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10 - Invasion by Porphyromonas gingivalis

Published online by Cambridge University Press:  21 August 2009

Özlem Yilmaz
Affiliation:
Department of Pathobiology, University of Washington, Seattle, Washington 98195, USA
Richard J. Lamont
Affiliation:
Department of Oral Biology, University of Florida, Gainesville, Florida 32610, USA
Richard J. Lamont
Affiliation:
University of Florida
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Summary

Porphyromonas gingivalis cells are Gram-negative, anaerobic, nonmotile short rods that produce black pigmented colonies on blood agar. The taxonomy of the species dates back to 1921 when Oliver and Wherry isolated an organism from a variety of oral and nonoral sites that they were to designate Bacterium melaninogenicum. This heterogeneous grouping was later subdivided into nonfermenters, weak fermenters, and strong fermenters. After a number of status changes within the genus Bacteroides, asaccharolytic oral isolates were assigned to the taxon P. gingivalis. The primary ecological niche of P. gingivalis is in the subgingival crevice, the gap between the surfaces of the tooth and the gingiva (gum); however, the organism can be found elsewhere in the mouth, including supragingival (above the gum) tooth surfaces, the tongue, tonsils, and buccal (cheek) mucosa. Although the species has been associated with odontogenic abscesses and nonoral infections (discussed later), the primary pathogenic potential of P. gingivalis is in periodontal disease. The periodontal tissues include the gingiva, periodontal ligament, and alveolar bone, and they constitute the supporting tissues of the teeth. Chronic destruction of the periodontium, such as occurs in periodontal diseases, can eventually lead to exfoliation of teeth and is the most common cause of tooth loss in adults. Periodontal diseases vary in severity and age of onset, and P. gingivalis is associated, either alone or in combination with other bacteria, with the most severe manifestations.

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Publisher: Cambridge University Press
Print publication year: 2004

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References

Banchereau, J. and Steinman, R. M. (1998). Dendritic cells and the control of immunity. Nature 392, 245–252CrossRefGoogle ScholarPubMed
Barkocy-Gallagher, G. A., Han, N., Patti, J. M., Whitlock, J., Progulske-Fox, A., and Lantz, M. S. (1996). Analysis of the prtP gene encoding porphypain, a cysteine proteinase of Porphyromonas gingivalis. J. Bacteriol. 178, 2734–2741CrossRefGoogle ScholarPubMed
Belton, C. M., Izutsu, K. T., Goodwin, P. C., Park, Y., and Lamont, R. J. (1999). Fluorescence image analysis of the association between Porphyromonas gingivalis and gingival epithelial cells. Cell. Microbiol. 1, 215–224CrossRefGoogle ScholarPubMed
Chen, T., Nakayama, K., Belliveau, L., and Duncan, M. J. (2001). Porphyromonas gingivalis gingipains and adhesion to epithelial cells. Infect. Immun. 69, 3048–3056CrossRefGoogle ScholarPubMed
Chiu, B. (1999). Multiple infections in carotid atherosclerotic plaques. Am. Heart J. 138, S534–536CrossRefGoogle ScholarPubMed
Curtis, M. A., Kuramitsu, H. K., Lantz, M., Macrina, F. L., Nakayama, K., Potempa, J., Reynolds, E. C., and Aduse-Opoku, J. (1999). Molecular genetics and nomenclature of proteases of Porphyromonas gingivalis. J. Periodont. Res. 34, 464–472CrossRefGoogle ScholarPubMed
