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The Demonstration and Measurement of Adenosine Triphosphate Release from Nerves

  • Thomas D. White

Abstract

In 1953, Holton and Holton observed that antidromic stimulation of the great auricular nerve of the rabbit ear perfused with Locke’s solution resulted in a specific increase in the optical density at 260 nm in samples of venous effluent. The differences in absorption spectra of samples of venous effluent were “typical of those produced by substances containing purine and pyrimidine rings, including ATP and its break-down products.” Later, Holton and Holton (1954) showed similar time courses for vasodilation caused by antidromic stimulation of the sensory nerve and that caused by injections of ATP. In a subsequent study, Holton (1959) demonstrated, using firefly luciferin-luciferase, that ATP was liberated when the great auricular nerve was stimulated. All these results led the Holtons to propose that ATP might be released from sensory nerve endings and have a possible role in chemical transmission. Notwithstanding the recent evidence that substance P may also be a likely candidate for the transmitter involved in the vasodilation responses following antidromic stimulation of sensory nerves (Gazelius et al, 1981), the studies of the Holtons stand out as the first to suggest a possible transmitter function for ATP or its derivatives.

Keywords

Synaptosomal Preparation Great Auricular Nerve Maximum Peak Height Smooth Muscle Preparation Propagate Action Potential 
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. Abood, L. G., Koketsu, K., and Miyamoto, S. 1962. Outflux of various phosphates during membrane depolarization of excitable tissues. Am. J. Physiol, 202: 469–474.PubMedGoogle Scholar
  2. Al-Humayyd, M., and White, T. D. 1983. Release of ATP from noradrenergic varicosities isolated from guinea-pig myenteric plexus (Abstr.). J. Neurochem. 4/(Suppl.): S79.Google Scholar
  3. Bauer, V., and Kuriyama, H. 1982. The nature of non-cholinergic, non-adrenergic transmission in longitudinal and circular muscles of the guinea-pig ileum. J. Physiol, 532: 375–391.Google Scholar
  4. Bauer, V., and Kuriyama, H. 1982. The nature of non-cholinergic, non-adrenergic transmission in longitudinal and circular muscles of the guinea-pig ileum. J. Physiol, 532: 375–391.Google Scholar
  5. Bender, A. S., Wu, P. H., and Phillis, J. W. 1981. The rapid uptake and release of [3H]adenosine by rat cerebral cortical synaptosomes. J. Neurochem, 36: 651–660.PubMedCrossRefGoogle Scholar
  6. Boyne, A. F. 1976. Isolation of synaptic vesicles from Narcine brasiliensis electric organ: Some influences on release of vesicular acetylcholine and ATP. Brain Res, 7 /4: 481–491.CrossRefGoogle Scholar
  7. Burnstock, G. 1979. Past and current evidence for the purinergic nerve hypothesis. In: Physiological and Regulatory Functions of Adenosine and Adenine Nucleotides, pp. 3–32. Ed. by Baer, H. P., and Drummond, G. I. Raven Press, New York.Google Scholar
  8. Burnstock, G. 1983. A comparison of receptors for adenosine and adenine nucleotides. In: Regulatory Function of Adenosine, pp. 49–62. Ed. by. Berne, R. M., Rail, T. W., and Rubio, R. Martinus Nijhoff, Boston.CrossRefGoogle Scholar
  9. Burnstock, G., Cocks, T., Kasakov, L., and Wong, H. K. 1978. Direct evidence for ATP release from non-adrenergic, non-cholinergic (“purinergic”) nerves in the guinea-pig taenia coli and bladder. Eur. J. Pharmacol, 49: 145–149.PubMedCrossRefGoogle Scholar
  10. Catterall, W. A. 1980. Neurotoxins that act on voltage-sensitive sodium channels in excitable membranes. Ann. Rev. Pharmacol. Toxicol, 20: 15–43.Google Scholar
  11. Chapman, A. G., Westerberg, E., and Siesjo, B. K. 1981. The metabolism of purine and pyrimidine nucleotides in rat cortex during insulin-induced hypoglycemia and recovery. J. Neurochem, 56: 179–189.CrossRefGoogle Scholar
