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. 1995 Oct;63(10):3878–3885. doi: 10.1128/iai.63.10.3878-3885.1995

Porphyromonas gingivalis invasion of gingival epithelial cells.

R J Lamont 1, A Chan 1, C M Belton 1, K T Izutsu 1, D Vasel 1, A Weinberg 1
PMCID: PMC173546  PMID: 7558295

Abstract

Porphyromonas gingivalis, a periodontal pathogen, can invade primary cultures of gingival epithelial cells. Optimal invasion occurred at a relatively low multiplicity of infection (i.e., 100) and demonstrated saturation at a higher multiplicity of infection. Following the lag phase, during which bacteria invaded poorly, invasion was independent of growth phase. P. gingivalis was capable of replicating within the epithelial cells. Invasion was an active process requiring both bacterial and epithelial cell energy production. Invasion was sensitive to inhibitors of microfilaments and microtubules, demonstrating that epithelial cell cytoskeletal rearrangements are involved in bacterial entry. P. gingivalis, but not epithelial cell, protein synthesis was necessary for invasion. Invasion within the epithelial cells was not blocked by inhibitors of protein kinase activity. Invasion was inhibited by protease inhibitors, suggesting that P. gingivalis proteases may be involved in the invasion process. Low-passage clinical isolates of P. gingivalis invaded with higher efficiency than the type strain. Serum inhibited invasion of the type strain but had no effect on the invasion of a clinical isolate. Invasion of gingival epithelial cells by P. gingivalis may contribute to the pathology of periodontal diseases.

