Prickle isoforms determine handedness of helical morphogenesis

  1. Bomsoo Cho
  2. Song Song
  3. Jeffrey D Axelrod  Is a corresponding author
  1. Stanford University School of Medicine, United States

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 Pkpk or Pksple 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.

Data availability

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.

Article and author information

Author details

  1. Bomsoo Cho

    Department of Pathology, Stanford University School of Medicine, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8970-9160
  2. Song Song

    Department of Pathology, Stanford University School of Medicine, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. 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.
    ORCID icon "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

© 2020, Cho et al.

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.

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  1. Bomsoo Cho
  2. Song Song
  3. Jeffrey D Axelrod
(2020)
Prickle isoforms determine handedness of helical morphogenesis
eLife 9:e51456.
https://doi.org/10.7554/eLife.51456

Share this article

https://doi.org/10.7554/eLife.51456

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