Cutler, C. W., Jotwani, R., Palucka, K. A., Davoust, J., Bell, D., and Banchereau, J. (1999). Evidence and a novel hypothesis for the role of dendritic cells and Porphyromonas gingivalis in adult periodontitis. J. Periodont. Res. 34, 406–412CrossRefGoogle Scholar
Darveau, R. P., Belton, C. M., Reife, R. A., and Lamont, R. J. (1998). Local chemokine paralysis: a novel pathogenic mechanism of Porphyromonas gingivalis. Infect. Immun. 66, 1660–1665Google ScholarPubMed
DeCarlo, A. A., Grenett, H. E., Harber, G. J., Windsor, L. J., Bodden, M. K., Birkedal-Hansen, B., and Birkedal-Hansen, H. (1998). Induction of matrix metalloproteinases and a collagen-degrading phenotype in fibroblasts and epithelial cells by secreted Porphyromonas gingivalis proteinase. J. Periodont. Res. 33, 408–420CrossRefGoogle Scholar
DeCarlo, A. A., Windsor, L. J., Bodden, M. K., Harber, G. J., Birkedal-Hansen, B., and Birkedal-Hansen, H. (1997). Activation and novel processing of matrix metalloproteinases by thiol-proteinase from the oral anaerobe Porphyromonas gingivalis. J. Dent. Res. 76, 1260–1270CrossRefGoogle ScholarPubMed
Deshpande, R. G., Khan, M. B., and Genco, C. A. (1998). Invasion of aortic and heart endothelial cells by Porphyromonas gingivalis. Infect. Immun. 66, 5337–5343Google ScholarPubMed
Devine, D. A., Marsh, P. D., Percival, R. S., Rangarajan, M., and Curtis, M. A. (1999). Modulation of antibacterial peptide activity by products of Porphyromonas gingivalis and Prevotella spp. Microbiology 145, 965–971CrossRefGoogle ScholarPubMed
Dorn, B. R., Burks, J. N., Seifert, K. N., and Progulske-Fox, A. (2000). Invasion of endothelial and epithelial cells by strains of Porphyromonas gingivalis. FEMS Microbiol. Lett. 187, 139–144CrossRefGoogle ScholarPubMed
Dorn, B. R., Dunn, W. A. Jr., and Progulske-Fox, , , A. (1999). Invasion of human coronary artery cells by periodontal pathogens. Infect. Immun. 67, 5792–5798Google ScholarPubMed
Dorn, B. R., Dunn, W. A. Jr., and Progulske-Fox, A. (2001). Porphyromonas gingivalis traffics to autophagosomes in human coronary artery endothelial cells. Infect. Immun. 69, 5698–5708CrossRefGoogle ScholarPubMed
Duncan, M. J., Nakao, S., Skobe, Z., and Xie, H. (1993). Interactions of Porphyromonas gingivalis with epithelial cells. Infect. Immun. 61, 2260–2265Google ScholarPubMed
Fletcher, J., Reddi, K., Poole, S., Nair, S., Henderson, B., Tabona, P., and Wilson, M. (1997). Interactions between periodontopathogenic bacteria and cytokines. J. Periodont. Res. 32, 200–205CrossRefGoogle ScholarPubMed
Fravalo, P., Menard, C., and Bonnaure-Mallet, M. (1996). Effect of Porphyromonas gingivalis on epithelial cell MMP-9 type IV collagenase production. Infect. Immun. 64, 4940–4945Google ScholarPubMed
Han, N., Whitlock, J., and Progulske-Fox, A. (1996). The hemagglutinin gene A (hagA) of Porphyromonas gingivalis 381 contains four large, contiguous, direct repeats. Infect. Immun. 64, 4000–4007Google ScholarPubMed
Haraszthy, V. I., Zambon, J. J., Trevisan, M., Zeid, M., and Genco, R. J. (2000). Identification of periodontal pathogens in atheromatous plaques. J. Periodontol. 71, 1554–1560CrossRefGoogle ScholarPubMed
Herzberg, M. C., MacFarlane, G. D., Liu, P., and Erickson, P. R. (1994). The platelet as an inflammatory cell in periodontal diseases: the interactions with Porphyromonas gingivalis. In Molecular Pathogenesis of Periodontal Disease, ed. R. Genco, S. Hamada, T. Lehner, J. McGhee, and S. Mergenhagen, pp. 247–256. Washington, DC: ASM Press.
