Slb/Wnt11 controls hypoblast cell migration and morphogenesis at the onset of zebrafish gastrulation

Abstract

Summary During vertebrate gastrulation, highly coordinated cellular rearrangements lead to the formation of the three germ layers, ectoderm, mesoderm and endoderm. In zebrafish, silberblick (slb)/wnt11 regulates normal gastrulation movements by activating a signalling pathway similar to the Frizzled-signalling pathway, which establishes epithelial planar cell polarity (PCP) in Drosophila. However, the cellular mechanisms by which slb/wnt11 functions during zebrafish gastrulation are still unclear. Using high-resolution two-photon confocal imaging followed by computer-assisted reconstruction and motion analysis, we have analysed the movement and morphology of individual cells in three dimensions during the course of gastrulation. We show that in slb-mutant embryos, hypoblast cells within the forming germ ring have slower, less directed migratory movements at the onset of gastrulation. These aberrant cell movements are accompanied by defects in the orientation of cellular processes along the individual movement directions of these cells. We conclude that slb/wnt11-mediated orientation of cellular processes plays a role in facilitating and stabilising movements of hypoblast cells in the germ ring, thereby pointing at a novel function of the slb/wnt11 signalling pathway for the regulation of migratory cell movements at early stages of gastrulation.

Csrp1 regulates dynamic cell movements of the mesendoderm and cardiac mesoderm through interactions with Dishevelled and Diversin

“…Formation of these cell protrusions is controlled by the planar cell polarity/noncanonical Wnt cascade (23). An intriguing possibility is that these pseudopodial processes might be formed via interplay between Csrp1 and the noncanonical Wnt pathway.…”

Initiation of convergence and extension movements of lateral mesoderm during zebrafish gastrulation

“…Embryonic morphology has been the primary assay, although study of the cellular bases of these defects have been initiated. For example, Wnt signaling controls cell elongation and orientation (Topczewski et al, 2001;Jessen et al, 2002;Kilian et al, 2003), orientation of cell division planes, (Gong et al, 2004), formation of and stability of cellular protrusions (Wallingford et al, 2000;Ulrich et al, 2003), and speed of cell movement (Topczewski et al, 2001;Jessen et al, 2002;Marlow et al, 2002). Additional pathways that influence C&E movements have been identified.…”

Collective mesendoderm migration relies on an intrinsic directionality signal transmitted through cell contacts

“…During gastrulation, this group leads the forming axis, migrating from the embryonic organizer to the animal pole, to later give rise to the hatching gland (13,14). The prechordal plate has been described as a cohesive group, the cohesion of which is thought to be required for effective migration (15,16).…”

“…In many described systems, such as angiogenesis or cancer strand migration, coherent group migration is achieved through the establishment of leading cells at the front that emit dynamic cytoplasmic extensions, whereas the following cells display a less dynamic stalk cell fate (19,20). Regarding prechordal plate, previous analyses have established that front cells emit frequent cytoplasmic extensions pointing toward the animal pole (14), but the behavior of posterior cells has not been analyzed, probably because it requires labeling some cells but not their neighbors, so as to clearly see their morphology. To achieve this, we injected plasmidic DNA, leading to mosaic expression, or performed cell transplantations from the embryonic shield of a labeled donor embryo to the shield of an unlabeled host.…”

“…3 B, D, and J), showing that E-cadherin is required for cell polarization and for the correct orientation of this polarity toward the animal pole. In addition to E-cadherin, the Wnt-PCP pathway, known in many systems to control cell polarity through cell-cell interactions, has been involved in plate cell migration (14,16,27) and in CIL in crest cells (5). To test for a potential role of the Wnt-PCP pathway in the orientation of cell polarity, we used a dominant-negative form of Dsh (DshDEP+), which specifically blocks the PCP pathway (28).…”