Adhesion strength, cell packing density, and cell surface buckling in pericellular matrix-mediated tissue cohesion.

Pericellular matrix-mediated cell-cell adhesion in Xenopus gastrula tissues is characterized by a spectrum of narrow and wide cell contacts that alternate with the non-adhesive surfaces of the interstitial space. Here we show, first, that knockdown of a pericellular matrix adhesion molecule, fibronectin, diminishes contact abundance and hence cell packing density, but without reducing adhesion strength. Second, we find that cell surfaces in gastrula tissues exhibit solid-like behavior in the form of buckling and crumpling, shape modifications which are typically seen in thin elastic films. We propose that both phenomena are explained by generic properties of the pericellular matrix: its compression and consequent stiffening by the interpenetration of matrix layers during adhesive contact formation. We argue that this renders part of the cell surface non-adhesive to form interstitial gaps, and gap surfaces as well as contacts prone to buckling and crumpling in step with cell contractility fluctuations. In this elasto-capillary model of tissue cohesion, the size of the interstitial space is determined by the abundance of pericellular matrix, not by adhesion strength.