Physical Analysis of Tissue Mechanics in Amphibian Gastrulation

Abstract

During morphogenesis, intercellular attachments constrain cell mobility so that embryonic tissues may (i) deform as solid sheets of tightly bound cells, (ii) disperse to migrate as separate cells or (iii) flow as multicellular liquids (in which cells remain aggregated yet can still slide past one another). By modelling deep germ layers as multicellular liquids in amphibian gastrulation, Davis and I have predicted, and then confirmed experimentally, (i) the area-invariance of deep-germ-layer surface tensions in vitro , (ii) spontaneous cell slippage in deformed deep—germ—layer cell aggregates and (iii) correlations of tissue surface tensions with tissue positioning in deep-germ-layer cell-sorting and aggregate—fusion experiments. Liquid—tissue flow involves intercalations of interior cells into expanding tissue interfaces (or withdrawal of surface cells from shrinking tissue interfaces). Tissue surface tensions are macroscopic reflections of the microscopic, tissue—specific adhesive differentials which direct these cell translocations. Such adhesive differentials may act independently of, or together with, active cell—shape changes, chemotaxis, contact guidance and/or haptotaxis in controlling embryonic tissue rearrangements. Deep cell intercalations in vivo occur throughout amphibian gastrulation: during ectodermal epiboly; during marginal—zone extension and convergence (and therefore blastopore closure); during mesodermal involution; and probably during the anterior spreading and axial extension (and therefore dorsal convergence) of involuted mesoderm. Tissue—surface—tension measurements may help determine (i) which of these cell—intercalation processes are active and which are passive, (ii) the specific contributions of various microscopic cell properties to the regulation of liquid—like germ—layer assembly and (iii) similarities and differences between in vitro and in vivo control mechanisms governing amphibian gastrulation.