1887

Abstract

The microbiota of the human oral mucosa consists of a myriad of bacterial species that normally exist in commensal harmony with the host. , an aetiological agent in severe forms of periodontitis (a chronic inflammatory disease), is a prominent component of the oral microbiome and a successful colonizer of the oral epithelium. This Gram-negative anaerobe can also exist within the host epithelium without the existence of overt disease. Gingival epithelial cells, the outer lining of the gingival mucosa, which function as an important part of the innate immune system, are among the first host cells colonized by . This review describes recent studies implicating the co-existence and intracellular adaptation of the organism in these target host cells. Specifically, recent findings on the putative mechanisms of persistence, intercellular dissemination and opportunism are highlighted. These new findings may also represent an original and valuable model for mechanistic characterization of other successful host-adapted, self-limiting, persistent intracellular bacteria in human epithelial tissues.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2008/021220-0
2008-10-01
2019-10-16
Loading full text...

Full text loading...

/deliver/fulltext/micro/154/10/2897.html?itemId=/content/journal/micro/10.1099/mic.0.2008/021220-0&mimeType=html&fmt=ahah

References

  1. Amieva, M. R., Salama, N. R., Tompkins, L. S. & Falkow, S. ( 2002; ). Helicobacter pylori enter and survive within multivesicular vacuoles of epithelial cells. Cell Microbiol 4, 677–690.[CrossRef]
    [Google Scholar]
  2. Belton, C. M., Izutsu, K. T., Goodwin, P. C., Park, Y. & Lamont, R. J. ( 1999; ). Fluorescence image analysis of the association between Porphyromonas gingivalis and gingival epithelial cells. Cell Microbiol 1, 215–223.[CrossRef]
    [Google Scholar]
  3. Bosshardt, D. D. & Lang, N. P. ( 2005; ). The junctional epithelium: from health to disease. J Dent Res 84, 9–20.[CrossRef]
    [Google Scholar]
  4. Brozovic, S., Sahoo, R., Barve, S., Shiba, H., Uriarte, S., Blumberg, R. S. & Kinane, D. F. ( 2006; ). Porphyromonas gingivalis enhances FasL expression via up-regulation of NFκB-mediated gene transcription and induces apoptotic cell death in human gingival epithelial cells. Microbiology 152, 797–806.[CrossRef]
    [Google Scholar]
  5. Byrne, G. I. & Ojcius, D. M. ( 2004; ). Chlamydia and apoptosis: life and death decisions of an intracellular pathogen. Nat Rev Microbiol 2, 802–808.[CrossRef]
    [Google Scholar]
  6. Chen, Z., Casiano, C. A. & Fletcher, H. M. ( 2001; ). Protease-active extracellular protein preparations from Porphyromonas gingivalis W83 induce N-cadherin proteolysis, loss of cell adhesion, and apoptosis in human epithelial cells. J Periodontol 72, 641–650.[CrossRef]
    [Google Scholar]
  7. Colombo, A. V., Silva, C. M., Haffajee, A. & Colombo, A. P. ( 2006; ). Identification of oral bacteria associated with crevicular epithelial cells from chronic periodontitis lesions. J Med Microbiol 55, 609–615.[CrossRef]
    [Google Scholar]
  8. Colombo, A. V., da Silva, C. M., Haffajee, A. & Colombo, A. P. ( 2007; ). Identification of intracellular oral species within human crevicular epithelial cells from subjects with chronic periodontitis by fluorescence in situ hybridization. J Periodontal Res 42, 236–243.[CrossRef]
    [Google Scholar]
  9. Coutinho-Silva, R., Perfettini, J. L., Persechini, P. M., Dautry-Varsat, A. & Ojcius, D. M. ( 2001; ). Modulation of P2Z/P2X(7) receptor activity in macrophages infected with Chlamydia psittaci. Am J Physiol Cell Physiol 280, C81–C89.
