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Infection and Immunity, March 2000, p. 1359-1365, Vol. 68, No. 3
0019-9567/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Coinvasion of Dentinal Tubules by Porphyromonas gingivalis and Streptococcus gordonii Depends upon Binding Specificity of Streptococcal Antigen I/II Adhesin

Robert M. Love,1 Malcolm D. McMillan,1 Yoonsuk Park,2 and Howard F. Jenkinson3,*

School of Dentistry, University of Otago, Dunedin, New Zealand1; Department of Oral Biology, University of Washington, Seattle, Washington2; and Department of Oral and Dental Science, University of Bristol Dental School, Bristol, United Kingdom3

Received 24 August 1999/Returned for modification 3 November 1999/Accepted 23 November 1999

Cell wall-anchored polypeptides of the antigen I/II family are produced by many species of oral streptococci. These proteins mediate adhesion of streptococci to salivary glycoproteins and to other oral microorganisms and promote binding of cells to collagen type I and invasion of dentinal tubules. Since infections of the root canal system have a mixed anaerobic bacterial etiology, we investigated the hypothesis that coadhesion of anaerobic bacteria with streptococci may facilitate invasive endodontic disease. Porphyromonas gingivalis ATCC 33277 cells were able to invade dentinal tubules when cocultured with Streptococcus gordonii DL1 (Challis) but not when cocultured with Streptococcus mutans NG8. An isogenic noninvasive mutant of S. gordonii, with production of SspA and SspB (antigen I/II family) polypeptides abrogated, was deficient in binding to collagen and had a 40% reduced ability to support adhesion of P. gingivalis. Heterologous expression of the S. mutans SpaP (antigen I/II) protein in this mutant restored collagen binding and tubule invasion but not adhesion to P. gingivalis or the ability to promote P. gingivalis coinvasion of dentin. An isogenic afimbrial mutant of P. gingivalis had 50% reduced binding to S. gordonii cells but was unaffected in the ability to coinvade dentinal tubules with S. gordonii wild-type cells. Expression of the S. gordonii SspA or SspB polypeptide on the surface of Lactococcus lactis cells endowed these bacteria with the abilities to bind P. gingivalis, penetrate dentinal tubules, and promote P. gingivalis coinvasion of dentin. The results demonstrate that collagen-binding and P. gingivalis-binding properties of antigen I/II polypeptides are discrete functions. Specificity of antigen I/II polypeptide recognition accounts for the ability of P. gingivalis to coinvade dentinal tubules with S. gordonii but not with S. mutans. This provides evidence that the specificity of interbacterial coadhesion may influence directly the etiology of pulpal and periapical diseases.

* Corresponding author. Mailing address: Department of Oral and Dental Science, University of Bristol Dental School, Lower Maudlin St., Bristol BS1 2LY, United Kingdom. Phone: (44) 117 928 4304. Fax: (44) 117 928 4428. E-mail: howard.jenkinson{at}bristol.ac.uk.

Infection and Immunity, March 2000, p. 1359-1365, Vol. 68, No. 3
0019-9567/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.


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