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The actions of barium and strontium on exocytosis and endocytosis in the synaptic terminal of goldfish bipolar cells

Guilherme Neves, Andreas Neef and Leon Lagnado

1. We investigated the properties of Ca²⁺-sensitive steps in the cycling of synaptic vesicles by comparing the actions of Ca²⁺, Ba²⁺ and Sr²⁺ in the synaptic terminal of depolarizing bipolar cells isolated from the retina of goldfish. FM1-43 fluorescence and capacitance measurements demonstrated that exocytosis, endocytosis and vesicle mobilization were maintained when external Ca²⁺ was replaced by either Ba²⁺ or Sr²⁺.
2. The rapidly releasable pool of vesicles (RRP) was equivalent to 1.5 % of the membrane surface area when measured in the presence of 2.5 mM Ca²⁺, but only 0.4 % in 2.5 mM Sr²⁺. The relative sizes of the RRP in Ca²⁺, Sr²⁺ and Ba²⁺ were 1.0, 0.28 and 0.1, respectively. We conclude that a smaller proportion of docked vesicles are available for fast exocytosis triggered by the influx of Sr²⁺ or Ba²⁺ compared to Ca²⁺.
3. The slow phase of exocytosis was not altered when Ca²⁺ was replaced by Ba²⁺, but it was accelerated 1.6-fold in Sr²⁺. The peak concentrations of Ca²⁺, Sr²⁺ and Ba²⁺ (measured using Mag-fura-5) were ~4, ~14 and ~60 µM, respectively. The order of efficiency for the stimulation of slow exocytosis was Ca²⁺ Sr²⁺ > Ba²⁺.
4. Exocytosis was prolonged after the influx of Sr²⁺ and Ba²⁺. Sr²⁺ was cleared from the synaptic terminal with the same time constant as Ca²⁺ (1.3 s), but Ba²⁺ was cleared 10-100 times more slowly. Although Ba²⁺ stimulates the slow release of a large number of vesicles, it did so less efficiently than Ca²⁺ or Sr²⁺.
5. The recovery of the membrane capacitance was equally rapid in Sr²⁺ and Ca²⁺, demonstrating that the fast mode of endocytosis could be triggered by either cation.

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