Pattern formation along signaling gradients driven by active droplet behaviour of cell groups

Hugh Z Ford, Giulia L Celora, Elizabeth R Westbrook, Mohit P Dalwadi, Benjamin J Walker, Hella Baumann, Cornelis J. Weijer, Philip Pearce (Lead / Corresponding author), Jonathan R Chubb (Lead / Corresponding author)

Research output: Working paper/PreprintPreprint

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Abstract

Gradients of extracellular signals organise cells in tissues. Although there are several models for how gradients can pattern cell behaviour, it is not clear how cells react to gradients when the population is undergoing 3D morphogenesis, in which cell-cell and cell-signal interactions are continually changing. Dictyostelium cells follow gradients of their nutritional source to feed and maintain their undifferentiated state. Using light sheet imaging to simultaneously monitor signaling, single cell and population dynamics, we show that the cells migrate towards nutritional gradients in swarms. As swarms advance, they deposit clumps of cells at the rear, triggering differentiation. Clump deposition is explained by a physical model in which cell swarms behave as active droplets: cells proliferate within the swarm, with clump shedding occurring at a critical population size, at which cells at the rear no longer perceive the gradient and are not retained by the emergent surface tension of the swarm. The droplet model predicts vortex motion of the cells within the swarm emerging from the local transfer of propulsion forces, a prediction validated by 3D tracking of single cells. This active fluid behaviour reveals a developmental mechanism we term textquotedblleftmusical chairstextquotedblright decision-making, in which the decision to proliferate or differentiate is determined by the position of a cell within the group as it bifurcates.Competing Interest StatementThe authors have declared no competing interest.
Original languageEnglish
Number of pages47
DOIs
Publication statusPublished - 9 Apr 2024

Publication series

NameBioRxiv
PublisherCold Spring Harbor Laboratory Press

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