Skip to main content
PMC home page
Infection and Immunity logoLink to Infection and Immunity
. 1992 Jan;60(1):189–195. doi: 10.1128/iai.60.1.189-195.1992

Mechanism of YadA-mediated serum resistance of Yersinia enterocolitica serotype O3.

D Pilz 1, T Vocke 1, J Heesemann 1, V Brade 1
PMCID: PMC257521  PMID: 1729182

Abstract

Complement activation via the alternative pathway was analyzed with isogenic strains of Yersinia enterocolitica serotype O3 differing in plasmid content (p- or p+ strains) or selective lack of YadA expression (YadA- strain). The p+ strain was serum resistant, even after antibody-enhanced complement activation. Serum sensitivity was observed with the p- and YadA- strains but was more pronounced in the p- strain. The p+ strain deposited less C5b-9(m) complexes on its surface than the p- and YadA- strains. No size difference, however, was detected with solubilized C5b-9(m) complexes obtained from resistant and sensitive strains. At the C3 level, it became evident that surface-bound C3b was degraded faster into iC3b on the p+ strain than on the p- and YadA- strains. Our results demonstrate that YadA inhibits complement activation at the C3 and C9 level. As a result, reduced amounts of C5b-9(m) are generated on the surface of YadA-bearing bacteria. In addition, YadA seems to protect against the lytic action of those C5b-9(m) complexes whose deposition could not be prevented.