  12. Chaudhry, A., Downie, J. W., and White, T. D. 1984. Tetrodotoxin-resistant release of ATP from superfused rabbit detrusor muscle during electrical field stimulation in the presence of luciferin-luciferase. Can. J. Physiol. Pharmacol, 62: 153–156.PubMedCrossRefGoogle Scholar
  13. Daval, J. L., and Barberis, C. 1981. Release of radiolabeled adenosine derivatives from superfused synaptosome beds. Biochem. Pharmacol 30: 2559–2561.PubMedCrossRefGoogle Scholar
  14. Detwiler, T. C., and Feinman, R. D. 1973. Kinetics of the thrombin-induced release of adenosine triphosphate by platelets. Comparison with release of calcium. Biochemistry, 12: 2462–2468.PubMedCrossRefGoogle Scholar
  15. Ewald, D. A. 1976. Potentiation of postjunctional cholinergic sensitivity of rat diaphragm muscle by high-energy-phosphate adenine nucleotides. J. Membrane Biol, 29: 47–65.CrossRefGoogle Scholar
  16. Fredholm, B. B., and Hedqvist, P. 1980. Modulation of neurotransmission by purine nucleotides and nucleosides. Biochem. Pharmacol, 29. 1635–1643.PubMedCrossRefGoogle Scholar
  17. Fredholm, B. B., and Vernet, L. 1979. Release of 3H-nucleosides from 3H-adenine labeled hypothalamic synaptosomes. Acta. Physiol. Scand, 106: 91–107.CrossRefGoogle Scholar
  18. Fredholm, B. B., Fried, G., and Hedqvist, P. 1982. Origin of adenosine released from rat vas deferens by nerve stimulation. Eur. J. Pharmacol, 79: 233–243.PubMedCrossRefGoogle Scholar
  19. Gazelius, B., Brodin, E., Olgart, L., and Panopoulos, P. 1981. Evidence that substance P is a mediator of antidromic vasodilatation using somatostatin as a release inhibitor. Acta. Physiol. Scand, 73: 155–159.CrossRefGoogle Scholar
  20. Goldman, D. E. 1943. Potential impedance and rectification in membrane. J. Gen. Physiol, 27: 37–60.PubMedCrossRefGoogle Scholar
  21. Holton, P. 1959. The liberation of adenosine triphosphate on antidromic stimulation of sensory nerves. J. Physiol, 145: 494–504.PubMedGoogle Scholar
  22. Holton, F. A., and Holton, P. 1953. The possibility that ATP is a transmitter at sensory nerve endings. J. Physiol, 119. 50 - 51 P.Google Scholar
  23. Holton, F. A., and Holton, P. 1954. The capillary dilator substances in dry powders of spinal roots: A possible role of adenosine triphosphate in chemical transmission from nerve endings. J. Physiol, 126: 124–140.PubMedGoogle Scholar
  24. Israel, M., Lesbats, B., Meunier, F. M., and Stinnakre, J. 1976. Postsynaptic release of adenosine triphosphate induced by single impulse transmitter action. Proc. R. Soc. Lond. B, 193: 461–468.PubMedCrossRefGoogle Scholar
  25. Jahr, C., and Jessel, T. M. 1983. ATP excites a subpopulation of rat dorsal horn neurones. Nature, 504: 730–733.CrossRefGoogle Scholar
  26. Jhamandas, K., and Dumbrille, A. 1980. Regional release of [3H]adenosine derivatives from rat brain in vivo: Effect of excitatory amino acids, opiate agonists, and benzodiazepines. Can. J. Physiol. Pharmacol, 55: 1262–1278.CrossRefGoogle Scholar
  27. Kao, C. Y. 1966. Tetrodotoxin, saxitoxin and their significance in the study of excitation phenomena. Pharmacol. Rev, 5: 997–1049.Google Scholar
  28. Karl, D. M., and Holm-Hansen, O. 1976. Effects of luciferin concentration on the quantitative assay of ATP using crude luciferase preparations. Anal. Biochem, 75: 100–112.PubMedCrossRefGoogle Scholar
  29. Katsuragi, T., and Su, C. 1980. Purine release from vascular adrenergic nerves by high potassium and a calcium ionophore, A-23187. J. Pharmacol. Exp. Ther, 215: 685–690.PubMedGoogle Scholar
  30. Kuroda, Y., and Mcllwain, H. 1974. Uptake and release of [14C]adenine derivatives at beds of mammalian cortical synaptosomes in a superfusion system. J. Neurochem, 22: 691–699.PubMedCrossRefGoogle Scholar
