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The number and distribution of AMPA receptor channels containing fast kinetic GluA3 and GluA4 subunits at auditory nerve synapses depend on the target cells

The neurotransmitter receptor subtype, number, density, and distribution relative to the location of transmitter release sites are key determinants of signal transmission. AMPA-type ionotropic glutamate receptors (AMPARs) containing GluA3 and GluA4 subunits are prominently expressed in subsets of ne...

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Autores principales: Rubio, María E., Matsui, Ko, Fukazawa, Yugo, Kamasawa, Naomi, Harada, Harumi, Itakura, Makoto, Molnár, Elek, Abe, Manabu, Sakimura, Kenji, Shigemoto, Ryuichi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer Berlin Heidelberg 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5676837/
https://www.ncbi.nlm.nih.gov/pubmed/28397107
http://dx.doi.org/10.1007/s00429-017-1408-0
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author Rubio, María E.
Matsui, Ko
Fukazawa, Yugo
Kamasawa, Naomi
Harada, Harumi
Itakura, Makoto
Molnár, Elek
Abe, Manabu
Sakimura, Kenji
Shigemoto, Ryuichi
author_facet Rubio, María E.
Matsui, Ko
Fukazawa, Yugo
Kamasawa, Naomi
Harada, Harumi
Itakura, Makoto
Molnár, Elek
Abe, Manabu
Sakimura, Kenji
Shigemoto, Ryuichi
author_sort Rubio, María E.
collection PubMed
description The neurotransmitter receptor subtype, number, density, and distribution relative to the location of transmitter release sites are key determinants of signal transmission. AMPA-type ionotropic glutamate receptors (AMPARs) containing GluA3 and GluA4 subunits are prominently expressed in subsets of neurons capable of firing action potentials at high frequencies, such as auditory relay neurons. The auditory nerve (AN) forms glutamatergic synapses on two types of relay neurons, bushy cells (BCs) and fusiform cells (FCs) of the cochlear nucleus. AN-BC and AN-FC synapses have distinct kinetics; thus, we investigated whether the number, density, and localization of GluA3 and GluA4 subunits in these synapses are differentially organized using quantitative freeze-fracture replica immunogold labeling. We identify a positive correlation between the number of AMPARs and the size of AN-BC and AN-FC synapses. Both types of AN synapses have similar numbers of AMPARs; however, the AN-BC have a higher density of AMPARs than AN-FC synapses, because the AN-BC synapses are smaller. A higher number and density of GluA3 subunits are observed at AN-BC synapses, whereas a higher number and density of GluA4 subunits are observed at AN-FC synapses. The intrasynaptic distribution of immunogold labeling revealed that AMPAR subunits, particularly GluA3, are concentrated at the center of the AN-BC synapses. The central distribution of AMPARs is absent in GluA3-knockout mice, and gold particles are evenly distributed along the postsynaptic density. GluA4 gold labeling was homogenously distributed along both synapse types. Thus, GluA3 and GluA4 subunits are distributed at AN synapses in a target-cell-dependent manner. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1007/s00429-017-1408-0) contains supplementary material, which is available to authorized users.
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spelling pubmed-56768372017-11-21 The number and distribution of AMPA receptor channels containing fast kinetic GluA3 and GluA4 subunits at auditory nerve synapses depend on the target cells Rubio, María E. Matsui, Ko Fukazawa, Yugo Kamasawa, Naomi Harada, Harumi Itakura, Makoto Molnár, Elek Abe, Manabu Sakimura, Kenji Shigemoto, Ryuichi Brain Struct Funct Original Article The neurotransmitter receptor subtype, number, density, and distribution relative to the location of transmitter release sites are key determinants of signal transmission. AMPA-type ionotropic glutamate receptors (AMPARs) containing GluA3 and GluA4 subunits are prominently expressed in subsets of neurons capable of firing action potentials at high frequencies, such as auditory relay neurons. The auditory nerve (AN) forms glutamatergic synapses on two types of relay neurons, bushy cells (BCs) and fusiform cells (FCs) of the cochlear nucleus. AN-BC and AN-FC synapses have distinct kinetics; thus, we investigated whether the number, density, and localization of GluA3 and GluA4 subunits in these synapses are differentially organized using quantitative freeze-fracture replica immunogold labeling. We identify a positive correlation between the number of AMPARs and the size of AN-BC and AN-FC synapses. Both types of AN synapses have similar numbers of AMPARs; however, the AN-BC have a higher density of AMPARs than AN-FC synapses, because the AN-BC synapses are smaller. A higher number and density of GluA3 subunits are observed at AN-BC synapses, whereas a higher number and density of GluA4 subunits are observed at AN-FC synapses. The intrasynaptic distribution of immunogold labeling revealed that AMPAR subunits, particularly GluA3, are concentrated at the center of the AN-BC synapses. The central distribution of AMPARs is absent in GluA3-knockout mice, and gold particles are evenly distributed along the postsynaptic density. GluA4 gold labeling was homogenously distributed along both synapse types. Thus, GluA3 and GluA4 subunits are distributed at AN synapses in a target-cell-dependent manner. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1007/s00429-017-1408-0) contains supplementary material, which is available to authorized users. Springer Berlin Heidelberg 2017-04-10 2017 /pmc/articles/PMC5676837/ /pubmed/28397107 http://dx.doi.org/10.1007/s00429-017-1408-0 Text en © The Author(s) 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided 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.
spellingShingle Original Article
Rubio, María E.
Matsui, Ko
Fukazawa, Yugo
Kamasawa, Naomi
Harada, Harumi
Itakura, Makoto
Molnár, Elek
Abe, Manabu
Sakimura, Kenji
Shigemoto, Ryuichi
The number and distribution of AMPA receptor channels containing fast kinetic GluA3 and GluA4 subunits at auditory nerve synapses depend on the target cells
title The number and distribution of AMPA receptor channels containing fast kinetic GluA3 and GluA4 subunits at auditory nerve synapses depend on the target cells
title_full The number and distribution of AMPA receptor channels containing fast kinetic GluA3 and GluA4 subunits at auditory nerve synapses depend on the target cells
title_fullStr The number and distribution of AMPA receptor channels containing fast kinetic GluA3 and GluA4 subunits at auditory nerve synapses depend on the target cells
title_full_unstemmed The number and distribution of AMPA receptor channels containing fast kinetic GluA3 and GluA4 subunits at auditory nerve synapses depend on the target cells
title_short The number and distribution of AMPA receptor channels containing fast kinetic GluA3 and GluA4 subunits at auditory nerve synapses depend on the target cells
title_sort number and distribution of ampa receptor channels containing fast kinetic glua3 and glua4 subunits at auditory nerve synapses depend on the target cells
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5676837/
https://www.ncbi.nlm.nih.gov/pubmed/28397107
http://dx.doi.org/10.1007/s00429-017-1408-0
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