Summary
The regulation of striatonigral and striatopallidal GABAergic neurons by glutamatergic afferents is thought to play a critical role in normal basal ganglia function. Here we report that in striatal slices about 17% of K+-induced endogenous GABA release was Ca2+-independent and this could be blocked by a GABA transport inhibitor. Activation of N-methyl-D-aspartate (NMDA)- and quisqualate-sensitive receptors induced endogenous GABA efflux only in the presence of a GABA transaminase inhibitor; this efflux was inhibited by 60–80% with a GABA transport inhibiter. NMDA-induced GABA release was blocked by phencyclidine, Mg2+ and CGS 19755. Quisqualate-induced GABA release was blocked completely by a combination of the metabotropic antagonist, L-AP3 and CNQX, a non-NMDA receptor antagonist. These data indicate that excitatory amino acid agonists-induced GABA release is distinct from that induced by high K+ depolarization.
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Bonanno G, Pittaluga A, Fedele E, Fontana G, Raiteri M (1993) Glutamic acid and γ- aminobutytric acid modulate each other's release through heterocarriers sited on the axon terminals of rat brain. J Neurochem 61: 222–230
Burke SP, Hablitz JJ (1994) Presynaptic depression of synaptic transmission mediated by activation of metabotropic glutamate receptors in rat neocortex. J Neurosci 14: 5120–5130
Choi DW (1988) Glutamate neurotoxicity and diseases of the nervous system. Neuron 1: 623–634
Clow DW, Jhamandas K (1989) Characterization of L-glutamate action on the release of endogenous dopamine from the rat caudate-putamen. J Pharmacol Exp Ther 248: 722–728
Davies CH, Starkey SJ, Pozza MF, Collingridge GL (1991) GABAB autoreceptors regulate the induction of LTP. Nature 349: 609–611
De Montigny P, Stobaugh JF, Givens RS, Carlson RG, Srinivasachar K, Sternson LA, Higuchi T (1987) Naphthalene-2,3-dicarboxaldehyde/cyanide ion: a rationally designed fluorogenic reagent for primary amines. Anal Chem 59: 1096–1101
Di Chiara G, Morelli M, Consolo S (1994) Modulatory functions of neurotransmitters in the striatum: ACh/dopamine/NMDA interactions. Trends Neurosci 17: 228–233
Drejer J, Honore T (1987) Phencyclidine analogues inhibit NMDA-stimulated [3H]GABA release from cultured cortex neurons. Eur J Pharmacol 143: 287–290
Duarte CB, Ferreira IL, Santos PF, Oliveira CR, Carvalho AP (1993) Glutamate increases the [Ca2+]i but stimulates Ca2+-independent release of [3H]GABA in cultured chick retina cells. Brain Res 611: 130–138
Girault JA, Spampinato U, Savaki HE, Glowinski SJ, Besson MJ (1986) In vivo release of [3H] τ-aminobutyric acid in the rat neostriatum. I. Characterization and topographical heterogeneity of the effects of dopaminergic and cholinergic agents. Neurosci 19: 1101–1108
Gram L (1988) Experimental studies and controlled clinical testing of valproate and vigabatrin. Acta Neurol Scand 78: 241–270
Graybiel AM (1990) Neurotransmitters and neuromodulators in the basal ganglia. Trends Neurosci 13: 244–254
Graybiel AM, Ragsdale CW (1983) Biochemical anatomy of the striatum. In: Emson PC (eds) Chemical neuroanatomy, 1st edn. Raven Press, New York, pp 427–504
Hammond EJ, Wilder BJ (1985) Gamma-vinyl GABA. Gen Pharmacol 16: 441–447
Harris KM, Miller RJ (1989) Excitatory amino acid-evoked release of [3H]GABA from hippocampal neurons in primary culture. Brain Res 482: 23–33
Jaffe EH, Cuello AC (1980) Release of τ-aminobutyric acid from the external plexiform layer of the rat olfactory bulb: possible dendritic involvement. Neuroscience 5: 1859–1869
Jahr CE, Nicoll RA (1980) Dendrodendritic inhibition: demonstration with intracellular recording. Science 207: 1473–1475
Janáky R, Saransaari P, Oja SS (1993) Release of GABA from rat hippocampal slices: involvement of quisqualate/N-methyl-D-aspartate-gated ionophores and extracellular magnesium. Neuroscience 53: 779–785
Johansen FF, Diemer NH (1991) Enhancement of GABA neurotransmission after cerebral ischemia in the rat reduces loss of hippocampal CA1 pyramidal cells. Acta Neurol Scand 84: 1–6
Johnson KM, Jeng YJ (1991) Pharmacological evidence for N-methyl-D-aspartate receptors on nigrostriatal dopaminergic nerve terminals. Can J Physiol Pharmacol 69: 1416–1421
