Skip to main content
PMC home page
Infection and Immunity logoLink to Infection and Immunity
. 1995 Feb;63(2):714–719. doi: 10.1128/iai.63.2.714-719.1995

Arthritogenicity of genetically manipulated Yersinia enterocolitica serotype O8 for Lewis rats.

K I Gaede 1, J Heesemann 1
PMCID: PMC173058  PMID: 7822048

Abstract

Yersinia enterocolitica strains of serotype O8 but not strains of other human pathogenic serotypes (e.g., O3 or O9) are able to induce a reactive arthritis-like disease in Lewis rats after intravenous inoculation (J. L. Hill and D. T. Yu, Infect. Immun. 55:721-726, 1987). To assess which bacterial components or pathogenic factors are crucial for arthritis induction, six genetically manipulated Y. enterocolitica O8 derivatives have been compared with the parental strain in Lewis rats. Neither differences in the length of the lipopolysaccharide side chain (smooth to semirough) of Y. enterocolitica O8 nor replacement of the virulence plasmid (pYVO8) of Y. enterocolitica O8 with that of the nonarthritogenic Y. enterocolitica O9 (pYVO9) had a significant influence on arthritogenic potential or virulence in rats. Transposon insertional inactivation of the plasmid gene yadA encoding the Yersinia adhesin and the collagen-binding protein or of the secretion of YopH resulted in decreased arthritogenicity (increase of the arthritogenic infectious dose) and pathogenicity (decreased persistence of the pathogen in spleens and livers of rats and increase of the 50% lethal dose for mice). However, mutants impaired in yersiniabactin production or uptake proved to be nonarthritogenic for rats, probably because of pronounced attenuation in virulence. From these results, we conclude that the arthritogenic potential of Y. enterocolitica serotype O8 is closely related to the virulence potential determined as the 50% lethal dose in mice and the ability to persist in lymphatic tissue of Lewis rats. A specific arthritogenic determinant of Y. enterocolitica could not be identified.

Full Text

The Full Text of this article is available as a PDF (244.3 KB).

