Synergistic virulence of Porphyromonas gingivalis and Treponema denticola in a murine periodontitis model
Summary Chronic periodontitis is characterized by the destruction of the tissues supporting the teeth and has been associated with the presence of a subgingival polymicrobial biofilm containing Porphyromonas gingivalis and Treponema denticola. We have investigated the potential synergistic virulence...
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| Veröffentlicht in: | Molecular oral microbiology Jg. 26; H. 4; S. 229 - 240 |
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| Format: | Journal Article |
| Sprache: | Englisch |
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Oxford, UK
Blackwell Publishing Ltd
01.08.2011
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| ISSN: | 2041-1006, 2041-1014, 2041-1014 |
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| Abstract | Summary
Chronic periodontitis is characterized by the destruction of the tissues supporting the teeth and has been associated with the presence of a subgingival polymicrobial biofilm containing Porphyromonas gingivalis and Treponema denticola. We have investigated the potential synergistic virulence of P. gingivalis and T. denticola using a murine experimental model of periodontitis. An inoculation regime of four intra‐oral doses of 1 × 1010P. gingivalis cells induced significant periodontal bone loss compared with loss in sham‐inoculated mice, whereas doses of 1 × 109 cells or lower did not induce bone loss. Inoculation with T. denticola with up to eight doses of 1 × 1010 cells failed to induce bone loss in this model. However, four doses of a co‐inoculum of a 1 : 1 ratio of P. gingivalis and T. denticola at 5 × 108 or 1 × 109 total bacterial cells induced the same level of bone loss as four doses of 1 × 1010P. gingivalis cells. Co‐inoculation induced strong P. gingivalis‐specific T‐cell proliferative and interferon‐γ‐dominant cytokine responses, and induced a strong T. denticola‐specific interferon‐γ dominant cytokine response. Only at the higher co‐inoculum dose of 1 × 1010 total cells was a T. denticola‐specific T‐cell proliferative response observed. These data show that P. gingivalis and T. denticola act synergistically to stimulate the host immune response and to induce alveolar bone loss in a murine experimental periodontitis model. |
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| AbstractList | Chronic periodontitis is characterized by the destruction of the tissues supporting the teeth and has been associated with the presence of a subgingival polymicrobial biofilm containing Porphyromonas gingivalis and Treponema denticola. We have investigated the potential synergistic virulence of P. gingivalis and T. denticola using a murine experimental model of periodontitis. An inoculation regime of four intra-oral doses of 1 × 10(10) P. gingivalis cells induced significant periodontal bone loss compared with loss in sham-inoculated mice, whereas doses of 1 × 10(9) cells or lower did not induce bone loss. Inoculation with T. denticola with up to eight doses of 1 × 10(10) cells failed to induce bone loss in this model. However, four doses of a co-inoculum of a 1 : 1 ratio of P. gingivalis and T. denticola at 5 × 10(8) or 1 × 10(9) total bacterial cells induced the same level of bone loss as four doses of 1 × 10(10) P. gingivalis cells. Co-inoculation induced strong P. gingivalis-specific T-cell proliferative and interferon-γ-dominant cytokine responses, and induced a strong T. denticola-specific interferon-γ dominant cytokine response. Only at the higher co-inoculum dose of 1 × 10(10) total cells was a T. denticola-specific T-cell proliferative response observed. These data show that P. gingivalis and T. denticola act synergistically to stimulate the host immune response and to induce alveolar bone loss in a murine experimental periodontitis model. Summary Chronic periodontitis is characterized by the destruction of the tissues supporting the teeth and has been associated with the presence of a subgingival polymicrobial biofilm containing Porphyromonas gingivalis and Treponema denticola. We have investigated the potential synergistic virulence of P. gingivalis and T. denticola using a murine experimental model of periodontitis. An inoculation regime of four intra‐oral doses of 1 × 1010P. gingivalis cells induced significant periodontal bone loss compared with loss in sham‐inoculated mice, whereas doses of 1 × 109 cells or lower did not induce bone