Skip to main content
NCBI home page
Infection and Immunity logoLink to Infection and Immunity
. 1994 May;62(5):1652–1657. doi: 10.1128/iai.62.5.1652-1657.1994

Systemic and mucosal immune responses in mice orally immunized with avirulent Salmonella typhimurium expressing a cloned Porphyromonas gingivalis hemagglutinin.

D M Dusek 1, A Progulske-Fox 1, T A Brown 1
PMCID: PMC186378  PMID: 8168925

Abstract

Porphyromonas gingivalis produces a variety of virulence factors that may have a function in the periodontal disease process. Determination of the role of these various factors in pathogenesis and identification of a means for protecting the host from the destructive effects of this organism are areas of vigorous investigation. In this study we demonstrate the potential of avirulent Salmonella typhimurium strains to stimulate a specific systemic and mucosal immune response to a cloned P. gingivalis hemagglutinin (HagB). An avirulent strain of S. typhimurium, chi 4072, expressing the hagB gene of P. gingivalis 381 on the plasmid pDMD1 was intragastrically administered to BALB/c mice. These mice mounted a serum immunoglobulin G (IgG) and IgA primary response against the hagB gene product and a mucosal immune response as measured by evaluation of saliva. IgA antibodies were also detected in bile. These results demonstrate the feasibility of using attenuated S. typhimurium strains as carriers of P. gingivalis virulence factors for subsequent evaluation of the systemic and mucosal immune response against these antigens. This system will provide a means for evaluating the virulence factors of P. gingivalis for their suitability in the construction of potential vaccines.

