Migrating mesoderm cells self-organize into a dynamic meshwork structure during chick gastrulation
- RIKEN Center for Biosystems Dynamics Research, Japan
Abstract
Migration of cell populations is a fundamental process in morphogenesis and disease. The mechanisms of collective cell migration of epithelial cell populations have been well studied. It remains unclear, however, how the highly motile mesenchymal cells, which migrate extensively throughout the embryo, are connected with each other and coordinated as a collective. During chick gastrulation, cells emerging from the primitive streak and migrating in the 3D space between ectoderm and endoderm (mesoderm region) exhibit a novel form of collective migration. Using live imaging and quantitative analysis, such as topological data analysis (TDA), we found that these cells undergo a novel form of collective migration, in which they form a meshwork structure while moving away from the primitive streak. Overexpressing a mutant form of N-cadherin was associated with reduced speed of tissue progression and directionality of the collective cell movement, whereas the speed of individual cells remains unchanged. To investigate how this meshwork arises, we utilized an agent-based theoretical model, which suggests that cell elongation, cell-cell adhesion, and cell density are the key parameters for the meshwork formation. These data provide novel insights into how a supracellular structure of migrating mesenchymal cells may arise in loosely connected cell populations.
Data availability
All source data obtained experimentally during this study are included in the manuscript and supporting files; source data files have been provided for Figures 1-4 and 6.. Custum Matlab scripts for the trajectory analysis shown in Figures 1D-J, 4F-K will be available after the manuscript will be accepted for publication at GitHub at https://github.com/RIKEN-PHB/Nakaya-Paper-Trajectory-Analysis. Figure 5 was created using the model detailed in Materials and Methods. All parameter values are shown in Materials and Methods.
Article and author information
Author details
Ayako Isomura-Matoba
Funding
Japan Society for the Promotion of Science (16K07385)
- Yukiko Nakaya
Japan Society for the Promotion of Science (19H14673)
- Mitsusuke Tarama
Japan Society for the Promotion of Science (22H05170)
- Tatsuo Shibata
Japan Science and Technology Agency (JPMJCR1852)
- Tatsuo Shibata
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2025, Nakaya et al.
This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.
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Migrating mesoderm cells self-organize into a dynamic meshwork structure during chick gastrulation
eLife 14:e84749.
https://doi.org/10.7554/eLife.84749
