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Infection and Immunity, March 2001, p. 1364-1372, Vol. 69, No. 3
0019-9567/01/$04.00+0   DOI: 10.1128/IAI.69.3.1364-1372.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

Interleukin-8 and Intercellular Adhesion Molecule 1 Regulation in Oral Epithelial Cells by Selected Periodontal Bacteria: Multiple Effects of Porphyromonas gingivalis via Antagonistic Mechanisms

George T.-J. Huang,1,2,3,* Daniel Kim,1 Jonathan K.-H. Lee,1 Howard K. Kuramitsu,4 and Susan Kinder Haake2,3,5

Section of Endodontics1 and Section of Periodontics,5 Division of Associated Clinical Specialities, Division of Oral Biology and Medicine and Orofacial Pain,2 and Dental and Craniofacial Research Institute,3 UCLA School of Dentistry, Los Angeles, California, and Department of Oral Biology and Microbiology, SUNY Buffalo School of Dental Medicine, Buffalo, New York4

Received 15 August 2000/Returned for modification 13 October 2000/Accepted 21 November 2000

Interaction of bacteria with mucosal surfaces can modulate the production of proinflammatory cytokines and adhesion molecules produced by epithelial cells. Previously, we showed that expression of interleukin-8 (IL-8) and intercellular adhesion molecule 1 (ICAM-1) by gingival epithelial cells increases following interaction with several putative periodontal pathogens. In contrast, expression of IL-8 and ICAM-1 is reduced after Porphyromonas gingivalis ATCC 33277 challenge. In the present study, we investigated the mechanisms that govern the regulation of these two molecules in bacterially infected gingival epithelial cells. Experimental approaches included bacterial stimulation of gingival epithelial cells by either a brief challenge (1.5 to 2 h) or a continuous coculture throughout the incubation period. The kinetics of IL-8 and ICAM-1 expression following brief challenge were such that (i) secretion of IL-8 by gingival epithelial cells reached its peak 2 h following Fusobacterium nucleatum infection whereas it rapidly decreased within 2 h after P. gingivalis infection and remained decreased up to 30 h and (ii) IL-8 and ICAM-1 mRNA levels were up-regulated rapidly 2 to 4 h postinfection and then decreased to basal levels 8 to 20 h after infection with either Actinobacillus actinomycetemcomitans, F. nucleatum, or P. gingivalis. Attenuation of IL-8 secretion was facilitated by adherent P. gingivalis strains. The IL-8 secreted from epithelial cells after F. nucleatum stimulation could be down-regulated by subsequent infection with P. gingivalis or its culture supernatant. Although these results suggested that IL-8 attenuation at the protein level might be associated with P. gingivalis proteases, the Arg- and Lys-gingipain proteases did not appear to be solely responsible for IL-8 attenuation. In addition, while P. gingivalis up-regulated IL-8 mRNA expression, this effect was overridden when the bacteria were continuously cocultured with the epithelial cells. The IL-8 mRNA levels in epithelial cells following sequential challenge with P. gingivalis and F. nucleatum and vice versa were approximately identical and were lower than those following F. nucleatum challenge alone and higher than control levels or those following P. gingivalis challenge alone. Thus, together with the protease effect, P. gingivalis possesses a powerful strategy to ensure the down-regulation of IL-8 and ICAM-1.

* Corresponding author. Mailing address: Division of Associated Clinical Specialties, Section of Endodontics, 23-087 CHS, UCLA School of Dentistry, 10833 Le Conte Ave., Los Angeles, CA 90095-1668. Phone: (310) 206-2691. Fax: (310) 794-4900. E-mail: gtjhuang{at}ucla.edu.

Infection and Immunity, March 2001, p. 1364-1372, Vol. 69, No. 3
0019-9567/01/$04.00+0   DOI: 10.1128/IAI.69.3.1364-1372.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.


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