Full text

PDF
1652

Images in this article

1654Image
on p.1654

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. ASHCROFT M. T., RITCHIE J. M., NICHOLSON C. C. CONTROLLED FIELD TRIAL IN BRITISH GUIANA SCHOOL CHILDREN OF HEAT-KILLED-PHENOLIZED AND ACETONE-KILLED LYOPHILIZED TYPHOID VACCINES. Am J Hyg. 1964 Mar;79:196–206. doi: 10.1093/oxfordjournals.aje.a120376. [DOI] [PubMed] [Google Scholar]
  2. BERTANI G., WEIGLE J. J. Host controlled variation in bacterial viruses. J Bacteriol. 1953 Feb;65(2):113–121. doi: 10.1128/jb.65.2.113-121.1953. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Binotto J., MacLachlan P. R., Sanderson K. E. Electrotransformation in Salmonella typhimurium LT2. Can J Microbiol. 1991 Jun;37(6):474–477. doi: 10.1139/m91-078. [DOI] [PubMed] [Google Scholar]
  4. Bom-van Noorloos A. A., van der Meer J. W., van de Gevel J. S., Schepens E., van Steenbergen T. J., Burger E. H. Bacteroides gingivalis stimulates bone resorption via interleukin-1 production by mononuclear cells. The relative role for B. gingivalis endotoxin. J Clin Periodontol. 1990 Aug;17(7 Pt 1):409–413. doi: 10.1111/j.1600-051x.1990.tb02338.x. [DOI] [PubMed] [Google Scholar]
  5. Brown T. A., Murphy B. R., Radl J., Haaijman J. J., Mestecky J. Subclass distribution and molecular form of immunoglobulin A hemagglutinin antibodies in sera and nasal secretions after experimental secondary infection with influenza A virus in humans. J Clin Microbiol. 1985 Aug;22(2):259–264. doi: 10.1128/jcm.22.2.259-264.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chen P. B., Davern L. B., Schifferle R., Zambon J. J. Protective immunization against experimental Bacteroides (Porphyromonas) gingivalis infection. Infect Immun. 1990 Oct;58(10):3394–3400. doi: 10.1128/iai.58.10.3394-3400.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Curtiss R., 3rd, Galan J. E., Nakayama K., Kelly S. M. Stabilization of recombinant avirulent vaccine strains in vivo. Res Microbiol. 1990 Sep-Oct;141(7-8):797–805. doi: 10.1016/0923-2508(90)90113-5. [DOI] [PubMed] [Google Scholar]
  8. Curtiss R., 3rd, Kelly S. M. Salmonella typhimurium deletion mutants lacking adenylate cyclase and cyclic AMP receptor protein are avirulent and immunogenic. Infect Immun. 1987 Dec;55(12):3035–3043. doi: 10.1128/iai.55.12.3035-3043.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cárdenas L., Clements J. D. Stability, immunogenicity and expression of foreign antigens in bacterial vaccine vectors. Vaccine. 1993;11(2):126–135. doi: 10.1016/0264-410x(93)90007-k. [DOI] [PubMed] [Google Scholar]
  10. Dusek D. M., Progulske-Fox A., Whitlock J., Brown T. A. Isolation and characterization of a cloned Porphyromonas gingivalis hemagglutinin from an avirulent strain of Salmonella typhimurium. Infect Immun. 1993 Mar;61(3):940–946. doi: 10.1128/iai.61.3.940-946.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ebersole J. L., Brunsvold M., Steffensen B., Wood R., Holt S. C. Effects of immunization with Porphyromonas gingivalis and Prevotella intermedia on progression of ligature-induced periodontitis in the nonhuman primate Macaca fascicularis. Infect Immun. 1991 Oct;59(10):3351–3359. doi: 10.1128/iai.59.10.3351-3359.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Evans R. T., Klausen B., Sojar H. T., Bedi G. S., Sfintescu C., Ramamurthy N. S., Golub L. M., Genco R. J. Immunization with Porphyromonas (Bacteroides) gingivalis fimbriae protects against periodontal destruction. Infect Immun. 1992 Jul;60(7):2926–2935. doi: 10.1128/iai.60.7.2926-2935.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Galán J. E., Nakayama K., Curtiss R., 3rd Cloning and characterization of the asd gene of Salmonella typhimurium: use in stable maintenance of recombinant plasmids in Salmonella vaccine strains. Gene. 1990 Sep 28;94(1):29–35. doi: 10.1016/0378-1119(90)90464-3. [DOI] [PubMed] [Google Scholar]
  14. Genco C. A., Kapczynski D. R., Cutler C. W., Arko R. J., Arnold R. R. Influence of immunization on Porphyromonas gingivalis colonization and invasion in the mouse chamber model. Infect Immun. 1992 Apr;60(4):1447–1454. doi: 10.1128/iai.60.4.1447-1454.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Genco R. J. Host responses in periodontal diseases: current concepts. J Periodontol. 1992 Apr;63(4 Suppl):338–355. doi: 10.1902/jop.1992.63.4s.338. [DOI] [PubMed] [Google Scholar]
  16. Hanahan D., Jessee J., Bloom F. R. Plasmid transformation of Escherichia coli and other bacteria. Methods Enzymol. 1991;204:63–113. doi: 10.1016/0076-6879(91)04006-a. [DOI] [PubMed] [Google Scholar]
