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Dynamics of activation in the voltage-sensing domain of Ciona intestinalis phosphatase Ci-VSP

Author

Listed:
  • Spencer C. Guo

    (The University of Chicago
    The University of Chicago)

  • Rong Shen

    (The University of Chicago)

  • Benoît Roux

    (The University of Chicago
    The University of Chicago
    The University of Chicago)

  • Aaron R. Dinner

    (The University of Chicago
    The University of Chicago
    The University of Chicago)

Abstract

The Ciona intestinalis voltage-sensing phosphatase (Ci-VSP) is a membrane protein containing a voltage-sensing domain (VSD) that is homologous to VSDs from voltage-gated ion channels responsible for cellular excitability. Previously published crystal structures of Ci-VSD in putative resting and active conformations suggested a helical-screw voltage sensing mechanism in which the S4 helix translocates and rotates to enable exchange of salt-bridge partners, but the microscopic details of the transition between the resting and active conformations remained unknown. Here, by combining extensive molecular dynamics simulations with a recently developed computational framework based on dynamical operators, we elucidate the microscopic mechanism of the resting-active transition at physiological membrane potential. Sparse regression reveals a small set of coordinates that distinguish intermediates that are hidden from electrophysiological measurements. The intermediates arise from a noncanonical helical-screw mechanism in which translocation, rotation, and side-chain movement of the S4 helix are only loosely coupled. These results provide insights into existing experimental and computational findings on voltage sensing and suggest ways of further probing its mechanism.

Suggested Citation

  • Spencer C. Guo & Rong Shen & Benoît Roux & Aaron R. Dinner, 2024. "Dynamics of activation in the voltage-sensing domain of Ciona intestinalis phosphatase Ci-VSP," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45514-6
    DOI: 10.1038/s41467-024-45514-6
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    References listed on IDEAS

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    4. Yoshimichi Murata & Hirohide Iwasaki & Mari Sasaki & Kazuo Inaba & Yasushi Okamura, 2005. "Phosphoinositide phosphatase activity coupled to an intrinsic voltage sensor," Nature, Nature, vol. 435(7046), pages 1239-1243, June.
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