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Curr Biol. 2015 Nov 2;25(21):2774-2784. doi: 10.1016/j.cub.2015.09.015. Epub 2015 Oct 1.

Mechanical strain determines the axis of planar polarity in ciliated epithelia.

Author information

1
Molecular Neurobiology Laboratory, Salk Institute for Biological Studies, La Jolla, CA 92037, USA.
2
Department of Biology, University of Virginia, Charlottesville, VA 22904, USA.
3
Molecular Neurobiology Laboratory, Salk Institute for Biological Studies, La Jolla, CA 92037, USA. Electronic address: kintner@salk.edu.

Abstract

Epithelia containing multiciliated cells align beating cilia along a common planar axis specified by the conserved planar cell polarity (PCP) pathway. Specification of the planar axis is also thought to require a long-range cue to align the axis globally, but the nature of this cue in ciliated and other epithelia remains poorly understood. We examined this issue using the Xenopus larval skin, where ciliary flow aligns to the anterior-posterior (A-P) axis. We first show that a planar axis initially arises in the developing skin during gastrulation, based on the appearance of polarized apical microtubules and cell junctions with increased levels of stable PCP components. This axis also arises in severely ventralized embryos, despite their deficient embryonic patterning. Because ventralized embryos still gastrulate, producing a mechanical force that strains the developing skin along the A-P axis, we asked whether this strain alone drives global planar patterning. Isolated skin explanted before gastrulation lacks strain and fails to acquire a global planar axis but responds to exogenous strain by undergoing cell elongation, forming polarized apical microtubules, and aligning stable components of the PCP pathway orthogonal to the axis of strain. The planar axis in embryos can be redirected by applying exogenous strain during a critical period around gastrulation. Finally, we provide evidence that apical microtubules and the PCP pathway interact to align the planar axis. These results indicate that oriented tissue strain generated by the gastrulating mesoderm plays a major role in determining the global axis of planar polarity of the developing skin.

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PMID:
26441348
PMCID:
PMC4631806
DOI:
10.1016/j.cub.2015.09.015
[Indexed for MEDLINE]
Free PMC Article

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