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Quantal puffs of intracellular Ca2+ evoked by inositol trisphosphate in Xenopus oocytes.

1. Ca2+ liberation induced in Xenopus oocytes by a poorly metabolized derivative of inositol 1,4,5‐trisphosphate (3‐deoxy‐3‐fluoro‐D‐myo‐inositol 1,4,5‐trisphosphate; 3‐F‐InsP3) was visualized using a video‐rate confocal microscope to image fluorescence signals reported by the indicator dye calcium green‐1. 2. Low (10‐30 nM) intracellular concentrations of 3‐F‐InsP3 evoked Ca2+ release as localized transient ‘puffs’. Progressively higher concentrations (30‐60 nM) gave rise to abortive Ca2+ waves triggered by puffs, and then (> 60 nM) to a sustained elevation of Ca2+ followed by the appearance of propagating Ca2+ waves. At concentrations up to that giving waves, the frequency of puffs increased as about the third power of [InsP3], whereas their amplitudes increased only slightly. 3. The rise of cytosolic Ca2+ during a puff began abruptly, and peaked within about 50 ms. The peak free Ca2+ level was about 180 nM, and the total amount of Ca2+ liberated was several attomoles (10(‐18) mol), too much to be accounted for by opening of a single InsP3‐gated channel. The subsequent decline of Ca2+ occurred over a few hundred milliseconds, determined largely by diffusion of Ca2+ away from the release site, rather than by resequestration. Lateral spread of Ca2+ was restricted to a few micrometres, consistent with an effective diffusion coefficient for Ca2+ ions of about 27 microns2 s‐1. 4. The peak amplitudes of puffs recorded at a given site were distributed in a roughly Gaussian manner, and a small proportion of sites consistently gave puffs much larger than the main population. Intervals between successive puffs at a single site were exponentially distributed, except for a progressive fall‐off in puffs seen at intervals shorter than about 10 s. Thus, triggering of puffs appeared to be stochastically determined after recovery from a refractory period. 5. There was little correlation between the occurrence of puffs at sites more than a few micrometres apart, indicating that puff sites can function autonomously, but closely (ca 2 microns) adjacent sites showed highly correlated behaviour. 6. Puffs arose from sites‐present at a density of about 1 per 30 microns2 in the animal hemisphere, located within a narrow band about 5‐7 microns below the plasma membrane. 7. We conclude that Ca2+ puffs represent a ‘quantal’ unit of InsP3‐evoked Ca2+ liberation, which may arise because local regenerative feedback by cytosolic Ca2+ ions causes the concerted opening of several closely clustered InsP3 receptor channels.