Houalet-Jeanne, S., Pellen-Mussi, P., Tricot-Doleux, S., Apiou, J., and Bonnaure-Mallet, M. (2001). Assessment of internalization and viability of Porphyromonas gingivalis in KB epithelial cells by confocal microscopy. Infect. Immun. 69, 7146–7151CrossRefGoogle ScholarPubMed
Huang, G. T., Haake, S. K., Kim, J. W., and Park, N. (1998). Differential expression of interleukin-8 and intercellular adhesion molecule-1 by human gingival epithelial cells in response to Actinobacillus actinomycetemcomitans or Porphyromonas gingivalis infection. Oral Microbiol. Immunol. 13, 301–309CrossRefGoogle ScholarPubMed
Huang, G. T., Kim, D., Lee, J. K., Kuramitsu, H. K., and Haake, S. K. (2001). Interleukin-8 and intercellular adhesion molecule 1 regulation in oral epithelial cells by selected periodontal bacteria: multiple effects of Porphyromonas gingivalis via antagonistic mechanisms. Infect. Immun. 69, 1364–1372CrossRefGoogle ScholarPubMed
Izutsu, K. T., Belton, C. M., Chan, A., Fatherazi, S., Kanter, J. P., Park, Y., and Lamont, R. J. (1996). Involvement of calcium in interactions between gingival epithelial cells and Porphyromonas gingivalis. FEMS Microbiol. Lett. 144, 145–150CrossRefGoogle ScholarPubMed
Kang, I. C. and Kuramitsu, H. K. (2002). Induction of monocyte chemoattractant protein-1 by Porphyromonas gingivalis in human endothelial cells. FEMS Immunol. Med. Microbiol. 34, 311–317CrossRefGoogle ScholarPubMed
Katz, J., Sambandam, V., Wu, J. H., Michalek, S. M., and Balkovetz, D. F. (2000). Characterization of Porphyromonas gingivalis-induced degradation of epithelial cell junctional complexes. Infect. Immun. 68, 1441–1449CrossRefGoogle ScholarPubMed
Khlgatian, M., Nassar, H., Chou, H. H., Gibson, F. C., and Genco, C. A. (2002). Fimbria-dependent activation of cell adhesion molecule expression in Porphyromonas gingivalis-infected endothelial cells. Infect. Immun. 70, 257–267CrossRefGoogle ScholarPubMed
Kontani, M., Kimura, S., Nakagawa, I., and Hamada, S. (1997). Adherence of Porphyromonas gingivalis to matrix proteins via a fimbrial cryptic receptor exposed by its own arginine-specific protease. Mol. Microbiol. 24, 1179–1187CrossRefGoogle Scholar
Kontani, M., Ono, H., Shibata, H., Okamura, Y., Tanaka, T., Fujiwara, T., Kimura, S., and Hamada, S. (1996). Cysteine protease of Porphyromonas gingivalis 381 enhances binding of fimbriae to cultured human fibroblasts and matrix proteins. Infect. Immun. 64, 756–762Google ScholarPubMed
Kuramitsu, H. K. (1998). Proteases of Porphyromonas gingivalis: what don't they do? Oral Microbiol. Immunol. 13, 263–270CrossRefGoogle Scholar
Kuramitsu, H. K., Qi, M., Kang, I. C., and Chen, W. (2001). Role for periodontal bacteria in cardiovascular diseases. Ann. Periodontol. 6, 41–47CrossRefGoogle ScholarPubMed
Lamont, R. J., Chan, A., Belton, C. M., Izutsu, K. T., Vasel, D., and Weinberg, A. (1995). Porphyromonas gingivalis invasion of gingival epithelial cells. Infect. Immun. 63, 3878–3885Google ScholarPubMed
Lamont, R. J. and Jenkinson, H. F. (1998). Life below the gum line: pathogenic mechanisms of Porphyromonas gingivalis. Microbiol. Mol. Biol. Rev. 62, 1244–1263Google ScholarPubMed
Lamont, R. J. and Jenkinson, H. F. (2000). Subgingival colonization by Porphyromonas gingivalis. Oral Microbiol. Immunol. 15, 341–349CrossRefGoogle ScholarPubMed
Lamont, R. J. and Yilmaz, O. (2002). In or out: the invasiveness of oral bacteria. Periodontology 2000 30, 61–69CrossRefGoogle ScholarPubMed
