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Differential cytokine expression in avian cells in response to invasion by Salmonella typhimurium, Salmonella enteritidis and Salmonella gallinarum

Institute for Animal Health, Compton, Berkshire RG20 7NN, UK¹
Department of Animal and Food Sciences, University of Delaware, 531 South College Avenue, Newark, DE 19717-1303, USA²

Author for correspondence: Paul Wigley. Tel: +44 116 255 1551. Fax: +44 116 257 7631. e-mail: Microwig{at}aol.com

Salmonella enterica 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 Salmonella gallinarum and Salmonella pullorum are important world-wide pathogens of poultry, little is understood of the mechanisms of pathogenesis of Salmonella 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 S. enteritidis and S. typhimurium, and the host specific serotype S. gallinarum, which rarely causes disease outside its main host, the chicken. The cytokines interleukin (IL)-1ß, IL-2, IL-6 and interferon (IFN)- were measured by quantitative RT-PCR, and production of IL-6 and IFN- was also determined through bioassays. All serotypes were invasive and had little effect on the production of IFN- compared with non-infected cells; S. enteritidis invasion caused a slight down-regulation of IL-2 production. For IL-1ß production, infection with S. typhimurium had little effect, whilst infection with S. gallinarum or S. enteritidis caused a reduction in IL-1ß mRNA levels. Invasion of S. typhimurium and S. enteritidis caused an eight- to tenfold increase in production of the pro-inflammatory cytokine IL-6, whilst invasion by S. gallinarum caused no increase. These findings correlate with the pathogenesis of Salmonella in poultry. S. typhimurium and S. enteritidis invasion produces a strong inflammatory response, that may limit the spread of Salmonella largely to the gut, whilst S. gallinarum does not induce an inflammatory response and may not be limited by the immune system, leading to the severe systemic disease fowl typhoid.

Keywords: Salmonella, cytokines, interleukin-6, chicken, inflammatory response

Abbreviations: CKC, chick kidney cells; CM, conditioned medium; C_t, threshold cycle value; DMEM, Dulbecco’s modified Eagle’s medium; FAM, 5-carboxyfluorescein; FBS, foetal bovine serum; IFN, interferon; IL, interleukin; PMN, polymorphonuclear cell; P/S, penicillin and streptomycin; rm, recombinant murine; TAMRA, N,N,N,N'-tetramethyl-6-carboxyrhodamine

The GenBank accession numbers for the sequences reported in this paper are AI982185 for chicken IL-6 cDNA and AJ250838 for the partial chicken IL-6 genomic sequence, respectively.

^a Present address: School of Pharmacy and Pharmaceutical Sciences, DeMontfort University, Leicester LE1 9BH, UK.

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