Skip to main content
Log in

Modulation of GABA-Augmented Norepinephrine Release in Female Rat Brain Slices by Opioids and Adenosine

  • Published:
Neurochemical Research Aims and scope Submit manuscript

Abstract

GABAA receptor activation augments electrically-stimulated release of norepinephrine (NE) from rat brain slices. Because this effect is not observed in synaptoneurosomes, GABA probably acts on inhibitory interneurons to disinhibit NE release. To determine whether opioids or adenosine influence GABA-augmented NE release, hypothalamic and cortical slices from female rats were superfused with GABA or vehicle in the presence and absence of 10 μM morphine or 100 μM adenosine. GABA augments [3H]NE release in the cortex and hypothalamus. Morphine alone has no effect on [3H]NE release, but attenuates GABA augmentation of [3H]NE release in both brain regions. Adenosine alone modestly inhibits [3H]NE release in the cortex, but not in the hypothalamus. Adenosine inhibits GABA-augmented [3H]NE release in both brain regions. The general protein kinase inhibitor H-7, augments [3H]NE release in both brain regions and may have additive effects with GABA in cortical slices. These results implicate opioid and adenosine interneurons and possibly protein kinases in regulating GABAergic influences on NE transmission.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

REFERENCES

  1. Dennis, T., Curet, O., Nishikawa, T., and Scatton, B. 1985. Further evidence for, and nature of, the facilitatory GABAergic influence on central noradrenergic transmission. Naunyn Schmiedebergs Arch. Pharmacol. 331:225–234.

    Google Scholar 

  2. Scatton, B., Lloyd, K. G., Zivkovic, B., Dennis, T., Claustre, Y., Dedek, J., Arbilla, S., Langer, S. Z., and Bartholini, G. 1987. Fengabine, a novel antidepressant GABAergic agent. II. Effect on cerebral noradrenergic, serotonergic and GABAergic transmission in the rat. J. Pharmacol. Exp. Ther. 241:251–257.

    Google Scholar 

  3. Fuchs, E., Mansky, T., Stock, K. W., Vijayan, E., and Wuttke, W. 1984. Involvement of catecholamines and glutamate in GABAergic mechanism regulatory to luteinizing hormone and prolactin secretion. Neuroendocrinol. 38:484–489.

    Google Scholar 

  4. Adler, B. A. and Crowley, W. R. 1986. Evidence for gammaaminobutyric acid modulation of ovarian hormonal effects on luteinizing hormone secretion and hypothalamic catecholamine activity in the female rat. Endocrinol. 118:91–97.

    Google Scholar 

  5. Hartman, R. D., He, J. R., and Barraclough, C. A. 1990. Gamma-aminobutyric acid-A and-B receptor antagonists increase luteinizing hormone-releasing hormone neuronal responsiveness to intracerebroventricular norepinephrine in ovariectomized estrogen-treated rats. Endocrinol. 127:1336–1345.

    Google Scholar 

  6. Suzdak, P. D. and Gianutsos, G. 1985. Differential coupling of GABA-A and GABA-B receptors to the noradrenergic system. J. Neural Transm. 62:77–89.

    Google Scholar 

  7. Gervais, R. 1987. Local GABAergic modulation of noradrenaline release in the rat olfactory bulb measured on superfused slices. Brain Res. 400:151–154.

    Google Scholar 

  8. Navarro, C. E., Cabrera, R. J., and Donoso, A. O. 1995. Interaction between glutamate and GABA on 3H-noradrenaline release from rat hypothalamus. Brain Res. Bull. 37:119–122.

    Google Scholar 

  9. Taniyama, K., Niwa, M., Kataoka, Y., and Yamashita, K. 1992. Activation of protein kinase C suppresses the gamma-aminobutyric acidB receptor-mediated inhibition of the vesicular release of noradrenaline and acetylcholine. J. Neurochem. 58:1239–1245.

    Google Scholar 

  10. Bonanno, G. and Raiteri, M. 1987. Release-regulating GABAA receptors are present on noradrenergic nerve terminals in selective areas of the rat brain. Synapse 1:254–257.

    Google Scholar 

  11. Peoples, R. W., Giridhar, J., and Isom, G. E. 1991. Gammaaminobutyric acid enhancement of potassium-stimulated release of [3H]norepinephrine by multiple mechanisms in rat cortical slices. Biochem. Pharmacol. 41:119–123.

