Tannerella forsythia (formerly Bacteroides forsythus) is one of the periodontal pathogens recently implicated in the development of periodontal disease. The cell-surface-associated, as well as the secreted, leucine-rich-repeat protein (BspA) of this bacterium have been suggested to play roles in bacterial adherence, and also in inflammation, by triggering release of pro-inflammatory cytokines from monocytes and chemokines from osteoblasts, leading to inflammation and bone resorption. In this study, we sought to determine the pathogenic potential of T. forsythia and the in vivo role of the BspA protein in pathogenesis in the mouse model of infection-induced alveolar bone loss. The results showed alveolar bone loss in mice infected with the T. forsythia wild-type strain, whereas the BspA mutant was impaired. In conclusion, evidence is presented in support of T. forsythia as an important organism involved in inducing alveolar bone loss, and the BspA protein is an important virulence factor of this bacterium.
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References
1.
Arakawa S, Nakajima T, Ishikura H, Ichinose S, Ishikawa I, Tsuchida N -2000-. Novel apoptosis-inducing activity in Bacteroides forsythus: a comparative study with three serotypes of Actinobacillus actinomycetemcomitans. Infect Immun68:4611–4615.
2.
Baker PJ, Evans RT, Roopenian DC -1994-. Oral infection with Porphyromonas gingivalis and induced alveolar bone loss in immunocompetent and severe combined immunodeficient mice. Arch Oral Biol39:1035–1040.
3.
Bird PS, Shakibaie F, Gemmell E, Polak B, Seymour GJ -2001-. Immune response to Bacteroides forsythus in a murine model. Oral Microbiol Immunol16:311–315.
4.
Braham PH, Moncla BJ -1992-. Rapid presumptive identification and further characterization of Bacteroides forsythus. J Clin Microbiol30:649–654.
5.
Evans RT, Klausen B, Sojar HT, Bedi GS, Sfintescu C, Ramamurthy NS, et al. -1992-. Immunization with Porphyromonas -Bacteroides- gingivalis fimbriae protects against periodontal destruction. Infect Immun60:2926–2935.
6.
Grossi SG, Zambon JJ, Ho AW, Koch G, Dunford RG, Machtei EE, et al. -1994-. Assessment of risk for periodontal disease. I. Risk indicators for attachment loss. J Periodontol65:260–267.
7.
Grossi SG, Genco RJ, Machtei EE, Ho AW, Koch G, Dunford R, et al. -1995-. Assessment of risk for periodontal disease. II. Risk indicators for alveolar bone loss. J Periodontol66:23–29.
8.
Hajishengallis G, Martin M, Sojar HT, Sharma A, Schifferle RE, DeNardin E, et al. -2002-. Dependence of bacterial protein adhesins on toll-like receptors for proinflammatory cytokine induction. Clin Diagn Lab Immunol9:403–411.
9.
Honma K, Kuramitsu HK, Genco RJ, Sharma A -2001-. Development of a gene inactivation system for Bacteroides forsythus: construction and characterization of a BspA mutant. Infect Immun69:4686–4690.
10.
Hughes CV, Malki G, Loo CY, Tanner AC, Ganeshkumar N -2003-. Cloning and expression of alpha-D-glucosidase and N-acetyl-beta-glucosaminidase from the periodontal pathogen, Tannerella forsythensis -Bacteroides forsythus-. Oral Microbiol Immunol18:309–312.
11.
Ishikura H, Arakawa S, Nakajima T, Tsuchida N, Ishikawa I -2003-. Cloning of the Tannerella forsythensis -Bacteroides forsythus- siaHI gene and purification of the sialidase enzyme. J Med Microbiol52:1101–1107.
12.
Kruisbeek AM -1998-. Isolation of mouse mononuclear cell populations. New York: John Wiley & Sons.
13.
Maiden MF, Pham C, Kashket S -2004-. Glucose toxicity effect and accumulation of methylgloxal by the periodontal pathogen Bacteroides forsythus. Anaerobe10:27–32.
14.
Marchesi JR, Sato T, Weightman AJ, Martin TA, Fry JC, Hiom SJ, et al. -1998-. Design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA. Appl Environ Microbiol64:795–799; erratum 64:2333.
15.
Murakami Y, Higuchi N, Nakamura H, Yoshimura F, Oppenheim FG -2002-. Bacteroides forsythus hemagglutinin is inhibited by N-acetylneuraminyllactose. Oral Microbiol Immunol17:125–128.
16.
Ruddy MJ, Shen F, Smith JB, Sharma A, Gaffen SL -2004-. Interleukin-17 regulates expression of the CXC chemokine LIX/CXCL5 in osteoblasts: implications for inflammation and neutrophil recruitment. J Leukoc Biol76:135–144.
17.
Sabet M, Lee SW, Nauman RK, Sims T, Um HS -2003-. The surface -S-- layer is a virulence factor of Bacteroides forsythus. Microbiology149:3617–3627.
18.
Saito T, Ishihara K, Kato T, Okuda K -1997-. Cloning, expression, and sequencing of a protease gene from Bacteroides forsythus ATCC 43037 in Escherichia coli. Infect Immun65:4888–4891.
19.
Sakamoto M, Takeuchi Y, Umeda M, Ishikawa I, Benno Y -2001-. Rapid detection and quantification of five periodontopathic bacteria by real-time PCR. Microbiol Immunol45:39–44.
20.
Sharma A, Sojar HT, Glurich I, Honma K, Kuramitsu HK, Genco RJ -1998-. Cloning, expression, and sequencing of a cell surface antigen containing a leucine-rich repeat motif from Bacteroides forsythus ATCC 43037. Infect Immun66:5703–5710.
21.
Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RL Jr -1998-. Microbial complexes in subgingival plaque. J Clin Periodontol25:134–144.
22.
Takemoto T, Kurihara H, Dahlén G -1997-. Characterization of Bacteroides forsythus isolates. J Clin Microbiol35:1378–1381.
23.
Tanner A, Maiden MF, Macuch PJ, Murray LL, Kent RL Jr -1998-. Microbiota of health, gingivitis, and initial periodontitis. J Clin Periodontol25:85–98.
24.
Yoneda M, Hirofuji T, Anan H, Matsumoto A, Hamachi T, Nakayama K, 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 Res36:237–243.
