Basal body contains a “latchbolt” to enable directional ciliary beat across epithelia

Abstract Motile cilia unify the orientation of their 9+2 axonemes across epithelia to drive directional liquid flows for various physiological functions. This planar polarity is believed to result from cytoskeleton-driven swiveling of the basal foot (BF), a basal body (BB) appendage that marks the axonemal orientation, in response to intrinsic and extrinsic cues. How and when the BF-axoneme relationship is established, however, are basic issues unaddressed. Here, we show that BFs and axonemal orientations are initially uncoupled and require a rotationally-asymmetric, Ccdc57-positive “latchbolt” in BB distal lumen to lock them in position. Furthermore, multicilia in individual mouse ependymal cells achieve uniform axonemal orientations and beat directions independently of BFs. Accordingly, Ccdc57-deficient multicilia display only cell-level directional beat but lack the planar polarity. This defect impairs cerebrospinal fluid flow, resulting in severe hydrocephalus, kyphosis, and high mortality in mice. These findings unravel brand-new mechanisms governing the planar polarity of epithelial motile cilia.