Supracellular organization confers directionality and mechanical potency to migrating pairs of cardiopharyngeal progenitor cells

Abstract
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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)

The following data sets were generated

1. Yue H
(2021) 3D-simulation-of-TVCs
Publicly available at Github (https://github.com).

https://github.com/HaicenYue/3D-simulation-of-TVCs.git

Article and author information

Author details

Yelena Y Bernadskaya

Center for Developmental Genetics, Department of Biology, New York University, New York, United States

For correspondence
yb372@nyu.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-6147-5825
Haicen Yue

Courant Institute of Mathematical Sciences and Department of Biology, New York University, New York, United States

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

Mathematics and Computational Medicine, University of North Carolina at Chapel Hill, Chapel Hill, United States

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

Center for Developmental Genetics, Department of Biology, New York University, New York, United States

For correspondence
lc121@nyu.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-5930-5667
Alex Mogilner

Courant Institute of Mathematical Sciences and Department of Biology, New York University, New York, United States

For correspondence
mogilner@cims.nyu.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-9310-3812

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

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.