., Whittaker V. P. Adenosine triphosphate. A constituent of cholinergic synaptic vesicles. Biochem J. 1974 Apr;140(1):1–12. doi: 10.1042/bj1400001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Ewald D. A. Potentiation of postjunctional cholinergic sensitivity of rat diaphragm muscle by high-energy-phosphate adenine nucleotides. J Membr Biol. 1976 Oct 20;29(1-2):47–65. doi: 10.1007/BF01868951. [DOI] [PubMed] [Google Scholar]
  11. Ginsborg B. L., Hirst G. D. The effect of adenosine on the release of the transmitter from the phrenic nerve of the rat. J Physiol. 1972 Aug;224(3):629–645. doi: 10.1113/jphysiol.1972.sp009916. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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. Pflugers Arch. 1981 Aug;391(2):85–100. doi: 10.1007/BF00656997. [DOI] [PubMed] [Google Scholar]
  13. Horn R., Brodwick M. S. Acetylcholine-induced current in perfused rat myoballs. J Gen Physiol. 1980 Mar;75(3):297–321. doi: 10.1085/jgp.75.3.297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hume R. I., Honig M. G. Excitatory action of ATP on embryonic chick muscle. J Neurosci. 1986 Mar;6(3):681–690. doi: 10.1523/JNEUROSCI.06-03-00681.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Jackson M. B. Kinetics of unliganded acetylcholine receptor channel gating. Biophys J. 1986 Mar;49(3):663–672. doi: 10.1016/S0006-3495(86)83693-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Jackson M. B. Spontaneous openings of the acetylcholine receptor channel. Proc Natl Acad Sci U S A. 1984 Jun;81(12):3901–3904. doi: 10.1073/pnas.81.12.3901. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. KRNJEVIC K., MITCHELL J. F. The release of acetylcholine in the isolated rat diaphragm. J Physiol. 1961 Feb;155:246–262. doi: 10.1113/jphysiol.1961.sp006625. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Katz B., Miledi R. A re-examination of curare action at the motor endplate. Proc R Soc Lond B Biol Sci. 1978 Dec 4;203(1151):119–133. doi: 10.1098/rspb.1978.0096. [DOI] [PubMed] [Google Scholar]
  19. Kidokoro Y., Anderson M. J., Gruener R. Changes in synaptic potential properties during acetylcholine receptor accumulation and neurospecific interactions in Xenopus nerve-muscle cell culture. Dev Biol. 1980 Aug;78(2):464–483. doi: 10.1016/0012-1606(80)90347-4. [DOI] [PubMed] [Google Scholar]
  20. Kolb H. A., Wakelam M. J. Transmitter-like action of ATP on patched membranes of cultured myoblasts and myotubes. Nature. 1983 Jun 16;303(5918):621–623. doi: 10.1038/303621a0. [DOI] [PubMed] [Google Scholar]
  21. Kuffler S. W., Yoshikami D. The number of transmitter molecules in a quantum: an estimate from iontophoretic application of acetylcholine at the neuromuscular synapse. J Physiol. 1975 Oct;251(2):465–482. doi: 10.1113/jphysiol.1975.sp011103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Manalis R. S. Voltage-dependent effect of curare at the frog neuromuscular junction. Nature. 1977 May 26;267(5609):366–368. doi: 10.1038/267366a0. [DOI] [PubMed] [Google Scholar]
  23. Ribeiro J. A., Sebastião A. M. On the role, inactivation and origin of endogenous adenosine at the frog neuromuscular junction. J Physiol. 1987 Mar;384:571–585. doi: 10.1113/jphysiol.1987.sp016470. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Ribeiro J. A., Sebastião A. M. On the type of receptor involved in the inhibitory action of adenosine at the neuromuscular junction. Br J Pharmacol. 1985 Apr;84(4):911–918. doi: 10.1111/j.1476-5381.1985.tb17385.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Ribeiro J. A., Walker J. The effects of adenosine triphosphate and adenosine diphosphate on transmission at the rat and frog neuromuscular junctions. Br J Pharmacol. 1975 Jun;54(2):213–218. doi: 10.1111/j.1476-5381.1975.tb06931.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Salpeter M. M., Elderfrawi M. E. Sizes of end plate compartments, densities of acetylcholine receptor and other quantitative aspects of neuromuscular transmission. J Histochem Cytochem. 1973 Sep;21(9):769–778. doi: 10.1177/21.9.769. [DOI] [PubMed] [Google Scholar]
  27. Silinsky E. M. Evidence for specific adenosine receptors at cholinergic nerve endings. Br J Pharmacol. 1980;71(1):191–194. doi: 10.1111/j.1476-5381.1980.tb10925.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Silinsky E. M. On the association between transmitter secretion and the release of adenine nucleotides from mammalian motor nerve terminals. J Physiol. 1975 May;247(1):145–162. doi: 10.1113/jphysiol.1975.sp010925. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Trautmann A. Curare can open and block ionic channels associated with cholinergic receptors. Nature. 1982 Jul 15;298(5871):272–275. doi: 10.1038/298272a0. [DOI] [PubMed] [Google Scholar]
  30. Whittaker V. P., Essman W. B., Dowe G. H. The isolation of pure cholinergic synaptic vesicles from the electric organs of elasmobranch fish of the family Torpedinidae. Biochem J. 1972 Jul;128(4):833–845. doi: 10.1042/bj1280833. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Yount R. G. ATP analogs. Adv Enzymol Relat Areas Mol Biol. 1975;43:1–56. doi: 10.1002/9780470122884.ch1. [DOI] [PubMed] [Google Scholar]
  32. Ziskind L., Dennis M. J. Depolarising effect of curare on embryonic rat muscles. Nature. 1978 Dec 7;276(5688):622–623. doi: 10.1038/276622a0. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES