Tumor necrosis factor-α mediates the early pathology in Salmonella infection of the gastrointestinal tract

Arnold, J. W.; Niesel, David W.; Annable, C R; Hess, Cynthia B.; Asuncion, Maria; Cho, Yang Ja; Peterson, Johnny W.; Klimpel, Gary R.

doi:10.1006/mpat.1993.1021

Cited by 75 publications

(55 citation statements)

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“…These groups also exhibited a more extensive inflammatory cell infiltrate in the muscle layer. Similar morphological changes in the intestinal tract have been observed during Salmonella typhimurium infections, which include generalized tissue inflammation, edema, and changes in mucin production (45). It has been proposed that TNF-␣ mediates tissue damage, cachexia, loss of mucus production, and death caused by bacterial septicemia (46).…”

Section: Discussionmentioning

confidence: 76%

IL-10 Is Critical for Host Resistance and Survival During Gastrointestinal Helminth Infection

Schopf

Hoffmann

Cheever

et al. 2002

The Journal of Immunology

198

168

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Resistance to many intestinal nematodes is dependent on the induction of polarized type 2 cytokine responses, whereas type 1 responses can exacerbate these infections. The contributions of IL-4 and IL-13 to the development of resistance have been well described for a variety of intestinal parasites; however, the role of IL-10 has not been previously investigated. In this study we infected IL-10-, IL-10/IL-4-, IL-10/IL-12-, IL-4-, and IL-12-deficient mice with Trichuris muris to determine whether IL-10 contributes to the development of immunity. Interestingly, T. muris-infected IL-10-, IL-4-, and IL-10/IL-4-deficient mice failed to expel the parasite, and animals deficient in IL-10 displayed marked morbidity and mortality. In contrast, double IL-10/IL-12-deficient mice were completely resistant and mounted a highly polarized type 2 cytokine response, demonstrating that the increased susceptibility of IL-10-deficient mice was dependent on IL-12. Further study suggested that the susceptibility of IL-10- and IL-10/IL-4-deficient mice was probably attributable to a marked increase in type 1 cytokine production in those animals. The mortality observed in T. muris-infected IL-10- and IL-10/IL-4-deficient mice correlated with increased inflammation, loss of Paneth cells, and absence of mucus in the cecum. Interestingly, survival was enhanced in T. muris-infected IL-10/IL-4-deficient mice if a broad spectrum antibiotic was administered, suggesting that an outgrowth of opportunistic bacteria was contributing to the high degree of morbidity and mortality. Overall, these studies reveal a critical role for IL-10 in the polarization of Th2 responses, development of resistance during T. muris infection, and maintenance of barrier function in the colon.

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Section: Discussionmentioning

confidence: 76%

IL-10 Is Critical for Host Resistance and Survival During Gastrointestinal Helminth Infection

Schopf

Hoffmann

Cheever

et al. 2002

The Journal of Immunology

198

168

View full text Add to dashboard Cite

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“…Despite the differences in the inflammatory responses observed in the intestines of mice and humans, murine ligated ileal loops have been used as a model to assess the contribution of putative virulence factors to the pathogenesis of Salmonella serotype Typhimurium-induced diarrhea (13). Since the infiltrate elicited by Salmonella serotype Typhimurium in murine ligated ileal loops is composed predominantly of mononuclear cells (2), this model is of questionable relevance for studying the pathogenesis of enterocolitis. In contrast, infection of rabbit ligated ileal loops with Salmonella serotype Typhimurium results in an infiltrate which contains neutrophils as the predominant cell type (19,32,33,104,106).…”

Section: The Use Of Animal Models To Study Enterocolitismentioning

confidence: 99%

Molecular Pathogenesis ofSalmonella entericaSerotype Typhimurium-Induced Diarrhea

et al. 2003

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“…Salmonella-mediated induction of IL-1β and IL-8 has been demonstrated in epithelial cell lines and in the jejunum of chickens, which do not have Peyer's patches (McCormick et al, 1993;Withanage et al, 2004;Zeng et al, 2003). Salmonella serovar Typhimurium infection of ligated intestinal loops in mice increases mRNA levels of IL-1, TNFα, and IL-6 along with secretion of TNFα protein (Arnold et al, 1993;Klimpel et al, 1995). However, in this study, TNFα mRNA levels were not significantly increased after ex vivo infection, indicating that TNFα may not be as critical to the early response to Salmonella in pigs as it is in mice.…”

Section: Discussionmentioning

confidence: 99%

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

Hyland

Brown

Murtaugh

2006

Veterinary Immunology and Immunopathology

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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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Tumor necrosis factor-α mediates the early pathology in Salmonella infection of the gastrointestinal tract

Cited by 75 publications

References 0 publications

IL-10 Is Critical for Host Resistance and Survival During Gastrointestinal Helminth Infection

IL-10 Is Critical for Host Resistance and Survival During Gastrointestinal Helminth Infection

Molecular Pathogenesis ofSalmonella entericaSerotype Typhimurium-Induced Diarrhea

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

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