The Dynamics of Morphogenesis in the Early Mouse Embryo

Abstract

SUMMARYOver the past two decades, our understanding of mouse development from implantation to gastrulation has grown exponentially with an upsurge of genetic, molecular, cellular, and morphogenetic information. New discoveries have exalted the role of extraembryonic tissues in orchestrating embryonic patterning and axial specification. At the same time, the identification of unexpected morphogenetic processes occurring during mouse gastrulation has challenged established dogmas and brought new insights into the mechanisms driving germ layer formation. In this article, we summarize the key findings that have reinvigorated the contemporary view of early postimplantation mammalian development.

Figure 1.

Aposition of tissues in blastocyst and early postimplantation embryo. Schematic representation of implanting blastocyst and early postimplantation embryos revealing the expansion of cell lineages but maintenance of the general spatial relationship in the conceptus.

Figure 2.

Cavitation of the epiblast at early postimplantation. Schematic representation of the transformation of the mouse egg cylinder from a solid mass to a hollow cup-shaped structure. Studies primarily using embryoid bodies (EBs) as in vitro models, complemented with the analysis of mouse embryos, have led to a cavitation model that involves an interplay of two signals—one promoting cell death and one cell survival (Coucouvanis and Martin 1995). The first (a death signal) is produced by, or dependent on, the adjacent layer of visceral endoderm cells. This signal is believed to act over short distances to create a cavity by inducing the apoptosis of epiblast cells that are internal, positioned at a distance from the visceral endoderm. The second (a survival signal) is mediated through contact with the basement membrane (BM) positioned at the epiblast/visceral endoderm interface. This second signal has been proposed to promote the survival of epiblast cells located adjacent to the visceral endoderm, which will come to line the resulting cavity. Subsequent studies have suggested a role for Bmp signaling in triggering the apoptosis taking place within the epiblast (Coucouvanis and Martin 1999).

Figure 3.

Differential cell populations and behaviors within the visceral endoderm. Depiction of the different cell populations comprising the visceral endoderm as defined by both position and morphology, as well as the key events of tissue displacement and the signaling activity taking place between E5.5 and E5.75.

Figure 4.

Remodeling of the conceptus concomitant with the onset of gastrulation. Schematic representation of the reshaping of the egg cylinder resulting in the alignment of the prospective anterior–posterior embryonic axis to first the short axis and then the long axis of the ellipsoidal cross section of the egg cylinder.

Figure 5.

Gastrulation: morphogenesis of mesoderm and endoderm. Depiction of the morphogenetic cellular behavior accompanying germ layer formation. At the primitive streak, cells undergo EMT, ingress, and migrate away to form the mesoderm. Cells fated to form the definitive endoderm undergo MET and egress into the epithelium of the embryonic visceral endoderm.