Abstract
The purpose of this study was to examine whether Bacteroides (Porphyromonas) gingivalis fimbriae, an important structure involved in attachment of the bacteria to periodontal tissues, activate macrophages and subsequently induce gene expression and production of interleukin-1 (IL-1) in the cells. The fimbriae increased glucose consumption and lysozyme activity in BALB/c macrophages, both criteria of macrophage activation of peritoneal macrophages, in a dose-dependent fashion. A marked increase in the mRNA level of the c-myc gene, an oncogene, in the cells was observed after a 1-h treatment with the fimbriae, and the level decreased rapidly after 3 h. The fimbriae (4 micrograms of protein per ml) markedly induced IL-1 alpha and IL-1 beta gene expression in the cells and IL-1 production. The expression of IL-1 alpha and IL-1 beta genes measured in terms of specific mRNA increased 1 h after the start of treatment and peaked at 6 h. Such increased expression of IL-1 beta was also observed in C3H/HeJ mice, a lipopolysaccharide low-responder strain. The fimbriae stimulated transcriptional activity of IL-1 beta in the cells, but not that of IL-1 alpha. We also observed that fimbriae-induced IL-1 gene expression was not regulated by endogenous prostaglandin triggered by the fimbriae. Therefore, these observations suggest that B. gingivalis fimbriae may be involved in the pathogenesis of adult periodontal disease via triggering of IL-1 production by monocytes/macrophages in periodontal diseases.
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Selected References
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- Bartold P. M. The effect of interleukin 1 beta on proteoglycans synthesized by human gingival fibroblasts in vitro. Connect Tissue Res. 1988;17(4):287–304. doi: 10.3109/03008208809017479. [DOI] [PubMed] [Google Scholar]
- Beresford J. N., Gallagher J. A., Gowen M., Couch M., Poser J., Wood D. D., Russell R. G. The effects of monocyte-conditioned medium and interleukin 1 on the synthesis of collagenous and non-collagenous proteins by mouse bone and human bone cells in vitro. Biochim Biophys Acta. 1984 Sep 7;801(1):58–65. doi: 10.1016/0304-4165(84)90212-5. [DOI] [PubMed] [Google Scholar]
- Bom-van Noorloos A. A., van Steenbergen T. J., Burger E. H. Direct and immune-cell-mediated effects of Bacteroides gingivalis on bone metabolism in vitro. J Clin Periodontol. 1989 Aug;16(7):412–418. doi: 10.1111/j.1600-051x.1989.tb01669.x. [DOI] [PubMed] [Google Scholar]
- Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
- Canalis E. Interleukin-1 has independent effects on deoxyribonucleic acid and collagen synthesis in cultures of rat calvariae. Endocrinology. 1986 Jan;118(1):74–81. doi: 10.1210/endo-118-1-74. [DOI] [PubMed] [Google Scholar]
- Charon J. A., Luger T. A., Mergenhagen S. E., Oppenheim J. J. Increased thymocyte-activating factor in human gingival fluid during gingival inflammation. Infect Immun. 1982 Dec;38(3):1190–1195. doi: 10.1128/iai.38.3.1190-1195.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dinarello C. A. Interleukin-1 and its biologically related cytokines. Adv Immunol. 1989;44:153–205. doi: 10.1016/s0065-2776(08)60642-2. [DOI] [PubMed] [Google Scholar]
- Gowen M., Wood D. D., Ihrie E. J., McGuire M. K., Russell R. G. An interleukin 1 like factor stimulates bone resorption in vitro. Nature. 1983 Nov 24;306(5941):378–380. doi: 10.1038/306378a0. [DOI] [PubMed] [Google Scholar]