    Google Scholar 

  12. Gonzalez, M. P., Oset-Gasque, M. J., Castro, E., Bugeda, J., Arce, C., and Parramon, M. 1992. Mechanism through which GABAA receptor modulates catecholamine secretion from bovine chromaffin cells. Neurosci. 47:487–494.

    Google Scholar 

  13. Hu, P. S., Jin, S., and Fredholm, B. B. 1992. Glycine and GABA potentiate 4-aminopyridine and/or N-methyl-D-aspartate induced [3H]-noradrenaline release from rat hippocampal slices. Acta Physiol. Scand. 145:77–78.

    Google Scholar 

  14. Fiber, J. M. and Etgen, A. M. 1997. GABA augments basal and electrically stimulated 3H-norepinephrine release in hypothalamic, preoptic area and cortical slices of female rats. Neurochem. Int. 31:769–780.

    Google Scholar 

  15. Fiber, J. M. and Etgen, A. M. 1998. Evidence that GABA augmentation of norepinephrine release is mediated by interneurons. Brain Res. 790:329–333.

    Google Scholar 

  16. Hagan, R. M. and Hughes, I. E. 1984. Opioid receptor sub-types involved in the control of transmitter release in cortex of the brain of the rat. Neuropharmacol. 23:491–495.

    Google Scholar 

  17. Werling, L. L., Brown, S. R., and Cox, B. M. 1987. Opioid receptor regulation of the release of norepinephrine in brain. Neuropharmacol. 26:987–996.

    Google Scholar 

  18. Peoples, R. W., Giridhar, J., and Isom, G. E. 1991. Gammaaminobutyric acidA (GABAA) receptor modulation of morphine inhibition of norepinephrine release. Biochem. Pharmacol. 42 Suppl:121–126.

    Google Scholar 

  19. Ebstein, R. P. and Daly, J. W. 1982. Release of norepinephrine and dopamine from brain vesicular preparations: effects of adenosine analogues. Cell. Mol. Neurobiol. 2:193–204.

    Google Scholar 

  20. Allgaier, C., Greber, R., and Hertting, G. 1991. Studies on the interaction between presynaptic alpha 2-adrenoceptors and adenosine A1 receptors located on noradrenergic nerve terminals. Naunyn Schmiedebergs Arch. Pharmacol. 344:187–192.

    Google Scholar 

  21. von Kugelgen, I., Spath, L., and Starke, K. 1992. Stable adenine nucleotides inhibit [3H]-noradrenaline release in rabbit brain cortex slices by direct action at presynaptic adenosine A1-receptors. Naunyn Schmiedebergs Arch. Pharmacol. 346:187–196.

    Google Scholar 

  22. von Kugelgen, I., Spath, L., and Starke, K. 1994. Evidence for P2-purinoceptor-mediated inhibition of noradrenaline release in rat brain cortex. Br. J. Pharmacol. 113:815–822.

    Google Scholar 

  23. Koch, H., Kugelgen, I., and Starke, K. 1997. P2-receptor-mediated inhibition of noradrenaline release in the rat hippocampus. Naunyn Schmiedebergs Arch. Pharmacol. 355:707–715.

    Google Scholar 

  24. Daschmann, B., Allgaier, C., Nakov, R., and Hertting, G. 1988. Staurosporine counteracts the phorbol ester-induced enhancement of neurotransmitter release in hippocampus. Arch. Int. Pharmacodyn. Ther. 296:232–245.

    Google Scholar 

  25. Dekker, L. V., De Graan, P. N., Pijnappel, P., Oestreicher, A. B., and Gispen, W. H. 1991. Noradrenaline release from streptolysin O-permeated rat cortical synaptosomes: effects of calcium, phorbol esters, protein kinase inhibitors, and antibodies to the neuron-specific protein kinase C substrate B-50 (GAP-43). J. Neurochem. 56:1146–1153.

    Google Scholar 

  26. Wang, H. Y. and Friedman, E. 1987. Protein kinase C: regulation of serotonin release from rat brain cortical slices. Eur. J. Pharmacol. 141:15–21.

    Google Scholar 

  27. Tsuda, K. and Masuyama, Y. 1990. The role of protein kinase C and calcium in the regulation of norepinephrine release from the vascular adrenergic neurons in hypertension. Am. J. Hypertens. 3:879–882.

    Google Scholar 

  28. Gillette, M. A. and Dacheux, R. F. 1996. Protein kinase modulation of GABAA currents in rabbit retinal rod bipolar cells. J. Neurophysiol. 76:3070–3086.

