Rapid transepithelial antigen transport in rat jejunum: Impact of sensitization and the hypersensitivity reaction

Berin, M. Cecilia; Kiliaan, Amanda J.; Yang, Ping; Groot, J.A.; Taminiau, J. A. J. M.; Perdue, Mary H.

doi:10.1016/s0016-5085(97)70180-x

Cited by 146 publications

(141 citation statements)

References 3 publications

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“…These cells can use FcεRI receptor for capturing IgE-complexed Ag. More interestingly, the sensitization can increase uptake of specific Ag via an endosomal transcellular pathway across tracheal and jejunal epithelium (64,65). Furthermore, in vitro-formed IgE IC, when administered through the airways, are more potent than Ag alone in inducing airway inflammatory responses in mice previously sensitized with the Ag (66).…”

Section: Discussionmentioning

confidence: 99%

CD23-Dependent Transcytosis of IgE and Immune Complex across the Polarized Human Respiratory Epithelial Cells

Palaniyandi

Tomei

et al. 2011

The Journal of Immunology

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IgE-mediated allergic inflammation occurs when allergens cross-link IgE on the surface of immune cells, thereby triggering the release of inflammatory mediators as well as enhancing Ag presentations. IgE is frequently present in airway secretions, and its level can be enhanced in human patients with allergic rhinitis and bronchial asthma. However, it remains completely unknown how IgE appears in the airway secretions. In this study, we show that CD23 (FcεRII) is constitutively expressed in established or primary human airway epithelial cells, and its expression is significantly upregulated when airway epithelial cells were subjected to IL-4 stimulation. In a transcytosis assay, human IgE or IgE-derived immune complex (IC) was transported across a polarized Calu-3 monolayer. Exposure of the Calu-3 monolayer to IL-4 stimulation also enhanced the transcytosis of either human IgE or the IC. A CD23-specific Ab or soluble CD23 significantly reduced the efficiency of IgE or IC transcytosis, suggesting a specific receptor-mediated transport by CD23. Transcytosis of both IgE and the IC was further verified in primary human airway epithelial cell monolayers. Furthermore, the transcytosed Ag–IgE complexes were competent in inducing degranulation of the cultured human mast cells. Because airway epithelial cells are the first cell layer to come into contact with inhaled allergens, our study implies CD23-mediated IgE transcytosis in human airway epithelial cells may play a critical role in initiating and contributing to the perpetuation of airway allergic inflammation.

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Section: Discussionmentioning

confidence: 99%

CD23-Dependent Transcytosis of IgE and Immune Complex across the Polarized Human Respiratory Epithelial Cells

Palaniyandi

Tomei

et al. 2011

The Journal of Immunology

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“…Studies examining T cell activation in the GALT in response to OVA feeding have shown that T cell proliferation can be observed in both the MLN and the PP (31,32). Soluble Ags (such as OVA or HRP) can readily be taken up by epithelial cells (33)(34)(35)(36) and delivered to the MLN by DCs migrating from the lamina propria (28). In contrast, particulate Ags are preferentially taken up by M cells overlying the PP (37,38).…”

Section: Discussionmentioning

confidence: 99%

Gastrointestinal Dendritic Cells Promote Th2 Skewing via OX40L

Blázquez

Berin

2008

The Journal of Immunology

141

123

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Mice can be sensitized to food proteins by oral administration with the adjuvant cholera toxin (CT), such that they undergo anaphylaxis when rechallenged with the sensitizing allergen. In contrast, feeding of Ags alone leads to oral tolerance. Our aim was to define the mechanisms by which gastrointestinal dendritic cells (DCs) participate in the deviation of tolerance to allergic sensitization in the gut in response to CT. BALB/c mice were fed with CT or PBS. The impact of CT on DC subsets in the mesenteric lymph node (MLN) was assessed by flow cytometry. Ag presentation assays were performed with DCs isolated from the MLN of PBS- or CT-fed mice, using OVA-specific CD4+ T cells as responder cells. Gene expression in MLN DCs was determined by real-time PCR, and neutralizing Abs were used to test the function of OX40 ligand (OX40L) in Th2 skewing. Oral administration of CT induced an increase in the total CD11c+ population in the MLN. CT induced a selective increase in migration of the CD11c+CD11b−CD8α− DC subset and the maturation of all DC subsets. Maturation of DCs in vivo enhanced T cell proliferation and cytokine secretion. Oral CT induced up-regulation of Jagged-2 and OX40L by MLN DCs. Neutralizing anti-OX40L Abs completely abrogated the CT-induced Th2 cytokine response. We show that oral CT induces selective DC migration, maturation, and T cell priming activity in the MLN. Th2 skewing is mediated by OX40L, and we speculate that this molecule may be an important inducer of allergic sensitization to food allergens.

