Role of BK channels and Kv4.2 channels in the electrophysiological properties of Merkel cells in rat whisker hair follicles

Merkel cells are excitable cells in the skin and the whisker hair follicles that detect tactile stimuli, leading to the sense of touch. Previous studies have identified Piezo2 channels as mechanical transducers in Merkel cells, and their activation excites Merkel cells to fire Ca²⁺ action potentials (APs), which subsequently transmit the tactile signal to Aβ-afferent terminals. However, ion channels involving the electrophysiological properties of Merkel cells remain incompletely studied. Here, we performed patch-clamp recordings from Merkel cells in rat whisker hair follicles to investigate K⁺ channels and their roles in the electrophysiological properties of Merkel cells. Robust outward currents could be evoked by depolarizing Merkel cells, which could be markedly inhibited by the voltage-gated K⁺ channel blocker tetraethylammonium (TEA). The outward currents were also significantly blocked by iberiotoxin, a big-conductance voltage- and calcium-activated K⁺ (BK) channel blocker, suggesting that BK channels contribute to the outward K⁺ currents in Merkel cells. Furthermore, the outward currents also consist of a rapidly inactivating current (IA), which could be inhibited by stromatoxin-1 and phrixotoxin-2, the Kv4.2 channel blockers. This indicates that Kv4.2 channels mediate the IA currents in Merkel cells. TEA and iberiotoxin significantly prolonged AP duration, indicating that BK channels play a role in AP repolarization in Merkel cells. Stromatoxin-1 depolarized the resting membrane potentials, indicating a role of Kv4.2 in the resting membrane potentials in Merkel cells. Collectively, our findings reveal the essential roles of BK channels and Kv4.2 channels in the intrinsic electrophysiological properties of Merkel cells, which may be essential in tactile signaling by Merkel cells.<b>NEW & NOTEWORTHY</b> Patch-clamp recordings were made from Merkel cells in rat whisker hair follicles. Big-conductance voltage- and calcium-activated K⁺ (BK) channels and Kv4.2 voltage-gated K⁺ channels were identified in Merkel cells. BK and Kv4.2 channels were involved in Merkel cell action potential repolarization and resting membrane potentials, respectively. By controlling the intrinsic electrophysiological properties of Merkel cells, BK and Kv4.2 channels may play a significant role in tactile encoding.