Inflammatory responses of a macrophage/epithelial cell co-culture model to mono and mixed infections with Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia

Microbes and Infection

Volumn 8, Issue 1, 2006, Pages 27-35

  Bodet, Charles ^a   Chandad, Fatiha ^a   Grenier, Daniel ^a  

^a UNIVERSITÉ LAVAL   (Canada)

Author keywords

Co culture; Cytokine; Epithelial cell; Inflammatory response; Lipopolysaccharide; Macrophage; Matrix metalloproteinase; Periodontitis; Porphyromonas gingivalis; Prostaglandin; Tannerella forsythia; Treponema denticola

Indexed keywords

CHEMOKINE; GELATINASE B; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; LIPOPOLYSACCHARIDE; PROSTAGLANDIN E2; RANTES; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; BACTERIUM CULTURE; CELL STRAIN U937; COCULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITHELIUM CELL; HELA CELL; INFLAMMATION; MACROPHAGE; MIXED INFECTION; NONHUMAN; PORPHYROMONAS GINGIVALIS; PRIORITY JOURNAL; TANNERELLA FORSYTHENSIS; TREPONEMA DENTICOLA; WHOLE CELL;

BACTEROIDACEAE; COCULTURE TECHNIQUES; CYTOKINES; DINOPROSTONE; EPITHELIAL CELLS; HELA CELLS; HUMANS; INFLAMMATION; LIPOPOLYSACCHARIDES; MACROPHAGES; MATRIX METALLOPROTEINASE 9; TREPONEMA DENTICOLA;

BACTERIA (MICROORGANISMS); FORSYTHIA; PORPHYROMONAS GINGIVALIS; TANNERELLA FORSYTHENSIS; TREPONEMA DENTICOLA;

EID: 31344439735     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2005.05.015     Document Type: Article

References (57)

