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Control of InsP₃-induced Ca²⁺ oscillations in permeabilized blowfly salivary gland cells: contribution of mitochondria

Bernhard Zimmermann

1. Many agonists linked to the generation of inositol 1,4,5-trisphosphate (InsP₃) and release of Ca²⁺ from intracellular stores induce repetitive transients in cytosolic Ca²⁺ whose frequency increases over a certain range of agonist concentrations.

2. In order to investigate the mechanisms underlying this frequency modulation, the fluorescent Ca²⁺ sensor mag-fura-2 was loaded into intracellular calcium stores and used to monitor InsP₃-induced dynamics of the intraluminal calcium concentration ([Ca²⁺]_L) in secretory cells of permeabilized blowfly Calliphora vicina salivary glands.

3. In this preparation, increasing concentrations of InsP₃ induced graded decreases in [Ca²⁺]_L that were often superimposed with repetitive [Ca²⁺]_L transients produced by sequential Ca²⁺ release and re-uptake. These [Ca²⁺]_L oscillations developed at frequencies of 3-11 min^-1 unrelated to the concentration of InsP₃ present.

4. In contrast, incremental concentrations of InsP₃ applied in the presence of the oxidizable mitochondrial substrates citrate, succinate, or pyruvate-malate induced repetitive [Ca²⁺]_L transients whose frequency increased with the concentration of InsP₃.

5. This InsP₃ concentration-dependent modulation of oscillation frequency was abolished after dissipating the mitochondrial membrane potential (_m) by combined treatment with carbonyl cyanide p-trifluoromethoxyphenyl hydrazone + oligomycin or after application of Ruthenium Red, an inhibitor of mitochondrial Ca²⁺ uptake.

6. Taken together, the data indicate that energized mitochondria exert negative control over the frequency of InsP₃-induced Ca²⁺ oscillations. It is concluded that mitochondria play a crucial role in determining the duration of the interspike period and, therefore, for the encoding of amplitude-modulated, InsP₃-liberating stimuli into the frequency of cytosolic Ca²⁺ oscillations.

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