Surface tensions of embryonic tissues predict their mutual envelopment behavior

Abstract

During embryonic development, certain tissues stream to their destinations by liquidlike spreading movements. According to the ‘differential adhesion hypothesis’, these movements are guided by cell-adhesion-generated tissue surface tensions (sigmas), operating in the same manner as surface tensions do in the mutual spreading behavior of immiscible liquids, among which the liquid of lower surface tension is always the one that spreads over its partner. In order to conduct a direct physical test of the ‘differential adhesion hypothesis’, we have measured the sigmas of aggregates of five chick embryonic tissues, using a parallel plate compression apparatus specifically designed for this purpose, and compared the measured values with these tissues' mutual spreading behaviors. We show that aggregates of each of these tissues behave for a time as elasticoviscous liquids with characteristic surface tension values. Chick embryonic limb bud mesoderm (sigma = 20.1 dyne/cm) is enveloped by pigmented epithelium (sigma = 12.6 dyne/cm) which, in turn, is enveloped by heart (sigma = 8.5 dyne/cm) which, in turn, is enveloped by liver (sigma = 4.6 dyne/cm) which, in turn, is enveloped by neural retina (sigma = 1.6 dyne/cm). Thus, as predicted, the tissues' surface tension values fall in the precise sequence required to account for their mutual envelopment behavior.