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Rearrangements between differentiating hair cells coordinate planar polarity

In addition to their ubiquitous apical-basal polarity, many epithelia are also polarized within the orthogonal plane, a phenomenon termed planar cell polarity. In the mammalian inner ear and the zebrafish lateral line, polarity is revealed through the orientation of mechanosensitive hair cells relative to each other and to the body axes. In each neuromast, the receptor organ of the lateral line, hair bundles are arranged in a mirror-symmetrical fashion. We showed that the establishment of mirror symmetry is preceded by rotational rearrangements between hair-cell pairs, a behavior consistently associated with the division of hair-cell precursors. Time-lapse imaging of trilobite mutants, which lack the core planar-cell-polarity constituent Vang-like protein 2 (Vangl2), showed that their misoriented hair cells correlate with misaligned divisions of hair-cell precursors and an inability to complete rearrangements accurately. Vangl2 is asymmetrically localized in the cells of the neuromast, a configuration required for the accurate completion of rearrangements. Manipulation of Vangl2 expression or of Notch signaling resulted in a uniform hair-cell polarity, indicating that rearrangements refine neuromast polarity with respect to the body axes.

Mitosis of a transit amplifying cell produces a pair of nascent hair cells (blue arrowhead). Roughly an hour later, the two cells begin to dance back and forth, resulting in about 70% of cases in an exchange of positions. The daughter cells eventually separate (pink arrowheads) and assume opposite morphological and functional polarities.