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Infection and Immunity, March 2000, p. 1441-1449, Vol. 68, No. 3
0019-9567/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Characterization of Porphyromonas gingivalis-Induced Degradation of Epithelial Cell Junctional Complexes

Jannet Katz,1,* Vijaya Sambandam,2,3 John H. Wu,2 Suzanne M. Michalek,1,4 and Daniel F. Balkovetz2,3,5

Department of Oral Biology,1 Department of Microbiology,4 Department of Medicine,2 and Department of Cell Biology,5 University of Alabama at Birmingham, Birmingham, Alabama 35294, and Veterans Administration Medical Center, Birmingham, Alabama 352333

Received 18 August 1999/Returned for modification 28 October 1999/Accepted 14 December 1999

Porphyromonas gingivalis is considered among the etiological agents of human adult periodontitis. Although in vitro studies have shown that P. gingivalis has the ability to invade epithelial cell lines, its effect on the epithelial barrier junctions is not known. Immunofluorescence analysis of human gingival epithelial cells confirmed the presence of tight-junction (occludin), adherens junction (E-cadherin), and cell-extracellular matrix junction (beta 1-integrin) transmembrane proteins. These transmembrane proteins are expressed in Madin-Darby canine kidney (MDCK) cells. In addition, MDCK cells polarize and therefore serve as a useful in vitro model for studies on the epithelial cell barrier. Using the MDCK cell system, we examined the effect of P. gingivalis on epithelial barrier function. Exposure of the basolateral surfaces of MDCK cells to P. gingivalis (>109 bacteria/ml) resulted in a decrease in transepithelial resistance. Immunofluorescence microscopy demonstrated decreases in the amounts of immunoreactive occludin, E-cadherin, and beta 1-integrin at specific times which were related to a disruption of cell-cell junctions in MDCK cells exposed to basolateral P. gingivalis. Disruption of cell-cell junctions was also observed upon apical exposure to bacteria; however, the effects took longer than those seen upon basolateral exposure. Cell viability was not affected by either basolateral or apical exposure to P. gingivalis. Western blot analysis demonstrated hydrolysis of occludin, E-cadherin, and beta 1-integrin in lysates derived from MDCK cells exposed to P. gingivalis. Immunoprecipitated occludin and E-cadherin molecules from MDCK cell lysates were also degraded by P. gingivalis, suggesting a bacterial protease(s) capable of cleaving these epithelial junction transmembrane proteins. Collectively, these data suggest that P. gingivalis is able to invade the deeper structures of connective tissues via a paracellular pathway by degrading epithelial cell-cell junction complexes, thus allowing the spread of the bacterium. These results also indicate the importance of a critical threshold concentration of P. gingivalis to initiate epithelial barrier destruction.

* Corresponding author. Mailing address: The University of Alabama at Birmingham, Departments of Microbiology and Oral Biology, 258 Bevill Biomedical Research Building, 845 19th St. South, Birmingham, Alabama 35294-2170. Phone: (205) 934-3470. Fax: (205) 934-1426. E-mail: jenny_katz{at}micro.microbio.uab.edu.

Infection and Immunity, March 2000, p. 1441-1449, Vol. 68, No. 3
0019-9567/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.


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