High temperature sensitivity is intrinsic to voltage-gated potassium channels

  1. Fan Yang
  2. Jie Zheng  Is a corresponding author
  1. University of California, Davis, United States

Abstract

Temperature-sensitive transient receptor potential (TRP) ion channels are members of the large tetrameric cation channels superfamily but are considered to be uniquely sensitive to heat, which has been presumed to be due to the existence of an unidentified temperature-sensing domain. Here we report that the homologous voltage-gated potassium (Kv) channels also exhibit high temperature sensitivity comparable to that of TRPV1, which is detectable under specific conditions when the voltage sensor is functionally decoupled from the activation gate through either intrinsic mechanisms or mutations. Interestingly, mutations could tune Shaker channel to be either heat-activated or heat-deactivated. Therefore, high temperature sensitivity is intrinsic to both TRP and Kv channels. Our findings suggest important physiological roles of heat-induced variation in Kv channel activities. Mechanistically our findings indicate that temperature-sensing TRP channels may not contain a specialized heat-sensor domain; instead, non-obligatory allosteric gating permits the intrinsic heat sensitivity to drive channel activation, allowing temperature-sensitive TRP channels to function as polymodal nociceptors.

Article and author information

Author details

  1. Fan Yang

    University of California, Davis, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Jie Zheng

    University of California, Davis, Davis, United States
    For correspondence
    jzheng@ucdavis.edu
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Richard Aldrich, The University of Texas at Austin, United States

Version history

  1. Received: May 4, 2014
  2. Accepted: July 15, 2014
  3. Accepted Manuscript published: July 16, 2014 (version 1)
  4. Version of Record published: August 7, 2014 (version 2)

Copyright

© 2014, Yang & Zheng

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Fan Yang
  2. Jie Zheng
(2014)
High temperature sensitivity is intrinsic to voltage-gated potassium channels
eLife 3:e03255.
https://doi.org/10.7554/eLife.03255

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https://doi.org/10.7554/eLife.03255

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