Oligodendrocytes regulate presynaptic properties and neurotransmission through BDNF signaling in the mouse brainstem

  1. Miae Jang
  2. Elizabeth Gould
  3. Jie Xu
  4. Eun Jung Kim
  5. Jun Hee Kim  Is a corresponding author
  1. University of Texas Health Science Center, United States

Abstract

Neuron-glia communication contributes to the precise control of synaptic functions. Oligodendrocytes near synapses detect and respond to neuronal activity, but their role in synapse development and plasticity remains largely unexplored. We show that oligodendrocytes modulate neurotransmitter release at presynaptic terminals through secretion of brain derived neurotrophic factor (BDNF). Oligodendrocyte-derived BDNF functions via presynaptic tropomyosin receptor kinase B (TrkB) to ensure fast, reliable neurotransmitter release and auditory transmission in the developing brain. In auditory brainstem slices from Bdnf+/- mice, reduction in endogenous BDNF significantly decreased vesicular glutamate release by reducing the readily releasable pool of glutamate vesicles, without altering presynaptic Ca2+ channel activation or release probability. Using conditional knockout mice, cell-specific ablation of BDNF in oligodendrocytes largely recapitulated this effect, which was recovered by BDNF or TrkB agonist application. This study highlights a novel function for oligodendrocytes in synaptic transmission and their potential role in activity-dependent refinement of presynaptic properties.

Data availability

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

Article and author information

Author details

  1. Miae Jang

    Department of Cellular and Integrative Physiology, University of Texas Health Science Center, San Antonio, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Elizabeth Gould

    Department of Cellular and Integrative Physiology, University of Texas Health Science Center, San Antonio, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Jie Xu

    Department of Cellular and Integrative Physiology, University of Texas Health Science Center, San Antonio, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Eun Jung Kim

    Department of Cellular and Integrative Physiology, University of Texas Health Science Center, San Antonio, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Jun Hee Kim

    Department of Cellular and Integrative Physiology, University of Texas Health Science Center, San Antonio, United States
    For correspondence
    kimjh@uthscsa.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0207-8410

Funding

National Institute on Deafness and Other Communication Disorders (R01 DC03157)

  • Jun Hee Kim

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 animal procedures were performed in accordance with the guidelines approved by the University of Texas Health Science Center, San Antonio (UTHSCSA) Institutional Animal Care and Use Committee protocols (#140045x).

Reviewing Editor

  1. Dwight E Bergles, Johns Hopkins University School of Medicine, United States

Publication history

  1. Received: September 21, 2018
  2. Accepted: April 17, 2019
  3. Accepted Manuscript published: April 18, 2019 (version 1)
  4. Version of Record published: May 7, 2019 (version 2)

Copyright

© 2019, Jang 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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  1. Miae Jang
  2. Elizabeth Gould
  3. Jie Xu
  4. Eun Jung Kim
  5. Jun Hee Kim
(2019)
Oligodendrocytes regulate presynaptic properties and neurotransmission through BDNF signaling in the mouse brainstem
eLife 8:e42156.
https://doi.org/10.7554/eLife.42156

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