  31. Li, P. P., and White, T. D. 1977. Rapid effects of veratridine, tetrodotoxin, gramicidin D, valinomycin and Na CN on the Na+, K+ and ATP contents of synaptosomes. J. Neurochem, 28: 961–915.CrossRefGoogle Scholar
  32. Lundin, A., and Thore, A. 1975. Analytical information obtainable by evaluation of the time course of firefly bioluminescence in the assay of ATP. Anal. Biochem, 66: 47–63.PubMedCrossRefGoogle Scholar
  33. Maire, J. C., Medilanski, J., and Straub, R. W. 1982. Uptake of adenosine and release of adenine derivatives in mammalian non-myelinated nerve fibres at rest and during activity. J. Physiol, 323: 589–602.PubMedGoogle Scholar
  34. McElroy, W. D., and DeLuca, M. 1981. The chemistry and applications of firefly luminescence. In: Bioluminescence and Chemiluminescence: Basic Chemistty and Analytical Applications, pp. 179–186. Ed. by DeLuca, M. E., and McElroy, W. D. Academic Press, New York.Google Scholar
  35. Minchin, M. C. W. 1980. Veratrum alkaloids as transmitter-releasing agents. J. Neurosci, 2: 111–121.Google Scholar
  36. Morel, N., and Meunier, F. M. 1981. Simultaneous release of acetylcholine and ATP from stimulated cholinergic synaptosomes. J. Neurochem, 36: 1766–1773.PubMedCrossRefGoogle Scholar
  37. Nagy, A., Shuster,T. A., and Rosenberg, M. D. 1983. Adenosine triphosphatase activity at the external surface of chicken brain synaptosomes. J. Neurochem, 40: 226–234.PubMedCrossRefGoogle Scholar
  38. Narahashi, T., Moore, J. W., and Scott, W. 1964. Tetrodotoxin blockage of sodium conductance on lobster giant axons. J. Gen. Physiol, 47: 965–974.PubMedCrossRefGoogle Scholar
  39. Newby, A. C., and Sala, G. B. 1982. A new procedure for haptenizing adenosine leading to a more specific radioimmunoassay method. Biochem. J, 20: 603–610.Google Scholar
  40. Phillis, J. W., and Wu, P. H. 1981. The role of adenosine and its nucleotides in central synaptic transmission. Progr. Neurobiol, 76: 187–239.CrossRefGoogle Scholar
  41. Phillis, J. W., Kostopoulos, G. K., and Limacher, J. J. 1974. Depression of corticospinal cells by various purines and pyrimidines. Can. J. Physiol. Pharmacol, 52: 1226–1229.PubMedCrossRefGoogle Scholar
  42. Phillis, J. W., Kostopoulos, G. K., and Limacher, J. J. 1975. A potent depressant action of adenine derivatives on cerebral cortical neurones. Eur. J. Pharmacol, 50: 125–129.CrossRefGoogle Scholar
  43. Pons, F., Bruns, R. F., and Daly, J. W. 1980. Depolarization-evoked accumulation of cyclic AMP in brain sites: The requisite intermediate adenosine is not derived from hydrolysis of released ATP. J. Neurochem, 54: 1319–1323.CrossRefGoogle Scholar
  44. Potter, P., and White, T. D. 1980. Release of adenosine 5’-triphosphate from synaptosomes from different regions of rat brain. Neuroscience, 5: 1351–1356.PubMedCrossRefGoogle Scholar
  45. Potter, P., and White, T. D. 1982. Lack of effect of 6-hydroxydopamine pretreatment on depolarization-induced release of ATP from rat brain synaptosomes. Eur. J. Pharmacol, 80: 143–147.PubMedCrossRefGoogle Scholar
  46. Romey, G., and Lazdunski, M. 1982. Lipid-soluble toxins thought to be specific for Na+ channels block Ca2 channels in neuronal cells. Nature, 297: 79–80.PubMedCrossRefGoogle Scholar
  47. Rutherford, A., and Burnstock, G. 1978. Neuronal and non-neuronal components in the overflow of labelled adenyl compounds from guinea-pig taenia coli. Eur. J. Pharmacol, 48: 195–202.PubMedCrossRefGoogle Scholar
  48. Schubert, P., Lee, K., West, M., Deadwyler, S., and Lynch, G. 1976. Stimulation-dependent release of 3H-adenosine derivatives from central axon terminals to target neurones. Nature, 260: 541–542.PubMedCrossRefGoogle Scholar
  49. Silinsky, E. M. 1975. On the association between transmitter secretion and the release of adenine dinucleotides from mammalian motor nerve terminals. J. Physiol, 247: 145–162.PubMedGoogle Scholar
