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A functional response to D1 dopamine receptor stimulation in the central nervous system: inhibition of the release of [3H]-serotonin from the rat substantia nigra

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Summary

The influence of dopamine receptor agonists on the calcium dependent electrically-evoked release of [3H]-serotonin was studied in the superfused rat substantia nigra. The electrically-evoked overflow of [3H]-serotonin was significantly inhibited by micromolar concentrations of exogenous dopamine and of the D1-selective dopamine receptor agonists, fenoldopam and SKF 38393. The inhibitory effects of dopamine and fenoldopam on [3H]-serotonin release were antagonized by the D1-selective dopamine receptor antagonist SCH 23390. S-sulpiride, an antagonist of D2 receptors failed to antagonize the inhibitory effects of dopamine on [3H]-serotonin release. Moreover, quinperol, the selective D2 receptor agonist did not modify the electrically-evoked release of [3H]-serotonin. In the presence of nomifensine, SCH 23390 but not S-sulpiride enhanced in a concentration dependent manner the electrically-evoked release of [3H]-serotonin. Under similar experimental conditions, exposure to fenoldopam did not inhibit the electrically-evoked release of [3H]-serotonin from rat hippocampal or hypothalamic slices. These results indicate that, in rat substantia nigra, exogenous as well as endogenous dopamine causes inhibition of serotonin release by activation of dopamine receptors of the D1-subtype.

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References

  • Adler-Graschinsky E, Langer SZ (1975) Possible role of a β-adrenoceptor in the regulation of noradrenaline release by nerve stimulation. Br J Pharmacol 53:43–50

    Google Scholar 

  • Arbilla S, Langer SZ (1980) Influence of monoamine oxidase inhibition on the release of [3H]dopamine elicited by potassium and by amphetamine from the rat substantia nigra and corpus striatum. Naunyn-Schmiedeberg's Arch Pharmacol 311:45–52

    Google Scholar 

  • Arbilla S, Langer SZ (1981) Stereoselectivity of presynaptic autoreceptors modulating dopamine release. Eur J Pharmacol 76:345–351

    Google Scholar 

  • Arbilla S, Kamal LA, Langer SZ (1979) Presynaptic GABA autoreceptors on gabaergic nerve endings of the rat substantia nigra. Eur J Pharmacol 57:211–217

    Google Scholar 

  • Arbilla S, Kamal LA, Langer SZ (1981) Inhibition by apomorphine of the potassium-evoked release of [3H]-γ-aminobutyric acid from the rat substantia nigra in vitro. Br J Pharmacol 74:389–397

    Google Scholar 

  • Arbilla S, Benkirane S, Langer SZ (1986) Activation of D1 dopamine receptors inhibits the evoked release of [3H]-serotonin in the rat substantia nigra. Br J Pharmacol 89: 793P

  • Aronin N, Difiglia M, Graveland GA, Schwartz WJ, Wu JY (1984) Localization of immunoreactive enkephalins in GABA synthesizing neurons of the rat neostriatum. Brain Res 300:376–380

    Google Scholar 

  • Baud P, Arbilla S, Langer SZ (1985) Inhibition of the electrically evoked release of [3H]acetylcholine in rat striatal slices: an experimental model for drugs that enhance dopaminergic neurotransmission. J Neurochem 44:331–337

    Google Scholar 

  • Benkirane S, Arbilla S, Langer SZ (1985) Supersensitivity of α2-adrenoceptors modulating [3H]-5HT release after noradrenergic denervation with DSP4. Eur J Pharmacol 119:131–133

    Google Scholar 

  • Benkirane S, Arbilla S, Langer SZ (1986) Newly synthesized noradrenaline mediates the α2-adrenoceptor inhibition of [3H]-5-hydroxytryptamine release induced by β-phenylethylamine in rat hippocampal slices. Eur J Pharmacol 131:189–198

    Google Scholar 

  • Celuch SM, Dubocovich ML, Langer SZ (1978) Stimulation of presynaptic β-adrenoceptors enhances [3H]-noradrenaline release during nerve stimulation in the perfused cat spleen. Br J Pharmacol 63:97–109

    Google Scholar 

  • Cubbedu LX, Hoffmann IS, James MK (1983) Frequency-dependent effects of neuronal uptake inhibitors on the autoreceptor-mediated modulation of dopamine and acetylcholine release from the rabbit striatum. J Pharmacol Exp Ther 226:88–94

    Google Scholar 

  • Dawson TM, Gehlert DR, Yamamura HI, Barnett A, Wamsley JK (1985) D-1 dopamine receptors in the rat brain: Autoradiographic localization using [3H]SCH 23390. Eur J Pharmacol 108:323–325

