Supracellular organization confers directionality and mechanical potency to migrating pairs of cardiopharyngeal progenitor cells
- New York University, United States
- University of North Carolina at Chapel Hill, United States
Abstract
Physiological and pathological morphogenetic events involve a wide array of collective movements, suggesting that multicellular arrangements confer biochemical and biomechanical properties contributing to tissue scale organization. The Ciona cardiopharyngeal progenitors provide the simplest model of collective cell migration, with cohesive bilateral cell pairs polarized along the leader-trailer migration path while moving between the ventral epidermis and trunk endoderm. We use the Cellular Potts Model to computationally probe the distributions of forces consistent with shapes and collective polarity of migrating cell pairs. Combining computational modeling, confocal microscopy, and molecular perturbations, we identify cardiopharyngeal progenitors as the simplest cell collective maintaining supracellular polarity with differential distributions of protrusive forces, cell-matrix adhesion, and myosin-based retraction forces along the leader-trailer axis. 4D simulations and experimental observations suggest that cell-cell communication helps establish a hierarchy to align collective polarity with the direction of migration, as observed with three or more cells in silico and in vivo. Our approach reveals emerging properties of the migrating collective: cell pairs are more persistent, migrating longer distances, and presumably with higher accuracy. Simulations suggest that cell pairs can overcome mechanical resistance of the trunk endoderm more effectively when they are polarized collectively. We propose that polarized supracellular organization of cardiopharyngeal progenitors confers emergent physical properties that determine mechanical interactions with their environment during morphogenesis.
Data availability
The code generated during this study is available on GitHub(https://github.com/HaicenYue/3D-simulation-of-TVCs.git)
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3D-simulation-of-TVCsPublicly available at Github (https://github.com).
Article and author information
Author details
Yelena Y Bernadskaya
Funding
National Institute of General Medical Sciences (GM108369-01A1)
- Yelena Y Bernadskaya
National Institute of General Medical Sciences (GM096032-09)
- Lionel Christiaen
Division of Mathematical Sciences (DMS-1950981)
- Alex Mogilner
U.S. Army (W911NF-17-1-041)
- Alex Mogilner
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2021, Bernadskaya 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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Supracellular organization confers directionality and mechanical potency to migrating pairs of cardiopharyngeal progenitor cells
eLife 10:e70977.
https://doi.org/10.7554/eLife.70977
