Mechanical heterogeneity along single cell-cell junctions is driven by lateral clustering of cadherins during vertebrate axis elongation

Abstract

Morphogenesis is governed by the interplay of molecular signals and mechanical forces across multiple length scales. The last decade has seen tremendous advances in our understanding of the dynamics of protein localization and turnover at sub-cellular length scales, and at the other end of the spectrum, of mechanics at tissue-level length scales. Integrating the two remains a challenge, however, because we lack a detailed understanding of the subcellular patterns of mechanical properties of cells within tissues. Here, in the context of the elongating body axis of Xenopus embryos, we combine tools from cell biology and physics to demonstrate that individual cell-cell junctions display finely-patterned local mechanical heterogeneity along their length. We show that such local mechanical patterning is essential for the cell movements of convergent extension and is imparted by locally patterned clustering of a classical cadherin. Finally, the patterning of cadherins and thus local mechanics along cell-cell junctions are controlled by Planar Cell Polarity signaling, a key genetic module for CE that is mutated in diverse human birth defects.

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Raw data from time-lapse imaging are available on Dryad.

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Article and author information

Author details

  1. Robert J Huebner

    Mol. Biosci, University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Abdul Naseer Malmi-Kakkada

    Mol. Biosci, 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:" 0000-0002-5429-4652
  3. Sena Sarikaya

    Mol. Biosci, University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Shinuo Weng

    Mol. Biosci, University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. D Thirumalai

    Department of Chemistry, University of Texas at Austin, Austin, United States
    For correspondence
    dave.thirumalai@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
  6. 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. Danelle Devenport, Princeton University, United States

Ethics

Animal experimentation: Animal work described here was performed in accordance with the UT Austin Institutional Animal Care and Use Committee protocol #AUP-2018-00225.

Version history

  1. Received: December 2, 2020
  2. Accepted: May 1, 2021
  3. Accepted Manuscript published: May 25, 2021 (version 1)
  4. Version of Record published: June 15, 2021 (version 2)

Copyright

© 2021, Huebner 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. Robert J Huebner
  2. Abdul Naseer Malmi-Kakkada
  3. Sena Sarikaya
  4. Shinuo Weng
  5. D Thirumalai
  6. John B Wallingford
(2021)
Mechanical heterogeneity along single cell-cell junctions is driven by lateral clustering of cadherins during vertebrate axis elongation
eLife 10:e65390.
https://doi.org/10.7554/eLife.65390

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https://doi.org/10.7554/eLife.65390

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