    Google Scholar 

  • Doxey JC, Lane AC, Roach AG, Virdee NK (1984) Comparison of the α-adrenoceptor antagonist profiles of idazoxan (RX 781094), yohimbine, rauwolseine and corynanthine. Naunyn-Schmiedeberg's Arch Pharmacol 325:136–144

    Google Scholar 

  • Dray A, Gonye TJ, Oakley NR, Tanner T (1976) Evidence for the existence of a raphe projection to the rat substantia nigra in rat. Brain Res 113:45–57

    Google Scholar 

  • Dubocovich ML, Langer SZ (1980) Dopamine and α-adrenoceptor agonists inhibit neurotransmission in the cat spleen through different presynaptic receptors. J Pharmacol Exp Ther 212: 144–152

    Google Scholar 

  • Feuerstein TJ, Hertting G, Lupp A, Neufang B (1986) False labelling of dopaminergic terminals in the rabbit caudate nucleus: uptake and release of [3H]-5-hydroxytryptamine. Br J Pharmacol 88:677–684

    Google Scholar 

  • Fonnum F, Grofova I, Rinvik E, Storn-Mathisen J, Walker F (1974) Origin and distribution of glutamate decarboxylase in substantia nigra of the cat. Brain Res 71:77–92

    Google Scholar 

  • Gale K, Guidotti A, Costa E (1977) Dopamine sensitive adenylate cyclase: location in substantia nigra. Science 195:503–505

    Google Scholar 

  • Galzin AM, Dubocovich ML, Langer SZ (1982) Presynaptic inhibition by dopamine receptor agonists of noradrenergic neurotransmission in the rabbit hypothalamus. J Pharmacol Exp Ther 221:461–471

    Google Scholar 

  • Galzin AM, Moret C, Langer SZ (1984) Evidence that exogenous but not endogenous norepinephrine activates the presynaptic alpha-2 adrenoceptors on serotonergic nerve endings in the rat hypothalamus. J Pharmacol Exp Ther 228:725–732

    Google Scholar 

  • Geffen LB, Jessell TM, Cuello AC, Iversen LL (1978) Release of dopamine from dendrites in rat substantia nigra. Nature 260:258–260

    Google Scholar 

  • Göthert M (1980) Serotonin-receptor-mediated modulating of Ca2+-dependent 5-hydroxytryptamine release from neurons of the rat brain cortex. Naunyn-Schmiedeberg's Arch Pharmacol 314:223–230

    Google Scholar 

  • Göthert M (1982) Modulation of serotonin release in the brain via presynaptic receptors. Tr Pharmacol Sci 11:437–440

    Google Scholar 

  • Hahn RA, Wardell JR, Sarau HW, Ridley PT (1982) Characterization of the peripheral and central effects of SK & F 82526, a novel dopamine receptor agonist. J Pharmacol Exp Ther 223:305–313

    Google Scholar 

  • Hentrich F, Göthert M, Greschuchna D (1985) Involvement of cAMP in modulation of noradrenaline release in the human pulmonary artery. Naunyn-Schmiedeberg's Arch Pharmacol 330:245–247

    Google Scholar 

  • Hertting G, Zumstein A, Jackisch R, Hoffmann I, Starke K (1980) Modulation by endogenous dopamine of the release of acetylcholine in the caudate nucleus of the rabbit. Naunyn-Schmiedeberg's Arch Pharmacol 315:111–117

    Google Scholar 

  • Hicks S, Schoemaker H, Langer SZ (1984) 5HT-receptor antagonist properties of SCH 23390 in vascular smooth muscle and brain. Eur J Pharmacol 105:339–342

    Google Scholar 

  • Hoyer D, Engel G, Kalkman HO (1985) Characterization of the 5HT recognition site in the rat brain: Binding studies with (−)-I125-iodocyanopindolol. Eur J Pharmacol 118:13–23

    Google Scholar 

  • Iorio LC, Barnett A, Leitz FJ, Houser VP, Korduba CA (1983) SCH 23390, a potential benzazepine antipsychotic with unique interaction on dopaminergic systems. J Pharmacol Exp Ther 226:462–468

    Google Scholar 

  • Jakobs KM, Aktories K, Schultz G (1981) Inhibition of adenylate cyclase by hormones and neurotransmitters. Adv Cyclic Nucleotides 14:173–187

    Google Scholar 

  • Kanazawa I, Emson PC, Cuello AC (1977) Evidence for the existence of substance P-containing fibres in striato-nigral and pallido-nigral pathways in the rat brain. Brain Res 119:447–453

    Google Scholar 

  • Kebabian J, Calne DB (1979) Multiple receptors for dopamine. Nature 277:93–96

    Google Scholar 

  • Langer SZ (1981) Presynaptic regulation of the release of catecholamines. Pharmacol Rev 32:337–362

