Salmonella enterica serovar Choleraesuis infection of the porcine jejunal Peyer's patch rapidly induces IL-1β and IL-8 expression

Abstract

Salmonella enterica serovar Choleraesuis is an enteric pathogen of swine, producing septicemia, enterocolitis, pneumonia, and hepatitis. The initial molecular events at the site of Salmonella infection are hypothesized to be critical in the initiation of innate and adaptive immune responses; however the acute immune response elicited by porcine intestinal tissues is not well understood. To address this need, we employed explants of jejunal Peyer's patch (JPP) mucosa from pigs to examine Salmonella-induced immune responses under controlled conditions as well as to overcome limitations of whole animal approaches. JPP explants mounted in Ussing chambers maintained normal histological structure for 2 h and stable short-circuit current and electrical conductance for 2.5 h. After ex vivo luminal exposure to Salmonella serovar Choleraesuis, JPP responded with an increase in mRNA expression of IL-1β and IL-8, but not TNFα. Increased IL-1β and IL-8 expression were dependent on efficient Salmonella adhesion and internalization, whereas mutant Salmonella did not induce inflammatory cytokine expression. Commensal enteric bacteria, present in some experiments, also did not induce inflammatory cytokine expression. These findings indicate that Salmonella uptake by Peyer's patch is important in the induction of an innate response involving expression of IL-1β and IL-8, and that ex vivo intestinal immune tissue explants provide an intact tissue model that will facilitate investigation of mucosal immunity in swine.Keywords animal models; swine; cytokines; interleukins; mucosal immunology IntroductionSalmonella enterica represents a serologically diverse group of enteric pathogens capable of infecting both animals and humans. Salmonella serovar Choleraesuis is a major enteric pathogen in swine which produces septicemia, enterocolitis, pneumonia, and hepatitis, and is a common cause of systemic disease (Schwartz, 1999). Ingested Salmonella invade epithelial cells of the small intestine, including those of the gut-associated lymphoid tissue (GALT). Peyer's patches and mesenteric lymph nodes constitute a part of the organized GALT which provides specific, acquired immune defense against bacterial pathogens (Mowat, 2003).*To whom correspondence should be addressed at: Department of Veterinary and Biomedical Sciences, University of Minnesota, 1971 Commonwealth Avenue, St. Paul, MN 55108, USA. Tel: 612-625-6735, Fax: 612-625-5203, email: murta001@umn.edu Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. To date, the innate mucosal immune response to Salmonella has not been described in pig...

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