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. 1986 Dec;6(4):349–362. doi: 10.1007/BF00711405

Effects of synaptic Activity on the metabolism and release of purines in the rat superior cervical ganglion

Marilyn W McCaman 1, Donald A McAfee 1
PMCID: PMC11567390  PMID: 3829101

Abstract

  1. The release of radioactive metabolites from isolated rat superior cervical ganglia was measured under various conditions following preloading with3H-adenosine.

  2. The3H label was recovered primarily in the adenosine metabolites, ATP, ADP, AMP, IMP, and inosine, rather than in adenosine itself.

  3. Increased release was evoked by preganglionic stimulation or by exposure to a high-K+ medium, whereas in a low-Ca2+-high-Mg2+ medium, both spontaneous release and evoked release of most metabolites were inhibited.

  4. Exposure of the ganglion to an atmosphere of N2 also increased the release of most labeled metabolites, but this release was not substantially affected by a low-Ca2+ medium.

  5. The fluorescent derivatives of the endogenous adenine-containing compounds present in the ganglion were prepared from homogenates and separated by high-performance liquid chromatography (HPLC). By the end of the testing period (6 hr), levels of ATP in the isolated ganglia had dropped to 10-20% of the initial values, while levels of ADP, AMP, and adenosine increased. There was little difference in these values between nonstimulated ganglia and those exposed to N2 or to a high-K+ medium.

Key words: adenosine, superior cervical ganglion, perfusion fluids, release of3H-adenosine, N6-etheno adenosine derivatives