    [Google Scholar]
  10. Curtis, M. A., Slaney, J. M. & Aduse-Opoku, J. ( 2005; ). Critical pathways in microbial virulence. J Clin Periodontol 32 (Suppl. 6), 28–38.[CrossRef]
    [Google Scholar]
  11. Cutler, C. W. & Jotwani, R. ( 2006; ). Dendritic cells at the oral mucosal interface. J Dent Res 85, 678–689.[CrossRef]
    [Google Scholar]
  12. Darveau, R. P., Belton, C. M., Reife, R. A. & Lamont, R. J. ( 1998; ). Local chemokine paralysis, a novel pathogenic mechanism for Porphyromonas gingivalis. Infect Immun 66, 1660–1665.
    [Google Scholar]
  13. Franchi, L., Kanneganti, T. D., Dubyak, G. R. & Nunez, G. ( 2007; ). Differential requirement of P2X7 receptor and intracellular K+ for caspase-1 activation induced by intracellular and extracellular bacteria. J Biol Chem 282, 18810–18818.[CrossRef]
    [Google Scholar]
  14. Geatch, D. R., Harris, J. I., Heasman, P. A. & Taylor, J. J. ( 1999; ). In vitro studies of lymphocyte apoptosis induced by the periodontal pathogen Porphyromonas gingivalis. J Periodontal Res 34, 70–78.[CrossRef]
    [Google Scholar]
  15. Gemmell, E., Prajaneh, S., Grieco, D. A., Taylor, J. J. & Seymour, G. J. ( 1999; ). Apoptosis in Porphyromonas gingivalis-specific T-cell lines. Oral Microbiol Immunol 14, 331–338.[CrossRef]
    [Google Scholar]
  16. Giacaman, R. A., Nobbs, A. H., Ross, K. F. & Herzberg, M. C. ( 2007; ). Porphyromonas gingivalis selectively up-regulates the HIV-1 coreceptor CCR5 in oral keratinocytes. J Immunol 179, 2542–2550.[CrossRef]
    [Google Scholar]
  17. Gouin, E., Gantelet, H., Egile, C., Lasa, I., Ohayon, H., Villiers, V., Gounon, P., Sansonetti, P. J. & Cossart, P. ( 1999; ). A comparative study of the actin-based motilities of the pathogenic bacteria Listeria monocytogenes, Shigella flexneri and Rickettsia conorii. J Cell Sci 112, 1697–1708.
    [Google Scholar]
  18. Gouin, E., Welch, M. D. & Cossart, P. ( 2005; ). Actin-based motility of intracellular pathogens. Curr Opin Microbiol 8, 35–45.[CrossRef]
    [Google Scholar]
  19. Hajishengallis, G. & Harokopakis, E. ( 2007; ). Porphyromonas gingivalis interactions with complement receptor 3 (CR3): innate immunity or immune evasion? Front Biosci 12, 4547–4557.[CrossRef]
    [Google Scholar]
  20. Hajishengallis, G., Tapping, R. I., Harokopakis, E., Nishiyama, S., Ratti, P., Schifferle, R. E., Lyle, E. A., Triantafilou, M., Triantafilou, K. & Yoshimura, F. ( 2006; ). Differential interactions of fimbriae and lipopolysaccharide from Porphyromonas gingivalis with the Toll-like receptor 2-centred pattern recognition apparatus. Cell Microbiol 8, 1557–1570.[CrossRef]
    [Google Scholar]
  21. Hasegawa, Y., Tribble, G. D., Baker, H. V., Mans, J. J., Handfield, M. & Lamont, R. J. ( 2008; ). Role of Porphyromonas gingivalis SerB in gingival epithelial cell cytoskeletal remodeling and cytokine production. Infect Immun 76, 2420–2427.[CrossRef]
    [Google Scholar]
  22. Herzberg, M. C. & Weyer, M. W. ( 1998; ). Dental plaque, platelets, and cardiovascular diseases. Ann Periodontol 3, 151–160.[CrossRef]
    [Google Scholar]
  23. Hiroi, M., Shimojima, T., Kashimata, M., Miyata, T., Takano, H., Takahama, M. & Sakagami, H. ( 1998; ). Inhibition by Porphyromonas gingivalis LPS of apoptosis induction in human peripheral blood polymorphonuclear leukocytes. Anticancer Res 18, 3475–3479.
