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A genetic basis for molecular asymmetry at vertebrate electrical synapses

  1. Adam C Miller  Is a corresponding author
  2. Alex C Whitebirch
  3. Arish N Shah
  4. Kurt C Marsden
  5. Michael Granato
  6. John O'Brien
  7. Cecilia B Moens
  1. Univeristy of Oregon, United States
  2. Fred Hutchinson Cancer Research Center, United States
  3. University of Pennsylvania Perelman School of Medicine, United States
  4. McGovern Medical School, University of Texas Health Sciences Center at Houston, United States
Research Article
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Cite this article as: eLife 2017;6:e25364 doi: 10.7554/eLife.25364

Abstract

Neural network function is based upon the patterns and types of connections made between neurons. Neuronal synapses are adhesions specialized for communication and they come in two types, chemical and electrical. Communication at chemical synapses occurs via neurotransmitter release whereas electrical synapses utilize gap junctions for direct ionic and metabolic coupling. Electrical synapses are often viewed as symmetrical structures, with the same components making both sides of the gap junction. By contrast, we show that a broad set of electrical synapses in zebrafish, Danio rerio, require two gap-junction-forming Connexins for formation and function. We find that one Connexin functions presynaptically while the other functions postsynaptically in forming the channels. We also show that these synapses are required for the speed and coordination of escape responses. Our data identify a genetic basis for molecular asymmetry at vertebrate electrical synapses and show they are required for appropriate behavioral performance.

Article and author information

Author details

  1. Adam C Miller

    Institute of Neuroscience, Univeristy of Oregon, Eugene, United States
    For correspondence
    acmiller@uoregon.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7519-3677
  2. Alex C Whitebirch

    Division of Basic Sciences, Fred Hutchinson Cancer Research Center, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Arish N Shah

    Division of Basic Sciences, Fred Hutchinson Cancer Research Center, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Kurt C Marsden

    Department of Cell and Developmental Biology, University of Pennsylvania Perelman School of Medicine, Philadelphia, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Michael Granato

    Department of Cell and Developmental Biology, University of Pennsylvania Perelman School of Medicine, Philadelphia, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. John O'Brien

    Department of Ophthalmology and Visual Science, McGovern Medical School, University of Texas Health Sciences Center at Houston, Houston, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0270-3442
  7. Cecilia B Moens

    Division of Basic Sciences, Fred Hutchinson Cancer Research Center, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Institute of Neurological Disorders and Stroke (F32NS074839)

  • Adam C Miller

National Institute of Mental Health (R01MH109498)

  • Michael Granato

National Eye Institute (R01EY012857)

  • John O'Brien

Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD076585)

  • Cecilia B Moens

National Institute of Neurological Disorders and Stroke (R21NS076950)

  • Cecilia B Moens

National Institute of Neurological Disorders and Stroke (K99/R00NS085035)

  • Adam C Miller

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

Ethics

Animal experimentation: All animals were raised in an Institutional Animal Care and Use Committee (IACUC)-approvedfacility at the Fred Hutchinson Cancer Research Center (Study ID 50552, Submittal ID 7237, IRO #1392).

Reviewing Editor

  1. Yang Dan, University of California, Berkeley, United States

Publication history

  1. Received: January 24, 2017
  2. Accepted: May 20, 2017
  3. Accepted Manuscript published: May 22, 2017 (version 1)
  4. Version of Record published: June 7, 2017 (version 2)

Copyright

© 2017, Miller et al.

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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