Neurochemical Research

, Volume 17, Issue 8, pp 741–747 | Cite as

Kappa opioid agonists inhibit transmitter release from guinea pig hippocampal mossy fiber synaptosomes

  • Robert L. Gannon
  • David M. Terrian
Original Articles

Abstract

Opioid agonists specific for the μ, δ, and κ opioid receptor subtypes were tested for their ability to modulate potassium-evoked release of L-glutamate and dynorphin B-like immunoreactivity from guinea pig hippocampal mossy fiber synaptosomes. The κ opioid agonists U-62,066E and (−) ethylketocyclazocine, but not the μ agonist [D-Ala2,N-MePhe4,Gly5-ol]-enkephalin (DAGO) nor the δ agonist [D-Pen2,5]enkephalin (DPDE), inhibited the potassium-evoked release of L-glutamate and dynorphin B-like immunoreactivity. U-62,066E, but not DAGO or DPDE, also inhibited the potassium-evoked rise in mossy fiber synaptosomal cytosolic Ca2+ levels, indicating a possible mechanism for κ agonist inhibition of transmitter release. DAGO and DPDE were found to be without any effect on cytosolic Ca2+ levels or transmitter release in this preparation. The U-62,066E inhibition of the potassium-evoked rise in synaptosomal cytosolic Ca2+ levels was partially attenuated by the opioid antagonist quadazocine and insensitive to the δ-opioid specific antagonist ICI 174,864 and the μ opioid-preferring antagonists naloxone and naltrexone. Quadazocine also reversed U-62,066E inhibition of the potassium-evoked release of L-glutamate, but not dynorphin B-like immunoreactivity. These results suggest that κ opioid agonists inhibit transmitter release from mossy fiber terminals through both κ opioid and non-κ opioid receptor mediated mechanisms.