    Google Scholar 

  • Langer SZ, Moret C (1982) Citalopram antagonizes the stimulation by lysergic acid diethylamide of presynaptic inhibitory autoreceptors in the rat hypothalamus. J Pharmacol Exp Ther 222:220–226

    Google Scholar 

  • Napier TC, Givens BS, Schultz DW, Bunney BS, Bresse GR, Mailman RB (1986) SCH 23390 effects on apomorphine-induced responses of nigral dopaminergic neurons. J Pharmacol Exp Ther 236:838–845

    Google Scholar 

  • Nieoullon A, Cheramy A, Glowinski J (1977) Release of dopamine in vivo from cat substantia nigra. Nature 266:375–377

    Google Scholar 

  • Onali P, Olianas MC, Gessa GL (1984) Selective blockade of dopamine D-1 receptors by SCH 23390 discloses striatal dopamine D-2 receptors mediating the inhibition of adenylate cyclase in rat. Eur J Pharmacol 99:127–128

    Google Scholar 

  • Parent A, Descarries L, Beaudet A (1985) Organization of ascending serotonin systems in the adult rat brain. A radioautographic study after intraventricular administration of [3H]-hydroxytryptamine. Neuroscience 6:115–138

    Google Scholar 

  • Pelayo F, Dubocovich ML, Langer SZ (1978) Possible role of cyclic nucleotides in regulation of noradrenaline release from rat pineal through presynaptic adrenoceptors. Nature 274:76–78

    Google Scholar 

  • Phillipson OT, Horn AS (1976) Substantia nigra of the rat contains a dopamine sensitive adenylate cyclase. Nature 261:418–420

    Google Scholar 

  • Phillipson OT, Emson PC, Horn AS, Jessel T (1977) Evidence concerning the anatomical location of the dopamine stimulated adenylate cyclase in the substantia nigra. Brain Res 136: 45–58

    Google Scholar 

  • Quik M, Emson PC, Joyce E (1979) Dissociation between the presynaptic dopamine-sensitive adenylate cyclase and [3H]spiperone binding in rat substantia nigra. Brain Res 167:355–365

    Google Scholar 

  • Schlicker E, Göthert M, Hillenbrand K (1985) Cyanopindolol is a highly potent and selective antagonist at the presynaptic serotonin autoreceptor in the rat brain cortex. Naunyn-Schmiedeberg's Arch Pharmacol 331:298–301

    Google Scholar 

  • 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 slices. J Neurochem 46:1711–1717

    Google Scholar 

  • Seder PE, Saran HM, Zirkle CL, Saunders HL (1978) The central effects of a novel dopamine agonist. Eur J Pharmacol 50: 419–430

    Google Scholar 

  • Spano PF, DiChiara G, Trabucchi M (1976) A dopamine sensitive adenylate cyclase in rat substantia nigra. J Neurochem 27: 1565–1568

    Google Scholar 

  • Stiles GL, Caron MG, Lefkowitz RJ (1984) β-Adrenergic receptors: biochemical mechanisms of physiological regulation. Physiol Rev 64:661–743

    Google Scholar 

  • Stoof JC, Kebabian J (1981) Opposing roles for D1 and D2 dopamine receptors in efflux of cyclic AMP from rat striatum. Nature 294:366–368

    Google Scholar 

  • Stoof JC, Kebabian J (1984) Two dopamine receptors: Biochemistry, physiology and pharmacology. Life Sci 35:2281–2296

    Google Scholar 

  • Tsuruta K, Frey EA, Grewe CW, Cote TE, Eskay RL, Kebabian JW (1981) Evidence that LY 141865 specifically stimulates the D-2 dopamine receptor. Nature 292:463–465

    Google Scholar 

  • U'Prichard DC, Mitrius JC, Kahn DJ, Perry BD (1983) The α2-adrenergic receptor: multiple affinity states and regulation of a receptor inversely coupled to adenylate cyclase. Biochem Psychopharmacology 36:53–72

    Google Scholar 

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Authors and Affiliations

  1. Department of Biology, Laboratoires d'Etudes et de Recherches Synthelabo (L.E.R.S), 58, rue de la Glacière, F-75013, Paris, France

    Sanaa Benkirane, Sonia Arbilla & Salomon Z. Langer

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  1. Sanaa Benkirane
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  2. Sonia Arbilla
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  3. Salomon Z. Langer
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Preliminary results of this publication have been presented to the British Pharmacological Society (Arbilla et al. 1986)

Send offprint requests to S. Z. Langer at the above address

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Benkirane, S., Arbilla, S. & Langer, S.Z. A functional response to D1 dopamine receptor stimulation in the central nervous system: inhibition of the release of [3H]-serotonin from the rat substantia nigra. Naunyn-Schmiedeberg's Arch Pharmacol 335, 502–507 (1987). https://doi.org/10.1007/BF00169115

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  • DOI: https://doi.org/10.1007/BF00169115

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