Advertisement

Naunyn-Schmiedeberg's Archives of Pharmacology

, Volume 338, Issue 5, pp 548–552 | Cite as

Sodium dependent 3H-noradrenaline release from rat neocortical slices in the absence of extracellular calcium presynaptic modulation by μ-opioid receptor and adenylate cyclase activation

  • Anton N. M. Schoffelmeer
  • Francois Hogenboom
  • Arie H. Mulder
Article

Summary

In Ca2+-free EGTA (1 mmol/l)-containing medium veratrine (3 μmol/l) and ouabain (100 μmol/l) strongly enhanced the efflux of 3H-noradrenaline from superfused rat brain neocortical slices prelabelled with the radioactive amine. In both cases 3H-noradrenaline release was prevented by tetrodotoxin (1 μmol/l). These effects of veratrine and ouabain were virtually additive and independent of whether the noradrenaline uptake carrier was blocked with 1 μmol/l desipramine or not. The adenylate cyclase activator forskolin (10 nmol/l–10 μmol/l) strongly enhanced veratrine- and ouabain-induced 3H-noradrenaline release, without affecting spontaneous tritium efflux. The release induced by both stimuli was profoundly inhibited by the selective μ-opioid receptor agonist [d-Ala, MePhe4, Gly-ol5]enkaphalin (DAGO, 3 nmol/l–1 μmol/l) in a concentration-dependent manner. The inhibitory effects of 1 μmol/l DAGO were abolished by 1 μmol/l naloxone. On the other hand, preincubation of the slices for 1 h with the δ-opioid receptor-selective irreversible ligand fentanyl isothiocyanate (1 pmol/l) did not change the inhibitory effects of DAGO.

These data show that veratrine- and ouabain-induced 3H-noradrenaline release from central noradrenergic nerve terminals is facilitated by increasing intracellular cyclic AMP levels and reduced by activation of presynaptic μ-opioid receptors, indicating the involvement of exocytotic neurotransmitter release. The results provide further evidence for the hypothesis that under these conditions neurotransmitter release from central noradrenergic neurons is triggerred by a Na+-induced efflux of Ca2+ ions from intracellular stores.

Key words

3H-noradrenaline release Veratrine Ouabain Intracellular calcium μ-Opioid receptor Cyclic AMP 

