The Reissner fiber under tension in vivo shows dynamic interaction with ciliated cells contacting the cerebrospinal fluid

  1. Celine Bellegarda
  2. Guillaume Zavard
  3. Lionel Moisan
  4. Françoise Brochard-Wyart
  5. Jean-François Joanny
  6. Ryan S Gray
  7. Yasmine Cantaut-Belarif
  8. Claire Wyart  Is a corresponding author
  1. Paris Brain Institute, Sorbonne Université, France
  2. Université Paris Cité, CNRS, MAP5, France
  3. Institut Curie, CNRS UMR168, France
  4. The University of Texas at Austin, United States
  5. Paris Brain Institute (ICM), Sorbonne Université, France

Abstract

The Reissner fiber (RF) is an acellular thread positioned in the midline of the central canal that aggregates thanks to the beating of numerous cilia from ependymal radial glial cells (ERGs) generating flow in the central canal of the spinal cord. RF together with cerebrospinal fluid (CSF)-contacting neurons (CSF-cNs) form an axial sensory system detecting curvature. How RF, CSF-cNs and the multitude of motile cilia from ERGs interact in vivo appears critical for maintenance of RF and sensory functions of CSF-cNs to keep a straight body axis, but is not well-understood. Using in vivo imaging in larval zebrafish, we show that RF is under tension and resonates dorsoventrally. Focal RF ablations trigger retraction and relaxation of the fiber’s cut ends, with larger retraction speeds for rostral ablations. We built a mechanical model that estimates RF stress diffusion coefficient D at 5 mm2/s and reveals that tension builds up rostrally along the fiber. After RF ablation, spontaneous CSF-cN activity decreased and ciliary motility changed, suggesting physical interactions between RF and cilia projecting into the central canal. We observed that motile cilia were caudally-tilted and frequently interacted with RF. We propose that the numerous ependymal motile monocilia contribute to RF's heterogenous tension via weak interactions. Our work demonstrates that under tension, the Reissner fiber dynamically interacts with motile cilia generating CSF flow and spinal sensory neurons.

Data availability

All code are accessible on GitHub and processed data from imaging and ablation experiments are available here:https://doi.org/10.5061/dryad.573n5tbc2

The following data sets were generated

Article and author information

Author details

  1. Celine Bellegarda

    Paris Brain Institute, Sorbonne Université, Paris, France
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4394-295X
  2. Guillaume Zavard

    Paris Brain Institute, Sorbonne Université, Paris, France
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8948-4387
  3. Lionel Moisan

    Université Paris Cité, CNRS, MAP5, Paris, France
    Competing interests
    No competing interests declared.
  4. Françoise Brochard-Wyart

    Institut Curie, CNRS UMR168, Paris, France
    Competing interests
    No competing interests declared.
  5. Jean-François Joanny

    Institut Curie, CNRS UMR168, Paris, France
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6966-3222
  6. Ryan S Gray

    Dell Pediatrics Research Institute, The University of Texas at Austin, Austin, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9668-6497
  7. Yasmine Cantaut-Belarif

    Paris Brain Institute, Sorbonne Université, Paris, France
    Competing interests
    No competing interests declared.
  8. Claire Wyart

    Paris Brain Institute (ICM), Sorbonne Université, 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

Funding

Human Frontier Science Program (2017/RG0063)

  • 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: Animal handling and procedures were validated by the Paris Brain Institute (ICM) and the French National Ethics Committee (ComiteNational de Reflexion Ethique sur l'Experimentation Animale; APAFIS # 2018071217081175) in agreement with EU legislation. All experimentswere performed on Danio rerio 3 days old larvae of AB Larvae raised in the same conditions.Experiments were performed at RT on 3 days post fertilization (dpf) larvae based on the protocol of each experiment.

Copyright

© 2023, Bellegarda 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.

Metrics

  • 854
    views
  • 167
    downloads
  • 1
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Celine Bellegarda
  2. Guillaume Zavard
  3. Lionel Moisan
  4. Françoise Brochard-Wyart
  5. Jean-François Joanny
  6. Ryan S Gray
  7. Yasmine Cantaut-Belarif
  8. Claire Wyart
(2023)
The Reissner fiber under tension in vivo shows dynamic interaction with ciliated cells contacting the cerebrospinal fluid
eLife 12:e86175.
https://doi.org/10.7554/eLife.86175

Share this article

https://doi.org/10.7554/eLife.86175

Further reading

    1. Physics of Living Systems
    James E Hammond, Ruth E Baker, Berta Verd
    Research Article

    Vertebrates have evolved great diversity in the number of segments dividing the trunk body, however, the developmental origin of the evolvability of this trait is poorly understood. The number of segments is thought to be determined in embryogenesis as a product of morphogenesis of the pre-somitic mesoderm (PSM) and the periodicity of a molecular oscillator active within the PSM known as the segmentation clock. Here, we explore whether the clock and PSM morphogenesis exhibit developmental modularity, as independent evolution of these two processes may explain the high evolvability of segment number. Using a computational model of the clock and PSM parameterised for zebrafish, we find that the clock is broadly robust to variation in morphogenetic processes such as cell ingression, motility, compaction, and cell division. We show that this robustness is in part determined by the length of the PSM and the strength of phase coupling in the clock. As previous studies report no changes to morphogenesis upon perturbing the clock, we suggest that the clock and morphogenesis of the PSM exhibit developmental modularity.

    1. Physics of Living Systems
    Emmanuel Akabuogu, Victor Carneiro da Cunha Martorelli ... Thomas A Waigh
    Research Article

    Bacterial biofilms are communities of bacteria usually attached to solid strata and often differentiated into complex structures. Communication across biofilms has been shown to involve chemical signaling and, more recently, electrical signaling in Gram-positive biofilms. We report for the first time, community-level synchronized membrane potential dynamics in three-dimensional Escherichia coli biofilms. Two hyperpolarization events are observed in response to light stress. The first requires mechanically sensitive ion channels (MscK, MscL, and MscS) and the second needs the Kch-potassium channel. The channels mediated both local spiking of single E. coli biofilms and long-range coordinated electrical signaling in E. coli biofilms. The electrical phenomena are explained using Hodgkin-Huxley and 3D fire-diffuse-fire agent-based models. These data demonstrate that electrical wavefronts based on potassium ions are a mechanism by which signaling occurs in Gram-negative biofilms and as such may represent a conserved mechanism for communication across biofilms.