Neuromodulation of enteropathogen internalization in Peyer's patches from porcine jejunum

Green, Benedict T.; Lyte, Mark; Kulkarni-Narla, Anjali; Brown, David R.

doi:10.1016/s0165-5728(03)00225-x

Cited by 86 publications

(61 citation statements)

References 36 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The abundant innervation of the spleen and Peyer's patches provides the anatomical basis for the interaction between the nervous and immune systems. For example, norepinephrine-containing nerve fibers localized in Peyer's patches modulate the internalization of pathogenic Salmonella choleraesuis into isolated jejunal Peyer's patches (28). However, there are no neural pathways directly connecting the hypothalamus with the Peyer's patches and spleen.…”

Section: Fig 4 Persistence Of Serovar Typhimurium Infection Inmentioning

confidence: 99%

Hypophysectomy and Neurointermediate Pituitary Lobectomy Reduce Serum Immunoglobulin M (IgM) and IgG and Intestinal IgA Responses toSalmonella entericaSerovar Typhimurium Infection in Rats

et al. 2006

View full text Add to dashboard Cite

The influence of anterior pituitary hormones on the gastrointestinal tract of humans and animals has been reported. Hypophysectomy (HYPOX) in the rat causes atrophy of the intestinal mucosa, reduction of gastric secretion and intestinal absorption, and increased susceptibility to infections. To our knowledge, there are no studies on the humoral immune response of the gut-associated lymphoid tissue after HYPOX. We have reported that decreased secretion of vasopressin and oxytocin due to neurointermediate pituitary lobectomy (NIL) diminishes humoral and cell-mediated immune responses. However, no data have been published on whether NIL can affect intestinal immune responses. We analyzed the effects of HYPOX and NIL on bacterial colonization of the intestinal lumen, Peyer's patches, and spleen as well as the serum immunoglobulin G (IgG) and IgM and specific intestinal IgA levels in response to Salmonella enterica serovar Typhimurium oral infection. Results showed the following: (i) Salmonella serovar Typhimurium was eliminated from the intestinal lumen at the same rate in rats that underwent a sham operation, HYPOX, and NIL; (ii) Salmonella serovar Typhimurium colonization of Peyer's patches and spleen was significantly higher in both HYPOX and NIL rats than in sham-operated rats; (iii) serum IgG and IgM and intestinal IgA against surface proteins of Salmonella serovar Typhimurium were significantly lower in HYPOX and NIL rats than in sham-operated rats; and (iv) compared to NIL rats, higher Peyer's patch and spleen bacterial colonization and decreased IgG, IgM, and IgA production were observed in HYPOX rats. We conclude that hormones from each pituitary lobe affect the systemic and gastrointestinal humoral immune responses through different mechanisms.Multidirectional interactions between nervous, endocrine, and immune systems in health and in the course of inflammatory and infectious diseases have been well established (5). The central nervous system (CNS) signals to the immune system via hormonal and neural pathways, and the immune system signals to the CNS through various cytokines. The CNS regulates the immune system via pituitary hormones, mainly growth hormone (GH) and prolactin (PRL), which are immunostimulatory (6,7,8,37,44,45,46), and the hypothalamic-pituitaryadrenocortical (HPA) axis, which inhibits immune responses and acts as an immunomodulator-immunosuppressor (16,61,67,68). Whereas most information regarding these interactions is related to systemic immune responses (6,7,16,37,46,61,67,68), much less is known about the interactions between the hypothalamus, the pituitary, and local gastrointestinal immune reactions (9,43,49).

show abstract

Section: Fig 4 Persistence Of Serovar Typhimurium Infection Inmentioning

confidence: 99%

Hypophysectomy and Neurointermediate Pituitary Lobectomy Reduce Serum Immunoglobulin M (IgM) and IgG and Intestinal IgA Responses toSalmonella entericaSerovar Typhimurium Infection in Rats

et al. 2006

View full text Add to dashboard Cite

show abstract

“…NE is taken up by E. coli (23) and stimulates the in vitro expression of the K99 pilus adhesin by enterotoxigenic E. coli (27) as well as growth, iron acquisition, motility, and the expression of Shiga-like toxins and LEE-encoded proteins by EHEC O157:H7 (16,29,30,39). NE also augments the adherence of E. coli O157:H7 to murine cecal explants in vitro (5) and the invasion of the porcine jejunal mucosa (18). NEcontaining neurons innervate all levels of the gastrointestinal tract and terminate in neural plexuses and the mucosa (24).…”

mentioning

confidence: 99%

The Neuroendocrine Stress Hormone Norepinephrine Augments Escherichia coli O157:H7-Induced Enteritis and Adherence in a Bovine Ligated Ileal Loop Model of Infection