- Gowen M., Wood D. D., Russell R. G. Stimulation of the proliferation of human bone cells in vitro by human monocyte products with interleukin-1 activity. J Clin Invest. 1985 Apr;75(4):1223–1229. doi: 10.1172/JCI111819. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Groudine M., Peretz M., Weintraub H. Transcriptional regulation of hemoglobin switching in chicken embryos. Mol Cell Biol. 1981 Mar;1(3):281–288. doi: 10.1128/mcb.1.3.281. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hanazawa S., Amano S., Hamano A., Katoh H., Honda T., Takada M., Hirose S., Kitano S. An Epstein-Barr virus-transformed B cell line produces autoregulatory interleukin-1 that regulates bone remodeling. Biochim Biophys Acta. 1989 Jun 15;1012(1):57–63. doi: 10.1016/0167-4889(89)90010-4. [DOI] [PubMed] [Google Scholar]
- Hanazawa S., Hirose K., Ohmori Y., Amano S., Kitano S. Bacteroides gingivalis fimbriae stimulate production of thymocyte-activating factor by human gingival fibroblasts. Infect Immun. 1988 Jan;56(1):272–274. doi: 10.1128/iai.56.1.272-274.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hanazawa S., Nakada K., Ohmori Y., Miyoshi T., Amano S., Kitano S. Functional role of interleukin 1 in periodontal disease: induction of interleukin 1 production by Bacteroides gingivalis lipopolysaccharide in peritoneal macrophages from C3H/HeN and C3H/HeJ mice. Infect Immun. 1985 Oct;50(1):262–270. doi: 10.1128/iai.50.1.262-270.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hanazawa S., Ohmori Y., Amano S., Hirose K., Miyoshi T., Kumegawa M., Kitano S. Human purified interleukin-1 inhibits DNA synthesis and cell growth of osteoblastic cell line (MC3T3-E1), but enhances alkaline phosphatase activity in the cells. FEBS Lett. 1986 Jul 28;203(2):279–284. doi: 10.1016/0014-5793(86)80758-x. [DOI] [PubMed] [Google Scholar]
- Hanazawa S., Tanaka S., Kin M., Amano S., Nakada K., Masuda T., Kitano S. Application of monoclonal antibodies to the detection of black-pigmented Bacteroides spp. in subgingival plaques by immunoslot blot assay. J Clin Microbiol. 1990 Oct;28(10):2248–2252. doi: 10.1128/jcm.28.10.2248-2252.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hönig J., Rordorf-Adam C., Siegmund C., Wiedemann W., Erard F. Increased interleukin-1 beta (IL-1 beta) concentration in gingival tissue from periodontitis patients. J Periodontal Res. 1989 Nov;24(6):362–367. doi: 10.1111/j.1600-0765.1989.tb00883.x. [DOI] [PubMed] [Google Scholar]
- Introna M., Hamilton T. A., Kaufman R. E., Adams D. O., Bast R. C., Jr Treatment of murine peritoneal macrophages with bacterial lipopolysaccharide alters expression of c-fos and c-myc oncogenes. J Immunol. 1986 Oct 15;137(8):2711–2715. [PubMed] [Google Scholar]
- Koga T., Nishihara T., Fujiwara T., Nisizawa T., Okahashi N., Noguchi T., Hamada S. Biochemical and immunobiological properties of lipopolysaccharide (LPS) from Bacteroides gingivalis and comparison with LPS from Escherichia coli. Infect Immun. 1985 Mar;47(3):638–647. doi: 10.1128/iai.47.3.638-647.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Krakauer T., Oppenheim J. J., Jasin H. E. Human interleukin 1 mediates cartilage matrix degradation. Cell Immunol. 1985 Mar;91(1):92–99. doi: 10.1016/0008-8749(85)90034-6. [DOI] [PubMed] [Google Scholar]
- Lindemann R. A., Economou J. S., Rothermel H. Production of interleukin-1 and tumor necrosis factor by human peripheral monocytes activated by periodontal bacteria and extracted lipopolysaccharides. J Dent Res. 1988 Aug;67(8):1131–1135. doi: 10.1177/00220345880670081401. [DOI] [PubMed] [Google Scholar]
