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(Received for publication, August 15, 1996, and in revised form, February 11, 1997)
From the Renal Division, Department of Medicine, Brigham and
Women's Hospital and Harvard Medical School,
Boston, Massachusetts 02115
A key feature of the ischemic epithelial cell
phenotype is the disruption of tight junctions (TJ). In a Manin-Darby
canine kidney cell model for ischemia-reperfusion/hypoxia-reoxygenation injury which employs inhibitors of glycolysis
(2-deoxy-D-glucose) and oxidative phosphorylation
(antimycin A), transepithelial electrical resistance, a measure of TJ
integrity, dropped rapidly, correlating well with declining ATP levels.
Although immunocytochemical studies revealed only subtle changes in the
distribution of the TJ proteins, zonula occludens (ZO)-1, ZO-2, and
cingulin, examination of the Triton X-100 solubilities of these
proteins, an indicator of cytoskeletal association, revealed a striking
shift of all three TJ proteins into the insoluble pool, consistent with
increased cytoskeletal interaction during ATP depletion. In addition,
rate-zonal centrifugation analysis of a detergent-soluble fraction
showed an increase in the amount of ZO-1 and ZO-2 in high density
fractions following ATP depletion, providing further evidence for
association of TJ proteins into a large complex possibly involving the
cytoskeleton. Analysis of immunoprecipitation data from
[35S]methionine-labeled cells revealed that ATP depletion
led to the association of a 240-kDa protein with the ZO-1-containing complex. Western blots of this protein immunoprecipitated with anti-ZO-1 antibodies confirmed its identity as fodrin, a protein believed to link membrane and other proteins to the actin-based cytoskeleton. Together, our data suggest that in the absence of major
immunocytochemical changes, ATP depletion leads TJ proteins to form
large insoluble complexes and associate with the cytoskeleton. We
propose a model in which a key, potentially regulated, step in the
generation of the ischemic epithelial cell phenotype is the interaction
between TJ proteins and fodrin and/or other cytoskeletal proteins.
Volume 272, Number 26,
Issue of June 27, 1997
pp. 16133-16139
©1997 by The American Society for Biochemistry and Molecular Biology, Inc.
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