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. 1985 Oct;50(1):262–270. doi: 10.1128/iai.50.1.262-270.1985

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.

S Hanazawa, K Nakada, Y Ohmori, T Miyoshi, S Amano, S Kitano
PMCID: PMC262166  PMID: 3876285

Abstract

Hot phenol-water-extracted lipopolysaccharide (LPS) from Bacteroides gingivalis 381 was purified by Sephadex G-100 chromatography with Tris buffer supplemented with sodium deoxycholate and EDTA (B-LPS). In the present study, B-LPS was examined for its ability to induce interleukin 1 (IL-1) production, a mitogenic response, and macrophage activation in LPS high-responder C3H/HeN and low-responder C3H/HeJ mice. A significant increase in IL-1 production was observed in C3H/HeN and C3H/HeJ peritoneal macrophages treated with various doses (1.0 to 50 micrograms/ml) of B-LPS. IL-1 production by C3H/HeN macrophages treated with B-LPS (10 micrograms/ml) was about seven times greater than that by C3H/HeJ macrophages. However, the IL-1 production induced by B-LPS (10 micrograms/ml) in C3H/HeN macrophages was four times lower compared with that induced by Escherichia coli O111 B4 LPS. Also, a significant increase in IL-1 production was found in human monocytes stimulated with B-LPS. That B-LPS-induced IL-1 exhibits some molecular weight heterogeneity was indicated from Sephadex G-75 gel filtration profiles. A significant, high mitogenic response by whole spleen cells with 1 X 10(5) to 5 X 10(4) cells of either mouse strain per well treated with B-LPS (10 to 50 micrograms/ml) was observed. However, the response of C3H/HeJ mice was less than that of the C3H/HeN strain. Also, glucose consumption assays indicated that enhanced macrophage activation occurred in C3H/HeN but not in C3H/HeJ mice treated with B-LPS. In light of recent studies showing that IL-1 stimulates bone resorption in a mouse calvaria system and collagenase production in fibroblasts, we suggest that B-LPS-induced IL-1 may play a significant role in the pathogenesis of adult periodontal disease.