loss. Inoculation with T. denticola with up to eight doses of 1 × 1010 cells failed to induce bone loss in this model. However, four doses of a co‐inoculum of a 1 : 1 ratio of P. gingivalis and T. denticola at 5 × 108 or 1 × 109 total bacterial cells induced the same level of bone loss as four doses of 1 × 1010P. gingivalis cells. Co‐inoculation induced strong P. gingivalis‐specific T‐cell proliferative and interferon‐γ‐dominant cytokine responses, and induced a strong T. denticola‐specific interferon‐γ dominant cytokine response. Only at the higher co‐inoculum dose of 1 × 1010 total cells was a T. denticola‐specific T‐cell proliferative response observed. These data show that P. gingivalis and T. denticola act synergistically to stimulate the host immune response and to induce alveolar bone loss in a murine experimental periodontitis model. Chronic periodontitis is characterized by the destruction of the tissues supporting the teeth and has been associated with the presence of a subgingival polymicrobial biofilm containing Porphyromonas gingivalis and Treponema denticola. We have investigated the potential synergistic virulence of P. gingivalis and T. denticola using a murine experimental model of periodontitis. An inoculation regime of four intra-oral doses of 1 × 10(10) P. gingivalis cells induced significant periodontal bone loss compared with loss in sham-inoculated mice, whereas doses of 1 × 10(9) cells or lower did not induce bone loss. Inoculation with T. denticola with up to eight doses of 1 × 10(10) cells failed to induce bone loss in this model. However, four doses of a co-inoculum of a 1 : 1 ratio of P. gingivalis and T. denticola at 5 × 10(8) or 1 × 10(9) total bacterial cells induced the same level of bone loss as four doses of 1 × 10(10) P. gingivalis cells. Co-inoculation induced strong P. gingivalis-specific T-cell proliferative and interferon-γ-dominant cytokine responses, and induced a strong T. denticola-specific interferon-γ dominant cytokine response. Only at the higher co-inoculum dose of 1 × 10(10) total cells was a T. denticola-specific T-cell proliferative response observed. These data show that P. gingivalis and T. denticola act synergistically to stimulate the host immune response and to induce alveolar bone loss in a murine experimental periodontitis model.Chronic periodontitis is characterized by the destruction of the tissues supporting the teeth and has been associated with the presence of a subgingival polymicrobial biofilm containing Porphyromonas gingivalis and Treponema denticola. We have investigated the potential synergistic virulence of P. gingivalis and T. denticola using a murine experimental model of periodontitis. An inoculation regime of four intra-oral doses of 1 × 10(10) P. gingivalis cells induced significant periodontal bone loss compared with loss in sham-inoculated mice, whereas doses of 1 × 10(9) cells or lower did not induce bone loss. Inoculation with T. denticola with up to eight doses of 1 × 10(10) cells failed to induce bone loss in this model. However, four doses of a co-inoculum of a 1 : 1 ratio of P. gingivalis and T. denticola at 5 × 10(8) or 1 × 10(9) total bacterial cells induced the same level of bone loss as four doses of 1 × 10(10) P. gingivalis cells. Co-inoculation induced strong P. gingivalis-specific T-cell proliferative and interferon-γ-dominant cytokine responses, and induced a strong T. denticola-specific interferon-γ dominant cytokine response. Only at the higher co-inoculum dose of 1 × 10(10) total cells was a T. denticola-specific T-cell proliferative response observed. These data show that P. gingivalis and T. denticola act synergistically to stimulate the host immune response and to induce alveolar bone loss in a murine experimental periodontitis model. Chronic periodontitis is characterized by the destruction of the tissues supporting the teeth and has been associated with the presence of a subgingival polymicrobial biofilm containing Porphyromonas gingivalis and Treponema denticola . We have investigated the potential synergistic virulence of P. gingivalis and T. denticola using a murine experimental model of periodontitis. An inoculation regime of four intra‐oral doses of 1 × 10 10 P. gingivalis cells induced significant periodontal bone loss compared with loss in sham‐inoculated mice, whereas doses of 1 × 10 9 cells or lower did not induce bone loss. Inoculation with T. denticola with up to eight doses of 1 × 10 10 cells failed to induce bone loss in this model. However, four doses of