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µ-Opioid receptor inhibits N-type Ca²⁺ channels in the calyx presynaptic terminal of the embryonic chick ciliary ganglion

Katsuaki Endo and Hiromu Yawo *

1. A study was made on the mechanisms by which enkephalins inhibit synaptic transmission at calyx-type presynaptic terminals in the ciliary ganglion of chick embryos at stages 39-40.

2. Excitatory postsynaptic currents (EPSCs) were recorded by nystatin-perforated patch clamp at low [Ca²⁺]_o and high [Mg²⁺]_o. [Leu⁵]enkephalin (L-ENK, 1-10 µM) reduced the quantal content (m) without changing the quantal size (q). This effect was antagonized by naloxone (1 µM). Similar results were observed under conventional whole-cell clamp of the postsynaptic neuron.

3. A specific agonist of the µ-opioid receptor, [D-Ala², M-Me-Phe⁴,Gly⁵]enkephalin-ol (DAMGO) reduced m without changing q. A specific agonist of the -opioid receptor, [d-Pen², d-Pen⁵]enkephalin (DPDPE) also reduced m without changing q.

4. Both L-ENK and [Met⁵]enkephalin (M-ENK) reduced the stimulus-dependent increment of the intraterminal Ca²⁺ concentration ([Ca²⁺]_t) without affecting the decay time constant of the intraterminal Ca²⁺ concentration and basal Ca²⁺ level. This effect was antagonized by naloxone. DAMGO reduced [Ca²⁺]_t more effectively than DPDPE.

5. When extracellular Ca²⁺ was replaced by Ba²⁺, the stimulus-dependent increment of the intraterminal Ba²⁺ concentration ([Ba²⁺]_t) was also reduced by L-ENK or DAMGO.

6. L-ENK reduced [Ca²⁺]_t even in the presence of 4-aminopyridine (4-AP), which blocks the transient K⁺ conductance during the falling phase of the presynaptic action potential. When N-type Ca²⁺ channels were blocked by -conotoxin GVIA (-CgTx_GVIA), the [Ca²⁺]_t was no longer sensitive to L-ENK and DAMGO.

7. It is suggested that enkephalins reduce the transmitter release through presynaptic opioid receptors. The µ-opioid receptor may suppress presynaptic Ca²⁺ influx by selectively inhibiting N-type Ca²⁺ channels.

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