The dual developmental origin of spinal cerebrospinal fluid-contacting neurons gives rise to distinct functional subtypes

Abstract Chemical and mechanical cues from the cerebrospinal fluid (CSF) can affect the development and function of the central nervous system (CNS). How such cues are detected and relayed to the CNS remains elusive. Cerebrospinal fluid-contacting neurons (CSF-cNs) situated at the interface between...

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Main Authors: Lydia Djenoune, Laura Desban, Johanna Gomez, Jenna R. Sternberg, Andrew Prendergast, Dominique Langui, Feng B. Quan, Hugo Marnas, Thomas O. Auer, Jean-Paul Rio, Filippo Del Bene, Pierre-Luc Bardet, Claire Wyart
Format: Article
Language:English
Published: Nature Publishing Group 2017-04-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-017-00350-1
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spelling doaj-cee34d7591db4642a247a6dcd272d2df2020-12-08T00:47:03ZengNature Publishing GroupScientific Reports2045-23222017-04-017111410.1038/s41598-017-00350-1The dual developmental origin of spinal cerebrospinal fluid-contacting neurons gives rise to distinct functional subtypesLydia Djenoune0Laura Desban1Johanna Gomez2Jenna R. Sternberg3Andrew Prendergast4Dominique Langui5Feng B. Quan6Hugo Marnas7Thomas O. Auer8Jean-Paul Rio9Filippo Del Bene10Pierre-Luc Bardet11Claire Wyart12Sorbonne UniversitésSorbonne UniversitésSorbonne UniversitésSorbonne UniversitésSorbonne UniversitésSorbonne UniversitésSorbonne UniversitésSorbonne UniversitésInstitut CurieSorbonne UniversitésInstitut CurieSorbonne UniversitésSorbonne UniversitésAbstract Chemical and mechanical cues from the cerebrospinal fluid (CSF) can affect the development and function of the central nervous system (CNS). How such cues are detected and relayed to the CNS remains elusive. Cerebrospinal fluid-contacting neurons (CSF-cNs) situated at the interface between the CSF and the CNS are ideally located to convey such information to local networks. In the spinal cord, these GABAergic neurons expressing the PKD2L1 channel extend an apical extension into the CSF and an ascending axon in the spinal cord. In zebrafish and mouse spinal CSF-cNs originate from two distinct progenitor domains characterized by distinct cascades of transcription factors. Here we ask whether these neurons with different developmental origins differentiate into cells types with different functional properties. We show in zebrafish larva that the expression of specific markers, the morphology of the apical extension and axonal projections, as well as the neuronal targets contacted by CSF-cN axons, distinguish the two CSF-cN subtypes. Altogether our study demonstrates that the developmental origins of spinal CSF-cNs give rise to two distinct functional populations of sensory neurons. This work opens novel avenues to understand how these subtypes may carry distinct functions related to development of the spinal cord, locomotion and posture.https://doi.org/10.1038/s41598-017-00350-1
collection DOAJ
language English
format Article
sources DOAJ
author Lydia Djenoune
Laura Desban
Johanna Gomez
Jenna R. Sternberg
Andrew Prendergast
Dominique Langui
Feng B. Quan
Hugo Marnas
Thomas O. Auer
Jean-Paul Rio
Filippo Del Bene
Pierre-Luc Bardet
Claire Wyart
spellingShingle Lydia Djenoune
Laura Desban
Johanna Gomez
Jenna R. Sternberg
Andrew Prendergast
Dominique Langui
Feng B. Quan
Hugo Marnas
Thomas O. Auer
Jean-Paul Rio
Filippo Del Bene
Pierre-Luc Bardet
Claire Wyart
The dual developmental origin of spinal cerebrospinal fluid-contacting neurons gives rise to distinct functional subtypes
Scientific Reports
author_facet Lydia Djenoune
Laura Desban
Johanna Gomez
Jenna R. Sternberg
Andrew Prendergast
Dominique Langui
Feng B. Quan
Hugo Marnas
Thomas O. Auer
Jean-Paul Rio
Filippo Del Bene
Pierre-Luc Bardet
Claire Wyart
author_sort Lydia Djenoune
title The dual developmental origin of spinal cerebrospinal fluid-contacting neurons gives rise to distinct functional subtypes
title_short The dual developmental origin of spinal cerebrospinal fluid-contacting neurons gives rise to distinct functional subtypes
title_full The dual developmental origin of spinal cerebrospinal fluid-contacting neurons gives rise to distinct functional subtypes
title_fullStr The dual developmental origin of spinal cerebrospinal fluid-contacting neurons gives rise to distinct functional subtypes
title_full_unstemmed The dual developmental origin of spinal cerebrospinal fluid-contacting neurons gives rise to distinct functional subtypes
title_sort dual developmental origin of spinal cerebrospinal fluid-contacting neurons gives rise to distinct functional subtypes
publisher Nature Publishing Group
series Scientific Reports
issn 2045-2322
publishDate 2017-04-01
description Abstract Chemical and mechanical cues from the cerebrospinal fluid (CSF) can affect the development and function of the central nervous system (CNS). How such cues are detected and relayed to the CNS remains elusive. Cerebrospinal fluid-contacting neurons (CSF-cNs) situated at the interface between the CSF and the CNS are ideally located to convey such information to local networks. In the spinal cord, these GABAergic neurons expressing the PKD2L1 channel extend an apical extension into the CSF and an ascending axon in the spinal cord. In zebrafish and mouse spinal CSF-cNs originate from two distinct progenitor domains characterized by distinct cascades of transcription factors. Here we ask whether these neurons with different developmental origins differentiate into cells types with different functional properties. We show in zebrafish larva that the expression of specific markers, the morphology of the apical extension and axonal projections, as well as the neuronal targets contacted by CSF-cN axons, distinguish the two CSF-cN subtypes. Altogether our study demonstrates that the developmental origins of spinal CSF-cNs give rise to two distinct functional populations of sensory neurons. This work opens novel avenues to understand how these subtypes may carry distinct functions related to development of the spinal cord, locomotion and posture.
url https://doi.org/10.1038/s41598-017-00350-1
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