a co‐inoculum of a 1 : 1 ratio of P. gingivalis and T. denticola at 5 × 10 8 or 1 × 10 9 total bacterial cells induced the same level of bone loss as four doses of 1 × 10 10 P. gingivalis cells. Co‐inoculation induced strong P. gingivalis ‐specific T‐cell proliferative and interferon‐γ‐dominant cytokine responses, and induced a strong T. denticola ‐specific interferon‐γ dominant cytokine response. Only at the higher co‐inoculum dose of 1 × 10 10 total cells was a T. denticola ‐specific T‐cell proliferative response observed. These data show that P. gingivalis and T. denticola act synergistically to stimulate the host immune response and to induce alveolar bone loss in a murine experimental periodontitis model. Chronic periodontitis is characterized by the destruction of the tissues supporting the teeth and has been associated with the presence of a subgingival polymicrobial biofilm containing Porphyromonas gingivalis and Treponema denticola. We have investigated the potential synergistic virulence of P. gingivalis and T. denticola using a murine experimental model of periodontitis. An inoculation regime of four intra-oral doses of 1 1010P. gingivalis cells induced significant periodontal bone loss compared with loss in sham-inoculated mice, whereas doses of 1 109 cells or lower did not induce bone loss. Inoculation with T. denticola with up to eight doses of 11010 cells failed to induce bone loss in this model. However, four doses of a co-inoculum of a 1:1 ratio of P. gingivalis and T. denticola at 5 108 or 1 109 total bacterial cells induced the same level of bone loss as four doses of 1 1010P. gingivalis cells. Co-inoculation induced strong P. gingivalis-specific T-cell proliferative and interferon- gamma -dominant cytokine responses, and induced a strong T. denticola-specific interferon- gamma dominant cytokine response. Only at the higher co-inoculum dose of 11010 total cells was a T. denticola-specific T-cell proliferative response observed. These data show that P. gingivalis and T. denticola act synergistically to stimulate the host immune response and to induce alveolar bone loss in a murine experimental periodontitis model. |
| Author | Dashper, S.G. O'Brien-Simpson, N.M. Reynolds, E.C. Orth, R.K-H. |
| Author_xml | – sequence: 1 givenname: R.K-H. surname: Orth fullname: Orth, R.K-H. organization: Oral Health CRC, Melbourne Dental School and Bio21 Institute, The University of Melbourne, Melbourne, Vic., Australia – sequence: 2 givenname: N.M. surname: O'Brien-Simpson fullname: O'Brien-Simpson, N.M. organization: Oral Health CRC, Melbourne Dental School and Bio21 Institute, The University of Melbourne, Melbourne, Vic., Australia – sequence: 3 givenname: S.G. surname: Dashper fullname: Dashper, S.G. organization: Oral Health CRC, Melbourne Dental School and Bio21 Institute, The University of Melbourne, Melbourne, Vic., Australia – sequence: 4 givenname: E.C. surname: Reynolds fullname: Reynolds, E.C. organization: Oral Health CRC, Melbourne Dental School and Bio21 Institute, The University of Melbourne, Melbourne, Vic., Australia |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/21729244$$D View this record in MEDLINE/PubMed |
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| References | Kesavalu, L., Walker, S.G., Holt, S.C., Crawley, R.R. and Ebersole, J.L. (1997) Virulence characteristics of oral treponemes in a murine model. Infect Immun 65: 5096-5102. Klausen, B., Evans, R.T., Ramamurthy, N.S. et al. (1991) Periodontal bone level and gingival proteinase activity on gnobiotic rats immunized with Bacteroides gingivalis. Oral Microbiol Immunol 6: 193-201. Kesavalu, L., Holt, S.C. and Ebersole, J.L. (1996) Trypsin-like protease activity of Porphyromonas gingivalis as a potential virulence factor in a murine lesion model. Microb Pathog 20: 1-10. Kesavalu, L., Sathishkumar, S., Bakthavatchalu, V. et al. (2007) Rat model of polymicrobial infection, immunity, and alveolar bone resorption in periodontal disease. Infect Immun 75: 1704-1712. O'Brien-Simpson, N.M., Paolini, R.A., Hoffmann, B., Slakeski, N., Dashper, S.G. and Reynolds, E.C. (2001) Role of RgpA, RgpB, and Kgp proteinases in virulence of Porphyromonas gingivalis W50 in a murine lesion model. Infect Immun 69: 7527-7534. Choi, J., Borrello, M.A., Smith, E., Cutler, C.W., Sojar, H. and Zauderer, M. (2001) Prior exposure of mice to Fusobacterium nucleatum modulates host response to Porphyromonas gingivalis. Oral Microbiol Immunol 16: 338-344. Yoneda, M., Hirofuji, T., Anan, H. et