Characterization of multiciliated ependymal cells that emerge in the neurogenic niche of the aged zebrafish brain

Abstract

In mammals, ventricular walls of the developing brain maintain a neurogenic niche, in which radial glial cells act as neural stem cells (NSCs) and generate new neurons in the embryo. In the adult brain, the neurogenic niche is maintained in the ventricular-subventricular zone (V-SVZ) of the lateral wall of lateral ventricles and the hippocampal dentate gyrus. In the neonatal V-SVZ, radial glial cells transform into astrocytic postnatal NSCs and multiciliated ependymal cells. On the other hand, in zebrafish, radial glial cells continue to cover the surface of the adult telencephalic ventricle and maintain a higher neurogenic potential in the adult brain. However, the cell composition of the neurogenic niche of the aged zebrafish brain has not been investigated. Here we show that multiciliated ependymal cells emerge in the neurogenic niche of the aged zebrafish telencephalon. These multiciliated cells appear predominantly in the dorsal part of the ventral telencephalic ventricular zone, which also contains clusters of migrating new neurons. Scanning electron microscopy and live imaging analyses indicated that these multiple cilia beat coordinately and generate constant fluid flow within the ventral telencephalic ventricle. Analysis of the cell composition by transmission electron microscopy revealed that the neurogenic niche in the aged zebrafish contains different types of cells, with ultrastructures similar to those of ependymal cells, transit-amplifying cells, and migrating new neurons in postnatal mice. These data suggest that the transformation capacity of radial glial cells is conserved but that its timing is different between fish and mice. J. Comp. Neurol. 524:2982-2992, 2016. © 2016 Wiley Periodicals, Inc.

Ciliary Beating Compartmentalizes Cerebrospinal Fluid Flow in the Brain and Regulates Ventricular Development

“…From fish to mammals, the brain ventricles of vertebrates are decorated with motile ciliated cells [ 12 , 14 , 15 , 16 , 17 , 24 , 25 , 26 , 27 ]. It is, however, less clear when these motile ciliated cells appear during development and whether they occupy specific spatial locations, which could facilitate their function.…”

“…In contrast, motile ciliated cells in the larval zebrafish brain ventricles appear to be monociliated and beat in a rotational movement, which is typical for monociliated cells, including sperm [ 41 ] and cells in the left-right organizer [ 42 ]. Few studies reported multiciliated ependymal cells in the adult zebrafish, in the ventricle wall located between the corpus cerebelli and the medulla oblongata [ 17 ] and in the diencephalic and telencephalic ventricle [ 25 , 26 ], where foxj1a is expressed [ 56 ]. It will be exciting to investigate whether these multiciliated cells and the monociliated cells we identified at larval stage arise from the same progenitor pool and co-exist in the adult zebrafish brain.…”

Cellular composition and organization of the spinal cord central canal during metamorphosis of the frog Xenopus laevis

“…The multiciliated cells that we identified in the cervical spinal cord of froglets do not seem to have counterparts in other nonmammalian species. For example, in zebrafish, multiciliated cells have only been described in the brain ventricles (Ogino et al ). Interestingly, in mammals multiciliated cells without proliferative capacity are present in macaque and human spinal cord (Alfaro‐Cervello et al, ), but not in rodents (Alfaro‐Cervello et al, ).…”

The role of motile cilia in the development and physiology of the nervous system

“…Already in 1836, the neuroanatomist Purkinje described ciliary beating on cells along the sheep ventricles [127]. Since then, these cells, referred to as ependymal cells (ECs), have been described in both fish [32,110,[128][129][130], amphibians [131][132][133] and mammals [16,123]. Traditionally, the ECs of the brain are defined as Foxj1positive, motile ciliated, cuboidal cells generating nearwall CSF flow [16,32,[133][134][135][136].…”