- Lomedico P. T., Gubler U., Hellmann C. P., Dukovich M., Giri J. G., Pan Y. C., Collier K., Semionow R., Chua A. O., Mizel S. B. Cloning and expression of murine interleukin-1 cDNA in Escherichia coli. 1984 Nov 29-Dec 5Nature. 312(5993):458–462. doi: 10.1038/312458a0. [DOI] [PubMed] [Google Scholar]
- Lorenzo J. A., Sousa S. L., Centrella M. Interleukin-1 in combination with transforming growth factor-alpha produces enhanced bone resorption in vitro. Endocrinology. 1988 Nov;123(5):2194–2200. doi: 10.1210/endo-123-5-2194. [DOI] [PubMed] [Google Scholar]
- Meikle M. C., Heath J. K., Reynolds J. J. Advances in understanding cell interactions in tissue resorption. Relevance to the pathogenesis of periodontal diseases and a new hypothesis. J Oral Pathol. 1986 May;15(5):239–250. doi: 10.1111/j.1600-0714.1986.tb00616.x. [DOI] [PubMed] [Google Scholar]
- Miyoshi T., Hanazawa S., Hirose K., Saitoh K., Amano S., Ohmori Y., Kitano S. Humoral antibody response against Bacteroides gingivalis-specific antigen recognized by monoclonal antibody in adult periodontal patients. Infect Immun. 1986 Aug;53(2):366–371. doi: 10.1128/iai.53.2.366-371.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mouton C., Hammond P. G., Slots J., Genco R. J. Serum antibodies to oral Bacteroides asaccharolyticus (Bacteroides gingivalis): relationship to age and periondontal disease. Infect Immun. 1981 Jan;31(1):182–192. doi: 10.1128/iai.31.1.182-192.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ohmori Y., Hanazawa S., Amano S., Hirose K., Kumegawa M., Kitano S. Effects of recombinant human interleukin 1 alpha and interleukin 1 beta on cell growth and alkaline phosphatase of the mouse osteoblastic cell line MC3T3-E1. Biochim Biophys Acta. 1988 Jun 8;970(1):22–30. doi: 10.1016/0167-4889(88)90218-2. [DOI] [PubMed] [Google Scholar]
- Ohmori Y., Hanazawa S., Amano S., Miyoshi T., Hirose K., Kitano S. Spontaneous production of thymocyte-activating factor by human gingival fibroblasts and its autoregulatory effect on their proliferation. Infect Immun. 1987 Apr;55(4):947–954. doi: 10.1128/iai.55.4.947-954.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sinden P. R., Walker D. M. Inflammatory cells extracted from chronically inflamed gingiva. J Periodontal Res. 1979 Nov;14(6):467–474. doi: 10.1111/j.1600-0765.1979.tb00246.x. [DOI] [PubMed] [Google Scholar]
- Tannenbaum C. S., Hamilton T. A. Lipopolysaccharide-induced gene expression in murine peritoneal macrophages is selectively suppressed by agents that elevate intracellular cAMP. J Immunol. 1989 Feb 15;142(4):1274–1280. [PubMed] [Google Scholar]
- Walsh L. J., Stritzel F., Yamazaki K., Bird P. S., Gemmell E., Seymour G. J. Interleukin-1 and interleukin-1 inhibitor production by human adherent cells stimulated with periodontopathic bacteria. Arch Oral Biol. 1989;34(9):679–683. doi: 10.1016/0003-9969(89)90073-3. [DOI] [PubMed] [Google Scholar]
- Yoshimura F., Takahashi K., Nodasaka Y., Suzuki T. Purification and characterization of a novel type of fimbriae from the oral anaerobe Bacteroides gingivalis. J Bacteriol. 1984 Dec;160(3):949–957. doi: 10.1128/jb.160.3.949-957.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yoshimura F., Takasawa T., Yoneyama M., Yamaguchi T., Shiokawa H., Suzuki T. Fimbriae from the oral anaerobe Bacteroides gingivalis: physical, chemical, and immunological properties. J Bacteriol. 1985 Aug;163(2):730–734. doi: 10.1128/jb.163.2.730-734.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]