This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Saved Citations Download to citation manager Request Permissions Request Reprints Add to My Marked Citations Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Citing Articles via Scopus Google Scholar Articles by Grenier, D. Articles by Mayrand, D. Search for Related Content PubMed PubMed Citation Articles by Grenier, D. Articles by Mayrand, D. Pubmed/NCBI databases Compound via MeSH Substance via MeSH Hazardous Substances DB IRON Social Bookmarking                         What's this?

The Capacity of Porphyromonas gingivalis to Multiply Under Iron-limiting Conditions Correlates with its Pathogenicity in an Animal Model

Groupe de Recherche en Ecologie Buccale, Daniel.Grenier{at}greb.ulaval.ca

V. Goulet

Groupe de Recherche en Ecologie Buccale

D. Mayrand

Faculté de Medecine Dentaire, and Faculte des Sciences et de Genie, Universite Laval, Quebec, Canada G1K 7P4

Isolates of Porphyromonas gingivalis have various abilities to induce infections in an animal model. The hypothesis of this study was that pathogenic strains of P. gingivalis could multiply under iron-limiting conditions, while non-pathogenic strains could not. Three pathogenic strains (W50, W83, and ATCC 49417) grew to a final optical density (660 nm) > 2 in horse serum, while the growth of the 3 non-pathogenic strains (ATCC 33277, LB13D-2, and HW24D-1) was negligible. When an excess of hemin or ferric chloride was added to the serum, significant growth of the non-pathogenic strains occurred. Under iron-limiting conditions, the pathogenic strains of P. gingivalis had a much lower requirement for human iron-loaded transferrin and hemin than the non-pathogenic strains. Proteolytic degradation of transferrin, which may be associated with the release of iron, was not markedly different for pathogenic and nonpathogenic strains. In addition, no relationship could be established between the level of 55Fe uptake from 55Fe-transferrin and the pathogenicity of strains. Our study provided evidence that the ability of P. gingivalis to multiply in vitro under iron-limiting conditions may be correlated with its ability to induce infections in an animal model. Isolates of P. gingivalis possessing a low requirement for iron are likely to have a higher potential for initiating periodontal infections.

Key Words: periodontal disease • Porphyromonas gingivalis • pathogenicity • iron • transferrin.

