We have assessed the relative contribution of Ca entry and Ca release from internal stores to the [Ca] transients evoked by purinergic receptor activation in bovine adrenal chromaffin cells. The [Ca] was recorded from single cells using ratiometric fura-2 microfluorometry. Two discrete groups of ATP-sensitive cells could be distinguished on the basis of their relative capacity to respond to ATP in the virtual absence of extracellular Ca. One group of cells (group I) failed to respond to ATP in the absence of Ca, was completely insensitive to UTP, and displayed suramin-blockable [Ca] transients when challenged with ATP in the presence of external Ca. ATP activated a prominent and rapidly inactivating Mn influx pathway in group I cells, as assessed by monitoring Mn quenching of fura-2 fluorescence. In contrast, a second group of ATP-sensitive cells (group II) exhibited pronounced [Ca] rises when challenged with ATP and UTP in the absence of Ca and was completely insensitive to suramin. ATP and UTP activated a delayed and less prominent Mn influx pathway in group II cells. Contrary to the nicotinic receptor agonist DMPP, which evoked a preferential release of epinephrine, ATP evoked a preferential release of norepinephrine, and UTP had no effect on secretion. Suramin nearly suppressed ATP-evoked norepinephrine release. We conclude that chromaffin cells contain two distinct and cell-specific purinoceptor subtypes. Although some cells express a P-type purinoceptor coupled to Ca release from internal stores and to the associated slow Ca refilling mechanism, other cells express a suramin-sensitive and UTP-insensitive purinoceptor exclusively coupled to Ca influx, probably an ATP-gated channel. It is suggested that the ATP-gated channel is preferentially localized to norepinephrine-secreting chromaffin cells and supports specifically hormone output from these cells. Thus, the biochemical pathways involved in the exocytotic release of the two major stress-related hormones appear to be regulated by distinct signaling systems.

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