    Google Scholar 

  29. Hu, H. Z. and Li, Z. W. 1997. Modulation of nicotinic ACh-, GABAA-and 5-HT3-receptor functions by external H-7, a protein kinase inhibitor, in rat sensory neurones. Br. J. Pharmacol. 122:1195–1201.

    Google Scholar 

  30. Beckman, M. L., Bernstein, E. M., and Quick, M. W. 1998. Protein kinase C regulates the interaction between a GABA transporter and syntaxin 1A. J. Neurosci. 18:6103–6112.

    Google Scholar 

  31. Stevens, C. F. and Sullivan, J. M. 1998. Regulation of the readily releasable vesicle pool by protein kinase C. Neuron 21:885–893.

    Google Scholar 

  32. Fiber, J. M. and Etgen, A. M. 1998. GABA-augmented 3H-norepinephrine release is modulated by opioids in brain slices from female rats. Soc. Neurosci. Abstr. 24:824.16.

    Google Scholar 

  33. Yamamoto, C. 1972. Activation of hippocampal neurons by mossy fiber stimulation in thin brain sections in vitro. Exp. Brain Res. 14:423–435.

    Google Scholar 

  34. Karkanias, G. B. and Etgen, A. M. 1993. Estradiol attenuates α2-adrenoceptor-mediated inhibition of hypothalamic norepinephrine release. J. Neurosci. 13:3448–3455.

    Google Scholar 

  35. Petitti, N. and Etgen, A. M. 1989. Progesterone depression of norepinephrine-stimulated cAMP accumulation in hypothalamic slices. Brain Res. Mol. Brain Res. 5:109–119.

    Google Scholar 

  36. Diez-Guerra, F. J., Augood, S., Emson, P. C., and Dyer, R. G. 1987. Opioid peptides inhibit the release of noradrenaline from slices of rat medial preoptic area. Exp. Brain Res. 66:378–384.

    Google Scholar 

  37. Bonanno, G. and Raiteri, M. 1987. A carrier for GABA uptake exists on noradrenaline nerve endings in selective rat brain areas but not on serotonin terminals. J. Neural Transm. 69:59–70.

    Google Scholar 

  38. Przewlocka, B., Lason, W., and Dziedzicka, M. 1990. Modulation of prodynorphin peptides release from the rat spinal cord in vitro. Neuropeptides 16:201–206.

    Google Scholar 

  39. Mulder, A. H., Hogenboom, F., Wardeh, G., and Schoffelmeer, A. N. 1987. Morphine and enkephalins potently inhibit [3H]noradrenaline release from rat brain cortex synaptosomes: further evidence for a presynaptic localization of mu-opioid receptors. J. Neurochem. 48:1043–1047.

    Google Scholar 

  40. Trendelenburg, A. U., Cox, S. L., Schelb, V., Klebroff, W., Khairallah, L., and Starke, K. 2000. Modulation of (3)H-noradrenaline release by presynaptic opioid, cannabinoid and bradykinin receptors and β-adrenoceptors in mouse tissues. Br. J. Pharmacol. 130:321–330.

    Google Scholar 

  41. Vathy, I. and Etgen, A. M. 1996. Effects of prenatal morphine and adult estrogen administration on μ-opioid inhibition of norepinephrine release from hypothalamic slices. Neuroendocrinol. 63:61–68.

    Google Scholar 

  42. Leahy, J. C. and Vallano, M. L. 1991. Differential effects of isoquinolinesulfonamide protein kinase inhibitors on CA1 responses in hippocampal slices. Neurosci. 44:361–370.

    Google Scholar 

  43. Corradetti, R., Pugliese, A. M., and Ropert, N. 1989. The protein kinase C inhibitor 1-(5-isoquinolinesulphonyl)-2-methylpiperazine (H-7) disinhibits CA1 pyramidal cells in rat hippocampal slices. Br. J. Pharmacol. 98:1376–1382.

    Google Scholar 

  44. Majewski, H., Kotsonis, P., Iannazzo, L., Murphy, T. V., and Musgrave, I. F. 1997. Protein kinase C and transmitter release. Clin. Exp. Pharmacol. Physiol. 24:619–623.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fiber, J.M., Etgen, A.M. Modulation of GABA-Augmented Norepinephrine Release in Female Rat Brain Slices by Opioids and Adenosine. Neurochem Res 26, 853–858 (2001). https://doi.org/10.1023/A:1011676505575

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1011676505575

Navigation