Reciprocal cell-ECM dynamics generate supracellular fluidity underlying spontaneous follicle patterning

During vertebrate embryogenesis, cell collectives engage in coordinated behavior to form tissue structures of increasing complexity. In the avian skin, assembly into follicles depends on intrinsic mechanical forces of the dermis, but how cell mechanics initiate pattern formation is not known. Here, we reconstitute the initiation of follicle patterning ex vivo using only freshly dissociated avian dermal cells and collagen. We find that contractile cells physically rearrange the extracellular matrix (ECM) and that ECM rearrangement further aligns cells. This exchange transforms a mechanically unlinked collective of dermal cells into a continuum, with coherent, long-range order. Combining theory with experiment, we show that this ordered cell-ECM layer behaves as an active contractile fluid that spontaneously forms regular patterns. Our study illustrates a role for mesenchymal dynamics in generating cell-level ordering and tissue-level patterning through a fluid instability-processes that may be at play across morphological symmetry-breaking contexts.

Automated summary

During vertebrate embryogenesis, cell collectives engage in coordinated behavior to form tissue structures of increasing complexity. The initiation of follicle patterning in avian skin is initiated by the mechanical rearrangement of extracellular matrix (ECM) by contractile cells, which further aligns the cells and transforms them into a continuum with coherent, long-range order. This ordered cell-ECM layer behaves as an active contractile fluid and spontaneously forms regular patterns, illustrating the role of mesenchymal dynamics in generating cell-level ordering and tissue-level patterning.