Hydrostatic pressure and lateral actomyosin tension control stretch and tension of the basement membrane in epithelia

Abstract

The shaping of epithelial tissues into functional organs often depend on asymmetries in mechanical tension present at the apical and basal sides of cells. Contraction of an actomyosin meshwork underlying the apical side of cells is known to generate apical tension. The basal side of cells is also associated with an actomyosin meshwork, but it is, in addition, connected to a specialized extracellular matrix, the basement membrane. However, how basal tension is generated, and the role of the basement membrane in this process, are not well understood. Here, using atomic force microscopy, we measure mechanical tension in the basal surface of the wing disc epithelium of Drosophila. We find that basal tension depends on both the actomyosin cytoskeleton and the basement membrane, and that it is proportional to lateral surface tension and hydrostatic pressure. Collagen IV turnover and mobility are slow indicating that the basement membrane can store elastic stresses. Our data suggest that elastic stresses in the basement membrane induced by basement membrane stretch are a key factor in the adjustment of basal tension. Hydrostatic pressure and lateral actomyosin contractility are two driving forces by which epithelial cells can maintain this basement membrane stretch.