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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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