Current Biology
Volume 22, Issue 23, 4 December 2012, Pages 2203-2212
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Article
Microtubules Enable the Planar Cell Polarity of Airway Cilia

https://doi.org/10.1016/j.cub.2012.09.046Get rights and content
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Summary

Background

Airway cilia must be physically oriented along the longitudinal tissue axis for concerted, directional motility that is essential for proper mucociliary clearance.

Results

We show that planar cell polarity (PCP) signaling specifies directionality and orients respiratory cilia. Within all airway epithelial cells, a conserved set of PCP proteins shows interdependent, asymmetric junctional localization; nonautonomous signaling coordinates polarization between cells; and a polarized microtubule (MT) network is likely required for asymmetric PCP protein localization. We find that basal bodies dock after polarity of PCP proteins is established and are polarized nearly simultaneously, and that refinement of basal body/cilium orientation continues during airway epithelial development. Unique to mature multiciliated cells, we identify PCP-regulated, planar polarized MTs that originate from basal bodies and interact, via their plus ends, with membrane domains associated with the PCP proteins Frizzled and Dishevelled. Disruption of MTs leads to misoriented cilia.

Conclusions

A conserved PCP pathway orients airway cilia by communicating polarity information from asymmetric membrane domains at the apical junctions, through MTs, to orient the MT and actin-based network of ciliary basal bodies below the apical surface.

Highlights

► PCP proteins are asymmetric at apical junctions in the airways before ciliogenesis ► PCP protein asymmetry and cilium orientation emerge gradually during development ► Cilium misorientation correlates with loss of PCP protein asymmetry in PCP mutants ► Microtubules appear to organize cilium orientation and PCP protein asymmetry

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