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The morphological transformation from oocyte to embryo is brought about by the structural components of the cell, the cytoskeleton. Cytoskeletal elements act to generate and maintain cellular asymmetries, cellular movement and morphologies, and to integrate signals and forces into morphogenetically coherent behavior. Because of its unique experimental accessibility, the Xenopus embryo provides a powerful model system in which to study the "body language" of early embryonic development.
FIG. 1. The origins of oocyte asymmetry. The oogonia undergoes a series of four mitotic divisions to produce a nest of primary oocytes. In the
nest, the primary oocytes are connected to one another by cytoplasmic bridges and retain their centrioles. The nuclei (Nuc) are located at the
periphery of the nest; the centrioles and most of the cytoplasm are localized to the central region. Chromosomes are arranged in a "bouquet"
configuration, which presumably reflects the organization of the final mitotic spindle. As oogenesis proceeds, the primary oocytes disconnect
from one another and become invested by a follicle to become "stage I" oocytes (according to the classification scheme of Dumont, 1972). Staining
of stage I oocytes with a monoclonal antiDNA antibody (bottom panel) reveals the mitochondrial mass (mm), the lampbrush chromosomes (lb)
localized in the center of the nucleus, and nucleoli (n) localized to the periphery of the nuclear envelope. (In the top panel, the oogonia and
oocytes are not drawn to scale: the oogonia has a diameter of -20 ~-tm, whereas a stage I oocyte has an initial diameter of -50 1-1m.)
FIG. 2. IF protein modification in the oocyte: When vimentin mRNA
is injected into the oocyte, the translated protein re~ains in the injected
hemisphere (see Dent et aL,1992). Two-dimensional gel analysis
of animal (An) or vegetally (Vg) injected oocytes reveals the same pattern
of post-translational modification of the exogenous vimentin protein,
even among the proteolytic fragments of vimentin (arrows). Similar
results have been obtained with the keratins (Bachant, 1993). This
observation suggests that the asymmetrical organization of IFs in the
oocyte is not due to regional differences in kinase/phosphatase activity,
but rather to factors that interact with the IFs. (The experiment
illustrated in this figure comes from the work of Leilah Backhus's undergraduate
honors thesis, submitted at the University of Colorado,
Boulder.)
FIG. 3. Cytoskeletal reorganization during maturation and the first
cell cycle. The egg contains a single animal-vegetal symmetry axis.
Upon fertilization, the sperm aster begins to form. The formation of
the sperm aster appears to impose a directionality to the cortical MT
system. The cortex moves along this cortical MT system, leading to the
reorganization of cytoplasmic components and the formation of the
nascent dorsal-ventral symmetry axis.
FIG. 4. Distribution of desmosomal components in the oocyte/embryo. Whole-mount immunofluorescence/confocal microscopy reveals the
reorganization of desmosomal components. Control staining of the oocyte reveals little nonspecific reactivity (a). Both a rabbit anti-desmoglein
(b) and a rabbit anti-desmoplakin (c) antibody specifically stain the cortical region of the oocyte. In the embryo (d), this cortical staining has
disappeared (small arrow) and anti-desmoplakin reactivity appears to be associated with the plasma membrane of deeper cells (large arrow),
particularly in regions where cells contact each other. At stage 15 and later (e), desmoplakin immunoreactivity is concentrated at the apical
regions of the lateral membrane of ectodermal cells (arrows). In the absence of primary antibody (f) there is no such staining (embryos in e and
fare both stage 30). Bars, l 0 .urn in a-c, 20 I'm in d, and 5 .urn in e and f.
FIG. 5. Keratin systems of embryo. Following fertilization keratins reassemble into two distinct filament systems, one cortical and the other
subcortical. Whole-mount immunoperoxidase staining of a 4-cell embryo (a) clearly reveals the cortical system. The cortical system eonsists of
large keratin filament bundles organized in a loose network in the vegetal hemisphere and finer filaments in the animal hemisphere. During
embryonic cell division cleavage furrows cut through the cortical keratin filament system (a) and divide it into smaller regions. Parts band c
show two frames from a serial section series of the cortical keratin filament system of an early gastrula stage embryo. Below the corti(:al keratin
system is a finer network of keratin filaments; these can be best seen in sections of the embryo (d). These keratin filaments tend to run around
the blastomeres and often appear associated with the plasma membrane (arrow). The arrows in c and d point to what appears to be a cleavage
furrow/midbody.
FIG. 6. Animal hemisphere sensitivity. To define the region of the
Xenopus embryo sensitive to the effects of anti-keratin antibodies, embryos
were injected at the 8-cell stage. Either the four animal hemisphere
blastomeres (animal4) or the four vegetal hemisphere bias tomeres
(vegetal 4) were injected with -·5 nl of a 9-mg/ml solution of
purified AE3 antibody. Embryos were then allowed to develop until
injected control embryos had completed gastrulation. At thil:; time the
area of the exposed yolk plug was measured (see Klymkowsky et aL,
1992) (area is displayed in pixels). Injection of antibody into the vegetal
hemisphere has no significant effect on the completion of gastrulation,
whereas injection in the animal hemisphere produces a gastrulation
defect similar to that seen in embryos injected at the 1-eell stage.
The result suggests that the integrity of the keratin system i£. required
primarily in the morphogenetically active animal region of the
embryo. (These data were taken from an experiment carried out by
M.W.K., Laurie Maynell, and David Shook.)
