In Xenopus and zebrafish gastrulae, PAPC attenuates planar cell polarity signaling and controls formation of an adhesive, yet flexible, contact at the ectoderm–mesoderm boundary.

Trogocytosis, in which cells nibble away parts of neighboring cells, is an intercellular cannibalism process conserved from protozoa to mammals. Its underlying molecular mechanisms are not well understood and are likely distinct from phagocytosis, a process that clears entire cells. Bi-directional contact repulsion induced by Eph/ephrin signaling involves transfer of membrane patches and full-length Eph/ephrin protein complexes between opposing cells, resembling trogocytosis. Here, we show that the phagocytic adaptor protein Gulp1 regulates EphB/ephrinB trogocytosis to achieve efficient cell rearrangements of cultured cells and during embryonic development. Gulp1 mediates trogocytosis bi-directionally by dynamic engagement with EphB/ephrinB protein clusters in cooperation with the Rac-specific guanine nucleotide exchange factor Tiam2. Ultimately, Gulp1’s presence at the Eph/ephrin cluster is a prerequisite for recruiting the endocytic GTPase dynamin. These results suggest that EphB/ephrinB trogocytosis, unlike other trogocytosis events, uses a phagocytosis-like mechanism to achieve efficient membrane scission and engulfment.

Xenopus gastrulation movements are in large part based on the rearrangement of cells by differential cell-on-cell migration within multilayered tissues. Different patterns of migration-based cell intercalation drive endoderm and mesoderm internalization and their positioning along their prospective body axes. C-cadherin, fibronectin, integrins, and focal contact components are expressed in all gastrula cells and play putative roles in cell-on-cell migration, but their actual functions in this respect are not yet understood. The gastrula can be subdivided into two motility domains, and in the vegetal, migratory domain, two modes of cell migration are discerned. Vegetal endoderm cells show ingression-type migration, a variant of amoeboid migration characterized by the lack of locomotory protrusions and by macropinocytosis as a mechanism of trailing edge resorption. Mesendoderm and prechordal mesoderm cells use lamellipodia in a mesenchymal mode of migration. Gastrula cell motility can be dissected into traits, such as cell polarity, adhesion, mobility, or protrusive activity, which are controlled separately yet in complex, combinatorial ways. Cells can instantaneously switch between different combinations of traits, showing plasticity as they respond to substratum properties.

The planar cell polarity pathway regulates cell polarity, adhesion, and rearrangement. Its cytoplasmic core components Prickle (Pk) and Dishevelled (Dvl) often localize as dense puncta at cell membranes to form antagonizing complexes and establish cell asymmetry. In vertebrates, Pk and Dvl have been implicated in actomyosin cortex regulation, but the mechanism of how these proteins control cell mechanics is unclear. Here we demonstrate that in Xenopus prechordal mesoderm cells, diffusely distributed, cytoplasmic Pk1 up-regulates the F-actin content of the cortex. This counteracts cortex down-regulation by Dvl2. Both factors act upstream of casein kinase II to increase or decrease cortical tension. Thus, cortex modulation by Pk1 and Dvl2 is translated into mechanical force and affects cell migration and rearrangement during radial intercalation in the prechordal mesoderm. Pk1 also forms puncta and plaques, which are associated with localized depletion of cortical F-actin, suggesting opposite roles for diffuse and punctate Pk1.