1887

Abstract

is a facultative intracellular pathogen that is capable of causing disease in a range of hosts. Although human salmonellosis is frequently associated with consumption of contaminated poultry and eggs, and the serotypes and are important world-wide pathogens of poultry, little is understood of the mechanisms of pathogenesis of in the chicken. Type III secretion systems play a key role in host cell invasiveness and trigger the production of pro-inflammatory cytokines during invasion of mammalian hosts. This results in a polymorphonuclear cell influx that contributes to the resulting enteritis. In this study, a chicken primary cell culture model was used to investigate the cytokine responses to entry by the broad host range serotypes and , and the host specific serotype , which rarely causes disease outside its main host, the chicken. The cytokines interleukin (IL)-1β, IL-2, IL-6 and interferon (IFN)-γ were measured by quantitative RT-PCR, and production of IL-6 and IFN-γ was also determined through bioassays. All serotypes were invasive and had little effect on the production of IFN-γ compared with non-infected cells; invasion caused a slight down-regulation of IL-2 production. For IL-1β production, infection with had little effect, whilst infection with or caused a reduction in IL-1β mRNA levels. Invasion of and caused an eight- to tenfold increase in production of the pro-inflammatory cytokine IL-6, whilst invasion by caused no increase. These findings correlate with the pathogenesis of in poultry. and invasion produces a strong inflammatory response, that may limit the spread of largely to the gut, whilst does not induce an inflammatory response and may not be limited by the immune system, leading to the severe systemic disease fowl typhoid.

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2000-12-01
2019-10-20
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References

  1. Baird, G. D., Manning, E. J. & Jones, P. W. ( 1985; ). Evidence for related virulence sequences in plasmids of Salmonella dublin and Salmonella typhimurium. J Gen Microbiol 131, 1815-1823.
    [Google Scholar]
  2. Barrow, P. A. ( 1996; ). Immunity to Salmonella and other bacteria. In Poultry Immunology: Poultry Science Symposium Series , pp. 243-263. Edited by T. F. Davison, T. R. Morris & L. N. Payne. Abingdon, UK:Carfax Publishing.
  3. Barrow, P. A. & Lovell, M. A. ( 1989; ). Invasion of Vero cells by Salmonella species. J Med Microbiol 28, 59-67.[CrossRef]
    [Google Scholar]
  4. Barrow, P. A. & Lovell, M. A. ( 1990; ). Experimental infection of egg-laying hens with Salmonella enteritidis phage type 4. Avian Pathol 20, 335-348.
    [Google Scholar]
  5. Barrow, P. A., Huggins, M. B., Lovell, M. A. & Simpson, J. M. ( 1987; ). Observations on the pathogenesis of experimental Salmonella typhimurium infection in chickens. Res Vet Sci 42, 194-199.
    [Google Scholar]
  6. Barrow, P. A., Huggins, M. B. & Lovell, M. A. ( 1994; ). Host specificity of Salmonella infection in chickens and mice is expressed in vivo primarily at the level of the reticuloendothelial system. Infect Immun 62, 4602-4610.
    [Google Scholar]
  7. Beug, H., von Kirchbach, A., Doderlein, G., Conscience, J.-F. & Graf, T. ( 1979; ). Chicken hematopoietic cells transformed by seven strains of defective avian leukemia viruses display three distinct phenotypes of differentiation. Cell 18, 375-390.[CrossRef]
    [Google Scholar]
  8. Darwin, K. H. & Miller, V. L. ( 1999; ). Molecular basis of the interaction of Salmonella with the intestinal mucosa. Clin Microbiol Rev 12, 405-428.
    [Google Scholar]
  9. Digby, M. R. & Lowenthal, J. W. ( 1995; ). Cloning and expression of the chicken interferon-γ gene. J Interferon Cytokine Res 15, 939-945.[CrossRef]
    [Google Scholar]
  10. Ding, A. H., Nathan, C. F. & Stuehr, D. J. ( 1988; ). Release of reactive nitrogen intermediates from mouse peritoneal macrophages: comparison of activating cytokines and evidence for independent production. J Immunol 141, 2407-2412.
    [Google Scholar]
  11. Eckman, L., Kagnoff, M. & Fierer, J. ( 1993; ). Epithelial cells secrete the chemokine interleukin-8 in response to bacterial entry. Infect Immun 61, 4569-4574.
    [Google Scholar]
  12. Galán, J. E. & Sansonetti, P. J. (1996). Molecular and cellular bases of Salmonella and Shigella interactions with hosts. In Escherichia coli and Salmonella: Cellular and Molecular Biology, pp. 2757–2773. Edited by F. C. Neidhardt and others. Washington DC: American Society for Microbiology.
