Skip to main content
SpringerLink
Log in

Differential Effect of Nicotinic Agonists on the [3H]Norepinephrine Release from Rat Hippocampal Slices

  • Published:
Neurochemical Research Aims and scope Submit manuscript

Abstract

The aim of this study was to investigate the mechanisms involved in the effect of nicotinic agonists on the [3H]norepinephrine ([3H]NE) release from rat hippocampal slices. The stimulatory effect of nicotine, cytisine, epibatidine and anatoxin-A was completely blocked by the nicotinic antagonist mecamylamine (10 μM). In contrast, the effect of dimethylphenylpiperazinium (DMPP) was only partially inhibited by mecamylamine but was completely blocked by the NE uptake inhibitor desipramine (DMI, 10 μM). Finally, the effect of lobeline was not affected by mecamylamine and was only partially blocked by DMI. Our data indicate that the majority of nicotinic agonists increase the release of [3H]NE exclusively via stimulation of nicotinic acetylcholine receptors (nAChRs). DMPP, in addition to the stimulation of nAChRs, also evokes a carrier-mediated release. Lobeline has no stimulatory effect on nAChRs, induces a carrier-mediated release and has a further action of unidentified mechanism. Our results suggest that special caution is required for the interpretation of data, when DMPP or lobeline are used as nicotinic agonists.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

REFERENCES

  1. Dani, J. A. 2001. Overview of nicotinic receptors and their roles in the central nervous system. Biol. Psychiatry 49:166–174.

    Google Scholar 

  2. McGehee, D. S., Heath, M. J., Gelber, S., Devay, P., and Role, L. W. 1995. Nicotine enhancement of fast excitatory synaptic transmission in CNS by presynaptic receptors. Science 269:1692–1696.

    Google Scholar 

  3. Gray, R., Rajan, A. S., Radcliffe, K. A., Yakehiro, M., and Dani, J. A. 1996. Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature 383:713–716.

    Google Scholar 

  4. Wonnacott, S. 1997. Presynaptic nicotinic ACh receptors. Trends Neurosci. 20:92–98.

    Google Scholar 

  5. Vizi, E. S. and Lendvai, B. 1999. Modulatory role of presynaptic nicotinic receptors in synaptic and non-synaptic chemical communication in the central nervous system. Brain Res. Rev. 30:219–235.

    Google Scholar 

  6. Alkondon, M., Pereira, E. F., and Albuquerque, E. X. 1998. alpha-bungarotoxin-and methyllycaconitine-sensitive nicotinic receptors mediate fast synaptic transmission in interneurons of rat hippocampal slices. Brain Res. 810:257–263.

    Google Scholar 

  7. Frazier, C. J., Buhler, A. V., Weiner, J. L., and Dunwiddie, T. V. 1998. Synaptic potentials mediated via alpha-bungarotoxin-bungarotoxin-sensitive nicotinic acetylcholine receptors in rat hippocampal interneurons. J. Neurosci. 18:8228–8235.

    Google Scholar 

  8. Albuquerque, E. X., Pereira, E. F., Mike, A., Eisenberg, H. M., Maelicke, A., and Alkondon, M. 2000. Neuronal nicotinic receptors in synaptic functions in humans and rats: Physiological and clinical relevance. Behav. Brain Res. 113:131–141.

    Google Scholar 

  9. Vizi, E. S. and Kiss, J. P. 1998. Neurochemistry and pharmacology of the major hippocampal transmitter systems: Synaptic and nonsynaptic interactions. Hippocampus 8:566–607.

    Google Scholar 

  10. Arqueros, L., Naquira, D., and Zunino, E. 1978. Nicotineinduced release of catecholamines from rat hippocampus and striatum. Biochem. Pharmacol. 27:2667–2674.

    Google Scholar 

  11. Sacaan, A. I., Dunlop, J. L., and Lloyd, G. K. 1995. Pharmacological characterization of neuronal acetylcholine gated ion channel receptor-mediated hippocampal norepinephrine and striatal dopamine release from rat brain slices. J. Pharmacol. Exp. Ther. 274:224–230.