al. (2001) Mixed infection of Porphyromonas gingivalis and Bacteroides forsythus in a murine abscess model: involvement of gingipains in a synergistic effect. J Periodontal Res 36: 237-243. Arroll, T.W., Centurion-Lara, A., Lukehart, S.A. and Van Voorhis, W.C. (1999) T-cell responses to Treponema pallidum subsp. pallidum antigens during the course of experimental syphilis infection. Infect Immun 67: 4757-4763. O'Brien-Simpson, N.M., Paolini, R.A. and Reynolds, E.C. (2000b) RgpA-Kgp peptide-based immunogens provide protection against Porphyromonas gingivalis challenge in a murine lesion model. Infect Immun 68: 4055-4063. Tam, V., O'Brien-Simpson, N.M., Pathirana, R.D., Frazer, L.T. and Reynolds, E.C. (2008) Characterization of T cell responses to the RgpA-Kgp proteinase-adhesin complexes of Porphyromonas gingivalis in BALB/c mice. J Immunol 181: 4150-4158. Stashenko, P., Goncalves, R.B., Lipkin, B., Ficarelli, A., Sasaki, H. and Campos-Neto, A. (2007) Th1 immune response promotes severe bone resorption caused by Porphyromonas gingivalis. Am J Pathol 170: 203-213. Tanner, A. (1992) Microbial etiology of periodontal diseases. Where are we? Where are we going? Curr Opin Dent 2: 12-24. Haffajee, A.D., Cugini, M.A., Tanner, A. et al. (1998) Subgingival microbiota in healthy, well-maintained elder and periodontitis subjects. J Clin Periodontol 25: 346-353. Lundqvist, C., Baranov, V., Teglund, S., Hammarstrom, S. and Hammarstrom, M. (1994) Cytokine profile and ultrastructure of intraepithelial gd T cells in chronically inflamed human gingiva suggest a cytotoxis effector function. J Immunol 153: 2302-2312. Verma, R.K., Rajapakse, S., Meka, A. et al. (2010b) Porphyromonas gingivalis and Treponema denticola mixed microbial infection in a rat model of periodontal disease. Interdiscip Perspect Infect Dis 2010: 605125. Tran, S.D. and Rudney, J.D. (1999) Improved multiplex PCR using conserved and species-specific 16S rRNA gene primers for simultaneous detection of Actinobacillus actinomycetemcomitans, Bacteroides forsythus, and Porphyromonas gingivalis. J Clin Microbiol 37: 3504-3508. Verma, R.K., Bhattacharyya, I., Sevilla, A. et al. (2010a) Virulence of major periodontal pathogens and lack of humoral immune protection in a rat model of periodontal disease. Oral Dis 16: 686-695. Umeda, M., Ishikawa, I., Benno, Y. and Mitsuoka, T. (1990) Improved detection of oral spirochetes with an anaerobic culture method. Oral Microbiol Immunol 5: 90-94. O'Brien-Simpson, N.M., Black, C.L., Bhogal, P.S. et al. (2000a) Serum immunoglobulin G (IgG) and IgG subclass responses to the RgpA-Kgp proteinase-adhesin complex of Porphyromonas gingivalis in adult periodontitis. Infect Immun 68: 2704-2712. O'Brien-Simpson, N.M., Pathirana, R.D., Paolini, R.A. et al. (2005) An immune response directed to proteinase and adhesin functional epitopes protects against Porphyromonas gingivalis-induced periodontal bone loss. J Immunol 175: 3980-3989. Pathirana, R.D., O'Brien-Simpson, N.M., Veith, P.D., Riley, P.F. and Reynolds, E.C. (2006) Characterization of proteinase-adhesin complexes of Porphyromonas gingivalis. Microbiology 152: 2381-2394. Socransky, S.S., Haffajee, A.D., Cugini, M.A., Smith, C. and Kent, R.L. Jr (1998) Microbial complexes in subgingival plaque. J Clin Periodontol 25: 134-144. Garcia, L., Tercero, J.C., Legido, B., Ramos, J.A., Alemany, J. and Sanz, M. (1998) Rapid detection of Actinobacillus actinomycetemcomitans, Prevotella intermedia and Porphyromona gingivalis by multiplex PCR. J Periodontal Res 33: 59-64. Salvador, S.L., Syed, S.A. and Loesche, W.J. (1987) Comparison of three dispersion procedures for quantitative recovery of cultivable species of subgingival spirochetes. J Clin Microbiol 25: 2230-2232. Gonzalez, D., Tzinabos, A.O., Genco, C.A. and Gibson, F.C. 3rd (2003) Immunization with Porphyromonas gingivalis capsular polysaccharide prevents P. gingivalis-elicited oral bone loss in a murine model. Infect Immun 71: 2283-2287. Rajapakse, P.S., O'Brien-Simpson, N.M., Slakeski, N., Hoffmann, B. and Reynolds, E.C. (2002) Immunization with the RgpA-Kgp proteinase-adhesin complexes of Porphyromonas gingivalis protects against periodontal bone loss in the rat periodontitis model. Infect Immun 70: 2480-2486. Baker, P.J. (2005) Genetic control of the immune response in pathogenesis. J Periodontol 76: 2042-2046. Baker, P.J., Evans, R.T. and Roopenian, D.C. (1994) Oral infection with Porphyromonas gingivalis induces alveolar bone loss in immunocompetent and severe combined immunodeficient