Differential cytokine expression in avian cells in response to invasion by Salmonella typhimurium, Salmonella enteritidis and Salmonella gallinarum.
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)-gamma were measured by quantitative RT-PCR, and production of IL-6 and IFN-gamma was also determined through bioassays. All serotypes were invasive and had little effect on the production of IFN-gamma 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.
Kaiser
Pete
P
Institute for Animal Health, Compton, Berkshire RG20 7NN, UK1.
Rothwell
Lisa
L
Institute for Animal Health, Compton, Berkshire RG20 7NN, UK1.
Galyov
Edouard E
EE
Institute for Animal Health, Compton, Berkshire RG20 7NN, UK1.
Barrow
Paul A
PA
Institute for Animal Health, Compton, Berkshire RG20 7NN, UK1.
Burnside
Joan
J
Department of Animal and Food Sciences, University of Delaware, 531 South College Avenue, Newark, DE 19717-1303, USA2.
Wigley
Paul
P
Institute for Animal Health, Compton, Berkshire RG20 7NN, UK1.
D000818:Animals; D001681:Biological Assay; D002460:Cell Line; D002478:Cells, Cultured; D002645:Chickens; D016207:Cytokines / Q000378:metabolism*; D007371:Interferon-gamma / Q000378:metabolism; D007375:Interleukin-1 / Q000378:metabolism; D007376:Interleukin-2 / Q000378:metabolism; D015850:Interleukin-6 / Q000235:genetics / Q000378:metabolism; D007668:Kidney / Q000166:cytology; D008262:Macrophage Activation; D008264:Macrophages / Q000276:immunology; D008969:Molecular Sequence Data; D020133:Reverse Transcriptase Polymerase Chain Reaction; D012475:Salmonella / Q000276:immunology / Q000472:pathogenicity*; D012477:Salmonella enteritidis / Q000276:immunology / Q000472:pathogenicity*; D012486:Salmonella typhimurium / Q000276:immunology / Q000472:pathogenicity*
D016207:Cytokines; D007375:Interleukin-1; D007376:Interleukin-2; D015850:Interleukin-6; D007371:Interferon-gamma