Regulation of Neuronal Axon Specification by Glia-Neuron Gap Junctions in C. elegans

  1. Lingfeng Meng
  2. Albert Zhang
  3. Yishi Jin
  4. Dong Yan  Is a corresponding author
  1. Duke Institute for Brain Sciences, United States
  2. University of California, San Diego, United States

Abstract

Axon specification is a critical step in neuronal development, and the function of glial cells in this process is not fully understood. Here we show that C. elegans GLR glial cells regulate axon specification of their nearby GABAergic RME neurons through GLR-RME gap junctions. Disruption of GLR-RME gap junctions causes misaccumulation of axonal markers in non-axonal neurites of RME neurons and converts microtubules in those neurites to form an axon-like assembly. We further uncover that GLR-RME gap junctions regulate RME axon specification through activation of the CDK-5 pathway in a calcium-dependent manner, involving a calpain clp-4. Therefore, our study reveals the function of glia-neuron gap junctions in neuronal axon specification and shows that calcium originated from glial cells can regulate neuronal intracellular pathways through gap junctions.

Article and author information

Author details

  1. Lingfeng Meng

    Department of Molecular Genetics and Microbiology, Duke Institute for Brain Sciences, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Albert Zhang

    Department of Molecular Genetics and Microbiology, Duke Institute for Brain Sciences, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Yishi Jin

    Neurobiology Section, Division of Biological Sciences, University of California, San Diego, San Diego, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9371-9860
  4. Dong Yan

    Department of Molecular Genetics and Microbiology, Duke Institute for Brain Sciences, Durham, United States
    For correspondence
    dong.yan@duke.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7542-1251

Funding

National Institute of Neurological Disorders and Stroke (NS094171(R01))

  • Dong Yan

Duke University School of Medicine (faculty startup)

  • Dong Yan

National Institute of Neurological Disorders and Stroke (NS076646 (R00))

  • Dong Yan

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

Reviewing Editor

  1. Oliver Hobert, Howard Hughes Medical Institute, Columbia University, United States

Version history

  1. Received: July 11, 2016
  2. Accepted: October 20, 2016
  3. Accepted Manuscript published: October 21, 2016 (version 1)
  4. Version of Record published: October 27, 2016 (version 2)

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

Metrics

  • 2,626
    views
  • 561
    downloads
  • 19
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Lingfeng Meng
  2. Albert Zhang
  3. Yishi Jin
  4. Dong Yan
(2016)
Regulation of Neuronal Axon Specification by Glia-Neuron Gap Junctions in C. elegans
eLife 5:e19510.
https://doi.org/10.7554/eLife.19510

Share this article

https://doi.org/10.7554/eLife.19510

Further reading

    1. Genetics and Genomics
    2. Neuroscience
    Kenneth Chiou, Noah Snyder-Mackler
    Insight

    Single-cell RNA sequencing reveals the extent to which marmosets carry genetically distinct cells from their siblings.

    1. Neuroscience
    Flavio J Schmidig, Simon Ruch, Katharina Henke
    Research Article

    We are unresponsive during slow-wave sleep but continue monitoring external events for survival. Our brain wakens us when danger is imminent. If events are non-threatening, our brain might store them for later consideration to improve decision-making. To test this hypothesis, we examined whether novel vocabulary consisting of simultaneously played pseudowords and translation words are encoded/stored during sleep, and which neural-electrical events facilitate encoding/storage. An algorithm for brain-state-dependent stimulation selectively targeted word pairs to slow-wave peaks or troughs. Retrieval tests were given 12 and 36 hr later. These tests required decisions regarding the semantic category of previously sleep-played pseudowords. The sleep-played vocabulary influenced awake decision-making 36 hr later, if targeted to troughs. The words’ linguistic processing raised neural complexity. The words’ semantic-associative encoding was supported by increased theta power during the ensuing peak. Fast-spindle power ramped up during a second peak likely aiding consolidation. Hence, new vocabulary played during slow-wave sleep was stored and influenced decision-making days later.