mice. Arch Oral Biol 39: 1035-1040. Washizu, M., Ishihara, K., Honma, K. and Okuda, K. (2003) Effects of a mixed infection with Porphyromonas gingivalis and Treponema denticola on abscess formation and immune responses in mice. Bull Tokyo Dent Coll 44: 141-147. Feuille, F., Ebersole, J.L., Kesavalu, L., Stepfen, M.J. and Holt, S.C. (1996) Mixed infection with Porphyromonas gingivalis and Fusobacterium nucleatum in a murine lesion model: potential synergistic effects on virulence. Infect Immun 64: 2094-2100. Kesavalu, L., Holt, S.C. and Ebersole, J.L. (1999) Lack of humoral immune protection against Treponema denticola virulence in a murine model. Infect Immun 67: 5736-5746. Tran, S.D., Rudney, J.D., Sparks, B.S. and Hodges, J.S. (2001) Persistent presence of Bacteroides forsythus as a risk factor for attachment loss in a population with low prevalence and severity of adult periodontitis. J Periodontol 72: 1-10. Byrne, S.J., Dashper, S.G., Darby, I.B., Adams, G.G., Hoffmann, B. and Reynolds, E.C. (2009) Progression of chronic periodontitis can be predicted by the levels of Porphyromonas gingivalis and Treponema denticola in subgingival plaque. Oral Microbiol Immunol 24: 469-477. Takeichi, O., Saito, I., Okamoto, Y., Tsurumachi, T. and Saito, T. (1998) Cytokine regulation on the synthesis of nitric oxide in vivo by chronically infected human polymorphonuclear leucocytes. Immunology 93: 275-280. Podwinska, J., Lusiak, M., Zaba, R. and Bowszyc, J. (2000) The pattern and level of cytokines secreted by Th1 and Th2 lymphocytes of syphilitic patients correlate to the progression of the disease. FEMS Immunol Med Microbiol 28: 1-14. Canale-Parola, E. (1977) Physiology and evolution of spirochetes. Bacteriol Rev 41: 181-204. Leschine, S.B. and Canale-Parola, E. (1980) Rifampin as a selective agent for isolation of oral spirochetes. J Clin Microbiol 12: 792-795. Frazer, L.T., O'Brien-Simpson, N.M., Slakeski, N. et al. (2006) Vaccination with recombinant adhesins from the RgpA-Kgp proteinase-adhesin complex protects against Porphyromonas gingivalis infection. Vaccine 24: 6542-6554. Takeuchi, Y., Umeda, M., Sakamoto, M., Benno, Y., Huang, Y. and Ishikawa, I. (2001) Treponema socranskii, Treponema denticola, and Porphyromonas gingivalis are associated with severity of periodontal tissue destruction. J Periodontol 72: 1354-1363. Loesche, W.J. (1988) The role of spirochetes in periodontal disease. Adv Dent Res 2: 275-283. Kesavalu, L., Holt, S.C. and Ebersole, J.L. (1998) Virulence of a polymicrobic complex, Treponema denticola and Porphyromonas gingivalis, in a murine model. Oral Microbiol Immunol 13: 373-377. Zubery, Y., Dunstan, C.R., Story, B.M. et al. (1998) Bone resorption caused by three periodontal pathogens in vivo in mice is mediated in part by prostaglandin. Infect Immun 66: 4158-4162. Shapira, L., Van Dyke, T.E. and Hart, T.C. (1992) A localized absence of interleukin-4 triggers periodontal disease activity: a novel hypothesis. Med Hypotheses 39: 319-322. Chan, E.C. and McLaughlin, R. (2000) Taxonomy and virulence of oral spirochetes. Oral Microbiol Immunol 15: 1-9. Chen, T., Abbey, K., Deng, W.J. and Cheng, M.C. (2005) The bioinformatics resource for oral pathogens. Nucleic Acids Res 33 (Web Server issue): W734-W740. O'Brien-Simpson, N.M., Veith, P.D., Dashper, S. and Reynolds, E. (2003) Porphyromonas gingivalis gingipains: the molecular teeth of a microbial vampire. Curr Protein Pept Sci 4: 409-426. Chan, E.C., Siboo, R., Touyz, L.Z., Qui, Y.S. and Klitorinos, A. (1993) A successful method for quantifying viable oral anaerobic spirochetes. Oral Microbiol Immunol 8: 80-83. Veith, P.D., Dashper, S.G., O'Brien-Simpson, N.M. et al. (2009) Major proteins and antigens of Treponema denticola. Biochim Biophys Acta 1794: 1421-1432. Baker, P.J., Dixon, M., Evans, R.T., Dufour, L., Johnson, E. and Roopenian, D.C. (1999) CD4+ T cells and the proinflammatory cytokines gamma interferon and interleukin-6 contribute to alveolar bone loss in mice. Infect Immun 67: 2804-2809. Lamont, R.J. and Jenkinson, H.F. (1998) Life below the gum line: pathogenic mechanisms of Porphyromonas gingivalis. Microbiol Mol Biol Rev 62: 1244-1263. Orth, R.K.H., O'Brien-Simpson, N.M., Dashper, S.G., 1993; 8 2000b; 68 2005; 175 2009; 80 2007; 75 2000; 15 2006; 24 2007; 170 2003; 4 2005; 76 2001; 16 2000a; 68 1994; 39 1998; 93 2005; 33 1992; 2 1996; 64 1996; 20 2009; 1794 2003; 44 1998; 13 2009; 24 2001; 72 2000; 28 1997; 65 2010a; 16 1994; 153 2006; 152 1992; 39 1999; 67 1977; 41 1993 2003; 71 1998; 62 