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Selected References

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  1. Bliska J. B., Galán J. E., Falkow S. Signal transduction in the mammalian cell during bacterial attachment and entry. Cell. 1993 Jun 4;73(5):903–920. doi: 10.1016/0092-8674(93)90270-z. [DOI] [PubMed] [Google Scholar]
  2. Blix I. J., Hars R., Preus H. R., Helgeland K. Entrance of Actinobacillus actinomycetemcomitans into HEp-2 cells in vitro. J Periodontol. 1992 Sep;63(9):723–728. doi: 10.1902/jop.1992.63.9.723. [DOI] [PubMed] [Google Scholar]
  3. Cimasoni G., McBride B. C. Adherence of Treponema denticola to modified hydroxyapatite. J Dent Res. 1987 Dec;66(12):1727–1729. doi: 10.1177/00220345870660120601. [DOI] [PubMed] [Google Scholar]
  4. Cimasoni G., Song M., McBride B. C. Effect of crevicular fluid and lysosomal enzymes on the adherence of streptococci and bacteroides to hydroxyapatite. Infect Immun. 1987 Jun;55(6):1484–1489. doi: 10.1128/iai.55.6.1484-1489.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Donnenberg M. S., Donohue-Rolfe A., Keusch G. T. A comparison of HEp-2 cell invasion by enteropathogenic and enteroinvasive Escherichia coli. FEMS Microbiol Lett. 1990 May;57(1-2):83–86. doi: 10.1016/0378-1097(90)90417-o. [DOI] [PubMed] [Google Scholar]
  6. Duncan M. J., Nakao S., Skobe Z., Xie H. Interactions of Porphyromonas gingivalis with epithelial cells. Infect Immun. 1993 May;61(5):2260–2265. doi: 10.1128/iai.61.5.2260-2265.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Ewanowich C. A., Melton A. R., Weiss A. A., Sherburne R. K., Peppler M. S. Invasion of HeLa 229 cells by virulent Bordetella pertussis. Infect Immun. 1989 Sep;57(9):2698–2704. doi: 10.1128/iai.57.9.2698-2704.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Falkow S. Bacterial entry into eukaryotic cells. Cell. 1991 Jun 28;65(7):1099–1102. doi: 10.1016/0092-8674(91)90003-h. [DOI] [PubMed] [Google Scholar]
  9. Finlay B. B., Falkow S. Common themes in microbial pathogenicity. Microbiol Rev. 1989 Jun;53(2):210–230. doi: 10.1128/mr.53.2.210-230.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Finlay B. B., Falkow S. Comparison of the invasion strategies used by Salmonella cholerae-suis, Shigella flexneri and Yersinia enterocolitica to enter cultured animal cells: endosome acidification is not required for bacterial invasion or intracellular replication. Biochimie. 1988 Aug;70(8):1089–1099. doi: 10.1016/0300-9084(88)90271-4. [DOI] [PubMed] [Google Scholar]
  11. Gaillard J. L., Berche P., Mounier J., Richard S., Sansonetti P. In vitro model of penetration and intracellular growth of Listeria monocytogenes in the human enterocyte-like cell line Caco-2. Infect Immun. 1987 Nov;55(11):2822–2829. doi: 10.1128/iai.55.11.2822-2829.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gharbia S. E., Shah H. N. Hydrolytic enzymes liberated by black-pigmented gram-negative anaerobes. FEMS Immunol Med Microbiol. 1993 Mar;6(2-3):139–145. doi: 10.1111/j.1574-695X.1993.tb00316.x. [DOI] [PubMed] [Google Scholar]
  13. Gibbons R. J. Bacterial adhesion to oral tissues: a model for infectious diseases. J Dent Res. 1989 May;68(5):750–760. doi: 10.1177/00220345890680050101. [DOI] [PubMed] [Google Scholar]
  14. Isogai H., Isogai E., Yoshimura F., Suzuki T., Kagota W., Takano K. Specific inhibition of adherence of an oral strain of Bacteroides gingivalis 381 to epithelial cells by monoclonal antibodies against the bacterial fimbriae. Arch Oral Biol. 1988;33(7):479–485. doi: 10.1016/0003-9969(88)90028-3. [DOI] [PubMed] [Google Scholar]
  15. Lamont R. J., Bevan C. A., Gil S., Persson R. E., Rosan B. Involvement of Porphyromonas gingivalis fimbriae in adherence to Streptococcus gordonii. Oral Microbiol Immunol. 1993 Oct;8(5):272–276. doi: 10.1111/j.1399-302x.1993.tb00573.x. [DOI] [PubMed] [Google Scholar]
  16. Lamont R. J., Hersey S. G., Rosan B. Characterization of the adherence of Porphyromonas gingivalis to oral streptococci. Oral Microbiol Immunol. 1992 Aug;7(4):193–197. doi: 10.1111/j.1399-302x.1992.tb00024.x. [DOI] [PubMed] [Google Scholar]
  17. Lamont R. J., Oda D., Persson R. E., Persson G. R. Interaction of Porphyromonas gingivalis with gingival epithelial cells maintained in culture. Oral Microbiol Immunol. 1992 Dec;7(6):364–367. doi: 10.1111/j.1399-302x.1992.tb00637.x. [DOI] [PubMed] [Google Scholar]
  18. Li J., Ellen R. P., Hoover C. I., Felton J. R. Association of proteases of Porphyromonas (Bacteroides) gingivalis with its adhesion to Actinomyces viscosus. J Dent Res. 1991 Feb;70(2):82–86. doi: 10.1177/00220345910700021501. [DOI] [PubMed] [Google Scholar]