1. G. Hutter, U. Schlagenhauf, G. Valenza, M. Horn, S. Burgemeister, H. Claus, and U. Vogel Molecular analysis of bacteria in periodontitis: evaluation of clone libraries, novel phylotypes and putative pathogens Microbiology 149 2003 67 75
2. I. Kroes, P.W. Lepp, and D.A. Relman Bacterial diversity within the human subgingival crevice Proc. Natl. Acad. Sci. USA 96 1999 14547 14552
3. B.J. Paster, S.K. Boches, J.L. Galvin, R.E. Ericson, C.N. Lau, V.A. Levanos, A. Sahasrabudhe, and F.E. Dewhirst Bacterial diversity in human subgingival plaque J. Bacteriol. 183 2001 3770 3783
4. A.D. Haffajee, and S.S. Socransky Microbial etiological agents of destructive periodontal diseases Periodontol. 2000 5 1994 78 111
5. S.S. Socransky, A.D. Haffajee, M.A. Cugini, C. Smith, and R.L. Kent Jr. Microbial complexes in subgingival plaque J. Clin. Periodontol. 25 1998 134 144
6. Y. Kasuga, K. Ishihara, and K. Okuda Significance of detection of Porphyromonas gingivalis, Bacteroides forsythus and Treponema denticola in periodontal pockets Bull. Tokyo Dent. Coll. 41 2000 109 117
7. M.N. Sela Role of Treponema denticola in periodontal diseases Crit. Rev. Oral Biol. Med. 12 2001 399 413
8. R.J. Lamont, and H.F. Jenkinson Life below the gum line: pathogenic mechanisms of Porphyromonas gingivalis Microbiol. Mol. Biol. Rev. 62 1998 1244 1263
9. N.M. O'Brien-Simpson, P.D. Veith, S.G. Dashper, and E.C. Reynolds Antigens of bacteria associated with periodontitis Periodontol. 2000 35 2004 101 134
10. R. Lux, J.N. Miller, N.H. Park, and W. Shi Motility and chemotaxis in tissue penetration of oral epithelial cell layers by Treponema denticola Infect. Immun. 69 2001 6276 6283
11. E. Andrian, D. Grenier, and M. Rouabhia In vitro models of tissue penetration and destruction by Porphyromonas gingivalis Infect. Immun. 72 2004 4689 4698
12. R.J. Lamont, A. Chan, C.M. Belton, K.T. Izutsu, D. Vasel, and A. Weinberg Porphyromonas gingivalis invasion of gingival epithelial cells Infect. Immun. 63 1995 3878 3885
13. J.D. Rudney, R. Chen, and G.J. Sedgewick Actinobacillus actinomycetemcomitans, Porphyromonas gingivalis, and Tannerella forsythensis are components of a polymicrobial intracellular flora within human buccal cells J. Dent. Res. 84 2005 59 63
14. H. Okada, and S. Murakami Cytokine expression in periodontal health and disease Crit. Rev. Oral Biol. Med. 9 1998 248 266
15. H. Birkedal-Hansen Role of cytokines and inflammatory mediators in tissue destruction J. Periodontal Res. 28 1993 500 510
16. J.J. Reynolds, R.M. Hembry, and M.C. Meikle Connective tissue degradation in health and periodontal disease and the roles of matrix metalloproteinases and their natural inhibitors Adv. Dent. Res. 8 1994 312 319
17. M.F. Kagnoff, and L. Eckmann Epithelial cells as sensors for microbial infection J. Clin. Invest. 100 1997 6 10
18. B.A. Dale Periodontal epithelium: a newly recognized role in health and disease Periodontol. 2000 30 2002 70 78
19. S.R. Hedges, W.W. Agace, and C. Svanborg Epithelial cytokine responses and mucosal cytokine networks Trends Microbiol. 3 1995 266 270
20. U. Zappa, M. Reinking-Zappa, H. Graf, and M. Espeland Cell populations and episodic periodontal attachment loss in humans J. Clin. Periodontol. 18 1991 508 515
21. K.S. Kornman, R.C. Page, and M.S. Tonetti The host response to the microbial challenge in periodontitis: assembling the players Periodontol. 2000 14 1997 33 53
22. I. Striz, A. Slavcev, J. Kalanin, M. Jaresova, and S.I. Rennard Cell-cell contacts with epithelial cells modulate the phenotype of human macrophages Inflammation 25 2001 241 246
23. C. Bodet, F. Chandad, and D. Grenier Modulation of cytokine production by Porphyromonas gingivalis in a macrophage and epithelial cell co-culture model Microbes Infect. 7 2005 448 456
24. S.B. Leschine, and E. Canale-Parola Rifampin as a selective agent for isolation of oral spirochetes J. Clin. Microbiol. 12 1980 792 795
25. R.P. Darveau, and R.E. Hancock Procedure for isolation of bacterial lipopolysaccharides from both smooth and rough Pseudomonas aeruginosa and Salmonella typhimurium strains J. Bacteriol. 155 1983 831 838
26. C.P. Schultz, V. Wolf, R. Lange, E. Mertens, J. Wecke, D. Naumann, and U. Zahringer Evidence for a new type of outer membrane lipid in oral spirochete Treponema denticola. Functioning permeation barrier without lipopolysaccharides J. Biol. Chem. 273 1998 15661 15666
27. C. Sundstrom, and K. Nilsson Establishment and characterization of a human histiocytic lymphoma cell line (U-937) Int. J. Cancer 17 1976 565 577
28. G. Rovera, D. Santoli, and C. Damsky Human promyelocytic leukemia cells in culture differentiate into macrophage-like cells when treated with a phorbol diester Proc. Natl. Acad. Sci. USA 76 1979 2779 2783
29. N.J. Lopez, S.S. Socransky, I. Da Silva, M.R. Japlit, and A.D. Haffajee Subgingival microbiota of Chilean patients with chronic periodontitis J. Periodontol. 75 2004 717 725
30. M. Kuboniwa, A. Amano, K.R. Kimura, S. Sekine, S. Kato, Y. Yamamoto, N. Okahashi, T. Iida, and S. Shizukuishi Quantitative detection of periodontal pathogens using real-time polymerase chain reaction with TaqMan probes Oral Microbiol. Immunol. 19 2004 168 176