2001; 69 1998; 66 1998; 25 1991; 6 1988; 2 2008; 181 2009; 77 1987; 25 2000; 79 2010b; 2010 1980; 12 1999; 37 2002; 70 1998; 6 2001; 36 1992; 60 1998; 33 1990; 5 e_1_2_6_51_1 e_1_2_6_53_1 e_1_2_6_32_1 e_1_2_6_30_1 e_1_2_6_19_1 e_1_2_6_13_1 e_1_2_6_36_1 e_1_2_6_11_1 e_1_2_6_17_1 e_1_2_6_55_1 Tanner A. (e_1_2_6_47_1) 1992; 2 e_1_2_6_15_1 e_1_2_6_38_1 e_1_2_6_57_1 e_1_2_6_43_1 e_1_2_6_41_1 Lundqvist C. (e_1_2_6_29_1) 1994; 153 e_1_2_6_9_1 e_1_2_6_5_1 e_1_2_6_7_1 e_1_2_6_24_1 e_1_2_6_3_1 e_1_2_6_28_1 e_1_2_6_45_1 e_1_2_6_26_1 e_1_2_6_52_1 e_1_2_6_54_1 e_1_2_6_10_1 e_1_2_6_31_1 Tran S.D. (e_1_2_6_49_1) 2000; 79 e_1_2_6_50_1 Kesavalu L. (e_1_2_6_20_1) 1997; 65 Kesavalu L. (e_1_2_6_22_1) 1999; 67 e_1_2_6_14_1 e_1_2_6_35_1 e_1_2_6_12_1 e_1_2_6_33_1 e_1_2_6_18_1 e_1_2_6_39_1 e_1_2_6_56_1 e_1_2_6_16_1 e_1_2_6_37_1 e_1_2_6_42_1 e_1_2_6_21_1 e_1_2_6_40_1 e_1_2_6_8_1 e_1_2_6_4_1 e_1_2_6_6_1 e_1_2_6_25_1 e_1_2_6_48_1 e_1_2_6_23_1 e_1_2_6_2_1 e_1_2_6_44_1 O’Brien‐Simpson N.M. (e_1_2_6_34_1) 2003; 4 e_1_2_6_27_1 e_1_2_6_46_1 |
| References_xml | – reference: Tanner, A. (1992) Microbial etiology of periodontal diseases. Where are we? Where are we going? Curr Opin Dent 2: 12-24. – reference: Choi, J., Borrello, M.A., Smith, E., Cutler, C.W., Sojar, H. and Zauderer, M. (2001) Prior exposure of mice to Fusobacterium nucleatum modulates host response to Porphyromonas gingivalis. Oral Microbiol Immunol 16: 338-344. – reference: Evans, R.T., Klausen, B., Sojar, H.T. et al. (1992) Immunization with Porphyromonas (Bacteroides) gingivalis fimbriae protects against periodontal destruction. Infect Immun 60: 2926-2935. – reference: Klausen, B., Evans, R.T., Ramamurthy, N.S. et al. (1991) Periodontal bone level and gingival proteinase activity on gnobiotic rats immunized with Bacteroides gingivalis. Oral Microbiol Immunol 6: 193-201. – reference: O'Brien-Simpson, N.M., Pathirana, R.D., Paolini, R.A. et al. (2005) An immune response directed to proteinase and adhesin functional epitopes protects against Porphyromonas gingivalis-induced periodontal bone loss. J Immunol 175: 3980-3989. – reference: Tam, V., O'Brien-Simpson, N.M., Pathirana, R.D., Frazer, L.T. and Reynolds, E.C. (2008) Characterization of T cell responses to the RgpA-Kgp proteinase-adhesin complexes of Porphyromonas gingivalis in BALB/c mice. J Immunol 181: 4150-4158. – reference: Chen, T., Abbey, K., Deng, W.J. and Cheng, M.C. (2005) The bioinformatics resource for oral pathogens. Nucleic Acids Res 33 (Web Server issue): W734-W740. – reference: Yoneda, M., Hirofuji, T., Anan, H. et al. (2001) Mixed infection of Porphyromonas gingivalis and Bacteroides forsythus in a murine abscess model: involvement of gingipains in a synergistic effect. J Periodontal Res 36: 237-243. – reference: Byrne, S.J., Dashper, S.G., Darby, I.B., Adams, G.G., Hoffmann, B. and Reynolds, E.C. (2009) Progression of chronic periodontitis can be predicted by the levels of Porphyromonas gingivalis and Treponema denticola in subgingival plaque. Oral Microbiol Immunol 24: 469-477. – reference: O'Brien-Simpson, N.M., Veith, P.D., Dashper, S. and Reynolds, E. (2003) Porphyromonas gingivalis gingipains: the molecular teeth of a microbial vampire. Curr Protein Pept Sci 4: 409-426. – reference: Gonzalez, D., Tzinabos, A.O., Genco, C.A. and Gibson, F.C. 3rd (2003) Immunization with Porphyromonas gingivalis capsular polysaccharide prevents P. gingivalis-elicited oral bone loss in a murine model. Infect Immun 71: 2283-2287. – reference: Socransky, S.S., Haffajee, A.D., Cugini, M.A., Smith, C. and Kent, R.L. Jr (1998) Microbial complexes in subgingival plaque. J Clin Periodontol 25: 134-144. – reference: O'Brien-Simpson, N.M., Paolini, R.A., Hoffmann, B., Slakeski, N., Dashper, S.G. and Reynolds, E.C. (2001) Role of RgpA, RgpB, and Kgp proteinases in virulence of Porphyromonas gingivalis W50 in a murine lesion model. Infect Immun 69: 7527-7534. – reference: Haffajee, A.D., Cugini, M.A., Tanner, A. et al. (1998) Subgingival microbiota in healthy, well-maintained elder and periodontitis subjects. J Clin Periodontol 25: 346-353. – reference: Zubery, Y., Dunstan, C.R., Story, B.M. et al. (1998) Bone resorption caused by three periodontal pathogens in vivo in mice is mediated in part by prostaglandin. Infect Immun 66: 4158-4162. – reference: Kesavalu, L., Holt, S.C. and Ebersole, J.L. (1999) Lack of humoral immune protection against Treponema denticola virulence in a murine model. Infect Immun 67: 5736-5746. – reference: Baker, P.J., Dixon, M., Evans, R.T., Dufour, L., Johnson, E. and