Prickle isoforms determine handedness of helical morphogenesis

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Abstract

Subcellular asymmetry directed by the planar cell polarity (PCP) signaling pathway orients numerous morphogenetic events in both invertebrates and vertebrates. Here, we describe a morphogenetic movement in which the intertwined socket and shaft cells of the Drosophila anterior wing margin mechanosensory bristles undergo PCP-directed apical rotation, inducing twisting that results in a helical structure of defined chirality. We show that the Frizzled/Vang PCP signaling module coordinates polarity among and between bristles and surrounding cells to direct this rotation. Furthermore, we show that dynamic interplay between two isoforms of the Prickle protein determines right- or left-handed bristle morphogenesis. We provide evidence that, Frizzled/Vang signaling couples to the Fat/Dachsous PCP directional signal in opposite directions depending on whether Pk^pk or Pk^sple predominates. Dynamic interplay between Pk isoforms is likely to be an important determinant of PCP outcomes in diverse contexts. Similar mechanisms may orient other lateralizing morphogenetic processes.

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All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for all figures containing quantitative data.

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Bomsoo Cho

Department of Pathology, Stanford University School of Medicine, Stanford, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-8970-9160
Song Song

Department of Pathology, Stanford University School of Medicine, Stanford, United States

Competing interests
The authors declare that no competing interests exist.
Jeffrey D Axelrod

Department of Pathology, Stanford University School of Medicine, Stanford, United States

For correspondence
jaxelrod@stanford.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-6094-7392

Funding

National Institute of General Medical Sciences (R01 GM097081)

Jeffrey D Axelrod

National Institute of General Medical Sciences (R37 GM059823)

Jeffrey D Axelrod

National Institute of General Medical Sciences (R35 GM131914)

Jeffrey D Axelrod

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: This study was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All of the animals were handled according to approved institutional animal care and use committee (IACUC) protocol (#11840) of Stanford University.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.