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. 1993 Jan;108(1):236–241. doi: 10.1111/j.1476-5381.1993.tb13468.x

Potentiation of miniature endplate potential frequency by ATP in Xenopus tadpoles.

W M Fu 1, S H Yang 1, S Y Lin-Shiau 1
PMCID: PMC1907709  PMID: 8428207

Abstract

1. Extracellular application of ATP (1 mM), a substance co-stored and co-released with acetylcholine in peripheral nervous systems, potentiated the spontaneous secretion of acetylcholine (ACh) but had no effect on the amplitude and decay time constant of miniature endplate potentials (m.e.p.ps) at neuromuscular synapses in Xenopus tadpoles. 2. alpha,beta-Methylene ATP (0.3 mM) and GTP (1 mM) were also effective in increasing m.e.p.p. frequency. On the other hand, ADP, AMP and adenosine (all at 1 mM) decreased m.e.p.p. frequency. 3. Unlike the transient effect of ATP analogue and GTP on m.e.p.p. frequency, the phorbol ester TPA (2 microM) which is a protein kinase C activator, increased m.e.p.p. frequency consistently and the effects lasted as long as the presence of TPA. 4. Staurosporine (0.5 microM) and H-7 (10 microM), which are protein kinase C inhibitors, each decreased the basal level of m.e.p.p. frequency and markedly inhibited the effects of both ATP and TPA. 5. These results suggest that there is a basal activity of cytosolic protein kinases in the nerve terminals of Xenopus tadpoles and the effect of ATP is probably mediated by the binding of membrane surface purinoceptors which in turn activates cytosolic protein kinases and increases ACh release.

