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

Author:

Bellegarda Celine1ORCID,Zavard Guillaume1ORCID,Moisan Lionel2,Brochard-Wyart Françoise3ORCID,Joanny Jean-François34ORCID,Gray Ryan S5ORCID,Cantaut-Belarif Yasmine1,Wyart Claire1ORCID

Affiliation:

1. Sorbonne Université, Paris Brain Institute (Institut du Cerveau, ICM), Institut National de la Santé et de la Recherche Médicale U1127, Centre National de la Recherche Scientifique Unité Mixte de Recherche 7225, Assistance Publique–Hôpitaux de Paris, Campus Hospitalier Pitié-Salpêtrière

2. Université Paris Cité, CNRS, MAP5

3. Paris Sciences et Lettres (PSL) University, Institut Curie, Sorbonne Université

4. Paris Sciences et Lettres (PSL) University, Collège de France

5. Dell Pediatrics Research Institute, The University of Texas at Austin

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.

Funder

Human Frontier Science Program

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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