  50. Slowiaczek, P., and Tattersall, M. H. N. 1982. The determination of purine levels in human and mouse plasma. Anal. Biochem, 125: 6–12.PubMedCrossRefGoogle Scholar
  51. Stone, T. W. 1981. Physiological roles for adenosine and adenosine triphosphate in the nervous system. Neuroscience, 6: 523–555.PubMedCrossRefGoogle Scholar
  52. Su, C. 1983. Purinergic neurotransmission and neuromodulation. Ann. Rev. Pharmacol., Toxicol, 25: 397–411.Google Scholar
  53. Su, C., Bevan, J. A., and Burnstock, G. 1971.3H-adenosine triphosphate: Release during stimulation of enteric nerves. Science, 775: 337–339.Google Scholar
  54. Sulakhe, P. V., and Phillis, J. W. 1975. The release of [3H]adenosine and its derivatives from cat sensorimotor cortex. Life Sci, 77: 551–556.CrossRefGoogle Scholar
  55. Ulbricht, W. 1969. The effect of veratridine on excitable membranes of nerve and muscle. Ergebn. Physiol, 67: 19–61.Google Scholar
  56. Villegas, J., Sevcik, C., Barnola, F. V., and Villegas, R. 1976. Grayanotoxin, veratrine, and tetrodotoxin-sensitive sodium pathways in the Schwann cell membrane of squid nerve fibres. J. Gen. Physiol, 67: 369–380.PubMedCrossRefGoogle Scholar
  57. Westfall, D. P., Hogaboom, G. K., Colby, J., O’Donnell, J. P., and Fedan, J. S. 1982. Direct evidence against a role of ATP as the nonadrenergic noncholinergic inhibitory neurotransmitter in guinea pig tenia coli. Proc. Natl. Acad. Sci, 79: 7041–7045.PubMedCrossRefGoogle Scholar
  58. White, T. D. 1977. Direct detection of depolarization-induced release of ATP from a synaptosomal preparation. Nature, 267: 61–68.CrossRefGoogle Scholar
  59. White, T. D. 1978. Release of ATP from a synaptosomal preparation by elevated extracellular K+ and by veratridine. J. Neurochem, 30: 329–336.PubMedCrossRefGoogle Scholar
  60. White, T. D. 1982. Release of ATP from isolated myenteric varicosities by nicotinic agonists. Eur.J. Pharmacol, 79: 333–334.PubMedCrossRefGoogle Scholar
  61. White, T. D., and Al-Humayyd, M. 1983. Acetylcholine releases ATP from varicosities isolated from guinea pig myenteric plexus. J. Neurochem, 40: 1069–1075.PubMedCrossRefGoogle Scholar
  62. White, T. D., and Leslie, R. A. 1982. Depolarization-induced release of adenosine 5’-triphosphate from isolated varicosities derived from the myenteric plexus of the guinea pig small intestine. J. Neurosci, 2: 206–215.PubMedGoogle Scholar
  63. White, T., Potter, P., and Wonnacott, S. 1980. Depolarization-induced release of ATP from cortical synaptosomes is not associated with acetylcholine release. J. Neurochem, 34: 1109–1112.PubMedCrossRefGoogle Scholar
  64. White, T., Potter, P., Moody, C., and Burnstock, G. 1981. Tetrodotoxin-resistant release of ATP from guinea-pig taenia coli and vas deferens during electrical field stimulation in the presence of luciferin-luciferase. Can. J. Physiol. Pharmacol, 59: 1094–1100.PubMedCrossRefGoogle Scholar
  65. Wojcik, W., Olianas, M., Paranti, M., Gentleman, S., and Neff, N. H. 1981. A simple fluorometric method for cAMP: Application to studies of brain adenylate cyclase activity. J. Cyclic Nucleotide Res, 7: 27–35.PubMedGoogle Scholar
  66. Wojcik, W. J., and Neff, N. H. 1982. Adenosine measurement by a rapid HPLC-fluorometric method: Induced changes of adenosine content in regions of rat brain. J. Neurochem, 39: 280–282.PubMedCrossRefGoogle Scholar
  67. Wojcik, W. J., and Neff, N. H. 1983. Location of adenosine release and adenosine A2 receptors to rat striatal neurons. Life Sci, 33: 755–763.PubMedCrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1985

Authors and Affiliations

  • Thomas D. White
    • 1
  1. 1.Department of PharmacologyDalhousie UniversityHalifaxCanada

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