Force propagation between epithelial cell doublets

Cell-generated forces play a major role in coordinating the large-scale
behavior of cell assemblies, in particular during development, wound
healing and cancer. Mechanical signals propagate faster than biochemical
signals but can have similar effects, especially in epithelial tissues
with strong cell-cell adhesion. However, a quantitative description of the
transmission chain from force generation in a sender cell, force
propagation across cell-cell boundaries, and the concomitant response of
receiver cells is missing. For a quantitative analysis of this important
situation, here we propose a minimal model system of two epithelial cells
on an H-pattern ("cell doublet"). After optogenetically
activating RhoA, a major regulator of cell contractility, in the sender
cell, we measure the mechanical response of the receiver cell by traction
force and monolayer stress microscopies. In general, we find that the
receiver cells show an active response so that the cell doublet forms a
coherent unit. However, force propagation and response of the receiver
cell also strongly depend on the mechano-structural polarization in the
cell assembly, which is controlled by cell-matrix adhesion to the adhesive
micropattern. We find that the response of the receiver cell is stronger
when the mechano-structural polarization axis is oriented perpendicular to
the direction of force propagation, reminiscent of the Poisson effect in
passive materials. We finally show that the same effects are at work in
small tissues. Our work demonstrates that cellular organization and active
mechanical response of a tissue is key to maintaining signal strength and
leads to the emergence of elasticity, which means that signals are not
dissipated like in a viscous system but can propagate over large
distances.