Dorsoventral Differences in Cell-Cell Interactions Modulate the Motile Behaviour of Cells from the Xenopus Gastrula

Abstract

When groups of cells from the inner marginal zone (mesendoderm) of the early Xenopus gastrula are placed on a fibronectin-coated substratum, the explants of the dorsal region spread into monolayers whereas those from the ventral region, though they adhere to the substratum, do not show this spreading reaction. This different behaviour is not reflected in the in vitro behaviour of the respective cells kept in isolation. No difference between dorsal and ventral cells was observed, when they were tested for lamellipodia-driven spreading, movement over the substratum or properties of integrin- and cadherin-mediated adhesion. However, cell contacts between individual dorsal cells are significantly less stable than those between ventral cells. The higher flexibility of the cell-cell contacts seems to determine the spreading behaviour of the dorsal explants, which includes lamellipodia-driven outward movement of the peripheral cells, rearrangements of the cells, building up a horizontal tension within the aggregate and intercalation of cells from above into the bottom layer. Ventral explants lack these properties. Staining for F-actin revealed a decisive difference of the supracellular organisation of the cytoskeleton that underlies the morphology of the different types of explants. Evidence for a higher flexibility of cell-cell contacts in the dorsal mesendoderm was also obtained in SEM studies on gastrulating embryos. Dorsal mesendodermal cells show stronger protrusive activity as compared to ventral mesendodermal cells. The meaning of these observations for the mechanisms of morphogenetic movements during gastrulation is central to the discussion.

Regulated adhesion as a driving force of gastrulation movements

“…A similar mechanism might be at play during mediolateral intercalation in Xenopus. Consistent with such a possibility, DV differences in adhesiveness have been seen within the coherent mesodermal sheets of the Xenopus embryo (Reintsch and Hausen, 2001). Here, the adhesive gradient might be set up under the control of a gradient of TGFβ/activin family members, which would not only induce different anterodorsal versus posteroventral mesodermal fates (Green et al, 1992), but also regulate C-cadherin-mediated adhesiveness (Brieher and Gumbiner, 1994), thereby linking embryonic patterning with appropriate morphogenesis through directed CE movements (Howard and Smith, 1993;Ninomiya et al, 2004).…”

“…A suspension of dissociated cells is pumped through the capillary, and attached cells are counted (Brieher et al, 1996). A variant of this assay uses coated glass slides instead of capillaries (Ogata et al, 2007;Reintsch and Hausen, 2001). Like the bead adhesion assay, these assays do not consider the influence on adhesiveness of other cell-surface molecules, which can be important in vivo Niessen and Gumbiner, 2002).…”

Regional requirements for Dishevelled signaling duringXenopusgastrulation: separable effects on blastopore closure, mesendoderm internalization and archenteron formation

“…Although the cells of the ventrolateral marginal zone undergo only limited convergent extension, they may also contribute mechanically to events driven on the dorsal side. Ventral marginal zone cells make stable, if not polarized, contacts with neighboring cells throughout gastrulation (Reintsch and Hausen, 2001). Stable attachments such as these may contribute to the establishment of tension around the circumference of the marginal zone.…”

Xenopus Cyr61regulates gastrulation movements and modulates Wnt signalling

“…In addition, the roles of cell adhesion molecules, such as laminin (Nakatsuji, 1986) and fibronectin (Marsden and DeSimone, 2001;Reintsch and Hausen, 2001;Winklbauer and Keller, 1996), in the regulation of gastrulation are becoming clearer, as are the functions of their receptors, including the integrins (Davidson et al, 2002;Ramos et al, 1996;Whittaker and DeSimone, 1993). The successful prosecution of gastrulation and cell fate specification requires the coordination and integration of all these activities.…”