This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Love, R. M.
Right arrow Articles by Jenkinson, H. F.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Love, R. M.
Right arrow Articles by Jenkinson, H. F.

 Previous Article  |  Next Article 

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.


This article has been cited by other articles:

  • Xu, P., Alves, J. M., Kitten, T., Brown, A., Chen, Z., Ozaki, L. S., Manque, P., Ge, X., Serrano, M. G., Puiu, D., Hendricks, S., Wang, Y., Chaplin, M. D., Akan, D., Paik, S., Peterson, D. L., Macrina, F. L., Buck, G. A. (2007). Genome of the Opportunistic Pathogen Streptococcus sanguinis. J. Bacteriol. 189: 3166-3175 [Abstract] [Full Text]  
  • Edwards, A. M., Grossman, T. J., Rudney, J. D. (2006). Fusobacterium nucleatum Transports Noninvasive Streptococcus cristatus into Human Epithelial Cells. Infect. Immun. 74: 654-662 [Abstract] [Full Text]  
  • Chhour, K.-L., Nadkarni, M. A., Byun, R., Martin, F. E., Jacques, N. A., Hunter, N. (2005). Molecular Analysis of Microbial Diversity in Advanced Caries. J. Clin. Microbiol. 43: 843-849 [Abstract] [Full Text]  
  • Byun, R., Nadkarni, M. A., Chhour, K.-L., Martin, F. E., Jacques, N. A., Hunter, N. (2004). Quantitative Analysis of Diverse Lactobacillus Species Present in Advanced Dental Caries. J. Clin. Microbiol. 42: 3128-3136 [Abstract] [Full Text]  
  • Sato, Y., Okamoto, K., Kagami, A., Yamamoto, Y., Igarashi, T., Kizaki, H. (2004). Streptococcus mutans Strains Harboring Collagen-binding Adhesin. JDR 83: 534-539 [Abstract] [Full Text]  
  • Engels-Deutsch, M., Pini, A., Yamashita, Y., Shibata, Y., Haikel, Y., Scholler-Guinard, M., Klein, J.-P. (2003). Insertional Inactivation of pac and rmlB Genes Reduces the Release of Tumor Necrosis Factor Alpha, Interleukin-6, and Interleukin-8 Induced by Streptococcus mutans in Monocytic, Dental Pulp, and Periodontal Ligament Cells. Infect. Immun. 71: 5169-5177 [Abstract] [Full Text]  
  • Yilmaz, O., Young, P. A., Lamont, R. J., Kenny, G. E. (2003). Gingival epithelial cell signalling and cytoskeletal responses to Porphyromonas gingivalis invasion. Microbiology 149: 2417-2426 [Abstract] [Full Text]  
  • Demuth, D. R., Irvine, D. C. (2002). Structural and Functional Variation within the Alanine-Rich Repetitive Domain of Streptococcal Antigen I/II. Infect. Immun. 70: 6389-6398 [Abstract] [Full Text]  
  • Munson, M.A., Pitt-Ford, T., Chong, B., Weightman, A., Wade, W.G. (2002). Molecular and Cultural Analysis of the Microflora Associated with Endodontic Infections. JDR 81: 761-766 [Abstract] [Full Text]  
  • Kolenbrander, P. E., Andersen, R. N., Blehert, D. S., Egland, P. G., Foster, J. S., Palmer, R. J. Jr. (2002). Communication among Oral Bacteria. Microbiol. Mol. Biol. Rev. 66: 486-505 [Abstract] [Full Text]  
  • Lamont, R. J., El-Sabaeny, A., Park, Y., Cook, G. S., Costerton, J. W., Demuth, D. R. (2002). Role of the Streptococcus gordonii SspB protein in the development of Porphyromonas gingivalis biofilms on streptococcal substrates. Microbiology 148: 1627-1636 [Abstract] [Full Text]  
  • Love, R.M., Jenkinson, H.F. (2002). INVASION OF DENTINAL TUBULES BY ORAL BACTERIA. CROBM 13: 171-183 [Abstract] [Full Text]  
  • Demuth, D. R., Irvine, D. C., Costerton, J. W., Cook, G. S., Lamont, R. J. (2001). Discrete Protein Determinant Directs the Species-Specific Adherence of Porphyromonas gingivalis to Oral Streptococci. Infect. Immun. 69: 5736-5741 [Abstract] [Full Text]  
  • Xie, H., Chung, W. O., Park, Y., Lamont, R. J. (2000). Regulation of the Porphyromonas gingivalis fimA (Fimbrillin) Gene. Infect. Immun. 68: 6574-6579 [Abstract] [Full Text]  
  • Chung, W. O., Demuth, D. R., Lamont, R. J. (2000). Identification of a Porphyromonas gingivalis Receptor for the Streptococcus gordonii SspB Protein. Infect. Immun. 68: 6758-6762 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»