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Dev Growth Differ
2001 Aug 01;434:327-42. doi: 10.1046/j.1440-169x.2001.00587.x.
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Of mice, frogs and flies: generation of membrane asymmetries in early development.
Müller HA
.
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Embryonic development begins with cleavage of the fertilized egg. Cleavage comprises two major processes: cytokinesis and formation of a polarized epithelial cell layer. The focus of this review is comparison of the generation of membrane polarity during embryonic cleavage in three different developmental model systems. In mammalian embryos, as exemplified by analysis of the mouse, generation of distinct membrane domains is uncoupled from cleavage divisions and is initiated in a specific developmental phase, called compaction. In Xenopus laevis embryos, generation of polarized blastomeres occurs simultaneously with cytokinesis. The origin of specific membrane domains of X. laevis polar blastomeres, however, can be traced back to oogenesis. Finally, in Drosophila melanogaster, generation of polarized cells occurs at cellularization. The relevance of cell adhesion, cell junctions and cytocortical scaffolds will be discussed for each of the model systems. Despite enormous morphologic differences, the three models share many common features; in particular, many important molecular interactions are conserved.
Fig. 1. Cleavage and membrane polarization in (A) mouse
and (B) Xenopus laevis embryos. (A) In the mouse, the first
three cleavage divisions occur without a major change in cell
surface or membrane polarities. At the 8-cell stage, the embryo
undergoes compaction resulting in polarization of the blastomeres
and establishment of apical (red) and basolateral (green)
membrane domains. (C) The polarized blastomeres undergo
symmetric (1) or asymmetric (2) cleavages, giving rise to blastomeres
that will either form the polarized trophectoderm epithelium
or the non-polarized inner cell mass of the blastocyst (see
A, left-hand panel). (B) In X. laevis, the oocyte plasma
membrane initially exhibits a character more like the basolateral
membrane of polarized epithelial cells. During maturation,
the membrane characteristics are converted into a more apical
(red) character. Cleavage results in massive insertion of plasma
membrane from internal pools, which form the basolateral
(green) membrane domains. Like mouse blastomeres, polarized
X. laevis blastomeres can undergo either symmetric (C 1) or
asymmetric (C 2) cell divisions.
Fig. 4. Composition of the furrow
canal in Xenopus laevis cleavage.
Embryos were treated with biotin-
X-NHS to label cell surface proteins
prior to the first cleavage
division. After fixation, biotin moieties
were detected by immunolabeling
with antibodies directed
against biotin (green). (A) Section
through the animal pole of a fertilized
egg before the first cleavage.
The entire plasma membrane is
labeled with biotin antibodies. (B)
Section through a cleavage stage
embryo; animal pole is up. Note
strong biotin labeling in the furrow
canal, which is marked by the
arrow. Arrowheads point to yolk
platelets, which exhibit a yellow
autofluorescence.