Lipid-mediated hydrophobic gating in the BK potassium channel

Fuente: arXiv
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Hauptverfasser: Coronel, Lucia, Di Muccio, Giovanni, Rothberg, Brad, Giacomello, Alberto, Carnevale, Vincenzo
Format: Preprint
Veröffentlicht: 2024
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author Coronel, Lucia
Di Muccio, Giovanni
Rothberg, Brad
Giacomello, Alberto
Carnevale, Vincenzo
author_facet Coronel, Lucia
Di Muccio, Giovanni
Rothberg, Brad
Giacomello, Alberto
Carnevale, Vincenzo
contents The large-conductance, calcium-activated potassium (BK) channel lacks the typical intracellular bundle-crossing gate present in most ion channels of the 6TM family. This observation, initially inferred from Ca$^{2+}$-free-pore accessibility experiments and recently corroborated by a CryoEM structure of the non-conductive state, raises a puzzling question: how can gating occur in absence of steric hindrance? To answer this question, we carried out molecular simulations and accurate free energy calculations to obtain a microscopic picture of the sequence of events that, starting from a Ca$^{2+}$-free state leads to ion conduction upon Ca$^{2+}$ binding. Our results highlight an unexpected role for annular lipids, which turn out to be an integral part of the gating machinery. Due to the presence of fenestrations, the "closed" Ca$^{2+}$-free pore can be occupied by the methyl groups from the lipid alkyl chains. This dynamic occupancy triggers and stabilizes the nucleation of a vapor bubble into the inner pore cavity, thus hindering ion conduction. By contrast, Ca$^{2+}$ binding results into a displacement of these lipids outside the inner cavity, lowering the hydrophobicity of this region and thus allowing for pore hydration and conduction. This lipid-mediated hydrophobic gating rationalizes several seemingly problematic experimental observations, including the state-dependent pore accessibility of blockers.
format Preprint
id arxiv_https___arxiv_org_abs_2405_04644
institution arXiv
publishDate 2024
record_format arxiv
spellingShingle Lipid-mediated hydrophobic gating in the BK potassium channel
Coronel, Lucia
Di Muccio, Giovanni
Rothberg, Brad
Giacomello, Alberto
Carnevale, Vincenzo
Biomolecules
Biological Physics
Chemical Physics
The large-conductance, calcium-activated potassium (BK) channel lacks the typical intracellular bundle-crossing gate present in most ion channels of the 6TM family. This observation, initially inferred from Ca$^{2+}$-free-pore accessibility experiments and recently corroborated by a CryoEM structure of the non-conductive state, raises a puzzling question: how can gating occur in absence of steric hindrance? To answer this question, we carried out molecular simulations and accurate free energy calculations to obtain a microscopic picture of the sequence of events that, starting from a Ca$^{2+}$-free state leads to ion conduction upon Ca$^{2+}$ binding. Our results highlight an unexpected role for annular lipids, which turn out to be an integral part of the gating machinery. Due to the presence of fenestrations, the "closed" Ca$^{2+}$-free pore can be occupied by the methyl groups from the lipid alkyl chains. This dynamic occupancy triggers and stabilizes the nucleation of a vapor bubble into the inner pore cavity, thus hindering ion conduction. By contrast, Ca$^{2+}$ binding results into a displacement of these lipids outside the inner cavity, lowering the hydrophobicity of this region and thus allowing for pore hydration and conduction. This lipid-mediated hydrophobic gating rationalizes several seemingly problematic experimental observations, including the state-dependent pore accessibility of blockers.
title Lipid-mediated hydrophobic gating in the BK potassium channel
topic Biomolecules
Biological Physics
Chemical Physics
url https://arxiv.org/abs/2405.04644