Journal of Cell Science, Supplement 17, 171-181 (1993)
Printed in Great Britain © The Company of Biologists Limited 1993
171
Apical junctions and cell signalling in epithelia
Daniel F. Woods and Peter J. Bryant
Developmental Biology Center, University of California, Irvine, CA 92717, USA
SUMMARY
Genetic analysis in Drosophila has led to the identifica
tion of several proteins that mediate cell-cell interactions
controlling the fate and proliferation of epithelial cells.
These proteins are localized or enriched in the adherens
and septate junctions at the apical end of the lateral
membranes between cells. The proteins localized or
enriched at adherens junctions include Notch, which is
important for the cell interactions controlling neuro
blast and bristle patterning; Boss and sevenless, which
are required for the cell interaction that establishes the
R7 photoreceptor cell; and Armadillo, required for the
wingless-dependent cell interactions that control seg
ment polarity and imaginal disc patterning. Proteins
localized at septate junctions include the product of the
tumor suppressor gene dig, which is required for sep
tate junction formation, apical basal cell polarity, and
the cell interactions that control proliferation. The
results suggest that the cell signalling events important
for cell fate determination and for cell proliferation con
trol in epithelia occur at the apical junctions. The migra
tion of the nucleus to the apical surface of the epithe
lium for mitosis may enable it to interact directly with
the junction-associated signalling mechanisms.
Key words: adherens junction, septate junction, epithelial cell,
mitosis, pattern formation, imaginal disc, ommatidia, Drosophila
INTRODUCTION
Epithelial cell layers protect the organism from its envi
ronment, separate different compartments of the organism,
transport materials from one compartment to another, and
produce both liquid- and solid-phase extracellular compo
nents of the body. These functions depend upon the phys
ical integrity and impermeability of the epithelial sheet, and
on the apical-basal polarity of its constituent cells. The spe
cialized junctions that are formed between adjacent epithe
lial cells are critical to epithelial properties: they provide a
strong physical attachment between cells, they provide a
tight barrier to transepithelial movement of molecules and
ions, and they restrict mobile membrane proteins to either
the apical or the basal-lateral membrane domain, thus con
tributing to apical-basal cell polarity (Rodriguez-Boulan
and Nelson, 1989). These functions of specialized junctions
have been revealed by molecular, physiological and cell
biological studies. However, evidence from genetic analy
sis is now suggesting an additional and critically important
role of apical cell junctions in the development of epithe
lial cell populations. These structures appear to mediate the
interactions between cells and their neighbors that control
both cell proliferation and the formation of spatial patterns
of differentiation.
Intercellular junctions of vertebrate epithelial cells
include, in apical-basal order (Fig. 1): tight junctions (also
called occluding junctions or zonulae occludens), adherens
junctions (also called belt desmosomes or zonulae
adherens), both of which form belts around the apical end
of the cell, as well as gap junctions and desmosomes scat
tered along the lateral membrane basal to the adherens junc
tions (Rodriguez-Boulan and Nelson, 1989). In arthropods
the tight junction is missing, but an additional junction, the
septate junction, is found basal to the adherens junction
(Figs 1 and 2).
Interactions between epithelial cells and their neighbors
control cell proliferation, differentiation and morphogen
esis, and these interactions must take place via the un
specialized lateral membrane or via the specialized junc
tions listed above. At the present state of knowledge any
or all of the specialized junctions connecting epithelial cells
could be involved in these cell interactions. Most investi
gations of cell communication have been focused on gap
junctions, at least in part because simple physiological tests
for their function are available. However, an increasing
volume of evidence points to the apical junctions as the
sites of developmentally significant cell interactions. Much
of this evidence comes from immunolocalization of pro
teins identified by genetic analysis in Drosophila, and a
summary of the locations of these proteins is presented in
Table 1.
MOLECULAR NATURE AND POSSIBLE
FUNCTIONS OF APICAL JUNCTIONS
Adherens junctions
The adherens junction is a thick density that forms a con
tinuous belt around the apical end of each epithelial cell