References

  1. Arch, J. R. S., and Newsholme, E. A. (1978). The control of the metabolism and the hormonal role of adenosine.Essays Biochem.1482–123. [PubMed] [Google Scholar]
  2. Banay-Schwartz, M., Guzman, T. de, and Lajtha, A. (1980). Nucleoside uptake by slices of mouse brain.J. Neurochem.35544–551. [DOI] [PubMed] [Google Scholar]
  3. Barberis, C., Minn, A., and Gayet, J. (1981). Adenosine transport into guinea-pig synaptosomes.J. Neurochem.36347–354. [DOI] [PubMed] [Google Scholar]
  4. Bencherif, M., Rubio, R., and Berne, R. M. (1985). Mechanisms and site of release of adenosine in nervous tissue.Physiologist28360. [Google Scholar]
  5. Bender, A. S., Wu, P. H., and Phillis, J. W. (1980). The characterization of3H-adenosine uptake into rat cerebral cortical synaptosomes.J. Neurochem.35629–640. [DOI] [PubMed] [Google Scholar]
  6. Berne, R. M., Rubio, R., and Curnish, R. R. (1974). Release of adenosine from ischaemic brain. Effect on cerebral vascular resistance and incorporation into cerebral adenine nucleotides.Circ. Res.35262–271. [Google Scholar]
  7. Burnstock, G. (1976). Purine nucleotides.Adv. Biochem. Psychopharmacol.15225–235. [PubMed] [Google Scholar]
  8. Burnstock, G. (1981). Neurotransmitters and trophic factors in the autonomic nervous system.J. Physiol. Lond.3131–35. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fox, I. H., and Kelley, W. N. (1978). The role of adenosine and 2-deoxy-adenosine in mammalian cells.Annu. Rev. Biochem.47655–686. [DOI] [PubMed] [Google Scholar]
  10. Fredholm, B. B., and Hedqvist, P. (1980). Modulation of neurotransmission by purine nucleotides and nucleosides.Biochem. Pharmacol.291635–1643. [DOI] [PubMed] [Google Scholar]
  11. Fredholm, B. B., Dunwiddie, T. V., Bergman, B., and Lindstrom, K. (1984). Levels of adenosine and adenine nucleotides in slices of rat hippocampus.Brain Res.295127–136. [DOI] [PubMed] [Google Scholar]
  12. Harkonnen, M. H., and Kauffman, F. C. (1974). Metabolic alterations in the axotomized superior cervical ganglion of the rat. I. Energy metabolism.Brain Res.65127–139. [DOI] [PubMed] [Google Scholar]
  13. Henon, B., and McAfee, D. A. (1983). The ionic basis of adenosine receptor actions on post-ganglionic neurones in the rat.J. Physiol. Lond.336607–620. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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. (Lond.)126124–140. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kato, A. C., Katz, H. S., and Collier, B. (1974). Absence of adenine nucleotide release from autonomic ganglion.Nature249576–577. [DOI] [PubMed] [Google Scholar]
  16. Kuroda, Y., and McIlwain, H. (1974). Uptake and release of (14C)-adenine derivatives at beds of mammalian cortical synaptosomes in a superfusion system.J. Neurochem.22691–699. [DOI] [PubMed] [Google Scholar]
  17. Levitt, B., Head, R. F., and Westfall, D. P. (1984). High pressure liquid chromatographic-fluorimetric detection of adenosine and adenine nucleotides: Application to endogenous content and electrically induced release of adenyl purines in guinea pig vas deferens.Anal. Biochem.13793–100. [DOI] [PubMed] [Google Scholar]
  18. Lowry, O. H., Rosebrough, N. J., Farr, A. C., and Randall, R. J. (1951). Protein measurements with the Folin phenol reagents.J. Biol. Chem.193265–275. [PubMed] [Google Scholar]
  19. 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. Lond.323589–602. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Maire, J. C., Medilanski, J., and Straub, R. W. (1984). Release of adenosine, inosine and hypoxanthine from rabbit non-myelinated nerve fibres at rest and during activity.J. Physiol. Lond.35767–77. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. McAfee, D. A. (1982). The superior cervical ganglion: Physiological considerations. InCholinergic Models (Goldberg, A., and Hanin, I., Eds.), Raven Press, New York, pp. 191–211. [Google Scholar]
  22. McAfee, D. A., and Henon, B. (1985). Adenosine and ATP. InNeurotransmitter Actions in the Vertebrate Nervous System (Rogawksy, M. A., and Barker, J. L., Eds.), Plenum Press, New York, pp. 481–502. [Google Scholar]
  23. McCaman, M. W. (1986). Uptake and metabolism of3H-adenosine byAplysia ganglia and by individual neurons.J. Neurochem. Vertebrate471026–1031. [DOI] [PubMed] [Google Scholar]
  24. McKenna, D. G., Briggs, C. A., Barnes, D. M., and McAfee, D. A. (1985). The sucrose gap recording technique applied to the rat superior cervical ganglion.Soc. Neurosci.111004. [Google Scholar]
