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Journal of Neuroscience, Vol 15, 3390-3399, Copyright © 1995 by Society for Neuroscience
Exocytosis in peptidergic nerve terminals exhibits two calcium- sensitive phases during pulsatile calcium entry
EP Seward, NI Chernevskaya and MC Nowycky
Department of Anatomy and Neurobiology, Medical College of Pennsylvania, Philadelphia 19129, USA.
The link between electrical activity, Ca2+ entry through voltage-gated
channels, and transmitter or hormone secretion is a central issue in
neurobiology. In peptidergic nerve terminals of the mammalian
neurohypophysis (NHP), secretion is elicited by patterned bursts of action
potentials (APs). All parameters of the bursts are important to elicit
efficient secretion, including AP frequency, AP broadening, burst duration,
and interburst interval (Leng, 1988). We have studied Ca(2+)-secretion
coupling of peptide-containing large dense-core vesicles (LDCV) in isolated
rat NHP terminals. Ca2+ influx through voltage-gated Ca2+ channels was
elicited and recorded by the whole-cell patch-clamp technique. Exocytosis
was monitored on line with high temporal resolution by the capacitance
detection technique (Neher and Marty, 1982). AP bursts were simulated by
depolarizing pulse trains that mimic pulsatile submembrane Ca2+ elevations
predicted for physiological stimuli. The characteristic capacitance
response (delta Cm) to a train of depolarizing pulses was triphasic. It
consisted of a threshold phase during which early pulses did not elicit
secretion, a subsequent secretory phase during which Cm increases were
coupled to depolarizing pulses, and a fatigued or inactivated state during
which additional Ca2+ entry was ineffective. Both the threshold phase and
secretory phase were correlated with the integrals of Ca2+ current. Ca2+
chelators affect both the threshold and secretory phase at submillimolar
concentrations. Thus, a "shell" rather than "microdomain" model of Ca2+
elevation is appropriate for analyzing Ca(2+)-secretion coupling in NHP
terminals (Nowycky and Pinter, 1993). We propose a two- step model, with a
ca(2+)-dependent preparatory step followed by a final exocytotic step that
is coupled to active Ca2+ influx. The results suggest that under
physiological conditions, APs early in a burst prepare an NHP terminal for
secretion, but later APs actually trigger exocytosis. Since NHP terminals
do not possess a readily releasable pool of vesicles that require only a
single Ca2+ step for exocytosis as seen in chromaffin cells (Neher and
Zucker, 1993) and melanotrophs (Thomas et al, 1993a), Ca(2+)-secretion
coupling mechanisms may be heterologous even within a single class of
vesicles.
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