Johnson KM, Jones SM (1990) Neuropharmacology of phencyclidine: basic mechanisms and therapeutic potential. Annu Rev Pharmacol Toxicol 30: 707–750
Jung MJ, Lippert B, Metcalf BW, Bohlen P, Schlechter PJ (1977) Gamma-vinyl GABA (4-amino-hex-5-enoic acid), a new selective irreversible inhibitor of GABA-T: effects on brain GABA metabolism in mice. J Neurochem 29: 787–802
Lehamann J, Scatton B (1982) Characterization of the excitatory amino acid receptor-mediated release of [3H]-acetylcholine from rat striatal slices. Brain Res 252: 77–89
Levi G, Raiteri M (1993) Carrier-mediated release of neurotransmitters. Trends Neurosci 16: 415–420
Lipton SA (1992) Models of neuronal injury in AIDS: another role for the NMDA receptor? Trends Neurosci 15: 75–79
Marchi M, Sanguineti P, Raiteri M (1990) Muscarinic receptors mediate direct inhibition of GABA release from rat striatal nerve terminals. Neurosci Lett 116: 347–351
Meldrum B, Garthwaite J (1990) Excitatory amino acid neurotoxicity and neurodegenerative disease. Trends Pharmacol Sci 11: 379–387
Mudrick LA, Heinemann U (1990) Quisqualate-induced changes in extracellular sodium and calcium concentrations persist in the combined presence of NMDA and non- NMDA receptor antagonists in rat hippocampus slices. Neurosci Lett 116: 172–178
Pin J-P, Bockaert J (1989) Two distinct mechanisms, differentially affected by excitatory amino acids, trigger GABA release from fetal mouse striatal neurons in primary culture. J Neurosci 9: 648–656
Salt TE, Eaton SA (1995) Distinct presynaptic metabotropic receptors for L-AP4 and CCG1 on gabaergic terminals: pharmacological evidence using novel α-methyl derivative mGluR antagonists, MAP4 and MCCG, in the rat thalamus in vivo. Neuroscience 65: 5–13
Schoepp DD, Conn PJ (1993) Metabotropic glutamate receptors in brain function and pathology. Trends Pharmacol Sci 14: 13–20
Shuaib A, Ijaz S, Hasan S, Kalra J (1992) Gamma-vinyl GABA prevents hippocampal and substantia nigra reticulata damage in repetitive transient forebrain ischemia. Brain Res 590: 13–17
Snell LD, Johnson KM (1986) Characterization of the inhibition of excitatory amino acid-induced neurotransmitter release in the rat striatum by phencyclidine-like drugs. J Pharmacol Exp Ther 238: 938–946
Sugita S, Uchimura N, Jiang ZG, North RA (1991) Distinct muscarinic receptors inhibit release of τ-aminobutyric acid and excitatory amino acids in mammalian brain. Proc Natl Acad Sci USA 88: 2608–2611
Suzdak PD, Frederiksen K, Andersen KE, Sorensen PO, Knutsen LJS, Nielsen EB (1992) NNC-711, a novel potent and selective gamma-aminobutyric acid uptake inhibitor: pharmacological characterization. Eur J Pharmacol 224: 189–198
Tihon C, Goren MB, Spitz E, Rickenberg HV (1977) Convenient elimination of trichloroacetic acid prior to radioimmunoassay of cyclic nucleotides. Anal Biochem 80: 652–653
Watkins JC, Krogsgarrd-Larsen P, Honore T (1990) Structure-activity relationships in the development of excitatory amino acid receptor agonists and competitve antagonists. Trends Pharmacol Sci 11: 25–33
Weiss S (1988) Excitatory amino acid-evoked release of γ-[3H] aminobutyric acid from striatal neurons in primary culture. J Neurochem 51: 435–441
Williams S, Lacaille JC (1992) GABAB receptor-mediated inhibitory postsynaptic potentials evoked by electrical stimulation and by glutamate stimulation of interneurons in stratum lacunosum-moleculare in hippocampal CA1 pyramidal cells in vitro. Synapse 11: 249–258
Wong EHF, Kemp JA (1991) Sites for antagonism on the N-methyl-D-aspartate receptor channel complex. Annu Rev Pharmacol Toxicol 31: 401–425
Yazulla S, Kleinschmidt J (1983) Carrier-mediated release of GABA from retinal horizontal cells. Brain Res 263: 63–75
Young AMJ, Bradford HF (1993) N-methyl-D-aspartate releases gamma-aminobutyric acid from rat striatum in vivo: a microdialysis study using a novel preloading method. J Neurochem 60: 487–492
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Wang, J., Lonart, G. & Johnson, K.M. Glutamate receptor activation induces carrier mediated release of endogenous GABA from rat striatal slices. J. Neural Transmission 103, 31–43 (1996). https://doi.org/10.1007/BF01292614
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DOI: https://doi.org/10.1007/BF01292614