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Selected References

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  1. ABOOD L. G., KOKETSU K., MIYAMOTO S. Outflux of various phosphates during membrane depolarization of excitable tissues. Am J Physiol. 1962 Mar;202:469–474. doi: 10.1152/ajplegacy.1962.202.3.469. [DOI] [PubMed] [Google Scholar]
  2. Berridge M. J. Inositol trisphosphate and diacylglycerol: two interacting second messengers. Annu Rev Biochem. 1987;56:159–193. doi: 10.1146/annurev.bi.56.070187.001111. [DOI] [PubMed] [Google Scholar]
  3. Boyd I. A., Forrester T. The release of adenosine triphosphate from frog skeletal muscle in vitro. J Physiol. 1968 Nov;199(1):115–135. doi: 10.1113/jphysiol.1968.sp008642. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cockcroft S., Stutchfield J. ATP stimulates secretion in human neutrophils and HL60 cells via a pertussis toxin-sensitive guanine nucleotide-binding protein coupled to phospholipase C. FEBS Lett. 1989 Mar 13;245(1-2):25–29. doi: 10.1016/0014-5793(89)80184-x. [DOI] [PubMed] [Google Scholar]
  5. De Mey J., Burnstock G., Vanhoutte P. M. Modulation of the evoked release of noradrenaline in canine saphenous vein via presynaptic receptors for adenosine but not ATP. Eur J Pharmacol. 1979 May 15;55(4):401–405. doi: 10.1016/0014-2999(79)90115-8. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. Dunwiddie T. V. Interactions between the effects of adenosine and calcium on synaptic responses in rat hippocampus in vitro. J Physiol. 1984 May;350:545–559. doi: 10.1113/jphysiol.1984.sp015217. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Forrester T. An estimate of adenosine triphosphate release into the venous effluent from exercising human forearm muscle. J Physiol. 1972 Aug;224(3):611–628. doi: 10.1113/jphysiol.1972.sp009915. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fu W. M., Poo M. M. ATP potentiates spontaneous transmitter release at developing neuromuscular synapses. Neuron. 1991 May;6(5):837–843. doi: 10.1016/0896-6273(91)90179-4. [DOI] [PubMed] [Google Scholar]
  10. Gurney M. E. Suppression of sprouting at the neuromuscular junction by immune sera. Nature. 1984 Feb 9;307(5951):546–548. doi: 10.1038/307546a0. [DOI] [PubMed] [Google Scholar]
  11. Henderson C. E., Huchet M., Changeux J. P. Neurite outgrowth from embryonic chicken spinal neurons is promoted by media conditioned by muscle cells. Proc Natl Acad Sci U S A. 1981 Apr;78(4):2625–2629. doi: 10.1073/pnas.78.4.2625. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Häggblad J., Heilbronn E. Externally applied adenosine-5'-triphosphate causes inositol triphosphate accumulation in cultured chick myotubes. Neurosci Lett. 1987 Feb 24;74(2):199–204. doi: 10.1016/0304-3940(87)90149-2. [DOI] [PubMed] [Google Scholar]
  14. Hökfelt T., Johansson O., Goldstein M. Chemical anatomy of the brain. Science. 1984 Sep 21;225(4668):1326–1334. doi: 10.1126/science.6147896. [DOI] [PubMed] [Google Scholar]
  15. Irvine R. F., Moor R. M. Micro-injection of inositol 1,3,4,5-tetrakisphosphate activates sea urchin eggs by a mechanism dependent on external Ca2+. Biochem J. 1986 Dec 15;240(3):917–920. doi: 10.1042/bj2400917. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Israël M., Lesbats B., Meunier F. M., Stinnakre J. Postsynaptic release of adenosine triphosphate induced by single impulse transmitter action. Proc R Soc Lond B Biol Sci. 1976 Jun 30;193(1113):461–468. doi: 10.1098/rspb.1976.0058. [DOI] [PubMed] [Google Scholar]
  17. Jahr C. E., Jessell T. M. ATP excites a subpopulation of rat dorsal horn neurones. Nature. 1983 Aug 25;304(5928):730–733. doi: 10.1038/304730a0. [DOI] [PubMed] [Google Scholar]
  18. Jan Y. N., Bowers C. W., Branton D., Evans L., Jan L. Y. Peptides in neuronal function: studies using frog autonomic ganglia. Cold Spring Harb Symp Quant Biol. 1983;48(Pt 1):363–374. doi: 10.1101/sqb.1983.048.01.040. [DOI] [PubMed] [Google Scholar]
  19. Keppens S., Vandekerckhove A., De Wulf H. Characterization of purinoceptors present on human liver plasma membranes. FEBS Lett. 1989 May 8;248(1-2):137–140. doi: 10.1016/0014-5793(89)80448-x. [DOI] [PubMed] [Google Scholar]
  20. Kidokoro Y., Saito M. Early cross-striation formation in twitching Xenopus myocytes in culture. Proc Natl Acad Sci U S A. 1988 Mar;85(6):1978–1982. doi: 10.1073/pnas.85.6.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Krishtal O. A., Marchenko S. M., Pidoplichko V. I. Receptor for ATP in the membrane of mammalian sensory neurones. Neurosci Lett. 1983 Jan 31;35(1):41–45. doi: 10.1016/0304-3940(83)90524-4. [DOI] [PubMed] [Google Scholar]