REFERENCES

• Bramanti TE, Holt SC ( 1991). Roles of porphyrins and host iron transport proteins in regulation of growth of Porphyromonas gingivalis W50. J Bacteriol 173:7330-7339.[Abstract/Free Full Text]
• Brochu V., Grenier D., Nakayama K., Mayrand D. (2001). Acquisition of iron from human transferrin by Porphyromonas gingivalis: a role for Arg- and Lysgingipain activities. Oral Microbiol Immunol 16:79-87.[CrossRef][Medline] [Order article via Infotrieve]
• Cutler CW, Arnolds RR, Schenkein HA (1993). Inhibition of C3 and IgG proteolysis enhances phagocytosis of Porphyromonas gingivalis. J Immunol 151:7016-7029.[Abstract]
• Genco CA (1995). Regulation of hemin and iron transport in Porphyromonas gingivalis. Adv Dent Res 9:41-47.[Abstract/Free Full Text]
• Grenier D., Bélanger M. (1991). Protective effect of Porphyromonas gingivalis outer membrane vesicles against bactericidal activity of human serum. Infect Immun 59:3004-3008.[Abstract/Free Full Text]
• Grenier D., Mayrand D. (1983). Etudes d'infections mixtes anaerobies comportant Bacteroides gingivalis. Can J Microbiol 29:612-618.[Medline] [Order article via Infotrieve]
• Grenier D., Mayrand D. (1987). Selected characteristics of pathogenic and nonpathogenic strains of Bacteroides gingivalis. J Clin Microbiol 25:738-740.[Abstract/Free Full Text]
• Haffajee AD, Socransky SS (1994). Microbial etiological agents of destructive periodontal diseases. Periodontol 2000 5:78-111.[CrossRef]
• Holt SC, Kesavalu L., Walker S., Genco CA (1999). Virulence factors of Porphyromonas gingivalis. Periodontol 2000 20:168-238.[CrossRef]
• Inoshita E., Iwakura K., Amano A., Tamagawa H., Shizukuishi S. (1991). Effect of transferrin on the growth of Porphyromonas gingivalis. J Dent Res 70:1258-1261.
• Kastelein P., van Steenbergen Tjm, Bras JM, de Graaff J. (1981). An experimentally induced phlegmonous abscess by a strain of Bacteroides gingivalis in guinea pigs and mice. Antonie van Leeuwenhoek J Microbiol 47:1-9.
• Magarinos B., Romalde JL, Lemos ML, Barja JL, Toranzo AE (1994). Iron uptake by Pasteurella piscicida and its role in pathogenicity for fish. Appl Environ Microbiol 60:2990-2998.[Abstract/Free Full Text]
• Mayrand D., McBride BC (1980). Ecological relationships of bacteria involved in a simple, mixed anaerobic infection. Infect Immun 27:44-50.[Abstract/Free Full Text]
• Mukherjee S. (1985). The role of crevicular fluid iron in periodontal disease. J Periodontol 56:22-27.[Medline] [Order article via Infotrieve]
• Mukherjee S., Murphy RA, Wawszkiewcz EJ (1988). Effect of hemoglobin and of ferric ammonium citrate on the virulence of periodontopathic bacteria. Oral Microbiol Immunol 3:192-295.[Medline] [Order article via Infotrieve]
• Neiders ME, Chen PB, Suido H., Reynolds HS, Zambon JJ, Shlossman M., et al. (1989). Heterogeneity of virulence among strains of Bacteroides gingivalis. J Periodontal Res 24:192-198.[CrossRef][Medline] [Order article via Infotrieve]
• Pintor M., Ferreiros CM, Criado MT (1993). Characterization of the transferrin-iron uptake system in Neisseria meningitidis. FEMS Microbiol Lett 112:159-166.[CrossRef][Medline] [Order article via Infotrieve]
• Sawada K., Kokeguchi S., Hongyo H., Sawada S., Miyamoto M., Maeda H., et al. (1999). Identification by subtractive hybridization of a novel insertion sequence specific for virulent strains of Porphyromonas gingivalis. Infect Immun 67:5621-5625.[Abstract/Free Full Text]
• Slots J., Ting M. ( 1999). Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis in human periodontal disease: occurrence and treatment. Periodontol 2000 20:82-121.[CrossRef]
• Sundqvist G., Johansson E. (1982). Bactericidal effect of pooled human serum on Bacteroides melaninogenicus, Bacteroides asaccharolyticus and Actinobacillus actinomycetemcomitans. Scand J Dent Res 90:29-36.[Medline] [Order article via Infotrieve]
• Sundqvist G., Figdor D., Hanstrom L., Sorlin S., Sandstrom G. (1991). Phagocytosis and virulence of different strains of Porphyromonas gingivalis. Scand J Dent Res 99:117-129.[Medline] [Order article via Infotrieve]
• Taylor PW (1983). Bactericidal and bacteriolytic activity of serum against Gram negative bacteria. Microb Rev 47:46-83.[Free Full Text]
• van Steenbergen TJ, Namavar F., de Graaff J. (1985). Chemiluminescence of human leukocytes by black-pigmented Bacteroides strains from dental plaque and other sites. J Periodontal Res 20:58-71.[CrossRef][Medline] [Order article via Infotrieve]
• van Steenbergen TJ, Kastelein P., Touw JJ, de Graaff J. (1982). Virulence of black-pigmented Bacteroides strains from periodontal pockets and other sites in experimentally induced skin lesions in mice. J Periodontal Res 17:41-49.[CrossRef][Medline] [Order article via Infotrieve]
• Wooldridge KG, Williams PH (1993). Iron uptake mechanisms of pathogenic bacteria. FEMS Microbiol Rev 12:325-348.[CrossRef][Medline] [Order article via Infotrieve]

Journal of Dental Research, Vol. 80, No. 7, 1678-1682 (2001)
DOI: 10.1177/00220345010800071501


CiteULike    Complore    Connotea    Del.icio.us    Digg    Reddit    Technorati    Twitter    What's this?

This article has been cited by other articles:

				J. Wu, X. Lin, and H. Xie Regulation of Hemin Binding Proteins by a Novel Transcriptional Activator in Porphyromonas gingivalis J. Bacteriol., January 1, 2009; 191(1): 115 - 122. [Abstract] [Full Text] [PDF]

				C. Bodet, M. Piche, F. Chandad, and D. Grenier Inhibition of periodontopathogen-derived proteolytic enzymes by a high-molecular-weight fraction isolated from cranberry J. Antimicrob. Chemother., April 1, 2006; 57(4): 685 - 690. [Abstract] [Full Text] [PDF]

				V. Goulet, B. Britigan, K. Nakayama, and D. Grenier Cleavage of Human Transferrin by Porphyromonas gingivalis Gingipains Promotes Growth and Formation of Hydroxyl Radicals Infect. Immun., August 1, 2004; 72(8): 4351 - 4356. [Abstract] [Full Text] [PDF]

				M. Paramaesvaran, K.-A. Nguyen, E. Caldon, J. A. McDonald, S. Najdi, G. Gonzaga, D. B. Langley, A. DeCarlo, M. J. Crossley, N. Hunter, et al. Porphyrin-Mediated Cell Surface Heme Capture from Hemoglobin by Porphyromonas gingivalis J. Bacteriol., April 15, 2003; 185(8): 2528 - 2537. [Abstract] [Full Text] [PDF]

This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Saved Citations Download to citation manager Request Permissions Request Reprints Add to My Marked Citations Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Citing Articles via Scopus Google Scholar Articles by Grenier, D. Articles by Mayrand, D. Search for Related Content PubMed PubMed Citation Articles by Grenier, D. Articles by Mayrand, D. Pubmed/NCBI databases Compound via MeSH Substance via MeSH Hazardous Substances DB IRON Social Bookmarking                         What's this?