Lamont, R. J., Oda, D., Persson, R. E., and Persson, G. R. (1992). Interaction of Porphyromonas gingivalis with gingival epithelial cells maintained in culture. Oral Microbiol. Immunol. 7, 364–367CrossRefGoogle ScholarPubMed
Li, L., Messas, E., Batista, E. L. Jr., Levine, R. A., and Amar, S. (2002). Porphyromonas gingivalis infection accelerates the progression of atherosclerosis in a heterozygous apolipoprotein E-deficient murine model. Circulation 105, 861–867CrossRefGoogle Scholar
Madianos, P. N., Papapanou, P. N., Nannmark, U., Dahlen, G., and Sandros, J. (1996). Porphyromonas gingivalis FDC381 multiplies and persists within human oral epithelial cells in vitro. Infect. Immun. 64, 660–664Google ScholarPubMed
Madianos, P. N., Papapanou, P. N., and Sandros, J. (1997). Porphyromonas gingivalis infection of oral epithelium inhibits neutrophil transepithelial migration. Infect. Immun. 65, 3983–3990Google ScholarPubMed
Nakagawa, I., Amano, A., Kuboniwa, M., Nakamura, T., Kawabata, S., and Hamada, S. (2002). Functional differences among FimA variants of Porphyromonas gingivalis and their effects on adhesion to and invasion of human epithelial cells. Infect. Immun. 70, 277–285CrossRefGoogle ScholarPubMed
Nakamura, T., Amano, A., Nakagawa, I., and Hamada, S., (1999). Specific interactions between Porphyromonas gingivalis fimbriae and human extracellular matrix proteins. FEMS Microbiol. Lett. 175, 267–272CrossRefGoogle ScholarPubMed
Nakayama, K., Yoshimura, F., Kadowaki, T., and Yamamoto, K. (1996). Involvement of arginine-specific cysteine proteinase (Arg-gingipain) in fimbriation of Porphyromonas gingivalis. J. Bacteriol. 178, 2818–2824CrossRefGoogle ScholarPubMed
Nakhjiri, S. F., Park, Y., Yilmaz, O., Chung, W. O., Watanabe, K., El-Sabaeny, A., Park, K., and Lamont, R. J. (2001). Inhibition of epithelial cell apoptosis by Porphyromonas gingivalis. FEMS Microbiol. Lett. 200, 145–149CrossRefGoogle ScholarPubMed
Nassar, H, Chou, H. H., Khlgatian, M., Gibson, F. C., Dyke, T. E., and Genco, C. A. (2002). Role for fimbriae and lysine-specific cysteine proteinase gingipain K in expression of interleukin-8 and monocyte chemoattractant protein in Porphyromonas gingivalis-infected endothelial cells. Infect. Immun. 70, 268–276CrossRefGoogle ScholarPubMed
Nisapakultorn, K., Ross, K. F., and Herzberg, M. C. (2001). Calprotectin expression in vitro by oral epithelial cells confers resistance to infection by Porphyromonas gingivalis. Infect. Immun. 69, 4242–4247CrossRefGoogle ScholarPubMed
Njoroge, T., Genco, R. J., Sojar, H. T., and Genco, C. A. (1997). A role for fimbriae in Porphyromanas gingivalis invasion of oral epithelial cells. Infect. Immun. 65, 1980–1984Google Scholar
Ogawa, T., Ogo, H., Uchida, H., and Hamada, S. (1994). Humoral and cellular immune responses to the fimbriae of Porphyromonas gingivalis and their synthetic peptides. J. Med. Microbiol. 40, 397–402CrossRefGoogle ScholarPubMed
Park, Y. and Lamont, R. J. (1998). Contact-dependent protein secretion in Porphyromonas gingivalis. Infect. Immun. 66, 4777–4782Google ScholarPubMed
Potempa, J., Pavloff, N., and Travis, J. (1995). Porphyromonas gingivalis: a proteinase/gene accounting audit. Trends Microbiol. 3, 430–434CrossRefGoogle ScholarPubMed
