1887

Abstract

The survival and fate of serotype Enteritidis in Henle-407 human intestinal epithelial cells was investigated during prolonged incubation to evaluate the persistence of causative microbes and the relationship to patients developing reactive arthritis. Most of the bacteria were killed and degraded quite soon after infection of the cells, but there were still live bacteria inside the cells for up to 14 days. These results suggest that in patients developing reactive arthritis the salmonellae could persist in the epithelial cells and spread within the host to the joint and be present there at the time of the inflammatory response. Production of marked amounts of nitric oxide was observed as a novel response to salmonella infection in human intestinal epithelial cells. The present experimental procedure appears to be a suitable model to further investigate host-bacteria interaction in HLA-B27 positive cells from patients developing reactive arthritis.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/00222615-45-6-463
1996-12-01
2024-12-04
Loading full text...

Full text loading...

/deliver/fulltext/jmm/45/6/medmicro-45-6-463.html?itemId=/content/journal/jmm/10.1099/00222615-45-6-463&mimeType=html&fmt=ahah

References

  1. Hook W. E. Salmonella species (including typhoid fever). In Mandell G. L., Douglas R. G., Bennett J. E. (eds) Principles and practice of infectious diseases New York: Churchill Livingstone; 19901700–1716
    [Google Scholar]
  2. Altmeyer R. M., McNem J. K., Bossio J. C., Rosenshine I., Finlay B. B., Galán J. E. Cloning and molecular characterization of a gene involved in Salmonella adherence and invasion of cultured epithelial cells. Mol Microbiol 1993; 7:89–98
    [Google Scholar]
  3. Elsinghorst E. A., Baron L. S., Kopecko D. J. Penetration of human intestinal epithelial cells by Salmonella: molecular cloning and expression of Salmonella typhi invasion determinants in Escherichia coli . Proc Natl Acad Sci USA 1989; 86:5173–5177
    [Google Scholar]
  4. Finlay B. B., Stambach M. N., Francis C. L. Identification and characterization of TnphoA mutants of Salmonella that are unable to pass through a polarized MDCK epithelial cell monolayer. Mol Microbiol 1988; 2:757–766
    [Google Scholar]
  5. Galán J. E., Curtiss R. III. Cloning and molecular characterization of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells. Proc Natl Acad Sci USA 1989; 86:6383–6387
    [Google Scholar]
  6. Lee C. A., Jones B. D., Falkow S. Identification of a Salmonella typhimurium invasion locus by selection for hyperinvasive mutants. Proc Natl Acad Sci USA 1992; 89:1847–1851
    [Google Scholar]
  7. Ginocchio C., Pace J., Galán J. E. Identification and molecular characterization of a Salmonella typhimurium gene involved in triggering the internalization of Salmonellae into cultured epithelial cells. Proc Natl Acad Sci USA 1992; 89:5976–5980
    [Google Scholar]
  8. Finlay B. B., Falkow S. Salmonella interactions with polarized human intestinal Caco-2 epithelial cells. J Infect Dis 1990; 162:1096–1106
    [Google Scholar]
  9. Francis C. L., Ryan T. A., Jones B. D., Smith S. J., Falkow S. Ruffles induced by Salmonella and other stimuli direct macropinocytosis of bacteria. Nature 1993; 364:639–642
    [Google Scholar]
  10. Ginocchio C. C., Olmsted S. B., Wells C. L., Galán J. E. Contact with epithelial cells induces the formation of surface appendages on Salmonella typhimurium . Cell 1994; 76:717–724
    [Google Scholar]
  11. Zierler M. K., Galán J. E. Contact with cultural epithelial cells stimulates secretion of Salmonella typhimurium invasion protein InvJ. Infect Immun 1995; 63:4024–4028
    [Google Scholar]
  12. Gahring L. C., Heffron F., Finlay B. B., Falkow S. Invasion and replication of Salmonella typhimurium in animal cells. Infect Immun 1990; 58:443–448
    [Google Scholar]
  13. Leung K. Y., Ruschkowski S. R., Finlay B. B. Isolation and characterization of the addA aminoglycoside-resistance gene from Salmonella choleraesuis . Mol Microbiol 1992; 6:2453–2460
    [Google Scholar]
  14. Stenger S., Thüring H., Röllinghoff M., Bogdan C. Tissue expression of inducible nitric oxide synthase is closely associated with resistance to Leishmania major . J Exp Med 1994; 180:783–793
    [Google Scholar]
