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J. Cell Biol.,
Volume 142, Number 4, August 24, 1998 1105-1119
Department of Molecular and Cellular Physiology, Stanford University School of Medicine, Stanford, California 94305-5345
Cadherin-mediated adhesion initiates cell reorganization into tissues, but the mechanisms and dynamics of such adhesion are poorly understood. Using
time-lapse imaging and photobleach recovery analyses
of a fully functional E-cadherin/GFP fusion protein, we
define three sequential stages in cell-cell adhesion and
provide evidence for mechanisms involving E-cadherin
and the actin cytoskeleton in transitions between these
stages. In the first stage, membrane contacts between
two cells initiate coalescence of a highly mobile, diffuse
pool of cell surface E-cadherin into immobile punctate aggregates along contacting membranes. These E-cadherin aggregates are spatially coincident with membrane attachment sites for actin filaments branching off
from circumferential actin cables that circumscribe
each cell. In the second stage, circumferential actin cables near cell-cell contact sites separate, and the resulting two ends of the cable swing outwards to the perimeter of the contact. Concomitantly, subsets of
E-cadherin puncta are also swept to the margins of the
contact where they coalesce into large E-cadherin plaques. This reorganization results in the formation of
a circumferential actin cable that circumscribes both
cells, and is embedded into each E-cadherin plaque at
the contact margin. At this stage, the two cells achieve
maximum contact, a process referred to as compaction. These changes in E-cadherin and actin distributions are
repeated when additional single cells adhere to large
groups of cells. The third stage of adhesion occurs as
additional cells are added to groups of >3 cells; circumferential actin cables linked to E-cadherin plaques on
adjacent cells appear to constrict in a purse-string action, resulting in the further coalescence of individual plaques into the vertices of multicell contacts. The reorganization of E-cadherin and actin results in the condensation of cells into colonies. We propose a model to
explain how, through strengthening and compaction,
E-cadherin and actin cables coordinate to remodel initial cell-cell contacts to the final condensation of cells into colonies.
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