Progulske-Fox, A., Tumwasorn, S., Lepine, G., Whitlock, J., Savett, D., Ferretti, J. J., and Banas, J. A. (1995). The cloning, expression and sequence analysis of second Porphyromonas gingivalis gene that encodes for a protein involved in hemagglutination. Oral Microbiol. Immunol. 10, 311–318CrossRefGoogle ScholarPubMed
Rudney, J. D., Chen, R., and Sedgewick, G. J. (2001). Intracellular Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis in buccal epithelial cells collected from human subjects. Infect. Immun. 69, 2700–2707CrossRefGoogle ScholarPubMed
Saglie, F. R., Pertuiset, J. H., Smith, C. T., Nestor, M. G., Carranza, F. A., Newman, M. G., Rezende, M. T., and Nisengard, R. (1987). The presence of bacteria in the oral epithelium in periodontal disease. III. Correlation with Langerhans cells. J. Periodontol. 58, 417–422CrossRefGoogle ScholarPubMed
Sandros, J., Madianos, P. N., and Papapanou, P. N. (1996). Cellular events concurrent with Porphyromonas gingivalis invasion of oral epithelium in vitro. Eur. J. Oral Sci. 104, 363–371CrossRefGoogle ScholarPubMed
Sandros, J., Papapanou, P. N., Nannmark, U., and Dahlen, G. (1994). Porphyromonas gingivalis invades human pocket epithelium in vitro. J. Periodont. Res. 29, 62–69CrossRefGoogle ScholarPubMed
Scannapieco, F. A. and Genco, R. J. (1999). Association of periodontal infections with atherosclerotic and pulmonary diseases. J. Periodont. Res. 34, 340–345CrossRefGoogle ScholarPubMed
Shibita, Y., Hayakawa, M., Takiguchi, H., Shiroza, T., and Abiko, Y. (1999). Determination and characterization of the hemagglutinin-associated short motifs found in Porphyromonas gingivalis multiple gene products. J. Biol. Chem. 274, 5012–5020CrossRefGoogle Scholar
Sojar, H. T., Han, Y., Hamada, N., Sharma, A., and Genco, R. J. (1999). Role of the amino-terminal region of Porphyromonas gingivalis fimbriae in adherence to epithelial cells. Infect. Immun. 67, 6173–6176Google ScholarPubMed
Sojar, H. T., Lee, J.-Y., and Genco, R. J. (1995). Fibronectin binding domain of P. gingivalis fimbriae. Biochem. Biophys. Res. Commun. 216, 785–792CrossRefGoogle ScholarPubMed
Sojar, H. T., Sharma, A., and Genco, R. J. (2002). Porphyromonas gingivalis fimbriae bind to cytokeratin of epithelial cells. Infect. Immun. 70, 96–101CrossRefGoogle ScholarPubMed
Tokuda, M., Duncan, M., Cho, M. I., and Kuramitsu, H. K. (1996). Role of Porphyromonas gingivalis protease activity in colonization of oral surfaces. Infect. Immun. 64, 4067–4073Google ScholarPubMed
Tonetti, M. S., Imboden, M. A., Gerber, L., Lang, N. P., Laissue, J., and Mueller, C. (1994). Localized expression of mRNA for phagocyte-specific chemotactic cytokines in human periodontal infections. Infect. Immun. 62, 4005–4014Google ScholarPubMed
Turner, C. E. (2000). Paxillin and focal adhesion signaling. Nat. Cell Biol. 2, E231–E236CrossRefGoogle Scholar
Wang, T., Zhang, Y., Chen, W., Park, Y., Lamont, R. J., and Hackett, M. (2002). Reconstructed protein arrays from 3D HPLC/tandem mass spectrometry and 2D gels: complementary approaches to Porphyromonas gingivalis protein expression. The Analyst 127, 1450–1456CrossRefGoogle ScholarPubMed
Watanabe, K., Onoe, T., Ozeki, M., Shimizu, Y., Sakayori, T., Nakamura, H., and Yoshimura, F. (1996). Sequence and product analyses of the four genes downstream from the fimbrillin gene (fimA) of the oral anaerobe Porphyromonas gingivalis. Microbiol. Immunol. 40, 725–734CrossRefGoogle ScholarPubMed