Selected References

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

  1. Aho K., Ahvonen P., Lassus A., Sievers K., Tiilikainen A. HL-A 27 in reactive arthritis. A study of Yersinia arthritis and Reiter's disease. Arthritis Rheum. 1974 Sep-Oct;17(5):521–526. doi: 10.1002/art.1780170505. [DOI] [PubMed] [Google Scholar]
  2. Ahvonen P., Sievers K., Aho K. Arthritis associated with Yersinia enterocolitica infection. Acta Rheumatol Scand. 1969;15(3):232–253. doi: 10.3109/rhe1.1969.15.issue-1-4.32. [DOI] [PubMed] [Google Scholar]
  3. Gaede K., Mack D., Heesemann J. Experimental Yersinia enterocolitica infection in rats: analysis of the immune response to plasmid-encoded antigens of arthritis-susceptible Lewis rats and arthritis-resistant Fischer rats. Med Microbiol Immunol. 1992;181(3):165–172. doi: 10.1007/BF00202056. [DOI] [PubMed] [Google Scholar]
  4. Granfors K., Jalkanen S., Lindberg A. A., Mäki-Ikola O., von Essen R., Lahesmaa-Rantala R., Isomäki H., Saario R., Arnold W. J., Toivanen A. Salmonella lipopolysaccharide in synovial cells from patients with reactive arthritis. Lancet. 1990 Mar 24;335(8691):685–688. doi: 10.1016/0140-6736(90)90804-e. [DOI] [PubMed] [Google Scholar]
  5. Granfors K., Jalkanen S., von Essen R., Lahesmaa-Rantala R., Isomäki O., Pekkola-Heino K., Merilahti-Palo R., Saario R., Isomäki H., Toivanen A. Yersinia antigens in synovial-fluid cells from patients with reactive arthritis. N Engl J Med. 1989 Jan 26;320(4):216–221. doi: 10.1056/NEJM198901263200404. [DOI] [PubMed] [Google Scholar]
  6. Gripenberg-Lerche C., Toivanen P. Yersinia associated arthritis in SHR rats: effect of the microbial status of the host. Ann Rheum Dis. 1993 Mar;52(3):223–228. doi: 10.1136/ard.52.3.223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Hammer M., Zeidler H., Klimsa S., Heesemann J. Yersinia enterocolitica in the synovial membrane of patients with Yersinia-induced arthritis. Arthritis Rheum. 1990 Dec;33(12):1795–1800. doi: 10.1002/art.1780331206. [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., Gaede K., Autenrieth I. B. Experimental Yersinia enterocolitica infection in rodents: a model for human yersiniosis. APMIS. 1993 Jun;101(6):417–429. [PubMed] [Google Scholar]
  10. 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]
  11. Heesemann J., Hantke K., Vocke T., Saken E., Rakin A., Stojiljkovic I., Berner R. Virulence of Yersinia enterocolitica is closely associated with siderophore production, expression of an iron-repressible outer membrane polypeptide of 65,000 Da and pesticin sensitivity. Mol Microbiol. 1993 Apr;8(2):397–408. doi: 10.1111/j.1365-2958.1993.tb01583.x. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. Heesemann J., Laufs R. Construction of a mobilizable Yersinia enterocolitica virulence plasmid. J Bacteriol. 1983 Aug;155(2):761–767. doi: 10.1128/jb.155.2.761-767.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hill J. L., Yu D. T. Development of an experimental animal model for reactive arthritis induced by Yersinia enterocolitica infection. Infect Immun. 1987 Mar;55(3):721–726. doi: 10.1128/iai.55.3.721-726.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Lauhio A., Lähdevirta J., Janes R., Kontiainen S., Repo H. Reactive arthritis associated with Shigella sonnei infection. Arthritis Rheum. 1988 Sep;31(9):1190–1193. doi: 10.1002/art.1780310917. [DOI] [PubMed] [Google Scholar]
  16. Merilahti-Palo R., Gripenberg-Lerche C., Söderström K. O., Toivanen P. Long term follow up of SHR rats with experimental yersinia associated arthritis. Ann Rheum Dis. 1992 Jan;51(1):91–96. doi: 10.1136/ard.51.1.91. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Mertz A. K., Batsford S. R., Curschellas E., Kist M. J., Gondolf K. B. Cationic Yersinia antigen-induced chronic allergic arthritis in rats. A model for reactive arthritis in humans. J Clin Invest. 1991 Aug;88(2):632–642. doi: 10.1172/JCI115348. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Nikkari S., Merilahti-Palo R., Saario R., Söderström K. O., Granfors K., Skurnik M., Toivanen P. Yersinia-triggered reactive arthritis. Use of polymerase chain reaction and immunocytochemical staining in the detection of bacterial components from synovial specimens. Arthritis Rheum. 1992 Jun;35(6):682–687. doi: 10.1002/art.1780350613. [DOI] [PubMed] [Google Scholar]
