Role of K channels in maintaining the synchrony of spontaneous Ca transients in the mural cells of rat rectal submucosal arterioles.

Mural cells in precapillary arterioles (PCAs) generate spontaneous Ca transients primarily arising from the periodic release of Ca from sarcoendoplasmic reticulum (SR/ER). The Ca release induces Ca-activated chloride channel (CaCC)-dependent depolarisations that spread to neighbouring mural cells to develop the synchrony of their Ca transients. Here, we explored the roles of K channels in maintaining the synchrony of spontaneous Ca transients. Intracellular Ca dynamics in mural cells were visualised by Cal-520 fluorescence Ca imaging in the submucosal PCAs of rat rectum. Increasing extracellular K concentration ([K]) from 5.9 to 29.7 mM converted synchronous spontaneous Ca transients into asynchronous, high-frequency Ca transients. Similarly, the blockade of inward rectifier K (K) channels with Ba (50 μM) or K7 voltage-dependent K (K7) channels with XE 991 (10 μM) disrupted the synchrony of spontaneous Ca transients, while the blockers for large-, intermediate- or small-conductance Ca-activated K channels had no effect. K2.1 immunoreactivity was detected in the arteriolar endothelium but not mural cells. In the PCAs that had been pretreated with XE 991 or Ba, nifedipine (1 μM) attenuated the asynchronous Ca transients but failed to restore their synchrony. In contrast, levcromakalim, an ATP-sensitive K channel opener, restored the synchronous Ca transients. Thus, constitutively active K7 and K channels appear to be involved in maintaining the relatively hyperpolarised membrane of mural cells. The hyperpolarised membrane prevents depolarisation-induced 'premature' Ca transients to ensure sufficient SR/ER Ca refilling that is required for regenerative Ca release resulting in synchronous Ca transients amongst the mural cells.