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, 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 that 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 both gap surfaces and contacts prone to buckling and crumpling in line with cell contractility fluctuations. In this elasto-capillary model of tissue cohesion, the size of the interstitial space is determined by the abundance of the pericellular matrix, not by adhesion strength.