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Selected References

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  1. 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]
  2. 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]
  3. 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]
  4. 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]
  5. Hanazawa S., Kato H., Yamaura K., Yamaguchi Y. Kinetics and mechanisms of macrophage activation by Corynebacterium anaerobium. Microbiol Immunol. 1978;22(3):155–166. doi: 10.1111/j.1348-0421.1978.tb00359.x. [DOI] [PubMed] [Google Scholar]
  6. Hausmann E., Raisz L. G., Miller W. A. Endotoxin: stimulation of bone resorption in tissue culture. Science. 1970 May 15;168(3933):862–864. doi: 10.1126/science.168.3933.862. [DOI] [PubMed] [Google Scholar]
  7. Hausmann E., Weinfeld N., Miller W. A. Effects of lipopolysaccharides on bone resorption in tissue culture. Calcif Tissue Res. 1972;9(4):272–282. doi: 10.1007/BF02061967. [DOI] [PubMed] [Google Scholar]
  8. Iino Y., Hopps R. M. The bone-resorbing activities in tissue culture of lipopolysaccharides from the bacteria Actinobacillus actinomycetemcomitans, Bacteroides gingivalis and Capnocytophaga ochracea isolated from human mouths. Arch Oral Biol. 1984;29(1):59–63. doi: 10.1016/0003-9969(84)90043-8. [DOI] [PubMed] [Google Scholar]
  9. Karkhanis Y. D., Zeltner J. Y., Jackson J. J., Carlo D. J. A new and improved microassay to determine 2-keto-3-deoxyoctonate in lipopolysaccharide of Gram-negative bacteria. Anal Biochem. 1978 Apr;85(2):595–601. doi: 10.1016/0003-2697(78)90260-9. [DOI] [PubMed] [Google Scholar]
  10. Kasper D. L. Chemical and biological characterization of the lipopolysaccharide of Bacteroides fragilis subspecies fragilis. J Infect Dis. 1976 Jul;134(1):59–66. doi: 10.1093/infdis/134.1.59. [DOI] [PubMed] [Google Scholar]
  11. Mansheim B. J., Onderdonk A. B., Kasper D. L. Immunochemical and biologic studies of the lipopolysaccharide of Bacteroides melaninogenicus subspecies asaccharolyticus. J Immunol. 1978 Jan;120(1):72–78. [PubMed] [Google Scholar]
  12. Mansheim B. J., Stenstrom M. L., Low S. B., Clark W. B. Measurement of serum and salivary antibodies to the oral pathogen Bacteroides asaccharolyticus in human subjects. Arch Oral Biol. 1980;25(8-9):553–557. doi: 10.1016/0003-9969(80)90067-9. [DOI] [PubMed] [Google Scholar]
  13. Mashimo P. A., Ellison S. A. Diffusate media for cultivation of oral anaerobic bacteria. Koku Eisei Gakkai Zasshi. 1972 Mar;22(1):38–44. doi: 10.5834/jdh.22.38. [DOI] [PubMed] [Google Scholar]
  14. Matsushima K., Bano M., Kidwell W. R., Oppenheim J. J. Interleukin 1 increases collagen type IV production by murine mammary epithelial cells. J Immunol. 1985 Feb;134(2):904–909. [PubMed] [Google Scholar]
  15. Meryon S. D., Perris A. D. Lipopolysaccharide-induced bone resorption is mediated by prostaglandins. Life Sci. 1981 Mar 2;28(9):1061–1065. doi: 10.1016/0024-3205(81)90754-2. [DOI] [PubMed] [Google Scholar]
  16. Mizel S. B. Studies on the purification and structure-functional relationships of murine lymphocyte activating factor (Interleukin 1). Mol Immunol. 1980 May;17(5):571–577. doi: 10.1016/0161-5890(80)90155-8. [DOI] [PubMed] [Google Scholar]
  17. Morrison D. C., Ryan J. L. Bacterial endotoxins and host immune responses. Adv Immunol. 1979;28:293–450. doi: 10.1016/s0065-2776(08)60802-0. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Nair B. C., Mayberry W. R., Dziak R., Chen P. B., Levine M. J., Hausmann E. Biological effects of a purified lipopolysaccharide from Bacteroides gingivalis. J Periodontal Res. 1983 Jan;18(1):40–49. doi: 10.1111/j.1600-0765.1983.tb00333.x. [DOI] [PubMed] [Google Scholar]
  20. Oppenheim J. J., Charon J. A., Luger T. A. Evidence for an in vivo inflammatory role of interleukin 1 (IL 1). Transplant Proc. 1982 Sep;14(3):553–555. [PubMed] [Google Scholar]
  21. Postlethwaite A. E., Lachman L. B., Mainardi C. L., Kang A. H. Interleukin 1 stimulation of collagenase production by cultured fibroblasts. J Exp Med. 1983 Feb 1;157(2):801–806. doi: 10.1084/jem.157.2.801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Ryan J. L., Glode L. M., Rosenstreich D. L. Lack of responsiveness of C3H/HeJ macrophages to lipopolysaccharide: the cellular basis of LPS-stimulated metabolism. J Immunol. 1979 Mar;122(3):932–935. [PubMed] [Google Scholar]
  23. Sandberg A. L., Raisz L. G., Goodson J. M., Simmons H. A., Mergenhagen S. E. Initiation of bone resorption by the classical and alternative C pathways and its mediation by prostaglandins. J Immunol. 1977 Oct;119(4):1378–1381. [PubMed] [Google Scholar]
  24. Slots J. Subgingival microflora and periodontal disease. J Clin Periodontol. 1979 Oct;6(5):351–382. doi: 10.1111/j.1600-051x.1979.tb01935.x. [DOI] [PubMed] [Google Scholar]
  25. Slots J. The predominant cultivable microflora of advanced periodontitis. Scand J Dent Res. 1977 Jan-Feb;85(2):114–121. doi: 10.1111/j.1600-0722.1977.tb00541.x. [DOI] [PubMed] [Google Scholar]
  26. Sveen K. The capacity of lipopolysaccharides from bacteroides, fusobacterium and veillonella to produce skin inflammation and the local and generalized Shwartzman reaction in rabbits. J Periodontal Res. 1977 Sep;12(5):340–350. doi: 10.1111/j.1600-0765.1977.tb01525.x. [DOI] [PubMed] [Google Scholar]
  27. Tanner A. C., Haffer C., Bratthall G. T., Visconti R. A., Socransky S. S. A study of the bacteria associated with advancing periodontitis in man. J Clin Periodontol. 1979 Oct;6(5):278–307. doi: 10.1111/j.1600-051x.1979.tb01931.x. [DOI] [PubMed] [Google Scholar]
  28. Tsai C. M., Frasch C. E. A sensitive silver stain for detecting lipopolysaccharides in polyacrylamide gels. Anal Biochem. 1982 Jan 1;119(1):115–119. doi: 10.1016/0003-2697(82)90673-x. [DOI] [PubMed] [Google Scholar]
  29. Wannemuehler M. J., Michalek S. M., Jirillo E., Williamson S. I., Hirasawa M., McGhee J. R. LPS regulation of the immune response: Bacteroides endotoxin induces mitogenic, polyclonal, and antibody responses in classical LPS responsive but not C3H/HeJ mice. J Immunol. 1984 Jul;133(1):299–305. [PubMed] [Google Scholar]
  30. White D., Mayrand D. Association of oral Bacteroides with gingivitis and adult periodontitis. J Periodontal Res. 1981 May;16(3):259–265. doi: 10.1111/j.1600-0765.1981.tb00974.x. [DOI] [PubMed] [Google Scholar]
  31. Williamson S. I., Wannemuehler M. J., Jirillo E., Pritchard D. G., Michalek S. M., McGhee J. R. LPS regulation of the immune response: separate mechanisms for murine B cell activation by lipid A (direct) and polysaccharide (macrophage-dependent) derived from Bacteroides LPS. J Immunol. 1984 Nov;133(5):2294–2300. [PubMed] [Google Scholar]
  32. Wright B. G., Rebers P. A. Procedure for determining heptose and hexose in lipopolysaccharides. Modification of the cysteine-sulfuric acid method. Anal Biochem. 1972 Oct;49(2):307–319. doi: 10.1016/0003-2697(72)90433-2. [DOI] [PubMed] [Google Scholar]

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