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“…13,32 Evidence has been provided that transepithelial transport of antigen in sensitized rodents is both faster and of greater magnitude because of its protected transcytosis within enterocyte endosomes. 31 Subsequent to mast cell activation, a sec- ond phase of enhanced transepithelial transport of antigen occurs because of loosening of intercellular tight junctions allowing additional intact antigen to move through the paracellular spaces. Here, we confirmed by HRP flux that the antigen was transported across the epithelium, both more rapidly and in larger quantity, in sensitized stressed rats than in naïve controls or in rats exposed to sham stress.…”

Section: Discussionmentioning

confidence: 99%

“…We previously showed in sensitized rodents that epithelial permeability is specifically enhanced for the antigen to which the animal has been sensitized; 31 this phenomenon is due to interleukin (IL)-4-up-regulated expression of CD23 (low-affinity IgE receptor) on epithelial cells, binding IgE antigen, and transporting the complex via endosomes across the cell (transcellular pathway). 33,34 Antigen delivered to the lamina propria then activates mast cells, and released mediators act on epithelial receptors to further increase permeability by loosening intercellular tight junctions (paracellular pathway).…”

Section: Transepithelial Antigen Transportmentioning

confidence: 99%

Chronic Psychological Stress in Rats Induces Intestinal Sensitization to Luminal Antigens

Yang

Jury

Söderholm

et al. 2006

The American Journal of Pathology

137

139

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There is increasing evidence that stress plays a role in the pathophysiology of chronic intestinal disorders, but the mechanisms remain unclear. Previous studies in rats have revealed that stress decreases gut barrier function and allows excessive uptake of luminal material. Here, we investigated whether chronic psychological stress acts to induce sensitization of intestinal tissues to oral antigens. Rats were subjected to 1 hour per day of water avoidance stress or sham stress daily for 10 days, and horseradish peroxidase (HRP) was delivered by gavage on day 5. Studies to determine sensitization were conducted on day 20. All stressed rats developed HRP-specific IgE antibodies, antigeninduced intestinal secretion, and increased numbers of inflammatory cells in gut mucosa. Luminal HRP was absorbed more readily by enterocytes of stressed animals. In addition, stressed rats had increased expression of interleukin-4 and decreased expression of interferon-␥ in gut mucosa, a cytokine profile that is typical of allergic conditions. Treatment of stressed rats with an antagonist to corticotropin-releasing hormone (previously shown to inhibit stress-enhanced gut permeability) eliminated the manifestations of intestinal hypersensitivity. Our results indicate that the presence of oral antigen during chronic psychological stress alters the immune response (to sensitization rather than oral tolerance) and causes subsequent antigen-induced gut pathophysiology. A number of publications 1-4 in recent years indicate that stress plays a role in gastrointestinal pathophysiology in conditions such as inflammatory bowel disease, irritable bowel syndrome (IBS), and food allergies. In inflammatory bowel disease and perhaps IBS, there is evidence that intestinal tissues may become sensitized to a luminal antigen and that subsequent encounter with the antigen initiates an inflammatory response that is involved in the pathophysiology of disease. [5][6][7][8][9] Although this theory remains controversial, it is clear that sensitization of intestinal tissues is a feature of food allergy. There is little information on the relationship between stress and intestinal anaphylaxis, although several reports indicate that psychological stress triggers allergic reactions in other organ systems.10 -12 With respect to detrimental reactions to oral antigens, immunogenic material must penetrate the intestinal epithelial barrier to contact and activate immune cells in the lamina propria. 13 In a sensitized host, immediate hypersensitivity reactions are initiated by antigen cross-linking of specific IgE antibodies bound to the surface of mucosal mast cells located in close proximity beneath the gut epithelium. Released mediators then act on nearby cells to induce both rapid (within minutes) changes in physiology and delayed (within hours to days) effects. 13,14 In allergic conditions in general, it is not clear how an individual develops sensitivity to a particular antigen. Genetic factors play a role, but persons can develop a hypersensitivity reaction ...

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Rapid transepithelial antigen transport in rat jejunum: Impact of sensitization and the hypersensitivity reaction

Cited by 146 publications

References 3 publications

CD23-Dependent Transcytosis of IgE and Immune Complex across the Polarized Human Respiratory Epithelial Cells

CD23-Dependent Transcytosis of IgE and Immune Complex across the Polarized Human Respiratory Epithelial Cells

Gastrointestinal Dendritic Cells Promote Th2 Skewing via OX40L

Chronic Psychological Stress in Rats Induces Intestinal Sensitization to Luminal Antigens

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