  13. Hardt, W.-D. & Galán, J. E. ( 1997; ). A secreted Salmonella protein with homology to an avirulence determinant of plant-pathogenic bacteria. Proc Natl Acad Sci USA 94, 9887-9892.[CrossRef]
    [Google Scholar]
  14. Henderson, S. C., Bounous, D. I. & Lee, M. D. ( 1999; ). Early events in the pathogenesis of avian salmonellosis. Infect Immun 67, 3580-3586.
    [Google Scholar]
  15. Hirana, T. (1994). Interleukin-6. In The Cytokine Handbook, 2nd edn, pp. 145–168. Edited by A. Thomson. London: Academic Press.
  16. Humphrey, T. J. ( 1999; ). Contamination of meat and eggs with Salmonella enterica serotype Enteritidis. In Salmonella enteritica Serotype Enteritidis in Humans and Animals , pp. 183-192. Edited by A. M. Saeed. Ames, IA:Iowa State University Press.
  17. Kaiser, P. & Mariani, P. ( 1999; ). Promoter sequence, exon:intron structure, and synteny of genetic location show that a chicken cytokine with T-cell proliferative activity is IL2 and not IL15. Immunogenetics 49, 26-35.[CrossRef]
    [Google Scholar]
  18. Kaiser, P., Wain, H. M. & Rothwell, L. ( 1998; ). Structure of the chicken interferon-γ gene, and comparison to mammalian homologues. Gene 207, 25-32.[CrossRef]
    [Google Scholar]
  19. Kogut, M. H., McGruder, E. D., Hargis, B. M., Corrier, D. E. & DeLoach, J. R. ( 1994a; ). Dynamics of avian inflammatory response to Salmonella-immune lymphokines: changes in avian blood leukocyte populations. Inflammation 18, 373-388.[CrossRef]
    [Google Scholar]
  20. Kogut, M. H., McGruder, E. D., Hargis, B. M., Corrier, D. E. & DeLoach, J. R. ( 1994b; ). Characterization of the pattern of inflammatory cell influx in chicks following the intraperitoneal administration of live Salmonella enteritidis and Salmonella enteritidis-immune lymphokines. Poult Sci 74, 8-17.
    [Google Scholar]
  21. Kogut, M. H., Tellez, G. I., McGruder, E. D., Hargis, B. M., Williams, J. D., Corrier, D. E. & DeLoach, J. D. ( 1994c; ). Heterophils are decisive components in early responses of chickens to Salmonella enteritidis infections. Microb Pathog 16, 141-151.[CrossRef]
    [Google Scholar]
  22. Kogut, M. H., McGruder, E. D., Hargis, B. M., Corrier, D. E. & DeLoach, J. R. ( 1995; ). In vivo activation of heterophil function in chickens following injection with Salmonella enteritidis-immune lymphokines. J Leukoc Biol 57, 56-62.
    [Google Scholar]
  23. Lambrecht, B., Gonze, M., Meulemans, G. & van den Berg, T. P. ( 2000; ). Production of antibodies against chicken interferon-gamma: demonstration of neutralizing activity and development of a quantitative ELISA. Vet Immunol Immunopathol 74, 137-144.[CrossRef]
    [Google Scholar]
  24. Lowenthal, J. W., Digby, M. R. & York, J. J. ( 1995; ). Production of interferon-γ by chicken T cells. J Interferon Cytokine Res 15, 933-938.[CrossRef]
    [Google Scholar]
  25. Lynagh, G. R. (1998). The role of IL-6 in the immune response to coccidia. PhD thesis, University of Bristol.
  26. McCormick, B. A., Miller, S. I., Carnes, D. & Madara, J. L. ( 1995; ). Transepithelial signalling to neutrophils by salmonellae: a novel virulence mechanism for gastroenteritis. Infect Immun 63, 2302-2309.
    [Google Scholar]
  27. McCormick, B. A., Parkos, C. A., Colgan, S. P., Carnes, D. K. & Madara, J. L. ( 1998; ). Apical secretion of a pathogen-elicited epithelial chemoattractant activity in response to surface colonization of intestinal epithelia by Salmonella typhimurium. J Immunol 160, 455-466.