  25. Newsholme, E. A., Challiss, R. A. J., and Crabtree, B. (1984). Substrate cycles: Their role in improving sensitivity in metabolic control.TIBSJune277–280. [Google Scholar]
  26. Phillis, J. W., and Barraco, R. A. (1985). Adenosine, adenylate cyclase, and transmitter release.Adv. Cyclic Nucl. Protein Phosphorylat.19243–257. [PubMed] [Google Scholar]
  27. Phillis, J. W., and Wu, P. H. (1981). The role of adenosine and its nucleotides in central synaptic transmission.Prog. Neurobiol.16187–329. [DOI] [PubMed] [Google Scholar]
  28. Potter, D. D., Furshpan, E. J., and Landis, S. C. (1983). Transmitter status in cultured rat sympathetic neurons: Plasticity and multiple function.Fed. Prod.421626–1632. [PubMed] [Google Scholar]
  29. Preston, M. R. (1983). Determination of adenine, adenosine, and related nucleotides at the low picomole level by reversed-phase high-performance liquid chromatography with fluorescence detection.J. Chromatogr.275178–182. [Google Scholar]
  30. Pull, I., and McIlwain, H. (1973). Output of [14C]adenine nucleotides and their derivatives from cerebral tissues.Biochem. J.136893–901. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Schubert, P., and Kreutzberg, G. W. (1974). Axonal transport of adenosine and uridine derivatives and transfer to post-synaptic neurons.Brain Res.76526–530. [DOI] [PubMed] [Google Scholar]
  32. Schubert, P., Lee, K., and Kreutzberg, G. W. (1982). Neuronal release of adenosine derivatives and modulation of signal processing in the CNS.Prog. Brain Res.55200–236. [DOI] [PubMed] [Google Scholar]
  33. Shimizu, H., Daly, J. W., and Creveling, C. R. (1969). A radioisotopic method for measuring the formation of adenosine 3′-5′-cyclic monophosphate in incubated slices of brain.J. Neurochem.161609–1619. [DOI] [PubMed] [Google Scholar]
  34. Silinsky, E. M. (1985). Calcium and transitter release—modulation by adenosine derivatives. InCalcium in Biological Systems (Rubin, R. P., Weiss, G. B., and Putney, J. W., Jr., Eds.), Plenum Press, New York, pp. 109–119. [Google Scholar]
  35. Sinicropi, D. V., Dombrowski, A., Montgomery, C. W., Evans, R. K., and Kauffman, F. C. (1980). Maintenance of the adult rat superior cervical ganglionin vitro: Comparison of organ and explant culture systems.J. Neurochem.341280–1287. [DOI] [PubMed] [Google Scholar]
  36. Stone, T. W. (1981). Physiological roles for adenosine and adenosine-5′-triphosphate in the nervous system.Neuroscience6523–551. [DOI] [PubMed] [Google Scholar]
  37. Su, C. (1983). Purinergic neurotransmission and neuromodulation.Annu. Rev. Pharmacol. Toxicol.23397–411. [DOI] [PubMed] [Google Scholar]
  38. Trams, E. G., and Lauter, C. J. (1974). On the sidedness of plasma membrane enzymes.Biochim. Biophys. Acta345180–197. [DOI] [PubMed] [Google Scholar]
  39. Westfall, D. P., Fedan, J. S., Colby, J., Hogaboom, G. K., and O'Donnell, J. P. (1983). Evidence for a contribution of purines to the neurogenic response of the guinea pig urinary bladder.Eur. J. Pharm.87415–422. [DOI] [PubMed] [Google Scholar]
  40. Williams, M. (1984). Mammalian central adenosine receptors. InHandbook of Neurochemistry, 2nd ed.,Vol. 5. (Lajtha, A., Ed.), Plenum Press, New York, pp. 1–26. [Google Scholar]
  41. Winn, H. R., Rubio, R., and Berne, R. M. (1981). Brain adenosine concentration during hypoxia in rat.Am. J. Physiol.241H235-H242. [DOI] [PubMed] [Google Scholar]
  42. Wojcik, W. J., and Neff, N. H. (1982). Adenosine measurement by a rapid HPLC-fluorimetric method: Induced changes of adenosine content in regions of rat brain.J. Neurochem.39280–282. [DOI] [PubMed] [Google Scholar]
  43. Wolinsky, E. J., and Patterson, P. H. (1985). Potassium-stimulated purine release by cultured sympathetic neurons.J. Neurosci.51680–1687. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Wu, P. H., and Phillis, J. W. (1984). Uptake by central nervous tissues as a mechanism for the regulation of extracellular adenosine concentrations.Neurochem. Int.6613–632. [DOI] [PubMed] [Google Scholar]
  45. Yoshioka, M., and Tamura, Z. (1976). Fluorimetric determination of adenine and adenosine and its nucleotides by high-performance liquid chromatography.J. Chromatogr.123220–224. [DOI] [PubMed] [Google Scholar]
  46. Zimmerman, H., Dowdall, M. J., and Lane, D. A. (1979). Purine salvage at the cholinergic nerve endings of theTorpedo electric organ: The central role of adenosine.Neuroscience4979–993. [DOI] [PubMed] [Google Scholar]

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