Watanabe, K., Yilmaz, O., Nakhjiri, S. F., Belton, C. M., and Lamont, R. J. (2001). Association of mitogen-activated protein kinase pathways with gingival epithelial cell responses to Porphyromonas gingivalis infection. Infect. Immun. 69, 6731–6737CrossRefGoogle ScholarPubMed
Weinberg, A., Belton, C. A., Park, Y., and Lamont, R. J. (1997). Role of fimbriae in Porphyromonas gingivalis invasion of gingival epithelial cells. Infect. Immun. 65, 313–316Google ScholarPubMed
Xie, H., Cai, S., and Lamont, R. J. (1997). Environmental regulation of fimbrial gene expression in Porphyromonas gingivalis. Infect. Immun. 65, 2265–2271Google ScholarPubMed
Xie, H., Chung, W., Park, Y., and Lamont, R. J. (2000). Regulation of the Porphyromonas gingivalis fimA (fimbrillin) gene. Infect Immun. 68, 6574–6579CrossRefGoogle ScholarPubMed
Xie, H. and Lamont, R. J. (1999). Promoter architecture of the Porphyromonas gingivalis fimbrillin gene. Infect. Immun. 67, 3227–3235Google ScholarPubMed
Yilmaz, Ö, Watanabe, K., and Lamont, R. J. (2002). Involvement of integrins in fimbriae-mediated binding and invasion by Porphyromonas gingivalis. Cell. Microbiol. 4, 305–314CrossRefGoogle ScholarPubMed
Yilmaz, Ö, Young, P. A., Lamont, R. J., and Kenny, G. E. (2003). Gingival epithelial cell signaling and cytoskeletal responses to Porphyromonas gingivalis invasion. Microbiology 149, 2417–2426CrossRefGoogle ScholarPubMed
Yun, P. L., DeCarlo, A. A., and Hunter, N. (1999). Modulation of major histocompatibility complex protein expression by human gamma interferon mediated by cysteine proteinase-adhesin polyproteins of Porphyromonas gingivalis. Infect. Immun. 67, 2986–2995Google ScholarPubMed
Zhang, J., Dong, H., Kashket, S., and Duncan, M. J. (1999). IL-8 degradation by Porphyromonas gingivalis proteases. Microb. Pathog. 26, 275–280CrossRefGoogle ScholarPubMed

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  • Invasion by Porphyromonas gingivalis
    • By Özlem Yilmaz, Department of Pathobiology, University of Washington, Seattle, Washington 98195, USA, Richard J. Lamont, Department of Oral Biology, University of Florida, Gainesville, Florida 32610, USA
  • Edited by Richard J. Lamont, University of Florida
  • Book: Bacterial Invasion of Host Cells
  • Online publication: 21 August 2009
  • Chapter DOI: https://doi.org/10.1017/CBO9780511546273.012
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  • Invasion by Porphyromonas gingivalis
    • By Özlem Yilmaz, Department of Pathobiology, University of Washington, Seattle, Washington 98195, USA, Richard J. Lamont, Department of Oral Biology, University of Florida, Gainesville, Florida 32610, USA
  • Edited by Richard J. Lamont, University of Florida
  • Book: Bacterial Invasion of Host Cells
  • Online publication: 21 August 2009
  • Chapter DOI: https://doi.org/10.1017/CBO9780511546273.012
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  • Invasion by Porphyromonas gingivalis
    • By Özlem Yilmaz, Department of Pathobiology, University of Washington, Seattle, Washington 98195, USA, Richard J. Lamont, Department of Oral Biology, University of Florida, Gainesville, Florida 32610, USA
  • Edited by Richard J. Lamont, University of Florida
  • Book: Bacterial Invasion of Host Cells
  • Online publication: 21 August 2009
  • Chapter DOI: https://doi.org/10.1017/CBO9780511546273.012
Available formats
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