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Hydrophobic gating in BK channels

Author

Listed:
  • Zhiguang Jia

    (University of Massachusetts)

  • Mahdieh Yazdani

    (University of Massachusetts)

  • Guohui Zhang

    (Washington University)

  • Jianmin Cui

    (Washington University)

  • Jianhan Chen

    (University of Massachusetts
    University of Massachusetts)

Abstract

The gating mechanism of transmembrane ion channels is crucial for understanding how these proteins control ion flow across membranes in various physiological processes. Big potassium (BK) channels are particularly interesting with large single-channel conductance and dual regulation by membrane voltage and intracellular Ca2+. Recent atomistic structures of BK channels failed to identify structural features that could physically block the ion flow in the closed state. Here, we show that gating of BK channels does not seem to require a physical gate. Instead, changes in the pore shape and surface hydrophobicity in the Ca2+-free state allow the channel to readily undergo hydrophobic dewetting transitions, giving rise to a large free energy barrier for K+ permeation. Importantly, the dry pore remains physically open and is readily accessible to quaternary ammonium channel blockers. The hydrophobic gating mechanism is also consistent with scanning mutagenesis studies showing that modulation of pore hydrophobicity is correlated with activation properties.

Suggested Citation

  • Zhiguang Jia & Mahdieh Yazdani & Guohui Zhang & Jianmin Cui & Jianhan Chen, 2018. "Hydrophobic gating in BK channels," Nature Communications, Nature, vol. 9(1), pages 1-8, December.
    • Handle: RePEc:nat:natcom:v:9:y:2018:i:1:d:10.1038_s41467-018-05970-3
    DOI: 10.1038/s41467-018-05970-3
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    Cited by:

    1. Davide Caprini & Francesco Battista & Paweł Zajdel & Giovanni Di Muccio & Carlo Guardiani & Benjamin Trump & Marcus Carter & Andrey A. Yakovenko & Eder Amayuelas & Luis Bartolomé & Simone Meloni & Yar, 2024. "Bubbles enable volumetric negative compressibility in metastable elastocapillary systems," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    2. Johansen B. Amin & Miaomiao He & Ramesh Prasad & Xiaoling Leng & Huan-Xiang Zhou & Lonnie P. Wollmuth, 2023. "Two gates mediate NMDA receptor activity and are under subunit-specific regulation," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    3. Guohui Zhang & Xianjin Xu & Zhiguang Jia & Yanyan Geng & Hongwu Liang & Jingyi Shi & Martina Marras & Carlota Abella & Karl L. Magleby & Jonathan R. Silva & Jianhan Chen & Xiaoqin Zou & Jianmin Cui, 2022. "An allosteric modulator activates BK channels by perturbing coupling between Ca2+ binding and pore opening," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    4. Gonçalo Paulo & Ke Sun & Giovanni Di Muccio & Alberto Gubbiotti & Blasco Morozzo della Rocca & Jia Geng & Giovanni Maglia & Mauro Chinappi & Alberto Giacomello, 2023. "Hydrophobically gated memristive nanopores for neuromorphic applications," Nature Communications, Nature, vol. 14(1), pages 1-9, December.
    5. Ruo-Xu Gu & Bert L. Groot, 2023. "Central cavity dehydration as a gating mechanism of potassium channels," Nature Communications, Nature, vol. 14(1), pages 1-12, December.

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