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Vol. 9, Issue 11, 3161-3177, November 1998
Department of Molecular and Cellular Physiology, Stanford
University School of Medicine, Stanford, California 94305-5345
Organization of proteins into structurally and
functionally distinct plasma membrane domains is an essential
characteristic of polarized epithelial cells. Based on studies with
cultured kidney cells, we have hypothesized that a mechanism for
restricting Na/K-ATPase to the basal-lateral membrane involves
E-cadherin-mediated cell-cell adhesion and integration of Na/K-ATPase
into the Triton X-100-insoluble ankyrin- and spectrin-based membrane
cytoskeleton. In this study, we examined the relevance of these in
vitro observations to the generation of epithelial cell polarity in
vivo during mouse kidney development. Using differential detergent
extraction, immunoblotting, and immunofluorescence
histochemistry, we demonstrate the following. First, expression of the
220-kDa splice variant of ankyrin-3 correlates with the development of
resistance to Triton X-100 extraction for Na/K-ATPase, E-cadherin, and
catenins and precedes maximal accumulation of Na/K-ATPase. Second,
expression of the 190-kDa slice variant of ankyrin-3 correlates with
maximal accumulation of Na/K-ATPase. Third, Na/K-ATPase, ankyrin-3, and
fodrin specifically colocalize at the basal-lateral plasma membrane of
all epithelial cells in which they are expressed and during all stages
of nephrogenesis. Fourth, the relative immunofluorescence staining
intensities of Na/K-ATPase, ankyrin-3, and fodrin become more similar
during development until they are essentially identical in adult
kidney. Thus, renal epithelial cells in vivo regulate the accumulation of E-cadherin-mediated adherens junctions, the membrane cytoskeleton, and Na/K-ATPase through sequential protein expression and assembly on
the basal-lateral membrane. These results are consistent with a
mechanism in which generation and maintenance of polarized
distributions of these proteins in vivo and in vitro involve cell-cell
adhesion, assembly of the membrane cytoskeleton complex, and
concomitant integration and retention of Na/K-ATPase in this complex.
Corresponding author. E-mail address:
wjnelson{at}leland.stanford.edu.
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