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Volume 17, Number 17, Issue of September 1, 1997 pp. 6565-6574
Copyright ©1997 Society for Neuroscience

-Opioid Receptor Activation Modulates Ca²⁺ Currents and Secretion in Isolated Neuroendocrine Nerve Terminals

Received Jan. 30, 1997; revised June 12, 1997; accepted June 16, 1997.

K. I. Rusin, D. R. Giovannucci, E. L. Stuenkel, and H. C. Moises

Department of Physiology, University of Michigan Medical School, Ann Arbor, Michigan 48109-0622

Whole-cell patch-clamp recordings were performed together with time-resolved measurements of membrane capacitance (C_m) in nerve terminals acutely dissociated from neurohypophysis of adult rats to investigate modulation of Ca²⁺ currents and secretion by activation of opioid receptors. Bath superfusion of the -opioid agonists U69,593 (0.3-1 µM), dynorphin A (1 µM), or U50,488H (1-3 µM) reversibly suppressed the peak amplitude of Ca²⁺ currents 32.7 ± 2.7% (in 41 of 56 terminals), 37.4 ± 5.3% (in 5 of 8 terminals), and 33.5 ± 8.1% (in 5 of 10 terminals), respectively. In contrast, tests in 11 terminals revealed no effect of the µ-opioid agonist [D-Pen^2,5]-enkephalin (1-3 µM; n = 7) or of the -agonist Tyr-D-Ala-Gly-N-Me-Phe-Gly-ol (1 µM; n = 4) on Ca²⁺ currents. Three components of high-threshold current were distinguished on the basis of their sensitivity to blockade by -conotoxin GVIA, nicardipine, and -conotoxin MVIIC: N-, L-, and P/Q-type current, respectively. Administration of U69,593 inhibited N-type current in these nerve terminals on average 32%, whereas L-type current was reduced 64%, and P/Q-type current was inhibited 28%. Monitoring of changes in C_m in response to brief depolarizing steps revealed that the -opioid-induced reductions in N-, L-, or P/Q-type currents were accompanied by attenuations in two kinetically distinct components of Ca²⁺-dependent exocytotic release. These data provide strong evidence of a functional linkage between blockade of Ca²⁺ influx through voltage-dependent Ca²⁺ channels and inhibitory modulation of release by presynaptic opioid receptors in mammalian central nerve endings.

Key words: -opioid receptor; Ca²⁺ currents; membrane capacitance; secretion; neuroendocrine nerve terminals; patch- clamp

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