et al. 2004

Self Cite

View full text Add to dashboard Cite

The role of the neuroendocrine environment in the pathogenesis of enteric bacterial infections is increasingly being recognized. Here we report that norepinephrine augments Escherichia coli O157:H7-induced intestinal inflammatory and secretory responses as well as bacterial adherence to intestinal mucosa in a bovine ligated ileal loop model of infection. Norepinephrine modulation of enteritis and adherence was dependent on the ability of E. coli O157:H7 to form attaching and effacing lesions.Enterohemorrhagic Escherichia coli (EHEC) causes acute gastroenteritis in humans that may be complicated by lifethreatening systemic sequelae depending on serotype-and host-specific factors (35). EHEC strains are defined by their ability to produce one or more Shiga-like toxins and to induce characteristic attaching and effacing (A/E) lesions on intestinal epithelia (33). A/E lesion formation relies on the injection of bacterial effectors via a type III secretion system and is determined by the locus of enterocyte effacement (LEE) (14). The LEE-encoded adhesin intimin is required for the colonization of calves and adult cattle by E. coli O157:H7 (6, 8) and for the colonization of humans by enteropathogenic E. coli (EPEC) (11). Type III secreted proteins also mediate the intestinal colonization of calves by EHEC serotypes O157:H7 and O26:H Ϫ (F. Dziva, P. van Diemen, M. Stevens, and T. Wallis, unpublished data), and EspB is required for the carriage and virulence of EPEC in humans (42).The host factors contributing to the colonization of ruminants and humans by EHEC are poorly understood. Recent studies have suggested that the neuroendocrine environment in the gastrointestinal tract may influence the outcome of infection, since the expression of virulence factors by diarrheagenic E. coli is augmented in vitro by the hormone norepinephrine (NE), which is released by the enteric nervous system under stress (3). NE is taken up by E. coli (23) and stimulates the in vitro expression of the K99 pilus adhesin by enterotoxigenic E. coli (27) as well as growth, iron acquisition, motility, and the expression of Shiga-like toxins and LEE-encoded proteins by EHEC O157:H7 (16,29,30,39). NE also augments the adherence of E. coli O157:H7 to murine cecal explants in vitro (5) and the invasion of the porcine jejunal mucosa (18). NEcontaining neurons innervate all levels of the gastrointestinal tract and terminate in neural plexuses and the mucosa (24). The influence of NE released into the gut on the carriage and virulence of gram-negative bacterial pathogens in vivo has received little attention to date.We have examined the effect of NE on the adherence and enteropathogenicity of E. coli O157:H7 in a bovine ligated ileal loop model of infection. This model permits the simultaneous testing of different treatments in discrete segments of the midileum for their effect on bacterial adherence and the induction of intestinal inflammatory and secretory responses (40). All animal procedures were performed in accordance with the Animals (Scientific P...

show abstract

“…Brown, unpublished observations). Exposure of porcine JPP to Salmonella serovar Choleraesuis strain SC-54 also did not significantly alter tissue conductance (Green et al, 2003). Comparisons of Salmonella serovars Choleraesuis, Typhimurium and Dublin exposure to porcine ligated intestinal loops indicated that serovar Dublin induced maximum tissue damage, while serovar Typhimurium induced greater amounts of epithelial swelling than serovar Choleraesuis (Bolton et al, 1999;Meyerholz and Stabel, 2003).…”

Section: Discussionmentioning

confidence: 86%

“…To quantitate intracellular bacteria, the follicle-containing region of the tissue was incubated at 37°C under 5% CO 2 in PBS containing 100 µg/ml gentamicin for 80 min to kill extracellular bacteria (Elsinghorst, ;Green et al, 2003). For assessment of total bacteria (adherent and intracellular), the follicle-containing JPP tissue was washed in three separate aliquots of PBS.…”

Section: Bacterial Quantitationmentioning

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

Self Cite

View full text Add to dashboard Cite

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...

show abstract

Neuromodulation of enteropathogen internalization in Peyer's patches from porcine jejunum

Cited by 86 publications

References 36 publications

Hypophysectomy and Neurointermediate Pituitary Lobectomy Reduce Serum Immunoglobulin M (IgM) and IgG and Intestinal IgA Responses toSalmonella entericaSerovar Typhimurium Infection in Rats

Hypophysectomy and Neurointermediate Pituitary Lobectomy Reduce Serum Immunoglobulin M (IgM) and IgG and Intestinal IgA Responses toSalmonella entericaSerovar Typhimurium Infection in Rats

The Neuroendocrine Stress Hormone Norepinephrine Augments Escherichia coli O157:H7-Induced Enteritis and Adherence in a Bovine Ligated Ileal Loop Model of Infection

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

Contact Info

Product

Resources

About