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

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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.

Data availability

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

The following data sets were generated

1. Wallingford JB et al
(2021) Data from:Mechanical heterogeneity along single cell-cell junctions is driven by lateral clustering of cadherins during vertebrate axis elongation
Dryad Digital Repository, doi: 10.5061/dryad.pg4f4qrph.

https://datadryad.org/stash/dataset/doi:10.5061/pg4f4qrph

Article and author information

Author details

Robert J Huebner

Mol. Biosci, University of Texas at Austin, Austin, United States

Competing interests
The authors declare that no competing interests exist.
Abdul Naseer Malmi-Kakkada

Mol. Biosci, University of Texas at Austin, Austin, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-5429-4652
Sena Sarikaya

Mol. Biosci, University of Texas at Austin, Austin, United States

Competing interests
The authors declare that no competing interests exist.
Shinuo Weng

Mol. Biosci, University of Texas at Austin, Austin, United States

Competing interests
The authors declare that no competing interests exist.
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.
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.

"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.

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.

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.