The Reissner fiber under tension in vivo shows dynamic interaction with ciliated cells contacting the cerebrospinal fluid
- Paris Brain Institute, Sorbonne Université, France
- Université Paris Cité, CNRS, MAP5, France
- Institut Curie, CNRS UMR168, France
- The University of Texas at Austin, United States
- 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
-
Data drom: The Reissner fiber under tension in vivo shows dynamic interaction with ciliated cells contacting the cerebrospinal fluidDryad Digital Repository, doi:10.5061/dryad.573n5tbc2.
Article and author information
Author details
Jean-François Joanny
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
-
- 910
- views
-
- 171
- downloads
-
- 2
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Citations by DOI
-
- 2
- citations for umbrella DOI https://doi.org/10.7554/eLife.86175
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)
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
