In many developing and regenerating systems, tissue pattern is established through gradients of informative morphogens, but we know little about how cells interpret these. Using experimental manipulation of early chick embryos including misexpression of an inducer (VG1 or ACTIVIN) and an inhibitor (BMP4), we test two alternative models for their ability to explain how the site of primitive streak formation is positioned relative to the rest of the embryo. In one model, cells read morphogen concentrations cell-autonomously. In the other, cells sense changes in morphogen status relative to their neighbourhood. We find that only the latter model can account for the experimental results, including some counter-intuitive predictions. This mechanism (which we name “neighbourhood watch” model) illuminates the classic “French Flag Problem” and how positional information is interpreted by a sheet of cells in a large developing system.
During primitive streak formation in the chick embryo, cells undergo mesendoderm specification and convergent extension at the same time and in the same cells. Previous work has implicated cVG1 (GDF3) as a key factor for induction of primitive streak identity and positioning the primitive streak, whereas FGF signalling was implicated in regulating cell intercalation via regulation of components of the WNT-planar cell polarity (PCP) pathway. FGF has also been reported to be able to induce a primitive streak (but lacking the most axial derivatives such as notochord/prechordal mesendoderm). These signals emanate from different cell populations in the embryo, so how do they interact to ensure that the same cells undergo both cell intercalation and acquire primitive streak identity? Here we begin to address this question by examining in more detail the ability of the two classes of signals in regulating the two developmental events. Using misexpression of inducers and/or exposure to inhibitors and in situ hybridisation, we study how these two signals regulate expression of Brachyury (TBXT) and PRICKLE1 as markers for the primitive streak and the PCP, respectively. We find that both signals can induce both properties, but while FGF seems to be required for induction of the streak by cVG1, it is not necessary for induction of PRICKLE1. The results are consistent with cVG1 being a common regulator for both primitive streak identity and the initiation of convergent extension that leads to streak elongation.
During early avian development, only a narrow band of cells (the edge cells, also called ‘margin of overgrowth’) at the rim of the embryo is responsible for blastoderm expansion by crawling over the vitelline membrane (VM) to cover the whole egg yolk in just 4 days (a process called epiboly). Surprisingly, this has not yet been studied in detail. Here we explore the edge cells of the chick embryo using in situ hybridization, immunohistochemistry and live imaging. Morphological and molecular properties reveal that the edge has a distinctive structure, being subdivided into sub-regions, including at least four distinct zones (which we name as leading, trailing, deep and stalk zones). This allows us to study reorganization of the edge region that accompanies reattachment of an explanted blastoderm to the VM. Immunohistochemistry uncovers distinct polarized cellular features resembling the process of collective cell migration described in other systems. Live imaging reveals dynamic lamellipodial and filopodial activity at the leading edge of the outermost cells. Our data provide evidence that edge cells are a distinct tissue. We propose that edge cells may be a useful model system for the study of wound healing and other closure events in epithelial cell sheets.
Classical studies have established that the marginal zone, a ring of extraembryonic epiblast immediately surrounding the embryonic epiblast (area pellucida) of the chick embryo is important in setting embryonic polarity by positioning the primitive streak, the site of gastrulation. The more external extraembryonic region (area opaca) was only thought to have nutritive and support functions. Using experimental embryology approaches, this study reveals three separable functions for this outer region: first, juxtaposition of the area opaca directly onto the area pellucida induces a new marginal zone from the latter; this induced domain is entirely posterior in character. Second, ablation and grafting experiments using an isolated anterior half of the blastoderm and pieces of area opaca suggest that the area opaca can influence the polarity of the adjacent marginal zone. Finally, we show that the loss of the ability of such isolated anterior half-embryos to regulate (re-establish polarity spontaneously) at the early primitive streak stage can be rescued by replacing the area opaca by one from a younger stage. These results uncover new roles of chick extraembryonic tissues in early development.
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