Adrenergic activation modulates the signal from the Reissner fiber to cerebrospinal fluid-contacting neurons during development

  1. Yasmine Cantaut-Belarif
  2. Adeline Orts Del'Immagine
  3. Margot Penru
  4. Guillaume Pézeron
  5. Claire Wyart  Is a corresponding author
  6. Pierre-Luc Bardet  Is a corresponding author
  1. Hôpital Pitié-Salpêtrière, Sorbonne Universités, UPMC Univ Paris 06, Inserm, CNRS, France
  2. Paris Brain Institute, ICM, Inserm U 1127, CNRS UMR 7225, Sorbonne Université, France
  3. Museum National d'Histoire Naturelle, France
  4. Institut du Cerveau et la Moelle épinière, Hôpital Pitié-Salpêtrière, Sorbonne Universités, UPMC Univ Paris 06, Inserm, CNRS, France

Abstract

The cerebrospinal fluid (CSF) contains an extracellular thread conserved in vertebrates, the Reissner fiber, which controls body axis morphogenesis in the zebrafish embryo. Yet, the signaling cascade originating from this fiber to ensure body axis straightening is not understood. Here, we explore the functional link between the Reissner fiber and undifferentiated spinal neurons contacting the CSF (CSF-cNs). First, we show that the Reissner fiber is required in vivo for the expression of urp2, a neuropeptide expressed in CSF-cNs. We show that the Reissner fiber is also required for embryonic calcium transients in these spinal neurons. Finally, we study how local adrenergic activation can substitute for the Reissner fiber-signaling pathway to CSF-cNs and rescue body axis morphogenesis. Our results show that the Reissner fiber acts on CSF-cNs and thereby contributes to establish body axis morphogenesis, and suggest it does so by controlling the availability of a chemical signal in the CSF.

Data availability

Data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for 5 figures. The raw RNA-seq data have been deposited in the ArrayExpress database at EMBL-EBI (www.ebi.ac.uk/arrayexpress) under accession number E-MTAB-9615.

The following data sets were generated

Article and author information

Author details

  1. Yasmine Cantaut-Belarif

    Institut du Cerveau et la Moelle épinière, Hôpital Pitié-Salpêtrière, Sorbonne Universités, UPMC Univ Paris 06, Inserm, CNRS, Paris, France
    Competing interests
    No competing interests declared.
  2. Adeline Orts Del'Immagine

    Institut du Cerveau et la Moelle épinière, Paris Brain Institute, ICM, Inserm U 1127, CNRS UMR 7225, Sorbonne Université, Paris, France
    Competing interests
    No competing interests declared.
  3. Margot Penru

    Institut du Cerveau et la Moelle épinière, Paris Brain Institute, ICM, Inserm U 1127, CNRS UMR 7225, Sorbonne Université, Paris, France
    Competing interests
    No competing interests declared.
  4. Guillaume Pézeron

    Molecular Physiology and Adaptation UMR 7221 - CNRS, Museum National d'Histoire Naturelle, Paris, France
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1395-6397
  5. Claire Wyart

    Neurophysiology & Systems neuroscience, Institut du Cerveau et la Moelle épinière, Hôpital Pitié-Salpêtrière, Sorbonne Universités, UPMC Univ Paris 06, Inserm, CNRS, Paris, France
    For correspondence
    claire.wyart@icm-institute.org
    Competing interests
    Claire Wyart, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1668-4975
  6. Pierre-Luc Bardet

    Institut du Cerveau et la Moelle épinière, Paris Brain Institute, ICM, Inserm U 1127, CNRS UMR 7225, Sorbonne Université, Paris, France
    For correspondence
    pierreluc.bardet@icm-institute.org
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1766-1318

Funding

Agence Nationale de la Recherche (ANR-10- IAIHU-06)

  • Yasmine Cantaut-Belarif
  • Margot Penru
  • Claire Wyart
  • Pierre-Luc Bardet

Agence Nationale de la Recherche (ANR-11-INBS-0011)

  • Yasmine Cantaut-Belarif
  • Adeline Orts Del'Immagine
  • Margot Penru
  • Claire Wyart
  • Pierre-Luc Bardet

HFSP (#RGP0063/2018)

  • Yasmine Cantaut-Belarif
  • Adeline Orts Del'Immagine
  • Claire Wyart
  • Pierre-Luc Bardet

Schlumberger Foundation (FSER/2017)

  • Claire Wyart

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All procedures were performed on zebrafish embryos in accordance with the European Communities Council Directive (2010/63/EU) and French law (87/848). This project is included the APAFIS project #16469-2018071217081175 approved by the French Ministry for Research for the Paris Brain Institute (ICM).

Copyright

© 2020, Cantaut-Belarif et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Yasmine Cantaut-Belarif
  2. Adeline Orts Del'Immagine
  3. Margot Penru
  4. Guillaume Pézeron
  5. Claire Wyart
  6. Pierre-Luc Bardet
(2020)
Adrenergic activation modulates the signal from the Reissner fiber to cerebrospinal fluid-contacting neurons during development
eLife 9:e59469.
https://doi.org/10.7554/eLife.59469

Share this article

https://doi.org/10.7554/eLife.59469

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