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

Neuron–glia communication contributes to the fine-tuning 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...

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Main Authors: Miae Jang, Elizabeth Gould, Jie Xu, Eun Jung Kim, Jun Hee Kim
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2019-04-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/42156
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author Miae Jang
Elizabeth Gould
Jie Xu
Eun Jung Kim
Jun Hee Kim
author_facet Miae Jang
Elizabeth Gould
Jie Xu
Eun Jung Kim
Jun Hee Kim
author_sort Miae Jang
collection DOAJ
description Neuron–glia communication contributes to the fine-tuning 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 the activity-dependent refinement of presynaptic properties.
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spelling doaj.art-2a49632ea78f4bef9aac25e54362f3952022-12-22T02:01:17ZengeLife Sciences Publications LtdeLife2050-084X2019-04-01810.7554/eLife.42156Oligodendrocytes regulate presynaptic properties and neurotransmission through BDNF signaling in the mouse brainstemMiae Jang0Elizabeth Gould1Jie Xu2Eun Jung Kim3Jun Hee Kim4https://orcid.org/0000-0003-0207-8410The Department of Cellular and Integrative Physiology, University of Texas Health Science Center, San Antonio, United StatesThe Department of Cellular and Integrative Physiology, University of Texas Health Science Center, San Antonio, United StatesThe Department of Cellular and Integrative Physiology, University of Texas Health Science Center, San Antonio, United States; Children's Medical Center, The Second Xiangya Hospital, Central South University, Changsha, ChinaThe Department of Cellular and Integrative Physiology, University of Texas Health Science Center, San Antonio, United StatesThe Department of Cellular and Integrative Physiology, University of Texas Health Science Center, San Antonio, United StatesNeuron–glia communication contributes to the fine-tuning 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 the activity-dependent refinement of presynaptic properties.https://elifesciences.org/articles/42156auditory brainstempresynaptic terminaloligodendrocytesBDNF
spellingShingle Miae Jang
Elizabeth Gould
Jie Xu
Eun Jung Kim
Jun Hee Kim
Oligodendrocytes regulate presynaptic properties and neurotransmission through BDNF signaling in the mouse brainstem
eLife
auditory brainstem
presynaptic terminal
oligodendrocytes
BDNF
title Oligodendrocytes regulate presynaptic properties and neurotransmission through BDNF signaling in the mouse brainstem
title_full Oligodendrocytes regulate presynaptic properties and neurotransmission through BDNF signaling in the mouse brainstem
title_fullStr Oligodendrocytes regulate presynaptic properties and neurotransmission through BDNF signaling in the mouse brainstem
title_full_unstemmed Oligodendrocytes regulate presynaptic properties and neurotransmission through BDNF signaling in the mouse brainstem
title_short Oligodendrocytes regulate presynaptic properties and neurotransmission through BDNF signaling in the mouse brainstem
title_sort oligodendrocytes regulate presynaptic properties and neurotransmission through bdnf signaling in the mouse brainstem
topic auditory brainstem
presynaptic terminal
oligodendrocytes
BDNF
url https://elifesciences.org/articles/42156
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AT jiexu oligodendrocytesregulatepresynapticpropertiesandneurotransmissionthroughbdnfsignalinginthemousebrainstem
AT eunjungkim oligodendrocytesregulatepresynapticpropertiesandneurotransmissionthroughbdnfsignalinginthemousebrainstem
AT junheekim oligodendrocytesregulatepresynapticpropertiesandneurotransmissionthroughbdnfsignalinginthemousebrainstem