  15. Denis M. Interferon-gamma-treated murine macrophages inhibit growth of tubercle bacilli via the generation of reactive nitrogen intermediates. Cell Immunol 1991; 132:150–157
    [Google Scholar]
  16. Rockett K. A., Awburn M. M., Cowden W. B., Clark I. A. Killing of Plasmodium falciparum in vitro by nitric oxide derivatives. Infect Immun 1991; 59:3280–3283
    [Google Scholar]
  17. Ignarro L. J., Buga G. M., Wood K. S., Byrns R. E., Chaudhuri G. Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc Natl Acad Sci USA 1987; 84:9265–9269
    [Google Scholar]
  18. Zembala M., Siedlar M., Marcinkiewicz J., Pryjma J. Human monocytes are stimulated for nitric oxide release in vitro by some tumor cells but not by cytokines and lipopolysaccharide. Eur J Immunol 1994; 24:435–439
    [Google Scholar]
  19. McCartney-Francis N., Allen J. B., Mizel D. E. Suppression of arthritis by an inhibitor of nitric oxide synthase. J Exp Med 1993; 178:749–754
    [Google Scholar]
  20. Assreuy J., Cunha F. Q., Epperlein M. Production of nitric oxide and superoxide by activated macrophages and killing of Leishmania major . Eur J Immunol 1994; 24:672–676
    [Google Scholar]
  21. Middleton S. J., Shorthouse M., Hunter J. O. Increased nitric oxide synthesis in ulcerative colitis. Lancet 1993; 341:465–466
    [Google Scholar]
  22. Boughton-Smith N. K., Evans S. M., Hawkey C. J. Nitric oxide synthase activity in ulcerative colitis and Crohn’s disease. Lancet 1993; 342:338–340
    [Google Scholar]
  23. Lundberg J. O. N., Farkas-Szallasi T., Weitzberg E. High nitric oxide production in human paranasal sinuses. Nat Med 1995; 1:370–373
    [Google Scholar]
  24. Mäki-Ikola O., Granfors K. The bacteriology of reactive arthritis. Rev Med Microbiol 1993; 4:144–150
    [Google Scholar]
  25. Inman R. D., Chui B., Johnston M. E. A., Vas S., Falk J. HLA class I-related impairment in IL-2 production and lymphocyte response to microbial antigens in reactive arthritis. J Immunol 1989; 142:4256–4260
    [Google Scholar]
  26. Mäki-Ikola O., Leirisalo-Repo M., Kantele A., Toivanen P., Granfors K. Salmonella-specific antibodies in reactive arthritis. J Infect Dis 1991; 164:1141–1148
    [Google Scholar]
  27. Kusters J. K., Mulders-Kremers G. A. W. M., van Doomik C. E. M., van der Zeijst B. A. M. Effects of multiplicity of infection, bacterial protein synthesis, and growth phase on adhesion to and invasion of human cell lines by Salmonella typhimurium . Infect Immun 1993; 61:5013–5020
    [Google Scholar]
  28. Granfors K., Jalkanen S., Lindberg A. A. Salmonella lipopolysaccharide in synovial fluid cells from patients with reactive arthritis. Lancet 1990; 335:685–688
    [Google Scholar]
  29. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227:680–685
    [Google Scholar]
  30. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 1979; 76:4350–4354
    [Google Scholar]
  31. Salomonsen J., Skojdt K., Crone M., Simonsen M. The chicken erythrocyte-specific MHC antigen. Characterization and purification of the B-G antigen by monoclonal antibodies. Immunogenetics 1987; 25:373–382
    [Google Scholar]
  32. Ding A. H., Nathan C. F., Stuehr D. J. Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages. Comparison of activating cytokines and evidence for independent production. J Immunol 1988; 141:2407–2412
    [Google Scholar]
  33. Hoogkamp-Korstanje J., de Koning J., Heesemann J. Persistence of Yersinia enterocolitica in man. Infection 1988; 16:81–85
    [Google Scholar]
  34. Francis C. L., Stambach M. N., Falkow S. Morphological and cytoskeletal changes in epithelial cells occur immediately upon interaction with Salmonella typhimurium grown under low-oxygen conditions. Mol Microbiol 1992; 6:3077–3087
    [Google Scholar]
  35. Drevets D. A., Canono B. P., Leenen P. J. M., Campbell P. A. Gentamicin kills intracellular Listeria monocytogenes . Infect Immun 1994; 62:2222–2228
    [Google Scholar]
  36. Garciadel Portillo F., Finlay B. B. Salmonella invasion of nonphagocytic cells induces formation of macropinosomes in the host cell. Infect Immun 1994; 62:4641–4645
    [Google Scholar]
  37. Tepperman B. L., Brown J. F., Whittle B. J. R. Nitric oxide synthase induction and intestinal epithelial cell viability in rats. Am J Physiol 1993; 265:G214–218
    [Google Scholar]
/content/journal/jmm/10.1099/00222615-45-6-463
Loading
/content/journal/jmm/10.1099/00222615-45-6-463
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error