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Small vertical movement of a K+ channel voltage sensor measured with luminescence energy transfer

Author

Listed:
  • David J. Posson

    (University of Illinois at Urbana-Champaign)

  • Pinghua Ge

    (University of Illinois at Urbana-Champaign)

  • Christopher Miller

    (Brandeis University)

  • Francisco Bezanilla

    (UCLA School of Medicine)

  • Paul R. Selvin

    (University of Illinois at Urbana-Champaign)

Abstract

Voltage-gated ion channels open and close in response to voltage changes across electrically excitable cell membranes1. Voltage-gated potassium (Kv) channels are homotetramers with each subunit constructed from six transmembrane segments, S1–S6 (ref. 2). The voltage-sensing domain (segments S1–S4) contains charged arginine residues on S4 that move across the membrane electric field2,3, modulating channel open probability. Understanding the physical movements of this voltage sensor is of fundamental importance and is the subject of controversy. Recently, the crystal structure of the KvAP4 channel motivated an unconventional ‘paddle model’ of S4 charge movement, indicating that the segments S3b and S4 might move as a unit through the lipid bilayer with a large (15–20-Å) transmembrane displacement5. Here we show that the voltage-sensor segments do not undergo significant transmembrane translation. We tested the movement of these segments in functional Shaker K+ channels by using luminescence resonance energy transfer to measure distances between the voltage sensors and a pore-bound scorpion toxin. Our results are consistent with a 2-Å vertical displacement of S4, not the large excursion predicted by the paddle model. This small movement supports an alternative model in which the protein shapes the electric field profile, focusing it across a narrow region of S4 (ref. 6).

Suggested Citation

  • David J. Posson & Pinghua Ge & Christopher Miller & Francisco Bezanilla & Paul R. Selvin, 2005. "Small vertical movement of a K+ channel voltage sensor measured with luminescence energy transfer," Nature, Nature, vol. 436(7052), pages 848-851, August.
  • Handle: RePEc:nat:nature:v:436:y:2005:i:7052:d:10.1038_nature03819
    DOI: 10.1038/nature03819
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    Cited by:

    1. Farha Khan & Matthias Elgeti & Samuel Grandfield & Aviv Paz & Fiona B. Naughton & Frank V. Marcoline & Thorsten Althoff & Natalia Ermolova & Ernest M. Wright & Wayne L. Hubbell & Michael Grabe & Jeff , 2023. "Membrane potential accelerates sugar uptake by stabilizing the outward facing conformation of the Na/glucose symporter vSGLT," Nature Communications, Nature, vol. 14(1), pages 1-12, December.

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