Spatial and temporal analysis of PCP protein dynamics during neural tube closure

  1. Mitchell T Butler
  2. John B Wallingford  Is a corresponding author
  1. University of Texas at Austin, United States

Abstract

Planar cell polarity (PCP) controls convergent extension and axis elongation in all vertebrates. Though asymmetric localization of PCP proteins is central to their function, we understand little about PCP protein localization during convergent extension. Here, we use quantitative live imaging to simultaneously monitor cell intercalation behaviors and PCP protein dynamics in the Xenopus laevis neural plate epithelium. We observed asymmetric enrichment of PCP proteins, but more interestingly, we observed tight correlation of PCP protein enrichment with actomyosin-driven contractile behavior of cell-cell junctions. Moreover, we found that the turnover rates of junctional PCP proteins also correlated with the contractile behavior of individual junctions. All of these dynamic relationships were disrupted when PCP signaling was manipulated. Together, these results provide a dynamic and quantitative view of PCP protein localization during convergent extension and suggest a complex and intimate link between the dynamic localization of core PCP proteins, actomyosin assembly, and polarized junction shrinking during cell intercalation in the closing vertebrate neural tube.

Data availability

Data generated or analysed during this study are included in the manuscript and supporting files

Article and author information

Author details

  1. Mitchell T Butler

    Department of Molecular Biosciences, University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3130-1186
  2. John B Wallingford

    Department of Molecular Biosciences, University of Texas at Austin, Austin, United States
    For correspondence
    wallingford@austin.utexas.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6280-8625

Funding

National Institute of General Medical Sciences (R01GM104853)

  • John B Wallingford

Eunice Kennedy Shriver National Institute of Child Health and Human Development (R21HD084072)

  • John B Wallingford

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) protocols (AUP-2015-00160) of the University of Texas at Austin.

Reviewing Editor

  1. Lilianna Solnica-Krezel, Washington University School of Medicine, United States

Publication history

  1. Received: March 7, 2018
  2. Accepted: July 25, 2018
  3. Accepted Manuscript published: August 6, 2018 (version 1)
  4. Version of Record published: August 29, 2018 (version 2)

Copyright

© 2018, Butler & Wallingford

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. Mitchell T Butler
  2. John B Wallingford
(2018)
Spatial and temporal analysis of PCP protein dynamics during neural tube closure
eLife 7:e36456.
https://doi.org/10.7554/eLife.36456
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