Supracellular organization confers directionality and mechanical potency to migrating pairs of cardiopharyngeal progenitor cells
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.
Document Details
- Document Type
- Pub Defense Publication
- Publication Date
- Nov 29, 2021
- Source ID
- 10.7554/elife.70977
Entities
People
- Alex Mogilner
- Calina Copos
- Haicen Yue
- Lionel Christiaen
- Yelena Y. Bernadskaya
Organizations
- Haukeland University Hospital
- National Institute of General Medical Sciences
- National Science Foundation Division of Mathematical Sciences
- New York University
- Sars International Centre for Marine Molecular Biology
- United States Army
- University of North Carolina at Chapel Hill