    [Google Scholar]
  24. Holt, S. C. & Ebersole, J. L. ( 2005; ). Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia: the “red complex”, a prototype polybacterial pathogenic consortium in periodontitis. Periodontol 2000 38, 72–122.[CrossRef]
    [Google Scholar]
  25. Hosogi, Y. & Duncan, M. J. ( 2005; ). Gene expression in Porphyromonas gingivalis after contact with human epithelial cells. Infect Immun 73, 2327–2335.[CrossRef]
    [Google Scholar]
  26. Jenkinson, H. F. & Lamont, R. J. ( 2005; ). Oral microbial communities in sickness and in health. Trends Microbiol 13, 589–595.[CrossRef]
    [Google Scholar]
  27. Kamath, S., Chen, M. L. & Chakrabarty, A. M. ( 2000; ). Secretion of nucleoside diphosphate kinase by mucoid Pseudomonas aeruginosa 8821: involvement of a carboxy-terminal motif in secretion. J Bacteriol 182, 3826–3831.[CrossRef]
    [Google Scholar]
  28. Kantarci, A. & Van Dyke, T. E. ( 2002; ). Neutrophil-mediated host response to Porphyromonas gingivalis. J Int Acad Periodontol 4, 119–125.
    [Google Scholar]
  29. Katz, J., Sambandam, V., Wu, J. H., Michalek, S. M. & Balkovetz, D. F. ( 2000; ). Characterization of Porphyromonas gingivalis-induced degradation of epithelial cell junctional complexes. Infect Immun 68, 1441–1449.[CrossRef]
    [Google Scholar]
  30. Khakh, B. S. & North, R. A. ( 2006; ). P2X receptors as cell-surface ATP sensors in health and disease. Nature 442, 527–532.[CrossRef]
    [Google Scholar]
  31. Kinane, D. F., Galicia, J. C., Gorr, S. U., Stathopoulou, P. G. & Benakanakere, M. ( 2008; ). P. gingivalis interactions with epithelial cells. Front Biosci 13, 966–984.[CrossRef]
    [Google Scholar]
  32. Kuboniwa, M., Hasegawa, Y., Mao, S., Shizukuishi, S., Amano, A., Lamont, R. J. & Yilmaz, O. ( 2008; ). P. gingivalis accelerates gingival epithelial cell progression through the cell cycle. Microbes Infect 10, 122–128.[CrossRef]
    [Google Scholar]
  33. Lamont, R. J. & Jenkinson, H. F. ( 2000; ). Subgingival colonization by Porphyromonas gingivalis. Oral Microbiol Immunol 15, 341–349.[CrossRef]
    [Google Scholar]
  34. Lamont, R. J., Chan, A., Belton, C. M., Izutsu, K. T., Vasel, D. & Weinberg, A. ( 1995; ). Porphyromonas gingivalis invasion of gingival epithelial cells. Infect Immun 63, 3878–3885.
    [Google Scholar]
  35. Li, L., Michel, R., Cohen, J., Decarlo, A. & Kozarov, E. ( 2008; ). Intracellular survival and vascular cell-to-cell transmission of Porphyromonas gingivalis. BMC Microbiol 8, 26 [CrossRef]
    [Google Scholar]
  36. Mao, S., Park, Y., Hasegawa, Y., Tribble, G. D., James, C. E., Handfield, M., Stavropoulos, M. F., Yilmaz, O. & Lamont, R. J. ( 2007; ). Intrinsic apoptotic pathways of gingival epithelial cells modulated by Porphyromonas gingivalis. Cell Microbiol 9, 1997–2007.[CrossRef]
    [Google Scholar]
  37. Mariathasan, S. & Monack, D. M. ( 2007; ). Inflammasome adaptors and sensors: intracellular regulators of infection and inflammation. Nat Rev Immunol 7, 31–40.[CrossRef]
    [Google Scholar]
  38. Marsh, P. D. ( 2006; ). Dental plaque as a biofilm and a microbial community – implications for health and disease. BMC Oral Health 6 (Suppl. 1), S14 [CrossRef]
    [Google Scholar]
  39. Marshall, R. I. ( 2004; ). Gingival defensins: linking the innate and adaptive immune responses to dental plaque. Periodontol 2000 35, 14–20.[CrossRef]