31. D. Grenier Demonstration of a bimodal coaggregation reaction between Porphyromonas gingivalis and Treponema denticola Oral Microbiol. Immunol. 7 1992 280 284
32. E.S. Yao, R.J. Lamont, S.P. Leu, and A. Weinberg Interbacterial binding among strains of pathogenic and commensal oral bacterial species Oral Microbiol. Immunol. 11 1996 35 41
33. M. Hashimoto, S. Ogawa, Y. Asai, Y. Takai, and T. Ogawa Binding of Porphyromonas gingivalis fimbriae to Treponema denticola dentilisin FEMS Microbiol. Lett. 226 2003 267 271
34. M. Yoneda, T. Yoshikane, N. Motooka, K. Yamada, K. Hisama, T. Naito, I. Okada, M. Yoshinaga, K. Hidaka, K. Imaizumi, K. Maeda, and T. Hirofuji Stimulation of growth of Porphyromonas gingivalis by cell extracts from Tannerella forsythia J. Periodontal Res. 40 2005 105 109
35. D. Grenier Nutritional interactions between two suspected periodontopathogens, Treponema denticola and Porphyromonas gingivalis Infect. Immun. 60 1992 5298 5301
36. D. Grenier, and D. Mayrand Periodontitis as an ecological imbalance H.K. Kuramitsu R.P. Ellen Oral Bacterial Ecology: The Molecular Basis 2000 Horizon Scientific Press: Wymondham Norfolk, UK 275 311
37. R. Kimizuka, T. Kato, K. Ishihara, and K. Okuda Mixed infections with Porphyromonas gingivalis and Treponema denticola cause excessive inflammatory responses in a mouse pneumonia model compared with monoinfections Microbes Infect. 5 2003 1357 1362
38. L. Kesavalu, S.C. Holt, and J.L. Ebersole Virulence of a polymicrobic complex, Treponema denticola and Porphyromonas gingivalis, in a murine model Oral Microbiol. Immunol. 13 1998 373 377
39. T. Takemoto, H. Kurihara, and G. Dahlen Characterization of Bacteroides forsythus isolates J. Clin. Microbiol. 35 1997 1378 1381
40. M. Yoneda, T. Hirofuji, H. Anan, A. Matsumoto, T. Hamachi, K. Nakayama, and K. Maeda Mixed infection of Porphyromonas gingivalis and Bacteroides forsythus in a murine abscess model: involvement of gingipains in a synergistic effect J. Periodontal Res. 36 2001 237 243
41. D.T. Graves, and D. Cochran The contribution of interleukin-1 and tumor necrosis factor to periodontal tissue destruction J. Periodontol. 74 2003 391 401
42. E.S. Van Amersfoort, T.J. Van Berkel, and J. Kuiper Receptors, mediators, and mechanisms involved in bacterial sepsis and septic shock Clin. Microbiol. Rev. 16 2003 379 414
43. A.D. Luster Chemokines - chemotactic cytokines that mediate inflammation N. Engl. J. Med. 338 1998 436 445
44. J. Gamonal, A. Bascones, O. Jorge, and A. Silva Chemokine RANTES in gingival crevicular fluid of adult patients with periodontitis J. Clin. Periodontol. 27 2000 675 681
45. R.B. Johnson, N. Wood, and F.G. Serio Interleukin-11 and IL-17 and the pathogenesis of periodontal disease J. Periodontol. 75 2004 37 43
46. G. Emingil, G. Atilla, and A. Huseyinov Gingival crevicular fluid monocyte chemoattractant protein-1 and RANTES levels in patients with generalized aggressive periodontitis J. Clin. Periodontol. 31 2004 829 834
47. A. Banbula, M. Bugno, A. Kuster, P.C. Heinrich, J. Travis, and J. Potempa Rapid and efficient inactivation of IL-6 gingipains, lysine- and arginine-specific proteinases from Porphyromonas gingivalis Biochem. Biophys. Res. Commun. 261 1999 598 602
48. C.C. Calkins, K. Platt, J. Potempa, and J. Travis Inactivation of tumor necrosis factor-alpha by proteinases (gingipains) from the periodontal pathogen, Porphyromonas gingivalis. Implications of immune evasion J. Biol. Chem. 273 1998 6611 6614
49. C.S. Nixon, M.J. Steffen, and J.L. Ebersole Cytokine responses to Treponema pectinovorum and Treponema denticola in human gingival fibroblasts Infect. Immun. 68 2000 5284 5292
50. Y. Asai, T. Jinno, and T. Ogawa Oral treponemes and their outer membrane extracts activate human gingival epithelial cells through toll-like receptor 2 Infect. Immun. 71 2003 717 725
51. Y.T. Teng, J. Sodek, and C.A. McCulloch Gingival crevicular fluid gelatinase and its relationship to periodontal disease in human subjects J. Periodontal Res. 27 1992 544 552
52. P.C. Smith, V.C. Munoz, L. Collados, and A.D. Oyarzun In situ detection of matrix metalloproteinase-9 (MMP-9) in gingival epithelium in human periodontal disease J. Periodontal Res. 39 2004 87 92
53. A.L. Ejeil, S. Igondjo-Tchen, S. Ghomrasseni, B. Pellat, G. Godeau, and B. Gogly Expression of matrix metalloproteinases (MMPs) and tissue inhibitors of metalloproteinases (TIMPs) in healthy and diseased human gingiva J. Periodontol. 74 2003 188 195
54. S. Offenbacher, P.A. Heasman, and J.G. Collins Modulation of host PGE2 secretion as a determinant of periodontal disease expression J. Periodontol. 64 1993 432 444
55. L.G. Raisz, C.C. Pilbeam, and P.M. Fall Prostaglandins: mechanisms of action and regulation of production in bone Osteoporos. Int. 3 Suppl. 1 1993 136 140
56. S. Offenbacher, B.M. Odle, R.C. Gray, and T.E. Van Dyke Crevicular fluid prostaglandin E levels as a measure of the periodontal disease status of adult and juvenile periodontitis patients J. Periodontal Res. 19 1984 1 13
57. L.J. Jin, P.O. Soder, W.K. Leung, E.F. Corbet, L.P. Samaranayake, B. Soder, and W.I. Davies Granulocyte elastase activity and PGE2 levels in gingival crevicular fluid in relation to the presence of subgingival periodontopathogens in subjects with untreated adult periodontitis J. Clin. Periodontol. 26 1999 531 540