    Google Scholar 

  12. Vizi, E. S., Sershen, H., Balla, A., Mike, A., Windisch, K., Juranyi, Z., and Lajtha, A. 1995. Neurochemical evidence of heterogeneity of presynaptic and somatodendritic nicotinic acetylcholine receptors. Ann. NY Acad. Sci. 757:84–99.

    Google Scholar 

  13. Clarke, P. B. and Reuben, M. 1996. Release of [3H]-noradrenaline from rat hippocampal synaptosomes by nicotine: Mediation by different nicotinic receptor subtypes from striatal [3H]-dopamine release. Br. J. Pharmacol. 117:595–606.

    Google Scholar 

  14. Brazell, M. P., Mitchell, S. N., and Gray, J. A. 1991. Effect of acute administration of nicotine on in vivo release of noradrenaline in the hippocampus of freely moving rats: A dose-response and antagonist study. Neuropharmacol. 30:823–833.

    Google Scholar 

  15. Mitchell, S. N. 1993. Role of the locus coeruleus in the noradrenergic response to a systemic administration of nicotine. Neuropharmacol. 32:937–949.

    Google Scholar 

  16. Sershen, H., Balla, A., Lajtha, A., and Vizi, E. S. 1997. Characterization of nicotinic receptors involved in the release of noradrenaline from the hippocampus. Neuroscience 77:121–130.

    Google Scholar 

  17. Vizi, E. S., Harsing, L. G., Zimanvi, I., and Gaal, G. 1985. Release and turnover of noradrenaline in isolated median eminence: Lack of negative feedback modulation. Neuroscience 16:907–916.

    Google Scholar 

  18. Richardt, G., Haass, M., Neeb, S., Hock, M., Lang, R. E., and Schomig, A. 1988. Nicotine-induced release of noradrenaline and neuropeptide Y in guinea pig heart. Klin. Wochenschr. 66:21–27.

    Google Scholar 

  19. Rana, B., McMorn, S. O., Reeve, H. L., Wyatt, C. N., Vaughan, P. F., and Peers, C. 1993. Inhibition of neuronal nicotinic acetylcholine receptors by imipramine and desipramine. Eur. J. Pharmacol. 250:247–251.

    Google Scholar 

  20. Vaughan, P. F., Kaye, D. F., Reeve, H. L., Ball, S. G., and Peers, C. 1993. Nicotinic receptor-mediated release of noradrenaline in the human neuroblastoma SH-SY5Y. J. Neurochem. 60:2159–2166.

    Google Scholar 

  21. Hennings, E. C., Kiss, J. P., and Vizi, E. S. 1997. Nicotinic acetylcholine receptor antagonist effect of fluoxetine in rat hippocampal slices. Brain Res. 759:292–294.

    Google Scholar 

  22. Kiss, J. P., Windisch, K., Balla, A., Sershen, H., and Lajtha, A. 1997. Dual effect of DMPP on the resting release of noradrenaline from rat hippocampal slices. Brain Res. Bull. 43:257–262.

    Google Scholar 

  23. Hennings, E. C., Kiss, J. P., De Oliveira, K., Toth, P. T., and Vizi, E. S. 1999. Nicotinic acetylcholine receptor antagonistic activity of monoamine uptake blockers in rat hippocampal slices. J. Neurochem. 73:1043–1050.

    Google Scholar 

  24. Aronstam, R. S. 1981. Interactions of tricyclic antidepressants with a synaptic ion channel. Life Sci. 28:59–64.

    Google Scholar 

  25. Langeloh, A., Bonisch, H., and Trendelenburg, U. 1987. The mechanism of the 3H-noradrenaline releasing effect of various substrates of uptake1: Multifactorial induction of outward transport. Naunyn Schmiedebergs Arch. Pharmacol. 336:602–610.

    Google Scholar 

  26. Niebler, M. and Trendelenburg, U. 1990. Mechanisms of the release of 3H-noradrenaline by dimethylphenylpiperazinium (DMPP) in the rat vas deferens. Naunyn Schmiedebergs Arch. Pharmacol. 341:43–49.

    Google Scholar 

  27. Decker, M. W., Brioni, J. D., Bannon, A. W., and Arneric, S. P. 1995. Diversity of neuronal nicotinic acetylcholine receptors: Lessons from behavior and implications for CNS therapeutics. Life Sci. 56:545–570.

