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Unexpected inhibitory regulation of glutamate release from rat cerebrocortical nerve terminals by presynaptic 5-hydroxytryptamine-2A receptors

✍ Scribed by Su-Jane Wang; Kai-Yun Wang; Wei-Chieh Wang; Talvinder S. Sihra


Publisher
John Wiley and Sons
Year
2006
Tongue
English
Weight
459 KB
Volume
84
Category
Article
ISSN
0360-4012

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✦ Synopsis


Abstract

Presynaptic 5‐HT~2A~ receptor modulation of glutamate release from rat cerebrocortical nerve terminals (synaptosomes) was investigated by using the 5‐HT~2A/2C~ receptor agonist (±)‐1‐[2,5‐dimethoxy‐4‐iodophenyl]‐2‐aminopropane (DOI). DOI potently inhibited 4‐aminopyridine (4AP)‐evoked glutamate release. Involvement of presynaptic 5‐HT~2A~ receptors in this modulation of 4AP‐evoked release was confirmed by blockade of the DOI‐mediated inhibition by the 5‐HT~2A~ receptor antagonist ketanserin but not by the 5‐HT~2C~ receptor antagonist RS102221. Inhibition of glutamate release by DOI was associated with a reduction of 4AP‐evoked depolarization and downstream elevation of cytoplasmic free calcium concentration ([Ca^2+^]~C~) mediated via P/Q‐ and N‐type voltage‐dependent Ca^2+^ channels (VDCCs). In contrast to the DOI effect on 4AP‐evoked release, the agonist had no effect on high external [K^+^] (30 mM)‐induced (KCl) stimulation of VDCCs or glutamate release. Likewise, release mediated by direct Ca^2+^ entry with Ca^2+^ ionophore (ionomycin) or by hypertonic sucrose was unaffected by DOI. Mechanistically, DOI modulation of 4AP‐evoked glutamate release appeared to involve a phospholipase C/protein kinase C signaling cascade, insofar as pretreatment of synaptosomes with the phospholipase C inhibitor U73122 or protein kinase C inhibitors Ro320432 or GF109203X all effectively occluded the inhibitory effect of the agonist. Together, these results suggest that presynaptic 5‐HT~2A~ receptors present on glutamatergic terminals effect an unexpected depression of glutamate release by negatively modulating nerve terminal excitability and downstream VDCC activation through a signaling cascade involving phospholipase C/protein kinase C. These observations invoke presynaptic inhibitory 5‐HT~2A~ receptor function as a potential target for drugs to mitigate the effects of excessive glutamatergic transmission. © 2006 Wiley‐Liss, Inc.