Global analysis of cell behavior and protein localization dynamics reveals region-specific functions for Shroom3 and N-cadherin during neural tube closure

  1. Austin T Baldwin
  2. Juliana Kim
  3. Hyemin Seo
  4. John B Wallingford  Is a corresponding author
  1. University of Texas at Austin, United States

Abstract

Failures of neural tube closure are common and serious birth defects, yet we have a poor understanding of the interaction of genetics and cell biology during neural tube closure. Additionally, mutations that cause neural tube defects (NTDs) tend to affect anterior or posterior regions of the neural tube but rarely both, indicating a regional specificity to NTD genetics. To better understand the regional specificity of cell behaviors during neural tube closure, we analyzed the dynamic localization of actin and N-cadherin via high-resolution tissue-level time-lapse microscopy during Xenopus neural tube closure. To investigate the regionality of gene function, we generated mosaic mutations in shroom3, a key regulator or neural tube closure. This new analytical approach elucidates several differences between cell behaviors during cranial/anterior and spinal/posterior neural tube closure, provides mechanistic insight into the function of shroom3 and demonstrates the ability of tissue-level imaging and analysis to generate cell-biological mechanistic insights into neural tube closure.

Data availability

We have deposited two types of files on Dryad: 'cell_surfaces' and 'junctions' are spreadsheets containing the frame-by-frame measurements of cell/junctions size, location, fluorescent protein localization, and other parameters. 'cell_surface_stats' and 'junction_stats' are spreadsheets of summary statistics generated from the frame-by-frame data describing overall changes in parameters in individual cells and junctions. These data can be downloaded at: https://doi.org/10.5061/dryad.zw3r2289b

The following data sets were generated

Article and author information

Author details

  1. Austin T Baldwin

    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:" 0000-0002-6099-0873
  2. Juliana Kim

    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:" 0000-0001-6634-4525
  3. Hyemin Seo

    Department of Molecular Biosciences, University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. 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

Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD099191)

  • John B Wallingford

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

Reviewing Editor

  1. Elke Ober, University of Copenhagen, Denmark

Ethics

Animal experimentation: Approved by IACUC at UT austin: AUP-2021-00167, Expiration date: 08/16/2024

Version history

  1. Preprint posted: January 19, 2021 (view preprint)
  2. Received: January 20, 2021
  3. Accepted: February 18, 2022
  4. Accepted Manuscript published: March 4, 2022 (version 1)
  5. Version of Record published: April 14, 2022 (version 2)

Copyright

© 2022, Baldwin 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. Austin T Baldwin
  2. Juliana Kim
  3. Hyemin Seo
  4. John B Wallingford
(2022)
Global analysis of cell behavior and protein localization dynamics reveals region-specific functions for Shroom3 and N-cadherin during neural tube closure
eLife 11:e66704.
https://doi.org/10.7554/eLife.66704

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https://doi.org/10.7554/eLife.66704

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