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. 1990 Oct;58(10):3394–3400. doi: 10.1128/iai.58.10.3394-3400.1990

Protective immunization against experimental Bacteroides (Porphyromonas) gingivalis infection.

P B Chen 1, L B Davern 1, R Schifferle 1, J J Zambon 1
PMCID: PMC313666  PMID: 2401568

Abstract

The effects of immunization in modulating the pathogenesis of Bacteroides (Porphyromonas) gingivalis infection in a murine model system were examined. BALB/c mice were immunized by intraperitoneal injection with B. gingivalis ATCC 53977 (one injection per week for 3 weeks), or with a lithium diiodosalicylate (LIS) extract (one injection per week for 3 weeks), or with lipopolysaccharide (LPS; one intravenous or intraperitoneal injection) from this same strain. Two weeks after the final immunization, the mice were challenged by subcutaneous injection of B. gingivalis ATCC 53977. Mice immunized with bacteria had no secondary lesions and no septicemia, whereas mice immunized with LIS extract had few secondary lesions and no septicemia. Mice immunized with LPS and nonimmunized mice demonstrated secondary abdominal lesions and septicemia after challenge. Bacterial cells and LIS extract, but not LPS, induced serum antibody and antigen reactive lymphocytes, as measured by enzyme-linked immunosorbent assay, immunoblot, Western immunoblot transfer, and in vitro lymphoproliferative responses. The present study suggests that immunization with a LIS extract or whole cells may induce a protective response against experimental B. gingivalis infection.

