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The Journal of Immunology, 2003, 171: 6164-6172.
Copyright © 2003 by The American Association of Immunologists

Proinflammatory Cytokines Disrupt Epithelial Barrier Function by Apoptosis-Independent Mechanisms 1

Matthias Bruewer*,{dagger}, Andreas Luegering*,{ddagger}, Torsten Kucharzik*,{ddagger}, Charles A. Parkos*, James L. Madara*,§, Ann M. Hopkins* and Asma Nusrat2,*

* Department of Pathology and Laboratory Medicine, Epithelial Pathobiology Research Unit, Emory University, Atlanta, GA, 30322; Departments of {dagger} General Surgery and {ddagger} Medicine B, University of Muenster, Muenster, Germany; and § Pritzker School of Medicine, University of Chicago, Chicago, IL

It is well known that inflammatory conditions of the intestinal mucosa result in compromised barrier function. Inflammation is characterized by an influx into the mucosa of immune cells that influence epithelial function by releasing proinflammatory cytokines such as IFN-{gamma} and TNF-{alpha}. Mucosal barrier function is regulated by the epithelial apical junctional complex (AJC) consisting of the tight junction and the adherens junction. Since the AJC regulates barrier function, we analyzed the influence of IFN-{gamma} and TNF-{alpha} on its structure/function and determined the contribution of apoptosis to this process using a model intestinal epithelial cell line, T84, and IFN-{gamma} and TNF-{alpha}. AJC structure/function was analyzed by confocal microscopy, biochemical analysis, and physiologic measurement of epithelial gate/fence function. Apoptosis was monitored by determining cytokeratin 18 cleavage and caspase-3 activation. IFN-{gamma} induced time-dependent disruptions in epithelial gate function that were potentiated by coincubation with TNF-{alpha}. Tight junction fence function was somewhat disrupted. Cytokine treatment was associated with internalization of AJC transmembrane proteins, junction adhesion molecule 1, occludin, and claudin-1/4 with minimal effects on the cytoplasmic plaque protein zonula occludens 1. Detergent solubility profiles of junction adhesion molecule 1 and E-cadherin and their affiliation with "raft-like" membrane microdomains were modified by these cytokines. Inhibition of cytokine-induced apoptosis did not block induced permeability defects; further emphasizing their primary influence on the epithelial AJC structure and barrier function. Our findings for the first time clearly separate the proapoptotic effects of IFN-{gamma} and TNF-{alpha} from their abilities to disrupt barrier function.


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Interferon-{gamma} and Tumor Necrosis Factor-{alpha} Synergize to Induce Intestinal Epithelial Barrier Dysfunction by Up-Regulating Myosin Light Chain Kinase Expression
Am. J. Pathol., February 1, 2005; 166(2): 409 - 419.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
S. Morimoto, N. Nishimura, T. Terai, S. Manabe, Y. Yamamoto, W. Shinahara, H. Miyake, S. Tashiro, M. Shimada, and T. Sasaki
Rab13 Mediates the Continuous Endocytic Recycling of Occludin to the Cell Surface
J. Biol. Chem., January 21, 2005; 280(3): 2220 - 2228.
[Abstract] [Full Text] [PDF]

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 J. Histochem. Cytochem.Home page
M. Go, T. Kojima, K.-i. Takano, M. Murata, S. Ichimiya, H. Tsubota, T. Himi, and N. Sawada
Expression and Function of Tight Junctions in the Crypt Epithelium of Human Palatine Tonsils
J. Histochem. Cytochem., December 1, 2004; 52(12): 1627 - 1638.
[Abstract] [Full Text] [PDF]

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 GutHome page
P R Gibson
Increased gut permeability in Crohn's disease: is TNF the link?
Gut, December 1, 2004; 53(12): 1724 - 1725.
[Full Text] [PDF]

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 Am. J. Physiol. Gastrointest. Liver Physiol.Home page
J. L. Watson, S. Ansari, H. Cameron, A. Wang, M. Akhtar, and D. M. McKay
Green tea polyphenol (-)-epigallocatechin gallate blocks epithelial barrier dysfunction provoked by IFN-{gamma} but not by IL-4
Am J Physiol Gastrointest Liver Physiol, November 1, 2004; 287(5): G954 - G961.
[Abstract] [Full Text] [PDF]

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 J. Immunol.Home page
M. Singer and P. J. Sansonetti
IL-8 Is a Key Chemokine Regulating Neutrophil Recruitment in a New Mouse Model of Shigella-Induced Colitis
J. Immunol., September 15, 2004; 173(6): 4197 - 4206.
[Abstract] [Full Text] [PDF]

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 GutHome page
S Zeissig, C Bojarski, N Buergel, J Mankertz, M Zeitz, M Fromm, and J D Schulzke
Downregulation of epithelial apoptosis and barrier repair in active Crohn's disease by tumour necrosis factor {alpha} antibody treatment
Gut, September 1, 2004; 53(9): 1295 - 1302.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Cell Physiol.Home page
M. Bruewer, A. M. Hopkins, M. E. Hobert, A. Nusrat, and J. L. Madara
RhoA, Rac1, and Cdc42 exert distinct effects on epithelial barrier via selective structural and biochemical modulation of junctional proteins and F-actin
Am J Physiol Cell Physiol, August 1, 2004; 287(2): C327 - C335.
[Abstract] [Full Text] [PDF]

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 J. Cell Sci.Home page
K. Turksen and T.-C. Troy
Barriers built on claudins
J. Cell Sci., May 15, 2004; 117(12): 2435 - 2447.
[Abstract] [Full Text] [PDF]


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