Calmodulin acts as a state-dependent switch to control a cardiac potassium channel opening.

Kang, Po Wei; Westerlund, Annie M; Shi, Jingyi; White, Kelli McFarland; Dou, Alex K; Cui, Amy H; Silva, Jonathan R; Delemotte, Lucie et al. · Sci Adv · 2020

basic_science · Level V

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Abstract

Calmodulin (CaM) and phosphatidylinositol 4,5-bisphosphate (PIP<sub>2</sub>) are potent regulators of the voltage-gated potassium channel KCNQ1 (K<sub>V</sub>7.1), which conducts the cardiac <i>I</i> <sub>Ks</sub> current. Although cryo-electron microscopy structures revealed intricate interactions between the KCNQ1 voltage-sensing domain (VSD), CaM, and PIP<sub>2</sub>, the functional consequences of these interactions remain unknown. Here, we show that CaM-VSD interactions act as a state-dependent switch to control KCNQ1 pore opening. Combined electrophysiology and molecular dynamics network analysis suggest that VSD transition into the fully activated state allows PIP<sub>2</sub> to compete with CaM for binding to VSD. This leads to conformational changes that alter VSD-pore coupling to stabilize open states. We identify a motif in the KCNQ1 cytosolic domain, which works downstream of CaM-VSD interactions to facilitate the conformational change. Our findings suggest a gating mechanism that integrates PIP<sub>2</sub> and CaM in KCNQ1 voltage-dependent activation, yielding insights into how KCNQ1 gains the phenotypes critical for its physiological function.