Coinvasion of dentinal tubules by Porphyromonas gingivalis and Streptococcus gordonii depends upon binding specificity of streptococcal antigen I/II adhesin - PubMed (original) (raw)

Coinvasion of dentinal tubules by Porphyromonas gingivalis and Streptococcus gordonii depends upon binding specificity of streptococcal antigen I/II adhesin

R M Love et al. Infect Immun. 2000 Mar.

Abstract

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.

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Figures

FIG. 1

FIG. 1

Transverse sections of human roots showing the invasion of dentinal tubules from the pulpal side by S. gordonii in coculture with P. gingivalis. Bacterial cells were stained (6) (A, D, and G) or detected immunohistochemically with antibodies to S. gordonii surface proteins (B, E, and H) or with antibodies to P. gingivalis cells (C, F, and I). (A, B, and C) Wild-type S. gordonii DL1 cocultured with P. gingivalis ATCC 33277; (D, E, and F) S. gordonii OB219 sspA sspB cocultured with P. gingivalis; (G, H, and I) S. gordonii OB576 sspA sspB expressing SpaP from S. mutans cocultured with P. gingivalis. P. gingivalis cells are detected in panel C only, even though tubule invasion by streptococci is restored in panel G. Bar, 50 μm.

FIG. 2

FIG. 2

Transverse sections of human roots showing the invasion of dentinal tubules by L. lactis strains in monoculture or in coculture with P. gingivalis. (A) Stained wild-type L. lactis MG1363 cells, showing some adhesion of bacteria to the dentin surface (arrow) but no invasion of dentinal tubules; (B) L. lactis cells expressing SspA polypeptide cocultured with P. gingivalis ATCC 33277 and stained (6), showing tubule invasion; (C) as in panel B but reacted with antibodies to SpaP (P1); (D) as in panel B but reacted with antibodies to P. gingivalis cells. Bar, 10 μm.

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