Cilia organize ependymal planar polarity.
Multiciliated epithelial cells, called ependymal cells, line the ventricles in the adult brain. Most ependymal cells are born prenatally and are derived from radial glia. Ependymal cells have a remarkable planar polarization that determines orientation of ciliary beating and propulsion of CSF. Disruption of ependymal ciliary beating, by injury or disease, results in aberrant CSF circulation and hydrocephalus, a common disorder of the CNS. Very little is known about the mechanisms guiding ependymal planar polarity and whether this organization is acquired during ependymal cell development or is already present in radial glia. Here we show that basal bodies in ependymal cells in the lateral ventricle walls of adult mice are polarized in two ways: (1) rotational; angle of individual basal bodies with respect to their long axis and (2) translational; the position of basal bodies on the apical surface of the cell. Conditional ablation of motile cilia disrupted rotational orientation, but translational polarity was largely preserved. In contrast, translational polarity was dramatically affected when radial glial primary cilia were ablated earlier in development. Remarkably, radial glia in the embryo have a translational polarity that predicts the orientation of mature ependymal cells. These results suggest that ependymal planar cell polarity is a multistep process initially organized by primary cilia in radial glia and then refined by motile cilia in ependymal cells.
Mirzadeh
Zaman
Z
Department of Neurosurgery, University of California San Francisco, San Francisco, California 94143, USA.
Han
Young-Goo
YG
Soriano-Navarro
Mario
M
García-Verdugo
Jose Manuel
JM
Alvarez-Buylla
Arturo
A
D000199:Actins / Q000378:metabolism; D000818:Animals; D016764:Cell Polarity / Q000502:physiology*; D002923:Cilia / Q000502:physiology / Q000648:ultrastructure; D004805:Ependyma / Q000166:cytology*; D004847:Epithelial Cells / Q000502:physiology*; D049452:Green Fluorescent Proteins / Q000235:genetics; D066298:In Vitro Techniques; D007381:Intermediate Filament Proteins / Q000235:genetics; D016547:Kinesins / Q000378:metabolism; D020547:Lateral Ventricles / Q000166:cytology; D051379:Mice; D008822:Mice, Transgenic; D018613:Microscopy, Confocal / Q000379:methods; D008854:Microscopy, Electron / Q000379:methods; D009419:Nerve Tissue Proteins / Q000235:genetics; D064231:Nestin; D014404:Tubulin / Q000378:metabolism
D000199:Actins; D007381:Intermediate Filament Proteins; C490202:Kif3a protein, mouse; D009419:Nerve Tissue Proteins; C577485:Nes protein, mouse; D064231:Nestin; D014404:Tubulin; D049452:Green Fluorescent Proteins; D016547:Kinesins