  17. Katz J., Leary R. M., Ward D. C., Harmon C. C., Michalek S. M. Humoral response to Porphyromonas (Bacteroides) gingivalis in rats: time course and T-cell dependence. Infect Immun. 1992 Sep;60(9):3579–3585. doi: 10.1128/iai.60.9.3579-3585.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kesavalu L., Ebersole J. L., Machen R. L., Holt S. C. Porphyromonas gingivalis virulence in mice: induction of immunity to bacterial components. Infect Immun. 1992 Apr;60(4):1455–1464. doi: 10.1128/iai.60.4.1455-1464.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kilian M., Mestecky J., Russell M. W. Defense mechanisms involving Fc-dependent functions of immunoglobulin A and their subversion by bacterial immunoglobulin A proteases. Microbiol Rev. 1988 Jun;52(2):296–303. doi: 10.1128/mr.52.2.296-303.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Klimpel K. W., Clark V. L. The RNA polymerases of Porphyromonas gingivalis and Fusobacterium nucleatum are unrelated to the RNA polymerase of Escherichia coli. J Dent Res. 1990 Sep;69(9):1567–1572. doi: 10.1177/00220345900690090601. [DOI] [PubMed] [Google Scholar]
  21. Kornman K. S., Robertson P. B. Clinical and microbiological evaluation of therapy for juvenile periodontitis. J Periodontol. 1985 Aug;56(8):443–446. doi: 10.1902/jop.1985.56.8.443. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. Mayrand D., Holt S. C. Biology of asaccharolytic black-pigmented Bacteroides species. Microbiol Rev. 1988 Mar;52(1):134–152. doi: 10.1128/mr.52.1.134-152.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. McArthur W. P., Magnusson I., Marks R. G., Clark W. B. Modulation of colonization by black-pigmented Bacteroides species in squirrel monkeys by immunization with Bacteroides gingivalis. Infect Immun. 1989 Aug;57(8):2313–2317. doi: 10.1128/iai.57.8.2313-2317.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Moore W. E., Holdeman L. V., Cato E. P., Smibert R. M., Burmeister J. A., Palcanis K. G., Ranney R. R. Comparative bacteriology of juvenile periodontitis. Infect Immun. 1985 May;48(2):507–519. doi: 10.1128/iai.48.2.507-519.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Progulske-Fox A., Tumwasorn S., Holt S. C. The expression and function of a Bacteroides gingivalis hemagglutinin gene in Escherichia coli. Oral Microbiol Immunol. 1989 Sep;4(3):121–131. doi: 10.1111/j.1399-302x.1989.tb00238.x. [DOI] [PubMed] [Google Scholar]
  27. Russell M. W., Brown T. A., Mestecky J. Preferential transport of IgA and IgA-immune complexes to bile compared with other external secretions. Mol Immunol. 1982 May;19(5):677–682. doi: 10.1016/0161-5890(82)90369-8. [DOI] [PubMed] [Google Scholar]
  28. Russell M. W., Brown T. A., Mestecky J. Role of serum IgA. Hepatobiliary transport of circulating antigen. J Exp Med. 1981 Apr 1;153(4):968–976. doi: 10.1084/jem.153.4.968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Russell M. W., Reinholdt J., Kilian M. Anti-inflammatory activity of human IgA antibodies and their Fab alpha fragments: inhibition of IgG-mediated complement activation. Eur J Immunol. 1989 Dec;19(12):2243–2249. doi: 10.1002/eji.1830191210. [DOI] [PubMed] [Google Scholar]
  30. Slots J., Listgarten M. A. Bacteroides gingivalis, Bacteroides intermedius and Actinobacillus actinomycetemcomitans in human periodontal diseases. J Clin Periodontol. 1988 Feb;15(2):85–93. doi: 10.1111/j.1600-051x.1988.tb00999.x. [DOI] [PubMed] [Google Scholar]
  31. Smith B. P., Reina-Guerra M., Hoiseth S. K., Stocker B. A., Habasha F., Johnson E., Merritt F. Aromatic-dependent Salmonella typhimurium as modified live vaccines for calves. Am J Vet Res. 1984 Jan;45(1):59–66. [PubMed] [Google Scholar]
  32. Socransky S. S., Haffajee A. D. The bacterial etiology of destructive periodontal disease: current concepts. J Periodontol. 1992 Apr;63(4 Suppl):322–331. doi: 10.1902/jop.1992.63.4s.322. [DOI] [PubMed] [Google Scholar]
  33. Van Winkelhoff A. J., Van der Velden U., Winkel E. G., de Graaff J. Black-pigmented Bacteroides and motile organisms on oral mucosal surfaces in individuals with and without periodontal breakdown. J Periodontal Res. 1986 Jul;21(4):434–439. doi: 10.1111/j.1600-0765.1986.tb01477.x. [DOI] [PubMed] [Google Scholar]
  34. Vieira J., Messing J. The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene. 1982 Oct;19(3):259–268. doi: 10.1016/0378-1119(82)90015-4. [DOI] [PubMed] [Google Scholar]
  35. Wilton J. M., Johnson N. W., Curtis M. A., Gillett I. R., Carman R. J., Bampton J. L., Griffiths G. S., Sterne J. A. Specific antibody responses to subgingival plaque bacteria as aids to the diagnosis and prognosis of destructive periodontitis. J Clin Periodontol. 1991 Jan;18(1):1–15. doi: 10.1111/j.1600-051x.1991.tb01112.x. [DOI] [PubMed] [Google Scholar]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES