Distinct roles for innexin gap junctions and hemichannels in mechanosensation

  1. Denise S Walker
  2. William R Schafer  Is a corresponding author
  1. MRC Laboratory of Molecular Biology, United Kingdom

Abstract

Mechanosensation is central to a wide range of functions, including tactile and pain perception, hearing, proprioception, and control of blood pressure, but identifying the molecules underlying mechanotransduction has proved challenging. In Caenorhabditis elegans, the avoidance response to gentle body touch is mediated by 6 touch receptor neurons (TRNs), and is dependent on MEC-4, a DEG/ENaC channel. We show that hemichannels containing the innexin protein UNC-7 are also essential for gentle touch in the TRNs, as well as harsh touch in both the TRNs and the PVD nociceptors. UNC-7 and MEC-4 do not colocalize, suggesting that their roles in mechanosensory transduction are independent. Heterologous expression of unc-7 in touch-insensitive chemosensory neurons confers ectopic touch sensitivity, indicating a specific role for UNC-7 hemichannels in mechanosensation. The unc-7 touch defect can be rescued by the homologous mouse gene Panx1 gene, thus, innexin/pannexin proteins may play broadly conserved roles in neuronal mechanotransduction.

Data availability

All data generated or analysed during this study are included in the manuscript.

Article and author information

Author details

  1. Denise S Walker

    Neurobiology Division, MRC Laboratory of Molecular Biology, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  2. William R Schafer

    Neurobiology Division, MRC Laboratory of Molecular Biology, Cambridge, United Kingdom
    For correspondence
    wschafer@mrc-lmb.cam.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6676-8034

Funding

Medical Research Council (MC-A023-5PB91)

  • William R Schafer

Wellcome (WT103784MA)

  • William R Schafer

National Institutes of Health (1R21DC015652)

  • William R Schafer

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Manuel Zimmer, Research Institute of Molecular Pathology, Vienna Biocenter and University of Vienna, Austria

Version history

  1. Received: July 26, 2019
  2. Accepted: January 28, 2020
  3. Accepted Manuscript published: January 29, 2020 (version 1)
  4. Version of Record published: February 10, 2020 (version 2)
  5. Version of Record updated: March 30, 2020 (version 3)

Copyright

© 2020, Walker & Schafer

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. Denise S Walker
  2. William R Schafer
(2020)
Distinct roles for innexin gap junctions and hemichannels in mechanosensation
eLife 9:e50597.
https://doi.org/10.7554/eLife.50597

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https://doi.org/10.7554/eLife.50597

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