Full text

PDF
189

Images in this article

192Image
on p.192

Selected References

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

  1. Acker G., Wartenberg K. Ultrastructure of lipopolysaccharides of Yersinia enterocolitica, Salmonella typhimurium and Escherichia coli. Zentralbl Bakteriol Orig A. 1976 Aug;235(4):439–452. [PubMed] [Google Scholar]
  2. Balligand G., Laroche Y., Cornelis G. Genetic analysis of virulence plasmid from a serogroup 9 Yersinia enterocolitica strain: role of outer membrane protein P1 in resistance to human serum and autoagglutination. Infect Immun. 1985 Jun;48(3):782–786. doi: 10.1128/iai.48.3.782-786.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Biesecker G., Müller-Eberhard H. J. The ninth component of human complement: purification and physicochemical characterization. J Immunol. 1980 Mar;124(3):1291–1296. [PubMed] [Google Scholar]
  4. Cornelis G., Laroche Y., Balligand G., Sory M. P., Wauters G. Yersinia enterocolitica, a primary model for bacterial invasiveness. Rev Infect Dis. 1987 Jan-Feb;9(1):64–87. doi: 10.1093/clinids/9.1.64. [DOI] [PubMed] [Google Scholar]
  5. Dziwisch L., Heesemann J., Kremer B. The microscopic double immunofluorescence technique, a method for quantitative differentiation between extra- and intracellularly located bacteria in isolated polymorphonuclear granulocytes. Med Microbiol Immunol. 1988;177(2):101–107. doi: 10.1007/BF00189531. [DOI] [PubMed] [Google Scholar]
  6. Emödy L., Heesemann J., Wolf-Watz H., Skurnik M., Kapperud G., O'Toole P., Wadström T. Binding to collagen by Yersinia enterocolitica and Yersinia pseudotuberculosis: evidence for yopA-mediated and chromosomally encoded mechanisms. J Bacteriol. 1989 Dec;171(12):6674–6679. doi: 10.1128/jb.171.12.6674-6679.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Falkow S. Bacterial entry into eukaryotic cells. Cell. 1991 Jun 28;65(7):1099–1102. doi: 10.1016/0092-8674(91)90003-h. [DOI] [PubMed] [Google Scholar]
  8. Heesemann J., Algermissen B., Laufs R. Genetically manipulated virulence of Yersinia enterocolitica. Infect Immun. 1984 Oct;46(1):105–110. doi: 10.1128/iai.46.1.105-110.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Heesemann J., Gross U., Schmidt N., Laufs R. Immunochemical analysis of plasmid-encoded proteins released by enteropathogenic Yersinia sp. grown in calcium-deficient media. Infect Immun. 1986 Nov;54(2):561–567. doi: 10.1128/iai.54.2.561-567.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Heesemann J., Keller C., Morawa R., Schmidt N., Siemens H. J., Laufs R. Plasmids of human strains of Yersinia enterocolitica: molecular relatedness and possible importance for pathogenesis. J Infect Dis. 1983 Jan;147(1):107–115. doi: 10.1093/infdis/147.1.107. [DOI] [PubMed] [Google Scholar]
  11. Joiner K. A. Complement evasion by bacteria and parasites. Annu Rev Microbiol. 1988;42:201–230. doi: 10.1146/annurev.mi.42.100188.001221. [DOI] [PubMed] [Google Scholar]
  12. Joiner K. A., Fries L. F., Schmetz M. A., Frank M. M. IgG bearing covalently bound C3b has enhanced bactericidal activity for Escherichia coli 0111. J Exp Med. 1985 Sep 1;162(3):877–889. doi: 10.1084/jem.162.3.877. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Joiner K. A., Hammer C. H., Brown E. J., Cole R. J., Frank M. M. Studies on the mechanism of bacterial resistance to complement-mediated killing. I. Terminal complement components are deposited and released from Salmonella minnesota S218 without causing bacterial death. J Exp Med. 1982 Mar 1;155(3):797–808. doi: 10.1084/jem.155.3.797. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Joiner K. A. Studies on the mechanism of bacterial resistance to complement-mediated killing and on the mechanism of action of bactericidal antibody. Curr Top Microbiol Immunol. 1985;121:99–133. doi: 10.1007/978-3-642-45604-6_6. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. Liang-Takasaki C. J., Grossman N., Leive L. Salmonellae activate complement differentially via the alternative pathway depending on the structure of their lipopolysaccharide O-antigen. J Immunol. 1983 Apr;130(4):1867–1870. [PubMed] [Google Scholar]
  17. Martinez R. J. Plasmid-mediated and temperature-regulated surface properties of Yersinia enterocolitica. Infect Immun. 1983 Sep;41(3):921–930. doi: 10.1128/iai.41.3.921-930.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Martinez R. J. Thermoregulation-dependent expression of Yersinia enterocolitica protein 1 imparts serum resistance to Escherichia coli K-12. J Bacteriol. 1989 Jul;171(7):3732–3739. doi: 10.1128/jb.171.7.3732-3739.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Miller V. L., Farmer J. J., 3rd, Hill W. E., Falkow S. The ail locus is found uniquely in Yersinia enterocolitica serotypes commonly associated with disease. Infect Immun. 1989 Jan;57(1):121–131. doi: 10.1128/iai.57.1.121-131.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Moll A., Manning P. A., Timmis K. N. Plasmid-determined resistance to serum bactericidal activity: a major outer membrane protein, the traT gene product, is responsible for plasmid-specified serum resistance in Escherichia coli. Infect Immun. 1980 May;28(2):359–367. doi: 10.1128/iai.28.2.359-367.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Pai C. H., DeStephano L. Serum resistance associated with virulence in Yersinia enterocolitica. Infect Immun. 1982 Feb;35(2):605–611. doi: 10.1128/iai.35.2.605-611.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Pilz D., Wachter E., Heesemann J., Brade V. Evasion of Yersinia enterocolitica serotype 03 from complement-mediated killing. Behring Inst Mitt. 1991 Feb;(88):183–193. [PubMed] [Google Scholar]
  23. Podack E. R., Kolb W. P., Müller-Eberhard H. J. The C5b-6 complex: formation, isolation, and inhibition of its activity by lipoprotein and the S-protein of human serum. J Immunol. 1978 Jun;120(6):1841–1848. [PubMed] [Google Scholar]
  24. Tertti R., Eerola E., Lehtonen O. P., Ståhlberg T. H., Viander M., Toivanen A. Virulence-plasmid is associated with the inhibition of opsonization in Yersinia enterocolitica and Yersinia pseudotuberculosis. Clin Exp Immunol. 1987 May;68(2):266–274. [PMC free article] [PubMed] [Google Scholar]
  25. Vandenbosch J. L., Rabert D. K., Jones G. W. Plasmid-associated resistance of Salmonella typhimurium to complement activated by the classical pathway. Infect Immun. 1987 Nov;55(11):2645–2652. doi: 10.1128/iai.55.11.2645-2652.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Wachter E., Brade V. Influence of surface modulations by enzymes and monoclonal antibodies on alternative complement pathway activation by Yersinia enterocolitica. Infect Immun. 1989 Jul;57(7):1984–1989. doi: 10.1128/iai.57.7.1984-1989.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Weninger J., Wartenberg K., Röllinghoff M. Immunological characterization of Yersinia enterocolitica O:9 and O:3 LPS antigens by monoclonal antibodies. Zentralbl Bakteriol Mikrobiol Hyg A. 1988 Nov;269(3):298–313. doi: 10.1016/s0176-6724(88)80173-1. [DOI] [PubMed] [Google Scholar]

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

RESOURCES