Roopenian, D.C. (1999) CD4+ T cells and the proinflammatory cytokines gamma interferon and interleukin-6 contribute to alveolar bone loss in mice. Infect Immun 67: 2804-2809. – reference: Loesche, W.J. (1988) The role of spirochetes in periodontal disease. Adv Dent Res 2: 275-283. – reference: Umeda, M., Ishikawa, I., Benno, Y. and Mitsuoka, T. (1990) Improved detection of oral spirochetes with an anaerobic culture method. Oral Microbiol Immunol 5: 90-94. – reference: Frazer, L.T., O'Brien-Simpson, N.M., Slakeski, N. et al. (2006) Vaccination with recombinant adhesins from the RgpA-Kgp proteinase-adhesin complex protects against Porphyromonas gingivalis infection. Vaccine 24: 6542-6554. – reference: Kesavalu, L., Holt, S.C. and Ebersole, J.L. (1998) Virulence of a polymicrobic complex, Treponema denticola and Porphyromonas gingivalis, in a murine model. Oral Microbiol Immunol 13: 373-377. – reference: Lundqvist, C., Baranov, V., Teglund, S., Hammarstrom, S. and Hammarstrom, M. (1994) Cytokine profile and ultrastructure of intraepithelial gd T cells in chronically inflamed human gingiva suggest a cytotoxis effector function. J Immunol 153: 2302-2312. – reference: Canale-Parola, E. (1977) Physiology and evolution of spirochetes. Bacteriol Rev 41: 181-204. – reference: Orth, R.K.H., O'Brien-Simpson, N.M., Dashper, S.G., Walsh, K.A. and Reynolds, E.C. (2009) An efficient method for enumerating oral spirochetes using flow cytometry. J Microbiol Methods 80: 123-128. – reference: Lamont, R.J. and Jenkinson, H.F. (1998) Life below the gum line: pathogenic mechanisms of Porphyromonas gingivalis. Microbiol Mol Biol Rev 62: 1244-1263. – reference: Salvador, S.L., Syed, S.A. and Loesche, W.J. (1987) Comparison of three dispersion procedures for quantitative recovery of cultivable species of subgingival spirochetes. J Clin Microbiol 25: 2230-2232. – reference: Tran, S.D., Rudney, J.D., Sparks, B.S. and Hodges, J.S. (2000) Attachment level loss associated with persistent presence of Bacteroides forsythus. J Dent Res 79: 217. – reference: Verma, R.K., Bhattacharyya, I., Sevilla, A. et al. (2010a) Virulence of major periodontal pathogens and lack of humoral immune protection in a rat model of periodontal disease. Oral Dis 16: 686-695. – reference: Kesavalu, L., Holt, S.C. and Ebersole, J.L. (1996) Trypsin-like protease activity of Porphyromonas gingivalis as a potential virulence factor in a murine lesion model. Microb Pathog 20: 1-10. – reference: Verma, R.K., Rajapakse, S., Meka, A. et al. (2010b) Porphyromonas gingivalis and Treponema denticola mixed microbial infection in a rat model of periodontal disease. Interdiscip Perspect Infect Dis 2010: 605125. – reference: O'Brien-Simpson, N.M., Paolini, R.A. and Reynolds, E.C. (2000b) RgpA-Kgp peptide-based immunogens provide protection against Porphyromonas gingivalis challenge in a murine lesion model. Infect Immun 68: 4055-4063. – reference: Takeichi, O., Saito, I., Okamoto, Y., Tsurumachi, T. and Saito, T. (1998) Cytokine regulation on the synthesis of nitric oxide in vivo by chronically infected human polymorphonuclear leucocytes. Immunology 93: 275-280. – reference: O'Brien-Simpson, N.M., Black, C.L., Bhogal, P.S. et al. (2000a) Serum immunoglobulin G (IgG) and IgG subclass responses to the RgpA-Kgp proteinase-adhesin complex of Porphyromonas gingivalis in adult periodontitis. Infect Immun 68: 2704-2712. – reference: Genco, C.A., Van Dyke, T. and Amar, S. (1998) Animal models for Porphyromonas gingivalis-mediated periodontal disease. Trends Microbiol 6: 444-449. – reference: Takeuchi, Y., Umeda, M., Sakamoto, M., Benno, Y., Huang, Y. and Ishikawa, I. (2001) Treponema socranskii, Treponema denticola, and Porphyromonas gingivalis are associated with severity of periodontal tissue destruction. J Periodontol 72: 1354-1363. – reference: Feuille, F., Ebersole, J.L., Kesavalu, L., Stepfen, M.J. and Holt, S.C. (1996) Mixed infection with Porphyromonas gingivalis and Fusobacterium nucleatum in a murine lesion model: potential synergistic effects on virulence. Infect Immun 64: 2094-2100. – reference: Kesavalu, L., Walker, S.G., Holt, S.C., Crawley, R.R. and Ebersole, J.L. (1997) Virulence characteristics of oral treponemes in a murine model. Infect Immun 65: 5096-5102. – reference: Podwinska, J., Lusiak, M., Zaba, R. and Bowszyc, J. (2000) The pattern and level of cytokines secreted by Th1 and Th2 lymphocytes of syphilitic patients correlate to the progression of the disease. FEMS Immunol Med Microbiol 28: 