    Google Scholar 

  28. Lippiello, P. M. and Fernandes, K. G. 1986. The binding of L-[3H]nicotine to a single class of high affinity sites in rat brain membranes. Mol. Pharmacol. 29:448–454.

    Google Scholar 

  29. Reavill, C., Walther, B., Stolerman, I. P., and Testa, B. 1990. Behavioural and pharmacokinetic studies on nicotine, cytisine and lobeline. Neuropharmacol. 29:619–624.

    Google Scholar 

  30. Damaj, M. I., Patrick, G. S., Creasy, K. R., and Martin, B. R. 1997. Pharmacology of lobeline, a nicotinic receptor ligand. J. Pharmacol. Exp. Ther. 282:410–419.

    Google Scholar 

  31. Nooney, J. M., Peters, J. A., and Lambert, J. J. 1992. A patch clamp study of the nicotinic acetylcholine receptor of bovine adrenomedullary chromaffin cells in culture. J. Physiol. 455:503–527.

    Google Scholar 

  32. Covernton, P. J., Kojima, H., Sivilotti, L. G., Gibb, A. J., and Colquhoun, D. 1994. Comparison of neuronal nicotinic receptors in rat sympathetic neurones with subunit pairs expressed in Xenopus oocytes. J. Physiol. 481:27–34.

    Google Scholar 

  33. Miller, D. K., Crooks, P. A., and Dwoskin, L. P. 2000. Lobeline inhibits nicotine-evoked [3H]dopamine overflow from rat striatal slices and nicotine-evoked (86)Rb(+) efflux from thalamic synaptosomes. Neuropharmacol. 39:2654–2662.

    Google Scholar 

  34. Grady, S., Marks, M. J., Wonnacott, S., and Collins, A. C. 1992. Characterization of nicotinic receptor-mediated [3H]dopamine release from synaptosomes prepared from mouse striatum. J. Neurochem. 59:848–856.

    Google Scholar 

  35. Teng, L., Crooks, P. A., Sonsalla, P. K., and Dwoskin, L. P. 1997. Lobeline and nicotine evoke [3H]overflow from rat striatal slices preloaded with [3H]dopamine: Differential inhibition of synaptosomal and vesicular [3H]dopamine uptake. J. Pharmacol. Exp. Ther. 280:1432–1444.

    Google Scholar 

  36. Santha, E., Sperlagh, B., Zelles, T., Zsilla, G., PT, T., Lendvai, B., Baranyi, M., and Vizi, E. S. 2000. Multiple cellular mechanisms mediate the effect of lobeline on the release of norepinephrine. J. Pharmacol. Exp. Ther. 294:302–307.

    Google Scholar 

  37. Teng, L., Crooks, P. A., and Dwoskin, L. P. 1998. Lobeline displaces [3H]dihydrotetrabenazine binding and releases [3H] dopamine from rat striatal synaptic vesicles: Comparison with d-amphetamine. J. Neurochem. 71:258–265.

    Google Scholar 

  38. Vizi, E. S. 2000. Role of high-affinity receptors and membrane transporters in nonsynaptic communication and drug action in the central nervous system. Pharmacol. Rev. 52:63–89.

    Google Scholar 

  39. Toth, P. T. and Vizi, E.S. 1998. Lobeline inhibits Ca2+ current in cultured neurones from rat sympathetic ganglia. Eur. J. Pharmacol. 363:75–80.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Pharmacology, Institute of Experimental Medicine, Hungarian Academy of Sciences, H-1450, Budapest, P.O.B. 67, Hungary

    J. P. Kiss, K. Windisch, K. De Oliveira, E. C. P. Hennings, A. Mike & B. K. Szász

Authors
  1. J. P. Kiss
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. K. Windisch
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. K. De Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. E. C. P. Hennings
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. A. Mike
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. B. K. Szász
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kiss, J.P., Windisch, K., De Oliveira, K. et al. Differential Effect of Nicotinic Agonists on the [3H]Norepinephrine Release from Rat Hippocampal Slices. Neurochem Res 26, 943–950 (2001). https://doi.org/10.1023/A:1012384517784

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1012384517784

Search

Navigation