INTRODUCTION
Cytokinesis of animal cells begins with a constriction mediated
by an actomyosin contractile apparatus. When this constriction
has narrowed maximally, the daughter cells can either move
apart and separate, as fibroblasts do, or they can cohere, as
early embryonic cells do. The latter way of completing
cytokinesis has been studied for many years in mammalian
embryos, especially in the mouse, and is termed compaction.
It is well established that compaction is dependent on E-
cadherin (Shirayoshi et al., 1983): the cadherin complex is
active, i.e. cytoskeleton linked, at regions of cell-cell contact
(Ohsugi et al., 1996), and in the presence of antibodies to this
cell adhesion molecule, blastomeres remain rounded instead of
cohering (Hyafil et al., 1980). To understand how cells cohere
after division, it is thus important to learn how the cadherin
complex is localized and activated in the right region of
daughter cells. In the mouse embryo, where cadherin is initially
present on the entire blastomere surface (Vestweber et al.,
1987), this may be achieved by local dephosphorylation of
tyrosine residues in pre-existing complexes (Ohsugi et al.,
1996).
In the 1970s and 80s, there was some interest in the role of
the cytoskeleton, particularly of microtubules, in the cohesion
of mouse blastomeres after division. One reason for this
interest is that microtubule arrays had been reported to be
present in large numbers adjacent to the surface mediating
cohesion (Ducibella and Anderson, 1975). Further EM and
conventional fluorescence microscopy studies, however, failed
to detect such microtubules (Houliston et al., 1987). Instead
microtubules were seen near the apical surface, and were thus
proposed to be involved in the polarization of cells during
compaction, rather than in mediating cohesion.
Evidence that microtubules might have a role in compaction
has come from experiments using drugs which perturb
microtubules, but such studies have been controversial. Several
early studies (Ducibella and Anderson, 1975; Ducibella, 1982),
finding that microtubule depolymerization at the 8-cell stage
(when compaction occurs) did not prevent flattening,
concluded that microtubules are not required. Another study,
however, found that nocodazole treatment at the 8-cell stage
accelerates flattening, while taxol reverses it (Maro and
Pickering, 1984). This led to the proposal that microtubules
have a role in constraining cell shape during compaction.
Interestingly, treatment of embryos at earlier stages, namely the
2- (Surani et al., 1980) or 4-cell (Ducibella, 1982) stages, led
to a failure of compaction. Additionally, these cells could not
serve as substrata for the spreading of 8-cell stage blastomeres
(Ducibella, 1982). These experiments seem to implicate
microtubules, at least prior to the 8-cell stage, in the production
of a surface suitable for cohesion. However, these results have
to be interpreted with caution because the treatments used led
to mitotic arrest, which causes cells to lose their adhesiveness
and round up. Hence, it is still not clear whether or not
3695 Journal of Cell Science 111, 3695-3703 (1998)
Printed in Great Britain © The Company of Biologists Limited 1998
JCS3864
During the first few cleavages of the zebrafish embryo,
daughter blastomeres are loosely associated immediately
after furrow ingression, but then gradually cohere.
Cohesion appears to be cadherin-dependent, as cadherin
and β-catenin are found at the membrane between
cohering blastomeres, and blastomeres fail to cohere in
calcium-free medium. Cadherin and β-catenin are not
initially found on the blastomere surface, but are deposited
specifically at the furrow surface. An array of parallel
microtubules is present on either side of the furrow tip
during ingression, as seen by confocal microscopy of α-
tubulin labelled embryos. Transient incubation of embryos
in 1 μg/ml nocodazole at the start of furrowing, which
causes a loss of the furrow array, inhibits the localization
of β-catenin to the furrow surface but does not prevent
furrow ingression. During ingression, intracellular
membranes are transported to the furrow, as shown by
labelling with DiD or DiOC
6
(3). Concentration of these
membranes near the furrow surface is microtubule-
dependent.
These findings suggest that microtubules are required for
cohesion of blastomeres because they mediate trafficking of
intracellular membranes to the furrow surface, where they
are exocytosed and allow cohesion via cadherins.
Key words: Cadherin, β-Catenin, Exocytosis, Microtubule,
Cytokinesis, Compaction
SUMMARY
Furrow-associated microtubule arrays are required for the cohesion of
zebrafish blastomeres following cytokinesis
Suresh Jesuthasan
Max-Planck-Institut für Entwicklungsbiologie, Spemannstr. 35/I, 72076 Tübingen, Germany
(e-mail: suresh.jesuthasan@tuebingen.mpg.de)
Accepted 12 October; published on WWW 18 November 1998