Formation of adherens junctions leads to the emergence of a tissue-level tension in epithelial monolayers

Abstract

Adherens junctions and desmosomes interface the cytoskeletons of adjacent cells into a mechanical syncitium. In doing so, intercellular junctions endow tissues with the strength needed to sustain mechanical stresses encountered in normal physiology and coordinate tension during morphogenesis. Though much is known about the biological mechanisms underlying junction formation, little is known about how tissue-scale mechanical properties are established. Here, we use deep AFM indentation to measure the apparent stiffness of epithelial monolayers reforming from dissociated cells and examine which cellular processes give rise to tissue-scale mechanics. We show that the formation of intercellular junctions coincided with an increase in the apparent stiffness of reforming monolayers that reflected the generation of a tissue-level tension. Tension rapidly increased reaching a maximum after 150 minutes before settling to a lower level over the next three hours as monolayers reached homeostasis. The emergence of tissue tension correlated with the formation of adherens junctions but not desmosomes. As a consequence, inhibition of any of the molecular mechanisms participating in adherens junction initiation, remodelling, and maturation significantly impeded the emergence of tissue-level tension in monolayers.