Key Words

Hippocampus mossy fiber opioids synaptosome glutamate dynorphin 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Gall, C. 1988. Seizures induce dramatic and distinctly different changes in enkephalin, dynorphin, and CCK immunoreactivities in mouse hippocampal mossy fibers. J. Neurosci. 8:1852–1862.Google Scholar
  2. 2.
    Kanamatsu, T., McGinty, J. F., Mitchell, C. L., and Hong, J. S. 1986. Dynorphin- and enkephalin-like immunoreactivity is altered in limbic-basal ganglia regions of rat brain after repeated electroconvulsive shock. J. Neurosci. 6:644–649.Google Scholar
  3. 3.
    McGinty, J. F., Henriksen, S. J., Goldstein, A., Terenius, L., and Bloom, F. E. 1983. Dynorphin is contained within hippocampal mossy fibers: immunochemical alterations after kainic acid administration and colchioine-induced neurotoxicity. Proc. Natl. Acad. Sci. USA. 80:589–593.Google Scholar
  4. 4.
    McLean, S., Rothman, R. B., Jacobson, A. E., Rice, K. C., and Herkenham, M. 1987. Distribution of opiate receptor subtypes and enkephalin and dynorphin immunoreactivity in the hippocampus of squirrel, guinea pig, rat, and hamster. J. Comp. Neurol. 255:497–510.Google Scholar
  5. 5.
    Stengaard-Pedersen, K., Fredens, K., and Larsson, L.-I. 1983. Comparative localization of enkephalin and cholecystokinin immunoreactivities and heavy metals in the hippocampus. Brain Res. 273:81–96.Google Scholar
  6. 6.
    Gannon, R. L., Baty, L. T., and Terrian, D. M. 1989. L(+)-2-Amino-4-phosphonobutyrate inhibits the release of both glutamate and dynorphin from guinea pig but not rat hippocampal mossy fiber synaptosomes. Brain Res. 495:151–155.Google Scholar
  7. 7.
    Terrian, D. M., Gannon, R. L., and Rea, M. A. 1990. Glutamate is the endogenous amino acid selectively released by rat hippocampal mossy fiber synaptosomes concomitantly with prodynorphin-derived peptides. Neurochem. Res. 15:1–5.Google Scholar
  8. 8.
    Terrian, D. M., Johnston, D., Claiborne, B. J., Ansah-Yiadom, R., Strittmatter, W. J., and Rea, M. A. 1988. Glutamate and dynorphin release from a subcellular fraction enriched in hippocampal mossy fiber synaptosomes. Brain Res. Bull. 21:343–351.Google Scholar
  9. 9.
    Kosterlitz, H. W. 1985. Opioid peptides and their receptors. Proc. R. Soc. Lond. B. 225:27–40.Google Scholar
  10. 10.
    Leslie, F. M. 1987. Methods used for the study of opioid receptors. Pharmac. Rev. 39:197–249.Google Scholar
  11. 11.
    Caudle, R. M., and Chavkin, C. 1990. Mu opioid receptor activation reduces inhibitory postsynaptic potentials in hippocampal CA3 pyramidal cells of rat and guinea pig. J. Pharmacol. Exp. Ther. 252:1361–1369.Google Scholar
  12. 12.
    Iwama, T., Ishihara, K., Satoh, M., and Takagi, H. 1986. Different effects of dynorphin A on in vitro guinea pig hippocampal CA3 pyramidal cells with various degrees of paired-pulse facilitation. Neurosci. Lett. 63:190–194.Google Scholar
  13. 13.
    Iwama, T., Ishara, K., Takagi, H., and Satoh, M. 1987. Possible mechanism involved in the inhibitory action of U-50,488H, an opioid κ agonist, on guinea pig hippocampal CA3 pyramidal neurons in vitro. J. Pharmacobio-Dyn. 10:564–570.Google Scholar
  14. 14.
    Martin, M. R. 1983. Naloxone and long term potentiation of hippocampal CA3 field potentials in vitro. Neuropeptides. 4:45–50.Google Scholar
  15. 15.
    Chavkin, C., James, I. F., and Goldstein, A. 1982. Dynorphin is a specific endogenous ligand of the κ opioid receptor. Nature. 215:413–415.Google Scholar
  16. 16.
    Moises, H. C., and Walker, J. M., 1985. Electrophysiological effects of dynorphin peptides on hippocampal pyramidal cells in rat. Eur. J. Pharm. 108:85–98.Google Scholar
  17. 17.
    Vonvoigtlander, P. F., Lahti, R. A., and Ludens, J. H. 1983. U-50,488: a selective and structurally novel non-mu (kappa) opioid agonist. J. Pharmacol. Exp. Ther. 224:7–12.Google Scholar
  18. 18.
    Gannon, R. L., and Terrian, D. M. 1991. U-50,488H inhibits dynorphin and glutamate release from guinea pig hippocampal mossy fiber terminals. Brain Res. 548:242–247.Google Scholar
  19. 19.
    Alzheimer, C., and Ten Bruggencate, G. 1990. Nonopoiod actions of the κ-opioid receptor agonists, U 50488H and U 69593, on electrophysiological properties of hippocampal CA3 neuronsin vitro. J. Pharmacol. Exp. Ther. 255:900–905.Google Scholar
  20. 20.
    Perry, D. C., and Grimes, L. M. 1989. Administration of kainic acid and colchicine alters μ and λ opiate binding in rat hippocampus. Brain Res. 477:100–108.Google Scholar
  21. 21.
    Grevel, J., and Sadée, W. 1983. An opiate binding site in the rat brain is highly selective for 4,5-epoxymorphinans. Science 221:1198–1201.Google Scholar
  22. 22.
    Perry, D. C., and Sadée, W. 1986. Autoradiography of λ binding sites in rat brain. Eur. J. Pharm. 129:147–158.Google Scholar
  23. 23.