    [Google Scholar]
  28. Marriott, I., Hammond, T. G., Thomas, E. K. & Bost, K. L. ( 1999; ). Salmonella efficiently enter and survive within cultured CD11c+ dendritic cells initiating cytokine expression. Eur J Immunol 29, 1107-1115.[CrossRef]
    [Google Scholar]
  29. Mirold, S., Rabsch, W., Rohde, M., Stender, S., Tschäpe, H., Rüssmann, H., Igwe, E. & Hardt, W.-D. ( 1999; ). Isolation of a temperate bacteriophage encoding the type III effector protein SopE from an epidemic Salmonella typhimurium strain. Proc Natl Acad Sci USA 96, 9845-9850.[CrossRef]
    [Google Scholar]
  30. Moody, A., Sellers, S. & Bumstead, N. ( 2000; ). Measuring infectious bursal disease virus RNA in blood by multiplex real-time quantitative RT-PCR. J Virol Methods 85, 55-64.[CrossRef]
    [Google Scholar]
  31. Nagaraja, K. V., Pomeroy, B. S. & Williams, J. E. ( 1991; ). Paratyphoid infections. In Diseases of Poultry , pp. 99-130. Edited by B. W. Calnek. Ames, IA:University of Iowa Press.
  32. Nakamura, K., Mitarai, Y., Yoshioka, M., Koizumi, N., Shibahara, T. & Nakajima, Y. ( 1998; ). Serum levels of interleukin-6, alpha1-acid glycoprotein, and corticosterone in two-week-old chickens inoculated with Escherichia coli lipopolysaccharides. Poult Sci 77, 908-911.[CrossRef]
    [Google Scholar]
  33. Ochman, O. & Groisman, E. A. ( 1996; ). Distribution of pathogenicity islands in Salmonella spp. Infect Immun 64, 5410-5412.
    [Google Scholar]
  34. Pomeroy, B. S. & Nagaraja, K. V. ( 1991; ). Fowl typhoid. In Diseases of Poultry , pp. 87-98. Edited by B. W. Calnek. Ames, IA:University of Iowa Press.
  35. Smith, H. W. ( 1955; ). Observations on experimental fowl typhoid. J Comp Pathol 65, 37-54.[CrossRef]
    [Google Scholar]
  36. Smith, H. W. ( 1956; ). The susceptibility of different chicken breeds to Salmonella gallinarum infection. Poult Sci 35, 701-705.[CrossRef]
    [Google Scholar]
  37. Smith, H. W. ( 1978; ). Transmissible pathogenic characteristics of invasive strains of Escherichia coli. J Am Vet Med Assoc 172, 601-607.
    [Google Scholar]
  38. Smith, H. W. & Tucker, J. F. ( 1975; ). The effect of antibiotic therapy on the excretion of Salmonella typhimurium by experimentally infected chickens. J Hyg 75, 272-292.
    [Google Scholar]
  39. van Snick, J., Cayphas, S., Vink, A., Uyttenhove, C., Coulie, P. G., Rubira, M. R. & Simpson, R. J. ( 1986; ). Purification and NH2-terminal amino acid sequence of a T-cell-derived lymphokine with growth factor activity for B-cell hybridomas. Proc Natl Acad Sci USA 83, 9679-9683.[CrossRef]
    [Google Scholar]
  40. Snoeyenbos, G. H. ( 1991; ). Pullorum disease. In Diseases of Poultry , pp. 73-86. Edited by B. W. Calnek. Ames, IA:University of Iowa Press.
  41. Sundick, R. S. & Gill-Dixon, C. ( 1997; ). A cloned chicken lymphokine homologous to both mammalian IL-2 and IL-15. J Immunol 159, 720-725.
    [Google Scholar]
  42. Sung, Y.-J., Hotchkiss, J. H., Austric, R. E. & Dietert, R. R. ( 1991; ). l-Arginine dependent production of a reactive nitrogen intermediate by macrophages of a uricotelic species. J Leukoc Biol 50, 49-56.
    [Google Scholar]
  43. Wall, P. G. & Ward, L. R. ( 1999; ). Epidemiology of Salmonella enterica serotype Enteritidis Phage Type 4 in England and Wales. In Salmonella enterica Serotype Enteritidis in Humans and Animals , pp. 19-26. Edited by A. M. Saeed. Ames, IA:Iowa State University Press.
  44. Weining, K. C., Sick, C., Kaspers, B. & Staeheli, P. ( 1998; ). A chicken homologue of mammalian interleukin-1β: cDNA cloning and purification of active recombinant protein. Eur J Biochem 258, 994-1000.[CrossRef]
    [Google Scholar]
  45. Weinstein, D. L., O’Neil, B. L., Hone, D. M. & Metcalf, E. S. ( 1998; ). Differential early interactions between Salmonella enterica serotype Typhi and two other pathogenic Salmonella serotypes with intestinal epithelial cells. Infect Immun 66, 2310-2318.
    [Google Scholar]
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