Synaptic coupling of inner ear sensory cells is controlled by brevican-based extracellular matrix baskets resembling perineuronal nets

BACKGROUND: Perineuronal nets (PNNs) are specialized aggregations of extracellular matrix (ECM) molecules surrounding specific neurons in the central nervous system (CNS). PNNs are supposed to control synaptic transmission and are frequently associated with neurons firing at high rates, including pr...

Descripción completa

Detalles Bibliográficos
Autores principales: Sonntag, Mandy, Blosa, Maren, Schmidt, Sophie, Reimann, Katja, Blum, Kerstin, Eckrich, Tobias, Seeger, Gudrun, Hecker, Dietmar, Schick, Bernhard, Arendt, Thomas, Engel, Jutta, Morawski, Markus
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6156866/
https://www.ncbi.nlm.nih.gov/pubmed/30253762
http://dx.doi.org/10.1186/s12915-018-0566-8
_version_ 1783358173586915328
author Sonntag, Mandy
Blosa, Maren
Schmidt, Sophie
Reimann, Katja
Blum, Kerstin
Eckrich, Tobias
Seeger, Gudrun
Hecker, Dietmar
Schick, Bernhard
Arendt, Thomas
Engel, Jutta
Morawski, Markus
author_facet Sonntag, Mandy
Blosa, Maren
Schmidt, Sophie
Reimann, Katja
Blum, Kerstin
Eckrich, Tobias
Seeger, Gudrun
Hecker, Dietmar
Schick, Bernhard
Arendt, Thomas
Engel, Jutta
Morawski, Markus
author_sort Sonntag, Mandy
collection PubMed
description BACKGROUND: Perineuronal nets (PNNs) are specialized aggregations of extracellular matrix (ECM) molecules surrounding specific neurons in the central nervous system (CNS). PNNs are supposed to control synaptic transmission and are frequently associated with neurons firing at high rates, including principal neurons of auditory brainstem nuclei. The origin of high-frequency activity of auditory brainstem neurons is the indefatigable sound-driven transmitter release of inner hair cells (IHCs) in the cochlea. RESULTS: Here, we show that synaptic poles of IHCs are ensheathed by basket-like ECM complexes formed by the same molecules that constitute PNNs of neurons in the CNS, including brevican, aggreccan, neurocan, hyaluronan, and proteoglycan link proteins 1 and 4 and tenascin-R. Genetic deletion of brevican, one of the main components, resulted in a massive degradation of ECM baskets at IHCs, a significant impairment in spatial coupling of pre- and postsynaptic elements and mild impairment of hearing. CONCLUSIONS: These ECM baskets potentially contribute to control of synaptic transmission at IHCs and might be functionally related to PNNs of neurons in the CNS. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12915-018-0566-8) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-6156866
institution National Center for Biotechnology Information
language English
publishDate 2018
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-61568662018-09-27 Synaptic coupling of inner ear sensory cells is controlled by brevican-based extracellular matrix baskets resembling perineuronal nets Sonntag, Mandy Blosa, Maren Schmidt, Sophie Reimann, Katja Blum, Kerstin Eckrich, Tobias Seeger, Gudrun Hecker, Dietmar Schick, Bernhard Arendt, Thomas Engel, Jutta Morawski, Markus BMC Biol Research Article BACKGROUND: Perineuronal nets (PNNs) are specialized aggregations of extracellular matrix (ECM) molecules surrounding specific neurons in the central nervous system (CNS). PNNs are supposed to control synaptic transmission and are frequently associated with neurons firing at high rates, including principal neurons of auditory brainstem nuclei. The origin of high-frequency activity of auditory brainstem neurons is the indefatigable sound-driven transmitter release of inner hair cells (IHCs) in the cochlea. RESULTS: Here, we show that synaptic poles of IHCs are ensheathed by basket-like ECM complexes formed by the same molecules that constitute PNNs of neurons in the CNS, including brevican, aggreccan, neurocan, hyaluronan, and proteoglycan link proteins 1 and 4 and tenascin-R. Genetic deletion of brevican, one of the main components, resulted in a massive degradation of ECM baskets at IHCs, a significant impairment in spatial coupling of pre- and postsynaptic elements and mild impairment of hearing. CONCLUSIONS: These ECM baskets potentially contribute to control of synaptic transmission at IHCs and might be functionally related to PNNs of neurons in the CNS. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12915-018-0566-8) contains supplementary material, which is available to authorized users. BioMed Central 2018-09-26 /pmc/articles/PMC6156866/ /pubmed/30253762 http://dx.doi.org/10.1186/s12915-018-0566-8 Text en © Morawski et al. 2018 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. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Sonntag, Mandy
Blosa, Maren
Schmidt, Sophie
Reimann, Katja
Blum, Kerstin
Eckrich, Tobias
Seeger, Gudrun
Hecker, Dietmar
Schick, Bernhard
Arendt, Thomas
Engel, Jutta
Morawski, Markus
Synaptic coupling of inner ear sensory cells is controlled by brevican-based extracellular matrix baskets resembling perineuronal nets
title Synaptic coupling of inner ear sensory cells is controlled by brevican-based extracellular matrix baskets resembling perineuronal nets
title_full Synaptic coupling of inner ear sensory cells is controlled by brevican-based extracellular matrix baskets resembling perineuronal nets
title_fullStr Synaptic coupling of inner ear sensory cells is controlled by brevican-based extracellular matrix baskets resembling perineuronal nets
title_full_unstemmed Synaptic coupling of inner ear sensory cells is controlled by brevican-based extracellular matrix baskets resembling perineuronal nets
title_short Synaptic coupling of inner ear sensory cells is controlled by brevican-based extracellular matrix baskets resembling perineuronal nets
title_sort synaptic coupling of inner ear sensory cells is controlled by brevican-based extracellular matrix baskets resembling perineuronal nets
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6156866/
https://www.ncbi.nlm.nih.gov/pubmed/30253762
http://dx.doi.org/10.1186/s12915-018-0566-8
work_keys_str_mv AT sonntagmandy synapticcouplingofinnerearsensorycellsiscontrolledbybrevicanbasedextracellularmatrixbasketsresemblingperineuronalnets
AT blosamaren synapticcouplingofinnerearsensorycellsiscontrolledbybrevicanbasedextracellularmatrixbasketsresemblingperineuronalnets
AT schmidtsophie synapticcouplingofinnerearsensorycellsiscontrolledbybrevicanbasedextracellularmatrixbasketsresemblingperineuronalnets
AT reimannkatja synapticcouplingofinnerearsensorycellsiscontrolledbybrevicanbasedextracellularmatrixbasketsresemblingperineuronalnets
AT blumkerstin synapticcouplingofinnerearsensorycellsiscontrolledbybrevicanbasedextracellularmatrixbasketsresemblingperineuronalnets
AT eckrichtobias synapticcouplingofinnerearsensorycellsiscontrolledbybrevicanbasedextracellularmatrixbasketsresemblingperineuronalnets
AT seegergudrun synapticcouplingofinnerearsensorycellsiscontrolledbybrevicanbasedextracellularmatrixbasketsresemblingperineuronalnets
AT heckerdietmar synapticcouplingofinnerearsensorycellsiscontrolledbybrevicanbasedextracellularmatrixbasketsresemblingperineuronalnets
AT schickbernhard synapticcouplingofinnerearsensorycellsiscontrolledbybrevicanbasedextracellularmatrixbasketsresemblingperineuronalnets
AT arendtthomas synapticcouplingofinnerearsensorycellsiscontrolledbybrevicanbasedextracellularmatrixbasketsresemblingperineuronalnets
AT engeljutta synapticcouplingofinnerearsensorycellsiscontrolledbybrevicanbasedextracellularmatrixbasketsresemblingperineuronalnets
AT morawskimarkus synapticcouplingofinnerearsensorycellsiscontrolledbybrevicanbasedextracellularmatrixbasketsresemblingperineuronalnets