Porous mesenchymal tissue as a fluid under tension

Porous mesenchymal tissues are ubiquitous in vertebrates and play essential roles in shaping embryonic structures and organs through interactions with their epithelial counterparts. Despite their importance, these tissues remain relatively understudied because their complex, stellate cell shapes and large extracellular spaces (filled with matrix or interstitial fluid) pose significant experimental and computational challenges. Here, we show that the chick presomitic mesoderm (PSM), a model stellate mesenchymal tissue, exhibits three unusual concurrent properties: (1) cells undergo fluid-like diffusion and rearrangement; (2) cell spacing is uniform; and (3) the tissue as a whole is under tension. How can such a sparse tissue sustain macroscopic tension while behaving like a fluid? Through numerical modeling, we find that cells must actively move away from their neighbors as they remodel contacts, a process reminiscent of contact inhibition of locomotion (CIL). We find that two distinct models of CIL, active crawling and active pulling, can both produce a tensioned, highly connected cellular network that diffuses and rearranges. We develop a set of simple kinetic equations that capture the dynamics of this remodeling in simulations and experiments. Together, our modeling and experimental results reveal a previously unrecognized role for CIL in regulating tissue mechanics beyond collective cell migration: CIL enables mesenchymal tissues to maintain integrity while continuously remodeling.