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Originally published In Press as doi:10.1074/jbc.M011477200 on April 9, 2001

J. Biol. Chem., Vol. 276, Issue 25, 22048-22055, June 22, 2001
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Reassembly of the Tight Junction after Oxidative Stress Depends on Tyrosine Kinase Activity*

Tobias N. MeyerDagger §, Catherine Schwesinger||, Jiuming YeDagger , Bradley M. DenkerDagger **, and Sanjay K. Nigam§Dagger Dagger

From the Dagger  Renal Division, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts 02115, the || Department of Surgery, Children's Hospital, Boston, Massachusetts 02115, and the § Department of Pediatrics and Medicine, Division of Nephrology and Hypertension, University of California in San Diego, La Jolla, California 92093

Oxidative stress compromises the tight junction, but the mechanisms underlying its recovery remain unclear. We developed a model in which oxidative stress reversibly disrupts the tight junction. Exposure of Madin-Darby canine kidney cells to hydrogen peroxide markedly reduced transepithelial resistance and disrupted the staining patterns of the tight junction proteins ZO-1 and occludin. These changes were reversed by catalase. The short-term reassembly of tight junctions was not dependent on new protein synthesis, suggesting that recovery occurs through re-utilization of existing proteins. Although ATP levels were reduced, the reduction was insufficient to explain the observed changes, since a comparable reduction of ATP levels (with 2-deoxy-D-glucose) did not induce these changes. The intracellular hydrogen peroxide scavenger pyruvate protected Madin-Darby canine kidney cells from loss of transepithelial resistance as did the heavy metal scavenger N,N,N',N'-tetrakis(2-pyridylmethyl)ethylenediamine. Of a wide variety of agents examined, only tyrosine kinase inhibitors and protein kinase C inhibitors markedly inhibited tight junction reassembly. During reassembly, tyrosine phosphorylation in or near the lateral membrane, was detected by immunofluorescence. The tyrosine kinase inhibitors genistein and PP-2 inhibited the recovery of transepithelial resistance and perturbed the relocalization of ZO-1 and occludin to the tight junction, indicating that tyrosine kinases, possibly members of the Src family, are critical for reassembly after oxidative stress.

* The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Supported by Deutsche-Forschungs-Gemeinschaft, Bonn, Germany, Grant Me 1760/1-1.

** Supported by National Institutes of Health Grant GM55223 and a Clinical Scientist Award from the National Kidney Foundation.

Dagger Dagger Supported by National Institutes of Health Grant DK53507. To whom correspondence should be addressed: University of California in San Diego, Depts. of Pediatrics and Medicine, Div. of Nephrology and Hypertension, 9500 Gilman Dr., La Jolla, CA 92093-0693. Tel.: 858-822-3482; Fax: 858-822-3483; E-mail: snigam@ucsd.edu.

Copyright © 2001 by The American Society for Biochemistry and Molecular Biology, Inc.
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