  19. Probst P., Hermann E., Fleischer B. Role of bacteria-specific T cells in the immunopathogenesis of reactive arthritis. Trends Microbiol. 1994 Sep;2(9):329–332. doi: 10.1016/0966-842x(94)90450-2. [DOI] [PubMed] [Google Scholar]
  20. Rakin A., Saken E., Harmsen D., Heesemann J. The pesticin receptor of Yersinia enterocolitica: a novel virulence factor with dual function. Mol Microbiol. 1994 Jul;13(2):253–263. doi: 10.1111/j.1365-2958.1994.tb00420.x. [DOI] [PubMed] [Google Scholar]
  21. Schmidt M., Sethi K. K. Production and characterization of monoclonal antibodies specific for pathogenic serogroups O:3, O:8, and O:9 of Yersinia enterocolitica. Zentralbl Bakteriol Mikrobiol Hyg A. 1987 Jun;265(1-2):113–123. doi: 10.1016/s0176-6724(87)80157-8. [DOI] [PubMed] [Google Scholar]
  22. Schulze-Koops H., Burkhardt H., Heesemann J., Kirsch T., Swoboda B., Bull C., Goodman S., Emmrich F. Outer membrane protein YadA of enteropathogenic yersiniae mediates specific binding to cellular but not plasma fibronectin. Infect Immun. 1993 Jun;61(6):2513–2519. doi: 10.1128/iai.61.6.2513-2519.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Skurnik M., Wolf-Watz H. Analysis of the yopA gene encoding the Yop1 virulence determinants of Yersinia spp. Mol Microbiol. 1989 Apr;3(4):517–529. doi: 10.1111/j.1365-2958.1989.tb00198.x. [DOI] [PubMed] [Google Scholar]
  24. Toivanen A., Granfors K., Lahesmaa-Rantala R., Leino R., Ståhlberg T., Vuento R. Pathogenesis of Yersinia-triggered reactive arthritis: immunological, microbiological and clinical aspects. Immunol Rev. 1985 Aug;86:47–70. doi: 10.1111/j.1600-065x.1985.tb01137.x. [DOI] [PubMed] [Google Scholar]
  25. Toivanen A., Merilahti-Palo R., Gripenberg C., Lahesmaa-Rantala R., Söderström K. O., Jaakkola U. M. Yersinia-associated arthritis in the rat: experimental model for human reactive arthritis? Acta Pathol Microbiol Immunol Scand C. 1986 Dec;94(6):261–269. doi: 10.1111/j.1699-0463.1986.tb02121.x. [DOI] [PubMed] [Google Scholar]
  26. Urman J. D., Zurier R. B., Rothfield N. F. Reiter's syndrome associated with champylobacter fetus infection. Ann Intern Med. 1977 Apr;86(4):444–445. doi: 10.7326/0003-4819-86-4-444. [DOI] [PubMed] [Google Scholar]
  27. VARTIAINEN J., HURRI L. ARTHRITIS DUE TO SALMONELLA TYPHIMURIUM. REPORT OF 12 CASES OF MIGRATORY ARTHRITIS IN ASSOCIATION WITH SALMONELLA TYPHIMURIUM INFECTION. Acta Med Scand. 1964 Jun;175:771–776. [PubMed] [Google Scholar]
  28. Viitanen A. M., Arstila T. P., Lahesmaa R., Granfors K., Skurnik M., Toivanen P. Application of the polymerase chain reaction and immunofluorescence techniques to the detection of bacteria in Yersinia-triggered reactive arthritis. Arthritis Rheum. 1991 Jan;34(1):89–96. doi: 10.1002/art.1780340114. [DOI] [PubMed] [Google Scholar]
  29. Vogel U., Autenrieth I. B., Berner R., Heesemann J. Role of plasmid-encoded antigens of Yersinia enterocolitica in humoral immunity against secondary Y. enterocolitica infection in mice. Microb Pathog. 1993 Jul;15(1):23–36. doi: 10.1006/mpat.1993.1054. [DOI] [PubMed] [Google Scholar]
  30. Yu D. T., Ogasawara M., Hill J. L., Kono D. H. Study of Reiter's syndrome, with special emphasis on Yersinia enterocolitica. Immunol Rev. 1985 Aug;86:27–45. doi: 10.1111/j.1600-065x.1985.tb01136.x. [DOI] [PubMed] [Google Scholar]
  31. van Eden W., Hogervorst E. J., Hensen E. J., van der Zee R., van Embden J. D., Cohen I. R. A cartilage-mimicking T-cell epitope on a 65K mycobacterial heat-shock protein: adjuvant arthritis as a model for human rheumatoid arthritis. Curr Top Microbiol Immunol. 1989;145:27–43. doi: 10.1007/978-3-642-74594-2_3. [DOI] [PubMed] [Google Scholar]

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

RESOURCES