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J Gen Physiol
1998 Nov 01;1125:559-67. doi: 10.1085/jgp.112.5.559.
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Submaximal responses in calcium-triggered exocytosis are explained by differences in the calcium sensitivity of individual secretory vesicles.
Blank PS
,
Cho MS
,
Vogel SS
,
Kaplan D
,
Kang A
,
Malley J
,
Zimmerberg J
.
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A graded response to calcium is the defining feature of calcium-regulated exocytosis. That is, there exist calcium concentrations that elicit submaximal exocytotic responses in which only a fraction of the available population of secretory vesicles fuse. The role of calcium-dependent inactivation in defining the calcium sensitivity of sea urchin eggsecretory vesicle exocytosis in vitro was examined. The cessation of fusion in the continued presence of calcium was not due to calcium-dependent inactivation. Rather, the calcium sensitivity of individual vesicles within a population of exocytotic vesicles is heterogeneous. Any specific calcium concentration above threshold triggered subpopulations of vesicles to fuse and the size of the subpopulations was dependent upon the magnitude of the calcium stimulus. The existence of multiple, stable subpopulations of vesicles is consistent with a fusion process that requires the action of an even greater number of calcium ions than the numbers suggested by models based on the assumption of a homogeneous vesicle population.
Figure 2. (A) Percent fusion vs. time, species differences. For comparable extents of fusion, L. pictus requires higher calcium concentration than S. purpuratus. The data were collected using a sample time of 0.02 (L. pictus) and 0.1 (S. purpuratus) s. (B) Rate, d(%fusion)/dt vs. time in the continued presence of calcium. The maximum rate of fusion is larger and occurs earlier in L. pictus compared with S. purpuratus. The data were low-pass filtered with a 1.0 Hz cutoff frequency before calculating the derivative using third order forward differences.
Figure 3. 30-min exposure to elevated calcium with S. purpuratus. Submaximal responses were maintained during the exposure of cortices to solutions containing 5 or 16 μM. The upward arrows signify addition of calcium. The smaller arrow represents the addition of either 5 or 16 μM calcium while the larger arrow represents the calcium concentration (>300 μM) used to fuse all the remaining vesicles. The presence of elevated calcium for 30 min had no effect on subsequent fusion resulting from exposure to a higher concentration of calcium. The sample time was 0.3 s.
Figure 4. Multiple calcium challenges. Enhanced fusion does not occur when cortices are challenged with a second application of 24 μM calcium, S. purpuratus. Cortices were washed and incubated in zero calcium for 0.5, 1.0, 3.0, 10.0, and 30 min (A–E) before the second calcium challenge. The upward and downward arrows signify addition and removal of calcium, respectively. The largest arrow represents the calcium concentration (>300 μM) used to fuse all remaining vesicles. The sample time was 0.15 s.
Figure 5. Additivity in the extent of fusion, S. purpuratus. The final extent of fusion is independent of the sequence of concentrations used to elicit the response. The upward and downward arrow signifies addition and removal of calcium. The calcium concentrations were 14, 24, and >300 μM (DP); 24 and >300 μM (SP). For clarity, only every 10th data point was plotted for SP. The sample time was 0.15 s.
Figure 7. (A) Calcium activation curves for S. purpuratus and L. pictus, average values (± SEM). Unchallenged cortices are represented by solid symbols and previously challenged cortices are represented by open symbols. The solid lines are the log-normal cumulative distribution function, %fusion = 50 · erfc{[pCa + log (10−6 M)]/\documentclass[10pt]{article}
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\begin{equation*}(\sqrt{2}{\cdot}W)\}\end{equation*}\end{document} , with W = 0.23 ± 0.02 and 0.24 ± 0.02 and midpoint M = 18.2 ± 0.6 and 44.8 ± 1.2 μM for S. purpuratus and L. pictus, respectively. (B) Distribution of calcium thresholds (probability density function) for S. purpuratus and L. pictus derived from the derivative of the log-normal cumulative distribution function. The total area under each curve is one, corresponding to 100% fusion.
Figure 6. (A) Fusion can occur during solution exchange, before establishing the stable, submaximal response, which is independent of the presence or absence of calcium. The upward and downward arrows signify addition and removal of 24 μM calcium, S. purpuratus. The absence of abrupt changes in fusion (inset) indicates that the solution exchange occurred during a time when previously activated vesicles are now fusing. T1 and T2 label the times of solution exchange. The sample time was 0.15 s. (B) Abrupt changes in fusion are observed only when calcium is removed before irreversible commitment to the fusion process. The upward and downward arrows signify addition and removal (Interrupted) of 70 μM calcium, S. purpuratus. The sample times were 0.15 and 0.05 s for Uninterrupted and Interrupted, respectively.
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