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

Autor: Bernadskaya YY; Center for Developmental Genetics, Department of Biology, New York University, New York, United States., Yue H; Courant Institute of Mathematical Sciences and Department of Biology, New York University, New York, United States., Copos C; Mathematics and Computational Medicine, University of North Carolina at Chapel Hill, Chapel Hill, United States., Christiaen L; Center for Developmental Genetics, Department of Biology, New York University, New York, United States.; Sars International Centre for Marine Molecular Biology, Bergen, Norway.; Department of Heart Disease, Haukeland University Hospital, Bergen, Norway., Mogilner A; Courant Institute of Mathematical Sciences and Department of Biology, New York University, New York, United States.
Jazyk: angličtina
Zdroj: ELife [Elife] 2021 Nov 29; Vol. 10. Date of Electronic Publication: 2021 Nov 29.
DOI: 10.7554/eLife.70977
Abstrakt: 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.
Competing Interests: YB, HY, CC, LC, AM No competing interests declared
(© 2021, Bernadskaya et al.)
Databáze: MEDLINE