Chicken innate immune response to oral infection with Salmonella enterica serovar Enteritidis

Marta Matulova,Karolina Varmuzova,Zbynek Zdrahal,Ivan Rychlik,Vladimir Babak,Frantisek Sisak,Hana Havlickova,Karel Stejskal

doi:10.1186/1297-9716-44-37

Abstract

The characterization of the immune response of chickens to Salmonella infection is usually limited to the quantification of expression of genes coding for cytokines, chemokines or antimicrobial peptides. However, processes occurring in the cecum of infected chickens are likely to be much more diverse. In this study we have therefore characterized the transcriptome and proteome in the chicken cecum after infection with Salmonella Enteritidis. Using a combination of 454 pyrosequencing, protein mass spectrometry and quantitative real-time PCR, we identified 48 down- and 56 up-regulated chicken genes after Salmonella Enteritidis infection. The most inducible gene was that coding for MMP7, exhibiting a 5952 fold induction 9 days post-infection. An induction of greater than 100 fold was observed for IgG, IRG1, SAA, ExFABP, IL-22, TRAP6, MRP126, IFNγ, iNOS, ES1, IL-1β, LYG2, IFIT5, IL-17, AVD, AH221 and SERPIN B. Since prostaglandin D2 synthase was upregulated and degrading hydroxyprostaglandin dehydrogenase was downregulated after the infection, prostaglandin must accumulate in the cecum of chickens infected with Salmonella Enteritidis. Finally, above mentioned signaling was dependent on the presence of a SPI1-encoded type III secretion system in Salmonella Enteritidis. The inflammation lasted for 2 weeks after which time the expression of the “inflammatory” genes returned back to basal levels and, instead, the expression of IgA and IgG increased. This points to an important role for immunoglobulins in the restoration of homeostasis in the cecum after infection.

Highlights

Salmonella enterica is one of the most frequent causative agents of human gastrointestinal disorders with the major sources of S. enterica isolates for the human population originating from farm animal production, pigs and poultry in particular
After applying all the quality selective criteria, 35 457 reads from the cecum of the non-infected chicken and 29 586 reads from the cecum of the infected chicken were included in the quantification of gene expression and we predicted that 54 genes might be downregulated and 78 genes upregulated in the cecum after Salmonella Enteritidis infection (Additional file 1)
Out of 9 genes downregulated after Salmonella Enteritidis infection expression of which we characterised in detail, 15hydroxyprostaglandin dehydrogenase (HPGD) might be directly involved in host defense. 15-hydroxyprostaglandin dehydrogenase is an enzyme involved in the inactivation of prostaglandin D2

Summary

Introduction

Salmonella enterica is one of the most frequent causative agents of human gastrointestinal disorders with the major sources of S. enterica isolates for the human population originating from farm animal production, pigs and poultry in particular. As poultry is a major source of Salmonella Enteritidis for humans, it is believed that the measures applied in chicken egg production, which will lead to a decrease of Salmonella Enteritidis prevalence, will affect the incidence of salmonellosis in the human population. The production of the above cytokines is either induced in epithelial cells and resident phagocytes, or is affected by infiltrating phagocytes or lymphocytes [6] This is clearly a simplified and an incomplete view of the chicken’s response to Salmonella infection as, for example, in mice genes not involved in cytokine signaling, e.g., Lcn, are induced in the small intestine upon infection with Salmonella enterica serovar Typhimurium [7]. When we tested whether these genes were induced in the cecum, 14 of them were upregulated in the cecum of orally infected chickens, one of them being a functional homologue of murine Lcn2 [6]

Methods

Results

Conclusion