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...
Main Authors: | , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
eLife Sciences Publications Ltd
2019-04-01
|
Series: | eLife |
Subjects: | |
Online Access: | https://elifesciences.org/articles/42156 |
_version_ | 1818028501141291008 |
---|---|
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. |
first_indexed | 2024-12-10T05:04:48Z |
format | Article |
id | doaj.art-2a49632ea78f4bef9aac25e54362f395 |
institution | Directory Open Access Journal |
issn | 2050-084X |
language | English |
last_indexed | 2024-12-10T05:04:48Z |
publishDate | 2019-04-01 |
publisher | eLife Sciences Publications Ltd |
record_format | Article |
series | eLife |
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 |
work_keys_str_mv | AT miaejang oligodendrocytesregulatepresynapticpropertiesandneurotransmissionthroughbdnfsignalinginthemousebrainstem AT elizabethgould oligodendrocytesregulatepresynapticpropertiesandneurotransmissionthroughbdnfsignalinginthemousebrainstem AT jiexu oligodendrocytesregulatepresynapticpropertiesandneurotransmissionthroughbdnfsignalinginthemousebrainstem AT eunjungkim oligodendrocytesregulatepresynapticpropertiesandneurotransmissionthroughbdnfsignalinginthemousebrainstem AT junheekim oligodendrocytesregulatepresynapticpropertiesandneurotransmissionthroughbdnfsignalinginthemousebrainstem |