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Molecular identity and function in transepithelial transport of K_ATP channels in alveolar epithelial cells

¹Centre de recherche, Centre hospitalier de l'Université de Montréal-Hôtel-Dieu, Québec H2W 1T7; and ²Département de médecine, Université de Montréal, Montréal, Québec H3C 3J7, Canada

Submitted 24 July 2003 ; accepted in final form 4 January 2004

K⁺ channels play a crucial role in epithelia by repolarizing cells and maintaining electrochemical gradient for Na⁺ absorption and Cl^- secretion. In the airway epithelium, the most frequently studied K⁺ channels are KvLQT1 and K_Ca. A functional role for K_ATP channels has been also suggested in the lung, where K_ATP channel openers activate alveolar clearance and attenuate ischemia-reperfusion injury. However, the molecular identity of this channel is unknown in airway and alveolar epithelial cells (AEC). We adopted an RT-PCR strategy to identify, in AEC, cDNA transcripts for Kir channels (Kir6.1 or 6.2) and sulfonylurea receptors (SUR1, 2A, or 2B) forming K_ATP channels. Only Kir6.1 and SUR2B were detected in freshly isolated and cultured alveolar cells. To determine the physiological role of K⁺ channels in the transepithelial transport of alveolar monolayers, we studied the effect, on total short-circuit currents (I_sc), of basolateral application of glibenclamide, an inhibitor of K_ATP channels, as well as clofilium, charybdotoxin, clotrimazole, and iberiotoxin, inhibitors of KvLQT1 and K_Ca channels, respectively. Interestingly, activity of the three types of K⁺ channels was detected, since all tested inhibitors decreased I_sc. Furthermore, these K⁺ channel inhibitors reduced amiloride-sensitive Na⁺ currents (mediated by ENaC) and completely abolished stimulation of Cl^- currents by forskolin. Conversely, pinacidil, an activator of K_ATP channels, increased Na⁺ and Cl^- transepithelial transport by 33–35%. These results suggest the presence, in AEC, of a K_ATP channel, formed from Kir6.1 and SUR2B subunits, which plays a physiological role, with KvLQT1 and K_Ca channels, in Na⁺ and Cl^- transepithelial transport.

lung; ATP-sensitive K⁺ channel; Kir6.1/SUR2B; Na⁺ and Cl^- transepithelial transport

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