Molecular dynamics of the pathogenic KCNQ2 variant G256W reveal mechanisms of channel dysfunction in epileptic encephalopathy

致病性KCNQ2变异体G256W的分子动力学揭示了癫痫性脑病中通道功能障碍的机制

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Abstract

Brain voltage-gated potassium channels containing the subunit KCNQ2 are essential for regulating electrical signals contributing to sensation, learning, memory, and motor control. De novo KCNQ2 variants are among the more common Mendelian causes of early life epilepsy and neurodevelopmental impairment. Some patients with KCNQ2 variants are affected with KCNQ2 developmental and epileptic encephalopathy (KCNQ2 DEE) characterized by seizures and developmental delays. Children with KCNQ2 DEE exhibit a range of impairment patterns that appear to be correlated with specific consequences of the variant for protein function. Here, we used all-atom molecular dynamics to analyze a pathogenic missense variant KCNQ2 G256W, located in the pore turret. G256W subunit simulations showed migration of the hydrophobic W256 sidechain towards the lipid membrane. This movement affected turret structure and mobility prominently involving K255. We identified novel hydrogen bonding interactions in the wild type KCNQ2 turret region which formed a network that extended to the selectivity filter and identified N258, H260P, and K283 as key residues. Simulations comparing WT and G256W tetrameric channels exhibited more conformationally unstable ion selectivity filters for G256W. We analyzed how different stoichiometries of wild type and G256W subunits, as expected in heterozygous individuals, impacted dynamics and compared the G256W results to three additional variants of the turret-selectivity filter network. Our results provide additional support for an integral role of the KCNQ2 turret selectivity filter stability. The majority of severe KCNQ2 DEE variants are clustered near the selectivity filter in the pore domain. Our study provides insights that may be broadly applicable to this clinically important allele subgroup.

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