Regulation of NMDA-induced [3H] dopamine release from rat hippocampal slices through sigma-1 binding sites

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Abstract

To examine the interaction between ionotropic glutamate receptors and s binding sites, we made use of [3H] dopamine release from rat hippocampal slices. Agonists for ionotropic glutamate receptors such as N-methyl-D-aspartate (NMDA), α-amino-3-hydroxy-5-methyl-4-isoxazolepropionate (AMPA) and kainate evoked release of [3H] dopamine from rat hippocampal slices, in a dose-dependent manner. (+ )-Pentazocine, a prototype s1 agonist, attenuated the NMDA-induced [3H] dopamine release dose-dependently and significantly as did non-competitive NMDA antagonists such as 5-methyl-10,11-dihydro-5H-dibe-nzo(a,b)cyclohepten-5,10-imine maleate (MK-801) and phencyclidine. In contrast, (+)-pentazocine had no effect on AMPA- or on kainate-induced [3H] dopamine release. Sigma-l receptor antagonists including N,N-dipropyl-2- 4-methoxy-3-(2-phen-ylethoxy)phenyl ethylamine monohydrochloride (NE-100), 1(cyclopropylmethyl)-4-(2’-(4”fluorophenyl)-2’-oxoethylpiperidine (DuP734) and 1-(cyclopropylmethyl)-4-(2’,4” -cianophenyl)-2’-oxoethyl)-piperidine hydrobromide (XJ448) prevented significantly the inhibitory effect of (+)-pentazocine on NMDA-induced [3H] dopamine release, without affecting the release of [3H] dopamine evoked by NMDA. The inhibitory effect of (+)-pentazocine on [3H] dopamine release was preserved even in the presence of tetrodotoxin. These results suggest that s1 binding sites selectively interact with the NMDA receptor channel complex among ionotropic glutamate receptors, and that s1 binding sites may be involved in modulating the release of dopamine in the rat hippocampus by interacting with the NMDA receptor on dopaminergic nerve terminal. © 1998 Elsevier Science Ltd. All rights reserved.

Introduction

The σ binding sites, originally identified as opiate binding sites, are involved in the action of some neuroleptics (Snyder and Largent, 1989) . The physiological function of σ binding sites and intracellular mechanisms responsible for the pharmacological effects of σ receptor ligands have remained to be determined.

Selective σ ligands have been reported to modulate the N-methyl-d-aspartate (NMDA) response, in vitro and in vivo. Monnet et al. (1990)Monnet et al. 1992aMonnet et al. 1992breported that σ ligands modulate NMDA-induced neuronal activation of CA3 pyramidal neurons and the release of [3H] norepinephrine from hippocampal slices. Sigma ligands have also been found to modulate NMDA-induced intracellular messengers such as cyclic guaninemonophosphate (cGMP) (Ferris et al., 1991) , arachidonic acid (Starr and Werling, 1994) and intracellular Ca2 concentration (Hayashi et al., 1995) . Sigma-1 ligands inhibited [3H] N- [1- (2-thienyl ) cyclohexyl] piperidine (TCP) binding to primary cultured neuronal cells, while σ1 ligands had no apparent effect on [3H] TCP binding to membrane preparations (Yamamoto et al., 1995aYamamoto et al. 1995b) . Moreover, σ1 ligands modulate the MK-801-induced hyperlocomotion in monoamine-depleted mice (Okuyama et al., 1996) . These findings suggest that σ1 binding sites may interact with the NMDA receptor channel complex even though the σ1 binding sites are not the NMDA receptor channel complex itself.

Glutamatergic dysfunction is likely to be involved in the etiology of schizophrenia as well as in dopaminergic hyperactivity (Creese et al., 1976; Toru et al., 1994) . Interactions of σ binding sites with other ionotropic glutamate receptors such as AMPA and kainate have not been fully studied.

We attempted to elucidate the possible involvement of σ binding sites in the regulation by the ionotropic glutamate receptor of the activity of dopaminergic neurons assessing [3H] dopamine release from rat hippocampal slices.

Section snippets

Materials

Male Wistar strain rats, weighing 180–250 g, were used. [3H] Dopamine (S.A. 1.70 and 1.85 TBq\mmol ) was purchased from Amersham, U.K. NMDA and kainate were purchased from Sigma Chemical Co. (St Louis, MO., USA) . α-amino-3-hydroxy-5-methyl-4-isoxazolepropionate (AMPA) was purchased from Research Biochemicals Incorporated (Natick, MA, USA) . N,N-dipropyl-2- [4-methoxy-3- (2-phenylethoxy) phenyl] ethylamine monohydrochloride (NE-100) , 1 (cyclop r o p y l m e t h y l ) -4- (2′- (4″-f l u o r o p

Ionotropic glutamate receptor agonists-induced [3H] dopamine release from rat hippocampal slices

To compare the potency of agonists for ionotropic glutamate receptors in releasing [3H] dopamine from rat hippocampal slices, S1 was determined based on the stimulation induced by 30 μM NMDA and S2 was determined by stimulation of different concentrations of each agonist. NMDA (3–300 μM) , kainate (3–300 μM) or AMPA (3–300 μM) dose-dependently evoked the release of [3H] dopamine from rat hippocampal slices (Fig. 1A) . Among the ionotropic glutamate receptor agonists tested, NMDA was the most

Discussion

We obtained evidence that σ1 ligands modulate the NMDA-induced [3H] dopamine release from rat hippocampal slices.

(+) -Pentazocine, a prototype of the σ1 receptor agonist, inhibited the [3H] dopamine release from rat hippocampal slices elicited by NMDA, while [3H] dopamine release elicited by either AMPA or kainate was not affected. This inhibitory effect of (+) -pentazocine on the NMDA-induced [3H] dopamine release was prevented by σ1 receptor antagonists such as NE-100, DuP734 and XJ448. Thus,

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