    [Google Scholar]
  40. McCormick, B. A. ( 2003; ). The use of transepithelial models to examine host-pathogen interactions. Curr Opin Microbiol 6, 77–81.[CrossRef]
    [Google Scholar]
  41. Nakagawa, I., Amano, A., Kuboniwa, M., Nakamura, T., Kawabata, S. & 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, 277–285.[CrossRef]
    [Google Scholar]
  42. Nakhjiri, S. F., Park, Y., Yilmaz, O., Chung, W. O., Watanabe, K., El-Sabaeny, A., Park, K. & Lamont, R. J. ( 2001; ). Inhibition of epithelial cell apoptosis by Porphyromonas gingivalis. FEMS Microbiol Lett 200, 145–149.[CrossRef]
    [Google Scholar]
  43. Nisapakultorn, K., Ross, K. F. & Herzberg, M. C. ( 2001; ). Calprotectin expression in vitro by oral epithelial cells confers resistance to infection by Porphyromonas gingivalis. Infect Immun 69, 4242–4247.[CrossRef]
    [Google Scholar]
  44. Offenbacher, S., Boggess, K. A., Murtha, A. P., Jared, H. L., Lieff, S., McKaig, R. G., Mauriello, S. M., Moss, K. L. & Beck, J. D. ( 2006; ). Progressive periodontal disease and risk of very preterm delivery. Obstet Gynecol 107, 29–36.[CrossRef]
    [Google Scholar]
  45. Ozaki, K. & Hanazawa, S. ( 2001; ). Porphyromonas gingivalis fimbriae inhibit caspase-3-mediated apoptosis of monocytic THP-1 cells under growth factor deprivation via extracellular signal-regulated kinase-dependent expression of p21 Cip/WAF1. Infect Immun 69, 4944–4950.[CrossRef]
    [Google Scholar]
  46. Potempa, J., Banbula, A. & Travis, J. ( 2000; ). Role of bacterial proteinases in matrix destruction and modulation of host responses. Periodontol 2000 24, 153–192.[CrossRef]
    [Google Scholar]
  47. Preshaw, P. M., Schifferle, R. E. & Walters, J. D. ( 1999; ). Porphyromonas gingivalis lipopolysaccharide delays human polymorphonuclear leukocyte apoptosis in vitro. J Periodontal Res 34, 197–202.[CrossRef]
    [Google Scholar]
  48. Rodrigues, P. H., Belanger, M., Dunn, W., Jr & Progulske-Fox, A. ( 2008; ). Porphyromonas gingivalis and the autophagic pathway: an innate immune interaction? Front Biosci 13, 178–187.[CrossRef]
    [Google Scholar]
  49. Rudney, J. D. & Chen, R. ( 2006; ). The vital status of human buccal epithelial cells and the bacteria associated with them. Arch Oral Biol 51, 291–298.[CrossRef]
    [Google Scholar]
  50. Rudney, J. D., Chen, R. & Sedgewick, G. J. ( 2005; ). Actinobacillus actinomycetemcomitans, Porphyromonas gingivalis, and Tannerella forsythensis are components of a polymicrobial intracellular flora within human buccal cells. J Dent Res 84, 59–63.[CrossRef]
    [Google Scholar]
  51. Scannapieco, F. A. ( 2006; ). Pneumonia in nonambulatory patients. The role of oral bacteria and oral hygiene. J Am Dent Assoc 137, 21S–25S.[CrossRef]
    [Google Scholar]
  52. Schroeder, H. E. & Listgarten, M. A. ( 1997; ). The gingival tissues: the architecture of periodontal protection. Periodontol 2000 13, 91–120.[CrossRef]
    [Google Scholar]
  53. Schwiebert, E. M. & Zsembery, A. ( 2003; ). Extracellular ATP as a signaling molecule for epithelial cells. Biochim Biophys Acta 1615, 7–32.[CrossRef]
    [Google Scholar]
  54. Sheets, S. M., Robles-Price, A. G., McKenzie, R. M., Casiano, C. A. & Fletcher, H. M. ( 2008; ). Gingipain-dependent interactions with the host are important for survival of Porphyromonas gingivalis. Front Biosci 13, 3215–3238.