  22. Laufer R., Changeux J. P. Calcitonin gene-related peptide elevates cyclic AMP levels in chick skeletal muscle: possible neurotrophic role for a coexisting neuronal messenger. EMBO J. 1987 Apr;6(4):901–906. doi: 10.1002/j.1460-2075.1987.tb04836.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Meunier F., Israël M., Lesbats B. Release of ATP from stimulated nerve electroplaque junctions. Nature. 1975 Oct 2;257(5525):407–408. doi: 10.1038/257407a0. [DOI] [PubMed] [Google Scholar]
  24. Moody C. J., Burnstock G. Evidence for the presence of P1-purinoceptors on cholinergic nerve terminals in the guinea-pig ileum. Eur J Pharmacol. 1982 Jan 8;77(1):1–9. doi: 10.1016/0014-2999(82)90527-1. [DOI] [PubMed] [Google Scholar]
  25. Morris A. P., Gallacher D. V., Irvine R. F., Petersen O. H. Synergism of inositol trisphosphate and tetrakisphosphate in activating Ca2+-dependent K+ channels. Nature. 1987 Dec 17;330(6149):653–655. doi: 10.1038/330653a0. [DOI] [PubMed] [Google Scholar]
  26. Mulle C., Benoit P., Pinset C., Roa M., Changeux J. P. Calcitonin gene-related peptide enhances the rate of desensitization of the nicotinic acetylcholine receptor in cultured mouse muscle cells. Proc Natl Acad Sci U S A. 1988 Aug;85(15):5728–5732. doi: 10.1073/pnas.85.15.5728. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Nitkin R. M., Smith M. A., Magill C., Fallon J. R., Yao Y. M., Wallace B. G., McMahan U. J. Identification of agrin, a synaptic organizing protein from Torpedo electric organ. J Cell Biol. 1987 Dec;105(6 Pt 1):2471–2478. doi: 10.1083/jcb.105.6.2471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Okajima F., Sato K., Sho K., Kondo Y. Stimulation of adenosine receptor enhances alpha 1-adrenergic receptor-mediated activation of phospholipase C and Ca2+ mobilization in a pertussis toxin-sensitive manner in FRTL-5 thyroid cells. FEBS Lett. 1989 May 8;248(1-2):145–149. doi: 10.1016/0014-5793(89)80450-8. [DOI] [PubMed] [Google Scholar]
  29. Osaka T., Joyner R. W. Developmental changes in the beta-adrenergic modulation of calcium currents in rabbit ventricular cells. Circ Res. 1992 Jan;70(1):104–115. doi: 10.1161/01.res.70.1.104. [DOI] [PubMed] [Google Scholar]
  30. 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]
  31. Salmons S., Sréter F. A. Significance of impulse activity in the transformation of skeletal muscle type. Nature. 1976 Sep 2;263(5572):30–34. doi: 10.1038/263030a0. [DOI] [PubMed] [Google Scholar]
  32. Schubert P., Lee K., Kreutzberg G. W. Neuronal release of adenosine derivatives and modulation of signal processing in the CNS. Prog Brain Res. 1982;55:225–238. doi: 10.1016/S0079-6123(08)64200-4. [DOI] [PubMed] [Google Scholar]
  33. Shapira R., Silberberg S. D., Ginsburg S., Rahamimoff R. Activation of protein kinase C augments evoked transmitter release. Nature. 1987 Jan 1;325(6099):58–60. doi: 10.1038/325058a0. [DOI] [PubMed] [Google Scholar]
  34. Shatz C. J. Impulse activity and the patterning of connections during CNS development. Neuron. 1990 Dec;5(6):745–756. doi: 10.1016/0896-6273(90)90333-b. [DOI] [PubMed] [Google Scholar]
  35. 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]
  36. Silinsky E. M., Ginsborg B. L. Inhibition of acetylcholine release from preganglionic frog nerves by ATP but not adenosine. Nature. 1983 Sep 22;305(5932):327–328. doi: 10.1038/305327a0. [DOI] [PubMed] [Google Scholar]
  37. Silinsky E. M., Hubbard J. I. Thermal synthesis of amino acids from a simulated primitive atmosphere. Nature. 1973 Jun 15;243(5407):404–405. doi: 10.1038/243404a0. [DOI] [PubMed] [Google Scholar]
  38. 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]
  39. Stone T. W. Purine receptors in the rat anococcygeus muscle. J Physiol. 1983 Feb;335:591–608. doi: 10.1113/jphysiol.1983.sp014553. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Tamaoki T., Nomoto H., Takahashi I., Kato Y., Morimoto M., Tomita F. Staurosporine, a potent inhibitor of phospholipid/Ca++dependent protein kinase. Biochem Biophys Res Commun. 1986 Mar 13;135(2):397–402. doi: 10.1016/0006-291x(86)90008-2. [DOI] [PubMed] [Google Scholar]
  41. Usdin T. B., Fischbach G. D. Purification and characterization of a polypeptide from chick brain that promotes the accumulation of acetylcholine receptors in chick myotubes. J Cell Biol. 1986 Aug;103(2):493–507. doi: 10.1083/jcb.103.2.493. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Xie Z. P., Poo M. M. Initial events in the formation of neuromuscular synapse: rapid induction of acetylcholine release from embryonic neuron. Proc Natl Acad Sci U S A. 1986 Sep;83(18):7069–7073. doi: 10.1073/pnas.83.18.7069. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. el-Moatassim C., Dornand J., Mani J. C. Extracellular ATP and cell signalling. Biochim Biophys Acta. 1992 Feb 19;1134(1):31–45. doi: 10.1016/0167-4889(92)90025-7. [DOI] [PubMed] [Google Scholar]

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