Cargando…

Opponent vesicular transporters regulate the strength of glutamatergic neurotransmission in a C. elegans sensory circuit

At chemical synapses, neurotransmitters are packaged into synaptic vesicles that release their contents in response to depolarization. Despite its central role in synaptic function, regulation of the machinery that loads vesicles with neurotransmitters remains poorly understood. We find that synapti...

Descripción completa

Detalles Bibliográficos
Autores principales: Choi, Jung-Hwan, Horowitz, Lauren Bayer, Ringstad, Niels
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8566550/
https://www.ncbi.nlm.nih.gov/pubmed/34732711
http://dx.doi.org/10.1038/s41467-021-26575-3
_version_ 1784594038464184320
author Choi, Jung-Hwan
Horowitz, Lauren Bayer
Ringstad, Niels
author_facet Choi, Jung-Hwan
Horowitz, Lauren Bayer
Ringstad, Niels
author_sort Choi, Jung-Hwan
collection PubMed
description At chemical synapses, neurotransmitters are packaged into synaptic vesicles that release their contents in response to depolarization. Despite its central role in synaptic function, regulation of the machinery that loads vesicles with neurotransmitters remains poorly understood. We find that synaptic glutamate signaling in a C. elegans chemosensory circuit is regulated by antagonistic interactions between the canonical vesicular glutamate transporter EAT-4/VGLUT and another vesicular transporter, VST-1. Loss of VST-1 strongly potentiates glutamate release from chemosensory BAG neurons and disrupts chemotaxis behavior. Analysis of the circuitry downstream of BAG neurons shows that excess glutamate release disrupts behavior by inappropriately recruiting RIA interneurons to the BAG-associated chemotaxis circuit. Our data indicate that in vivo the strength of glutamatergic synapses is controlled by regulation of neurotransmitter packaging into synaptic vesicles via functional coupling of VGLUT and VST-1.
format Online
Article
Text
id pubmed-8566550
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher Nature Publishing Group UK
record_format MEDLINE/PubMed
spelling pubmed-85665502021-11-19 Opponent vesicular transporters regulate the strength of glutamatergic neurotransmission in a C. elegans sensory circuit Choi, Jung-Hwan Horowitz, Lauren Bayer Ringstad, Niels Nat Commun Article At chemical synapses, neurotransmitters are packaged into synaptic vesicles that release their contents in response to depolarization. Despite its central role in synaptic function, regulation of the machinery that loads vesicles with neurotransmitters remains poorly understood. We find that synaptic glutamate signaling in a C. elegans chemosensory circuit is regulated by antagonistic interactions between the canonical vesicular glutamate transporter EAT-4/VGLUT and another vesicular transporter, VST-1. Loss of VST-1 strongly potentiates glutamate release from chemosensory BAG neurons and disrupts chemotaxis behavior. Analysis of the circuitry downstream of BAG neurons shows that excess glutamate release disrupts behavior by inappropriately recruiting RIA interneurons to the BAG-associated chemotaxis circuit. Our data indicate that in vivo the strength of glutamatergic synapses is controlled by regulation of neurotransmitter packaging into synaptic vesicles via functional coupling of VGLUT and VST-1. Nature Publishing Group UK 2021-11-03 /pmc/articles/PMC8566550/ /pubmed/34732711 http://dx.doi.org/10.1038/s41467-021-26575-3 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Choi, Jung-Hwan
Horowitz, Lauren Bayer
Ringstad, Niels
Opponent vesicular transporters regulate the strength of glutamatergic neurotransmission in a C. elegans sensory circuit
title Opponent vesicular transporters regulate the strength of glutamatergic neurotransmission in a C. elegans sensory circuit
title_full Opponent vesicular transporters regulate the strength of glutamatergic neurotransmission in a C. elegans sensory circuit
title_fullStr Opponent vesicular transporters regulate the strength of glutamatergic neurotransmission in a C. elegans sensory circuit
title_full_unstemmed Opponent vesicular transporters regulate the strength of glutamatergic neurotransmission in a C. elegans sensory circuit
title_short Opponent vesicular transporters regulate the strength of glutamatergic neurotransmission in a C. elegans sensory circuit
title_sort opponent vesicular transporters regulate the strength of glutamatergic neurotransmission in a c. elegans sensory circuit
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8566550/
https://www.ncbi.nlm.nih.gov/pubmed/34732711
http://dx.doi.org/10.1038/s41467-021-26575-3
work_keys_str_mv AT choijunghwan opponentvesiculartransportersregulatethestrengthofglutamatergicneurotransmissioninaceleganssensorycircuit
AT horowitzlaurenbayer opponentvesiculartransportersregulatethestrengthofglutamatergicneurotransmissioninaceleganssensorycircuit
AT ringstadniels opponentvesiculartransportersregulatethestrengthofglutamatergicneurotransmissioninaceleganssensorycircuit