    Peterson, G. L. 1977. A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal. Biochem. 83:346–356.Google Scholar
  24. 24.
    Terrian, D. M., Hernandez, P. G., Rea, M. A., and Peters, R. I. 1989. ATP release, adenosine formation, and modulation of dynorphin and glutamic acid release by adenosine analogues in rat hippocampal mossy fiber synaptosomes. J. Neurochem. 53:1390–1399.Google Scholar
  25. 25.
    Graham, L. T. Jr., and Aprison, M. H. 1966. Fluorometric determination of aspartate, glutamate, and λ-aminobutyrate in nerve tissue using enzymic methods. Anal. Biochem. 15:487–497.Google Scholar
  26. 26.
    Grynkiewicz, G., Poenie, M., and Tsien, R. Y. 1985. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260:3440–3448.Google Scholar
  27. 27.
    Goldstein, A. 1984. Biology and Chemistry of the dynorphin peptides. Pages 95–145,in Udenfriend, S., and Meienhofer, J. (eds.), The Peptides, Vol. 6, Academic Press, New York.Google Scholar
  28. 28.
    Vonvoigtlander, P. F., and Lewis, R. A. 1988. Analgesic and mechanistic evaluation of spiradoline, a potent kappa opioid. J. Pharmacol. Exp. Ther. 246:259–262.Google Scholar
  29. 29.
    Magnan, J., Paterson, J., Tavani, A., and Kosterlitz, H. W. 1982. The binding spectrum of narcotic analgesic drugs with different agonist and antagonist properties. Naunyn-Schmied. Arch. Pharmacol. 319:197–205.Google Scholar
  30. 30.
    Takemori, A. E., Ho, B. Y., Naeseth, J. S., and Portoghese, P. S. 1988. Norbinaltorphimine, a highly selective kappa-opioid antagonist in analgesic and receptor binding assays. J. Pharmacol. Exp. Ther. 246:255–258.Google Scholar
  31. 31.
    Ward, S. J., Pierson, A. K., and Michne, W. F. 1983. Multiple opioid receptor profile in vitro and activity in vivo of the potent opioid antagonist WIN 44,441-3. Life Sci. 33 (Suppl.):303–306.Google Scholar
  32. 32.
    Zukin, R. S., Eghbali, M., Olive, D., Unterwald, E. M., and Tempel, A. 1988. Characterization and visualization of rat and guinea pig brain κ opioid receptors: evidence for κ1 and κ2 opioid receptors. Proc. Natl. Acad. Sci. USA. 85:4061–4065.Google Scholar
  33. 33.
    Iyengar, S., Kim, H. S., and Wood, P. L. 1986. Effects of kappa opiate agonists on neurochemical and neuroendocrine indices: evidence for kappa receptor subtypes. Life Sci. 39:637–644.Google Scholar
  34. 34.
    Xiang, J.-Z., Adamson, P., Brammer, M. J., and Campbell, I. C. 1990. the κ-opiate agonist U50488H decreases the entry of45Ca into rat cortical synaptosomes by inhibiting N- but not L-type calcium channels. Neuropharm. 29:439–444.Google Scholar
  35. 35.
    Gross, R. A., and Macdonald, R. L. 1987. Dynorphin A seiectively reduces a large transient (N-type) calcium current of mouse dorsal root ganglion neurons in cell culture. Proc. Natl. Acad. Sci. USA. 84:5469–5473.Google Scholar
  36. 36.
    Terrian, D. M., Damron, D. S., Dorman, R. V., and Gannon, R. L. 1989. Effects of calcium antagonists on the evoked release of dynorphin A(1–8) and availability of intraterminal calcium in rat hippocampal mossy fiber synaptosomes. Neurosci. Lett. 106:322–327.Google Scholar
  37. 37.
    Terrian, D. M., Dorman, R. V., and Gannon, R. L. 1990. Characterization of the presynaptic calcium channels involved in glutamate exocytosis from rat hippocampal mossy fiber synaptosomes. Neurosci. Lett. 119:211–214.Google Scholar
  38. 38.
    Houser, C. R., Miyashiro, J. E., Swartz, B. E., Walsh, G. O., Rich, J. R., and Delgado-Escueta, A. V. 1990. Altered patterns of dynorphin immunoreactivity suggest mossy fiber reorganization in human hippocampal epilepsy. J. Neurosci. 10:267–282.Google Scholar
  39. 39.
    Represa, A., Robain, O., Tremblay, E., and Ben-Ari, Y. 1989. Hippocampal plasticity in childhood epilepsy. Neurosci. Lett. 99:351–355.Google Scholar
  40. 40.
    Sutula, T., Cascino, G., Cavazos, J., Parada, I., and Ramirez, L. 1989. Mossy fiber synaptic reorganization in the epileptic human temporal lobe. Ann. Neurol. 26:321–330.Google Scholar
  41. 41.
    Ben-Ari, Y., and Represa, A. 1990. Brief seizure episodes induce long-term potentiation and mossy fibre sprouting in the hippocampus. Trends Neurosci. 13:312–318.Google Scholar
  42. 42.
    Cronin, J., and Dudek, F. E. 1988. Chronic seizures and collateral sprouting of dentate mossy fibers after kainic acid treatment in rats. Brain Res. 474:181–184.Google Scholar
  43. 43.
    Gail, C., Lauterborn, J., Isackson, P., and White, J. 1990. Seizures, neuropeptide regulation, and mRNA expression in the hippocampus. Prog. Brain Res. 83:371–390.Google Scholar

Copyright information

© Plenum Publishing Corporation 1992

Authors and Affiliations

  • Robert L. Gannon
    • 1
  • David M. Terrian
    • 1
  1. 1.Department of Anatomy and Cell BiologyEast Carolina University, School of MedicineGreenville

Personalised recommendations