Phosphatidylinositol 4,5-bisphosphate (PIP2) regulates KCNQ3 K channels by interacting with four cytoplasmic channel domains
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Phosphatidylinositol 4,5-bisphosphate (PIP2) in the plasma membrane regulates the function of many ion channels, including M-type (potassium voltage-gated channel subfamily Q member (KCNQ), Kv7) K channels; however, the molecular mechanisms involved remain unclear. To this end, we here focused on the KCNQ3 subtype that has the highest apparent affinity for PIP2 and performed extensive mutagenesis in regions suggested to be involved in PIP2 interactions among the KCNQ family. Using perforated patch-clamp recordings of het-erologously transfected tissue culture cells, total internal reflection fluorescence microscopy, and the zebrafish (Danio rerio) voltage-sensitive phosphatase to deplete PIP2 as a probe, we found that PIP2 regulates KCNQ3 channels through four different domains: 1) the A–B helix linker that we previously identified as important for both KCNQ2 and KCNQ3, 2) the junction between S6 and the A helix, 3) the S2–S3 linker, and 4) the S4 –S5 linker. We also found that the apparent strength of PIP2 interactions within any of these domains was not coupled to the voltage dependence of channel activation. Extensive homology modeling and docking simulations with the WT or mutant KCNQ3 channels and PIP2 were consistent with the experimental data. Our results indicate that PIP2 modulates KCNQ3 channel function by interacting synergistically with a minimum of four cytoplasmic domains. © 2018 Choveau et al.
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Cell membranes; Electrophysiology; Fluorescence microscopy; Refractive index; Tissue culture; Cytoplasmic channels; Cytoplasmic domains; Docking simulations; Molecular mechanism; Patch clamp recording; Phosphatidylinositol 4 ,5-Bisphosphate; Tissue culture cells; Total internal reflection fluorescence microscopy; Cell proliferation; phosphatidylinositol 4,5 bisphosphate; potassium channel KCNQ3; phosphatidylinositol 4,5 bisphosphate; potassium channel KCNQ3; protein binding; animal cell; Article; binding affinity; carboxy terminal sequence; cell membrane; channel gating; CHO cell line; controlled study; crystal structure; cytoplasm; depolarization; hydrogen bond; molecular docking; mutagenesis; mutation; nonhuman; patch clamp technique; priority journal; protein dephosphorylation; total internal reflection fluorescence microscopy; wild type; zebra fish; alpha helix; amino acid sequence; animal; chemistry; Cricetulus; genetics; human; metabolism; molecular model; protein domain; Amino Acid Sequence; Animals; CHO Cells; Cricetulus; Cytoplasm; Humans; KCNQ3 Potassium Channel; Models, Molecular; Mutation; Phosphatidylinositol 4,5-Diphosphate; Protein Binding; Protein Conformation, alpha-Helical; Protein Domains
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