Coupling between hydrodynamic forces and planar cell polarity orients mammalian motile cilia

Author:  ["Boris Guirao","Alice Meunier","Stéphane Mortaud","Andrea Aguilar","Jean-Marc Corsi","Laetitia Strehl","Yuki Hirota","Angélique Desoeuvre","Camille Boutin","Young-Goo Han","Zaman Mirzadeh","Harold Cremer","Mireille Montcouquiol","Kazunobu Sawamoto","Nathalie Spassky"]

Publication:  Nature Cell Biology

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Tags:  Cilia   Morphogenesis   Biological

Abstract

Motile cilia direct efficient, oriented flow, which is ensured by alignment of their beating. In mammalian brain ventricles, coupling between hydrodynamic forces and the planar cell polarity protein Vangl2 allows cilia that have docked in random orientation to reorient in a uniform direction. In mammals, motile cilia cover many organs, such as fallopian tubes, respiratory tracts and brain ventricles. The development and function of these organs critically depend on efficient directional fluid flow ensured by the alignment of ciliary beating. To identify the mechanisms involved in this process, we analysed motile cilia of mouse brain ventricles, using biophysical and molecular approaches. Our results highlight an original orientation mechanism for ependymal cilia whereby basal bodies first dock apically with random orientations, and then reorient in a common direction through a coupling between hydrodynamic forces and the planar cell polarity (PCP) protein Vangl2, within a limited time-frame. This identifies a direct link between external hydrodynamic cues and intracellular PCP signalling. Our findings extend known PCP mechanisms by integrating hydrodynamic forces as long-range polarity signals, argue for a possible sensory role of ependymal cilia, and will be of interest for the study of fluid flow-mediated morphogenesis.

Cite this article

Guirao, B., Meunier, A., Mortaud, S. et al. Coupling between hydrodynamic forces and planar cell polarity orients mammalian motile cilia. Nat Cell Biol 12, 341–350 (2010). https://doi.org/10.1038/ncb2040

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