1-14. – reference: Chan, E.C. and McLaughlin, R. (2000) Taxonomy and virulence of oral spirochetes. Oral Microbiol Immunol 15: 1-9. – reference: Tran, S.D. and Rudney, J.D. (1999) Improved multiplex PCR using conserved and species-specific 16S rRNA gene primers for simultaneous detection of Actinobacillus actinomycetemcomitans, Bacteroides forsythus, and Porphyromonas gingivalis. J Clin Microbiol 37: 3504-3508. – reference: Garcia, L., Tercero, J.C., Legido, B., Ramos, J.A., Alemany, J. and Sanz, M. (1998) Rapid detection of Actinobacillus actinomycetemcomitans, Prevotella intermedia and Porphyromona gingivalis by multiplex PCR. J Periodontal Res 33: 59-64. – reference: Rajapakse, P.S., O'Brien-Simpson, N.M., Slakeski, N., Hoffmann, B. and Reynolds, E.C. (2002) Immunization with the RgpA-Kgp proteinase-adhesin complexes of Porphyromonas gingivalis protects against periodontal bone loss in the rat periodontitis model. Infect Immun 70: 2480-2486. – reference: Kesavalu, L., Sathishkumar, S., Bakthavatchalu, V. et al. (2007) Rat model of polymicrobial infection, immunity, and alveolar bone resorption in periodontal disease. Infect Immun 75: 1704-1712. – reference: Pathirana, R.D., O'Brien-Simpson, N.M., Veith, P.D., Riley, P.F. and Reynolds, E.C. (2006) Characterization of proteinase-adhesin complexes of Porphyromonas gingivalis. Microbiology 152: 2381-2394. – reference: Veith, P.D., Dashper, S.G., O'Brien-Simpson, N.M. et al. (2009) Major proteins and antigens of Treponema denticola. Biochim Biophys Acta 1794: 1421-1432. – reference: Chan, E.C., Siboo, R., Touyz, L.Z., Qui, Y.S. and Klitorinos, A. (1993) A successful method for quantifying viable oral anaerobic spirochetes. Oral Microbiol Immunol 8: 80-83. – reference: Washizu, M., Ishihara, K., Honma, K. and Okuda, K. (2003) Effects of a mixed infection with Porphyromonas gingivalis and Treponema denticola on abscess formation and immune responses in mice. Bull Tokyo Dent Coll 44: 141-147. – reference: Arroll, T.W., Centurion-Lara, A., Lukehart, S.A. and Van Voorhis, W.C. (1999) T-cell responses to Treponema pallidum subsp. pallidum antigens during the course of experimental syphilis infection. Infect Immun 67: 4757-4763. – reference: Shapira, L., Van Dyke, T.E. and Hart, T.C. (1992) A localized absence of interleukin-4 triggers periodontal disease activity: a novel hypothesis. Med Hypotheses 39: 319-322. – reference: Lee, S.F., Andrian, E., Rowland, E. and Marquez, I.C. (2009) Immune response and alveolar bone resorption in a mouse model of Treponema denticola infection. Infect Immun 77: 694-698. – reference: Leschine, S.B. and Canale-Parola, E. (1980) Rifampin as a selective agent for isolation of oral spirochetes. J Clin Microbiol 12: 792-795. – reference: Stashenko, P., Goncalves, R.B., Lipkin, B., Ficarelli, A., Sasaki, H. and Campos-Neto, A. (2007) Th1 immune response promotes severe bone resorption caused by Porphyromonas gingivalis. Am J Pathol 170: 203-213. – reference: Baker, P.J., Evans, R.T. and Roopenian, D.C. (1994) Oral infection with Porphyromonas gingivalis induces alveolar bone loss in immunocompetent and severe combined immunodeficient mice. Arch Oral Biol 39: 1035-1040. – reference: Tran, S.D., Rudney, J.D., Sparks, B.S. and Hodges, J.S. 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Chronic periodontitis is characterized by the destruction of the tissues supporting the teeth and has been associated with the presence of a... Chronic periodontitis is characterized by the destruction of the tissues supporting the teeth and has been associated with the presence of a subgingival... |
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| SubjectTerms | alveolar bone loss Alveolar Bone Loss - microbiology animal model Animal models Animals Biofilms Bone (alveolar) Bone loss chronic periodontitis Chronic Periodontitis - immunology Chronic Periodontitis - microbiology Cytokines Data processing Disease Models, Animal DNA, Bacterial - analysis gamma -Interferon Immune response Inoculation Interferon-gamma - biosynthesis Interleukin-4 - biosynthesis Leukocyte Count Lymphocytes T Mice Mice, Inbred BALB C Microbial Interactions - physiology Periodontitis Porphyromonas Porphyromonas gingivalis Porphyromonas gingivalis - immunology T-Lymphocytes - immunology Teeth Treponema Treponema denticola Treponema denticola - immunology Virulence |
| Title | Synergistic virulence of Porphyromonas gingivalis and Treponema denticola in a murine periodontitis model |
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