  19. Mayrand D., Holt S. C. Biology of asaccharolytic black-pigmented Bacteroides species. Microbiol Rev. 1988 Mar;52(1):134–152. doi: 10.1128/mr.52.1.134-152.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Meyer D. H., Sreenivasan P. K., Fives-Taylor P. M. Evidence for invasion of a human oral cell line by Actinobacillus actinomycetemcomitans. Infect Immun. 1991 Aug;59(8):2719–2726. doi: 10.1128/iai.59.8.2719-2726.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Oda D., Watson E. Human oral epithelial cell culture I. Improved conditions for reproducible culture in serum-free medium. In Vitro Cell Dev Biol. 1990 Jun;26(6):589–595. doi: 10.1007/BF02624208. [DOI] [PubMed] [Google Scholar]
  22. Oelschlaeger T. A., Guerry P., Kopecko D. J. Unusual microtubule-dependent endocytosis mechanisms triggered by Campylobacter jejuni and Citrobacter freundii. Proc Natl Acad Sci U S A. 1993 Jul 15;90(14):6884–6888. doi: 10.1073/pnas.90.14.6884. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Richardson W. P., Sadoff J. C. Induced engulfment of Neisseria gonorrhoeae by tissue culture cells. Infect Immun. 1988 Sep;56(9):2512–2514. doi: 10.1128/iai.56.9.2512-2514.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Rosenshine I., Duronio V., Finlay B. B. Tyrosine protein kinase inhibitors block invasin-promoted bacterial uptake by epithelial cells. Infect Immun. 1992 Jun;60(6):2211–2217. doi: 10.1128/iai.60.6.2211-2217.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Rosenshine I., Finlay B. B. Exploitation of host signal transduction pathways and cytoskeletal functions by invasive bacteria. Bioessays. 1993 Jan;15(1):17–24. doi: 10.1002/bies.950150104. [DOI] [PubMed] [Google Scholar]
  26. Sandros J., Papapanou P. N., Nannmark U., Dahlén G. Porphyromonas gingivalis invades human pocket epithelium in vitro. J Periodontal Res. 1994 Jan;29(1):62–69. doi: 10.1111/j.1600-0765.1994.tb01092.x. [DOI] [PubMed] [Google Scholar]
  27. Sandros J., Papapanou P., Dahlén G. Porphyromonas gingivalis invades oral epithelial cells in vitro. J Periodontal Res. 1993 May;28(3):219–226. doi: 10.1111/j.1600-0765.1993.tb01072.x. [DOI] [PubMed] [Google Scholar]
  28. Sansonetti P. J. Bacterial pathogens, from adherence to invasion: comparative strategies. Med Microbiol Immunol. 1993 Nov;182(5):223–232. doi: 10.1007/BF00579621. [DOI] [PubMed] [Google Scholar]
  29. Slots J., Genco R. J. Black-pigmented Bacteroides species, Capnocytophaga species, and Actinobacillus actinomycetemcomitans in human periodontal disease: virulence factors in colonization, survival, and tissue destruction. J Dent Res. 1984 Mar;63(3):412–421. doi: 10.1177/00220345840630031101. [DOI] [PubMed] [Google Scholar]
  30. Slots J., Gibbons R. J. Attachment of Bacteroides melaninogenicus subsp. asaccharolyticus to oral surfaces and its possible role in colonization of the mouth and of periodontal pockets. Infect Immun. 1978 Jan;19(1):254–264. doi: 10.1128/iai.19.1.254-264.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Slots J., Listgarten M. A. Bacteroides gingivalis, Bacteroides intermedius and Actinobacillus actinomycetemcomitans in human periodontal diseases. J Clin Periodontol. 1988 Feb;15(2):85–93. doi: 10.1111/j.1600-051x.1988.tb00999.x. [DOI] [PubMed] [Google Scholar]
  32. Small P. L., Isberg R. R., Falkow S. Comparison of the ability of enteroinvasive Escherichia coli, Salmonella typhimurium, Yersinia pseudotuberculosis, and Yersinia enterocolitica to enter and replicate within HEp-2 cells. Infect Immun. 1987 Jul;55(7):1674–1679. doi: 10.1128/iai.55.7.1674-1679.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Socransky S. S., Haffajee A. D. The bacterial etiology of destructive periodontal disease: current concepts. J Periodontol. 1992 Apr;63(4 Suppl):322–331. doi: 10.1902/jop.1992.63.4s.322. [DOI] [PubMed] [Google Scholar]
  34. Sreenivasan P. K., Meyer D. H., Fives-Taylor P. M. Requirements for invasion of epithelial cells by Actinobacillus actinomycetemcomitans. Infect Immun. 1993 Apr;61(4):1239–1245. doi: 10.1128/iai.61.4.1239-1245.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. St Geme J. W., 3rd, Falkow S. Haemophilus influenzae adheres to and enters cultured human epithelial cells. Infect Immun. 1990 Dec;58(12):4036–4044. doi: 10.1128/iai.58.12.4036-4044.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Tilney L. G., Portnoy D. A. Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes. J Cell Biol. 1989 Oct;109(4 Pt 1):1597–1608. doi: 10.1083/jcb.109.4.1597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. van Winkelhoff A. J., van Steenbergen T. J., de Graaff J. The role of black-pigmented Bacteroides in human oral infections. J Clin Periodontol. 1988 Mar;15(3):145–155. doi: 10.1111/j.1600-051x.1988.tb01561.x. [DOI] [PubMed] [Google Scholar]

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