Abbreviations

DAGO

[d-Ala2, McPhe4, Gly-ol5]enkephalin

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Baker PF, Crawford AC (1975) A note on the mechanism by which inhibitors of the sodium pump accelerate spontaneous release of transmitter from motor nerve terminals. J Physiol (Lond) 247:209–226CrossRefGoogle Scholar
  2. Baldessarini RJ (1975) Release of catecholamines. In: Iversen LL, Iversen SD, Snyder SH (eds) Handbook of psychopharmacology, vol 3. Plenum Press, New York London, pp 37–137Google Scholar
  3. Blaustein MP (1979) The role of calcium in catecholamine release from adrenergic nerve terminals. In: Paton DM (ed) The release from adrenergic neurons. Pergamon Press, Oxford, pp 39–58CrossRefGoogle Scholar
  4. Bönisch H, Trendelenburg U (1987) Veratridine-induced outward transport of 3H-noradrenaline from adrenergic nerves of the rat vas deferens. Naunyn-Schmiedeberg's Arch Pharmacol 336:621–630CrossRefGoogle Scholar
  5. Bönisch H, Fuchs G, Graefe K-H (1986) Sodium-dependence of saturability of carrier-mediated noradrenaline efflux from noradrenergic neurones in the rat vas deferens. Naunyn-Schmiedeberg's Arch Pharmacol 332:131–134CrossRefGoogle Scholar
  6. DeLorenzo RJ (1981) The calmodulin hypothesis of neurotransmitter. Cell Calcium 2:365–385CrossRefGoogle Scholar
  7. Dunkley PR, Baker CM, Robinson PJ (1986) Depolarization-dependent protein phosphorylation in rat cortical synaptosomes: characterization of active protein kinases by phosphopeptide analysis of substrates. J Neurochem 46:1692–1703CrossRefGoogle Scholar
  8. Göthert M, Pohl I-M, Wehking E (1979) Effects of presynaptic modulators on Ca2+-induced noradrenaline release from central noradrenergic neurons. Naunyn-Schmiedeberg's Arch Pharmacol 307:21–27CrossRefGoogle Scholar
  9. Hagan RM, Hughes IE (1984) Opioid receptor subtypes in the control of transmitter release in cortex of the brain of the rat. Neuropharmacology 23:491–495CrossRefGoogle Scholar
  10. Illes P (1986) Mechanisms of receptor-mediated modulation of transmitter release in noradrenergic, cholinergic and sensory neurones. Neuroscience 17:909–928CrossRefGoogle Scholar
  11. Kehr W (1974) A method for the isolation and determination of 3-methoxytyramine in rat brain tissue. Naunyn-Schmiedeberg's Arch Pharmacol 284:149–158CrossRefGoogle Scholar
  12. Langer SZ (1981) Presynaptic regulation of the release of catecholamines. Pharmacol Rev 32:337–362Google Scholar
  13. Magyar K, Nguyen TT, Török TL, Tóth PT (1987) [3H]Noradrenaline release from rabbit pulmonary artery: sodium-pump-dependent sodium-calcium exchange. J Physiol (Lond) 393:29–42CrossRefGoogle Scholar
  14. Mulder AH (1982) An overview of subcellular localization, release and termination of action of amine, amino acid and peptide neurotransmitters in the central nervous system. In: Buys RM, Pevet P, Swaab DF (eds) Progr Brain Res, vol 55. Chemical transmission in the brain. Elsevier, Amsterdam, pp 135–156Google Scholar
  15. Mulder AH, Hogenboom F, Wardeh G, Schoffelmeer ANM (1987) Morphine and enkephalins potently inhibit 3H-noradrenaline release from rat brain cortex synaptosomes: further evidence for a presynaptic localization of μ-opioid receptors. J Neurochem 48:1043–1047CrossRefGoogle Scholar
  16. Nairn AC, Hemmings HC, Greengard P (1985) Protein kinases in the brain. Ann Rev Biochem 54:931–976CrossRefGoogle Scholar
  17. Narahashi T (1974) Chemicals as tools in the study of excitable membranes. Physiol Rev 54:813–889CrossRefGoogle Scholar
  18. Nestler EJ, Greengard P (1983) Protein phosphorylation in the brain. Nature 305:583–588CrossRefGoogle Scholar
  19. Orrego F (1979) Criteria for the identification of central neurotransmitters and their application to studies with some nerve tissue preparations in vitro. Neuroscience 4:1037–1057CrossRefGoogle Scholar
  20. Reuter H (1983) Calcium channel modulation by neurotransmitters, enzymes and drugs. Nature 301:569–574CrossRefGoogle Scholar
  21. Rice KC, Jacobson AE, Burke TR, Bajwa BS, Streaty RA, Klee WA (1983) Irreversible ligands with high selectivity towards δ or μ opiate receptors. Science 220:314–316CrossRefGoogle Scholar
  22. Schoffelmeer ANM; Mulder AH (1983a) 3H-noradrenaline release from brain slices induced by an increase in the intracellular sodium concentration: role of intracellular calcium stores. J Neurochem 40:615–621CrossRefGoogle Scholar
  23. Schoffelmeer ANM; Mulder AH (1983b) 3H-noradrenaline release from rat neocortical slices in the absence of extracellular Ca2+ and its presynaptic alpha 2-adrenergic modulation. A study on the possible role of cyclic AMP. Naunyn-Schmiedeberg's Arch Pharmacol 323:188–192CrossRefGoogle Scholar
  24. Schoffelmeer ANM, Mulder AH (1984) Presynaptic opiate receptor- and alpha2-adrenoceptor-mediated inhibition of noradrenaline release in the rat brain: role of hyperpolarization? European J Pharmacol 105:129–135CrossRefGoogle Scholar
  25. Schoffelmeer ANM, Hogenboom F, Mulder AH (1985) Evidence for a presynaptic adenylate cyclase system facilitating [3H]norepinephrine release from rat brain neocortex slices and synaptosomes. J Neurosci 5:2685–2689CrossRefGoogle Scholar
  26. Schoffelmeer ANM; Wierenga EA, Mulder AH (1986) Role of adenylate cyclase in presynaptic α2-adrenoceptor and μ-opioid receptor mediated inhibition of [3H]noradrenaline release from rat brain cortex slices. J Neurochem 46:1711–1717CrossRefGoogle Scholar
  27. Schoffelmeer ANM, Rice KC, Heijna M, Hogenboom F, Mulder AH (1988) Fentanyl thiocyanate reveals the existence of physically associated μ- and δ-opioid receptors mediating inhibition of adenylate cyclase in rat neostriatum. Eur J Pharmacol 149:179–182CrossRefGoogle Scholar
  28. Seamon KB, Padgett W, Daly JW (1981) Forskolin: a unique diterpene activator of adenylate cyclase in membranes and in intact cells. Proc Natl Acad Sci USA 78:3363–3367CrossRefGoogle Scholar
  29. Siegelbaum S, Camardo JS, Kandell ER (1982) Serotonin and cAMP close single K+ channels in Aplysia sensory neurons. Nature 299:413–417CrossRefGoogle Scholar
  30. Starke K (1987) Presynaptic α-autoreceptors. Rev Physiol Biochem Pharmacol 107:73–146CrossRefGoogle Scholar
  31. Stjärne L (1978) Facilitation and receptor-mediated regulation of noradrenaline secretion by control of recruitment of varicosities as well as by control of electro-secretory coupling. Neuroscience 3:1147–1155CrossRefGoogle Scholar
  32. Taube HD, Starke K, Borowski E (1977) Presynaptic receptor systems on the noradrenergic neurones of rat brain. Naunyn-Schmiedeberg's Arch Pharmacol 299:123–141CrossRefGoogle Scholar
  33. Török TL, Magyar K (1986) Ouabain-evoked [3H]noradrenaline release from the rabbit pulmonary artery in calcium-free solution. Quart J Exp Physiol 71:105–114CrossRefGoogle Scholar
  34. Vizi ES (1978) Na+- K+-activated adenosinetriphosphatase as a trigger in transmitter release. Neuroscience 3:367–384CrossRefGoogle Scholar
  35. Weiner N (1979) Multiple factors regulating the release of norepinephrine consequent to nerve stimulation. Fed Proc 38:2193–2202PubMedGoogle Scholar
  36. Weiner J, Schoffelmeer ANM, Mulder AH (1981) Studies on the role of Na+, K+ and Cl ion permeabilities in K+-induced release of 3H-noradrenaline from rat brain slices and its presynaptic alpha2-adrenergic modulation. Naunyn-Schmiedeberg's Arch Pharmacol 317:103–109CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 1988

Authors and Affiliations

  • Anton N. M. Schoffelmeer
    • 1
  • Francois Hogenboom
    • 1
  • Arie H. Mulder
    • 1
  1. 1.Department of PharmacologyFree University, Medical FacultyBT AmsterdamThe Netherlands

Personalised recommendations