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Selected References

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  1. Bramanti T. E., Wong G. G., Weintraub S. T., Holt S. C. Chemical characterization and biologic properties of lipopolysaccharide from Bacteroides gingivalis strains W50, W83, and ATCC 33277. Oral Microbiol Immunol. 1989 Dec;4(4):183–192. doi: 10.1111/j.1399-302x.1989.tb00250.x. [DOI] [PubMed] [Google Scholar]
  2. Chen P. B., Neiders M. E., Millar S. J., Reynolds H. S., Zambon J. J. Effect of immunization on experimental Bacteroides gingivalis infection in a murine model. Infect Immun. 1987 Oct;55(10):2534–2537. doi: 10.1128/iai.55.10.2534-2537.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Chen P., Bochacki V., Reynolds H. S., Beanan J., Tatakis D. N., Zambon J. J., Genco R. J. The use of monoclonal antibodies to detect Bacteroides gingivalis in biological samples. Infect Immun. 1986 Dec;54(3):798–803. doi: 10.1128/iai.54.3.798-803.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chen P., Doroszczak N. Differences in lymphoproliferative responses to the bacterium Actinomyces viscosus in various mammalian species. Arch Oral Biol. 1982;27(4):319–324. doi: 10.1016/0003-9969(82)90161-3. [DOI] [PubMed] [Google Scholar]
  5. Eisenstein T. K., Killar L. M., Sultzer B. M. Immunity to infection with Salmonella typhimurium: mouse-strain differences in vaccine- and serum-mediated protection. J Infect Dis. 1984 Sep;150(3):425–435. doi: 10.1093/infdis/150.3.425. [DOI] [PubMed] [Google Scholar]
  6. Elkins K. L., Stashak P. W., Baker P. J. Prior exposure to subimmunogenic amounts of some bacterial lipopolysaccharides induces specific immunological unresponsiveness. Infect Immun. 1987 Dec;55(12):3085–3092. doi: 10.1128/iai.55.12.3085-3092.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Grenier D., Mayrand D. Selected characteristics of pathogenic and nonpathogenic strains of Bacteroides gingivalis. J Clin Microbiol. 1987 Apr;25(4):738–740. doi: 10.1128/jcm.25.4.738-740.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hitchcock P. J., Brown T. M. Morphological heterogeneity among Salmonella lipopolysaccharide chemotypes in silver-stained polyacrylamide gels. J Bacteriol. 1983 Apr;154(1):269–277. doi: 10.1128/jb.154.1.269-277.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Isibasi A., Ortiz V., Vargas M., Paniagua J., González C., Moreno J., Kumate J. Protection against Salmonella typhi infection in mice after immunization with outer membrane proteins isolated from Salmonella typhi 9,12,d, Vi. Infect Immun. 1988 Nov;56(11):2953–2959. doi: 10.1128/iai.56.11.2953-2959.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Kastelein P., van Steenbergen T. J., Bras J. M., de Graaff J. An experimentally induced phlegmonous abscess by a strain of Bacteroides gingivalis in guinea pigs and mice. Antonie Van Leeuwenhoek. 1981 Mar;47(1):1–9. doi: 10.1007/BF00399062. [DOI] [PubMed] [Google Scholar]
  11. Kimura A., Gulig P. A., McCracken G. H., Jr, Loftus T. A., Hansen E. J. A minor high-molecular-weight outer membrane protein of Haemophilus influenzae type b is a protective antigen. Infect Immun. 1985 Jan;47(1):253–259. doi: 10.1128/iai.47.1.253-259.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  13. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  14. Lu Y. S., Afendis S. J., Pakes S. P. Identification of immunogenic outer membrane proteins of Pasteurella multocida 3:A in rabbits. Infect Immun. 1988 Jun;56(6):1532–1537. doi: 10.1128/iai.56.6.1532-1537.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Marchesi V. T., Andrews E. P. Glycoproteins: isolation from cellmembranes with lithium diiodosalicylate. Science. 1971 Dec 17;174(4015):1247–1248. doi: 10.1126/science.174.4015.1247. [DOI] [PubMed] [Google Scholar]
  16. Matthews-Greer J. M., Gilleland H. E., Jr Outer membrane protein F (porin) preparation of Pseudomonas aeruginosa as a protective vaccine against heterologous immunotype strains in a burned mouse model. J Infect Dis. 1987 Jun;155(6):1282–1291. doi: 10.1093/infdis/155.6.1282. [DOI] [PubMed] [Google Scholar]
  17. Millar S. J., Chen P. B., Hausmann E. Monoclonal antibody for identification of Bacteroides gingivalis lipopolysaccharide. J Clin Microbiol. 1987 Dec;25(12):2437–2439. doi: 10.1128/jcm.25.12.2437-2439.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Millar S. J., Goldstein E. G., Levine M. J., Hausmann E. Modulation of bone metabolism by two chemically distinct lipopolysaccharide fractions from Bacteroides gingivalis. Infect Immun. 1986 Jan;51(1):302–306. doi: 10.1128/iai.51.1.302-306.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Montaraz J. A., Winter A. J. Comparison of living and nonliving vaccines for Brucella abortus in BALB/c mice. Infect Immun. 1986 Aug;53(2):245–251. doi: 10.1128/iai.53.2.245-251.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Mukkur T. K., McDowell G. H., Stocker B. A., Lascelles A. K. Protection against experimental salmonellosis in mice and sheep by immunisation with aromatic-dependent Salmonella typhimurium. J Med Microbiol. 1987 Aug;24(1):11–19. doi: 10.1099/00222615-24-1-11. [DOI] [PubMed] [Google Scholar]
  21. Munson R. S., Jr, Shenep J. L., Barenkamp S. J., Granoff D. M. Purification and comparison of outer membrane protein P2 from Haemophilus influenzae type b isolates. J Clin Invest. 1983 Aug;72(2):677–684. doi: 10.1172/JCI111017. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Murray P. A., Levine M. J., Reddy M. S., Tabak L. A., Bergey E. J. Preparation of a sialic acid-binding protein from Streptococcus mitis KS32AR. Infect Immun. 1986 Aug;53(2):359–365. doi: 10.1128/iai.53.2.359-365.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Neiders M. E., Chen P. B., Suido H., Reynolds H. S., Zambon J. J., Shlossman M., Genco R. J. Heterogeneity of virulence among strains of Bacteroides gingivalis. J Periodontal Res. 1989 May;24(3):192–198. doi: 10.1111/j.1600-0765.1989.tb02005.x. [DOI] [PubMed] [Google Scholar]
  24. Okuda K., Kato T., Naito Y., Takazoe I., Kikuchi Y., Nakamura T., Kiyoshige T., Sasaki S. Protective efficacy of active and passive immunizations against experimental infection with Bacteroides gingivalis in ligated hamsters. J Dent Res. 1988 May;67(5):807–811. doi: 10.1177/00220345880670050201. [DOI] [PubMed] [Google Scholar]
  25. Saukkonen K., Abdillahi H., Poolman J. T., Leinonen M. Protective efficacy of monoclonal antibodies to class 1 and class 3 outer membrane proteins of Neisseria meningitidis B:15:P1.16 in infant rat infection model: new prospects for vaccine development. Microb Pathog. 1987 Oct;3(4):261–267. doi: 10.1016/0882-4010(87)90059-3. [DOI] [PubMed] [Google Scholar]
  26. Shapiro M. E., Onderdonk A. B., Kasper D. L., Finberg R. W. Cellular immunity to Bacteroides fragilis capsular polysaccharide. J Exp Med. 1982 Apr 1;155(4):1188–1197. doi: 10.1084/jem.155.4.1188. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Udhayakumar V., Muthukkaruppan V. R. Protective immunity induced by outer membrane proteins of Salmonella typhimurium in mice. Infect Immun. 1987 Mar;55(3):816–821. doi: 10.1128/iai.55.3.816-821.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Van Steenbergen T. J., Delemarre F. G., Namavar F., De Graaff J. Differences in virulence within the species Bacteroides gingivalis. Antonie Van Leeuwenhoek. 1987;53(4):233–244. doi: 10.1007/BF00393930. [DOI] [PubMed] [Google Scholar]
  29. Vuopio-Varkila J., Karvonen M., Saxén H. Protective capacity of antibodies to outer-membrane components of Escherichia coli in a systemic mouse peritonitis model. J Med Microbiol. 1988 Feb;25(2):77–84. doi: 10.1099/00222615-25-2-77. [DOI] [PubMed] [Google Scholar]
  30. Williams G. D., Holt S. C. Characteristics of the outer membrane of selected oral Bacteroides species. Can J Microbiol. 1985 Mar;31(3):238–250. doi: 10.1139/m85-046. [DOI] [PubMed] [Google Scholar]
  31. Yoshimura F., Watanabe K., Takasawa T., Kawanami M., Kato H. Purification and properties of a 75-kilodalton major protein, an immunodominant surface antigen, from the oral anaerobe Bacteroides gingivalis. Infect Immun. 1989 Nov;57(11):3646–3652. doi: 10.1128/iai.57.11.3646-3652.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. van Steenbergen T. J., Kastelein P., Touw J. J., de Graaff J. Virulence of black-pigmented Bacteroides strains from periodontal pockets and other sites in experimentally induced skin lesions in mice. J Periodontal Res. 1982 Jan;17(1):41–49. doi: 10.1111/j.1600-0765.1982.tb01129.x. [DOI] [PubMed] [Google Scholar]

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