    [Google Scholar]
  55. Socransky, S. S. & Haffajee, A. D. ( 1992; ). The bacterial etiology of destructive periodontal disease: current concepts. J Periodontol 63, 322–331.[CrossRef]
    [Google Scholar]
  56. Surprenant, A., Rassendren, F., Kawashima, E., North, R. A. & Buell, G. ( 1996; ). The cytolytic P2Z receptor for extracellular ATP identified as a P2X receptor (P2X7). Science 272, 735–738.[CrossRef]
    [Google Scholar]
  57. Tribble, G. D., Mao, S., James, C. E. & Lamont, R. J. ( 2006; ). A Porphyromonas gingivalis haloacid dehalogenase family phosphatase interacts with human phosphoproteins and is important for invasion. Proc Natl Acad Sci U S A 103, 11027–11032.[CrossRef]
    [Google Scholar]
  58. Tsuda, K., Furuta, N., Inaba, H., Kawai, S., Hanada, K., Yoshimori, T. & Amano, A. ( 2008; ). Functional analysis of α5β1 integrin and lipid rafts in invasion of epithelial cells by Porphyromonas gingivalis using fluorescent beads coated with bacterial membrane vesicle. Cell Struct Funct 101010, 1111–1112.
    [Google Scholar]
  59. Velmurugan, K., Chen, B., Miller, J. L., Azogue, S., Gurses, S., Hsu, T., Glickman, M., Jacobs, W. R., Jr, Porcelli, S. A. & Briken, V. ( 2007; ). Mycobacterium tuberculosis nuoG is a virulence gene that inhibits apoptosis of infected host cells. PLoS Pathog 3, e110 [CrossRef]
    [Google Scholar]
  60. Weinberg, A., Krisanaprakornkit, S. & Dale, B. A. ( 1998; ). Epithelial antimicrobial peptides: review and significance for oral applications. Crit Rev Oral Biol Med 9, 399–414.[CrossRef]
    [Google Scholar]
  61. Xia, Q., Wang, T., Taub, F., Park, Y., Capestany, C. A., Lamont, R. J. & Hackett, M. ( 2007; ). Quantitative proteomics of intracellular Porphyromonas gingivalis. Proteomics 7, 4323–4337.[CrossRef]
    [Google Scholar]
  62. Yilmaz, O., Watanabe, K. & Lamont, R. J. ( 2002; ). Involvement of integrins in fimbriae-mediated binding and invasion by Porphyromonas gingivalis. Cell Microbiol 4, 305–314.[CrossRef]
    [Google Scholar]
  63. 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.[CrossRef]
    [Google Scholar]
  64. Yilmaz, O., Jungas, T., Verbeke, P. & Ojcius, D. M. ( 2004; ). Activation of the phosphatidylinositol 3-kinase/Akt pathway contributes to survival of primary epithelial cells infected with the periodontal pathogen Porphyromonas gingivalis. Infect Immun 72, 3743–3751.[CrossRef]
    [Google Scholar]
  65. Yilmaz, O., Verbeke, P., Lamont, R. J. & Ojcius, D. M. ( 2006; ). Intercellular spreading of Porphyromonas gingivalis infection in primary gingival epithelial cells. Infect Immun 74, 703–710.[CrossRef]
    [Google Scholar]
  66. Yilmaz, O., Yao, L., Maeda, K., Rose, T. M., Lewis, E. L., Duman, M., Lamont, R. J. & Ojcius, D. M. ( 2008; ). ATP scavenging by the intracellular pathogen Porphyromonas gingivalis inhibits P2X7-mediated host-cell apoptosis. Cell Microbiol 10, 863–875.[CrossRef]
    [Google Scholar]
  67. Zaborina, O., Li, X., Cheng, G., Kapatral, V. & Chakrabarty, A. M. ( 1999; ). Secretion of ATP-utilizing enzymes, nucleoside diphosphate kinase and ATPase, by Mycobacterium bovis BCG: sequestration of ATP from macrophage P2Z receptors? Mol Microbiol 31, 1333–1343.[CrossRef]
    [Google Scholar]
  68. Zhang, Y., Wang, T., Chen, W., Yilmaz, O., Park, Y., Jung, I. Y., Hackett, M. & Lamont, R. J. ( 2005; ). Differential protein expression by Porphyromonas gingivalis in response to secreted epithelial cell components. Proteomics 5, 198–211.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2008/021220-0
Loading
/content/journal/micro/10.1099/mic.0.2008/021220-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error