Role of mast cells in chronic stress induced colonic epithelial barrier dysfunction in the rat

Santos, Javier; Yang, Ping; Söderholm, Johan D.; Benjamin, Michelle; Perdue, M.H.

doi:10.1136/gut.48.5.630

Cited by 266 publications

(256 citation statements)

References 45 publications

(45 reference statements)

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“…In two recent studies (29,33), our laboratory found that rats exposed to chronic stress develop a prolonged barrier defect to macromolecules and epithelial mitochondrial damage (29). Longer exposure to stress induces bacterial internalization into the epithelium and inflammatory cell infiltration in the lamina propria, suggesting that stress can be important in the initiation of intestinal inflammation (33).…”

Section: Discussionmentioning

confidence: 99%

“…Quantitative analysis of HRP uptake in intracellular endosomes and paracellular HRP transport were performed on coded high-magnification photomicrographs, 12 per rat (3 rats/group). The total area of HRP-containing endosomes within colonocytes was determined in an area of 300 m 2 in the apical region of the cells, by using a computerized image analysis system (Kontron Mop Videoplan, Kontron, Eching, Germany) (28,29).…”

Section: Epithelial Uptake Of Hrpmentioning

confidence: 99%

See 1 more Smart Citation

Neonatal maternal separation predisposes adult rats to colonic barrier dysfunction in response to mild stress

Söderholm¹,

Yates²,

Gareau³

et al. 2002

American Journal of Physiology-Gastrointestinal and Liver Physi

207

206

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. Neonatal maternal separation predisposes adult rats to colonic barrier dysfunction in response to mild stress. Am J Physiol Gastrointest Liver Physiol 283: G1257-G1263, 2002. First published August 28, 2002 10.1152/ajpgi.00314.2002Intestinal dysfunction is related to stress and early life events, but the mechanisms are largely unknown. Our aim was to determine whether early trauma predisposes adult rats to intestinal mucosal dysfunction in response to stress. Neonatal Sprague-Dawley rats were individually separated from their mothers for 3 h/day at 4-21 days of age. Between days 80 and 90, separated and control rats were subjected to mild acute stress (30-min water avoidance) or sham stress. Mucosal barrier function and ion transport were assessed in colonic tissues mounted in Ussing chambers. Mild stress increased short-circuit current, conductance, and transepithelial transport of macromolecules in separated rats, while having minimal effects in controls. Pretreatment of the separated rats with a corticotropin-releasing hormone (CRH) antagonist, the peptide ␣-helical CRH(9-41) injected intraperitoneally 20 min before stress, abolished the stress-induced mucosal changes. Our results indicate that neonatal trauma can induce phenotypic changes in adulthood, including enhanced vulnerability of the gut mucosa to stress via mechanisms involving peripherally located CRH receptors.behavior; corticotropin-releasing hormone; electron microscopy; ion transport; intestinal permeability HUMANS EXPERIENCE STRESS OF various types during daily life, and adequate responses to these stressors are necessary for survival. If the severity or the chronicity of the stressful experience exceeds the adaptive capacity, the individual will be predisposed to illness and disease in multiple organ systems (21). A large number of studies have shown that early-life experience plays an important role in stress responsiveness throughout life (8). In animal models, neonatal adversity can result in permanent functional changes in the stress-mediating systems of the central nervous system (15). For example, newborn rats subjected to maternal separation demonstrate increased release of corticotropinreleasing hormone (CRH), altered expression of glucocorticoid receptors, as well as changes in the norepinephrine and GABA systems (3, 4). Recently, it was also shown in humans that adverse early-life events are associated with hyperresponsiveness to stress and alterations in the hypothalamic-pituitaryadrenal (HPA) axis (10).There is evidence that early-life trauma and ongoing psychological stress can affect the clinical course of intestinal disorders (16,17,20,26) and also reactivate inflammation in experimental colitis (6,9,22,25). The mechanisms underlying stress-induced exacerbations of intestinal diseases are, however, largely unknown. One possible link between intestinal disease and stress is a change in mucosal function. Our previous studies have shown that acute stress in rats induces enhanced intestinal epithelial permeability to macromolecu...

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Section: Discussionmentioning

confidence: 99%

Section: Epithelial Uptake Of Hrpmentioning

confidence: 99%

Neonatal maternal separation predisposes adult rats to colonic barrier dysfunction in response to mild stress

Söderholm¹,

Yates²,

Gareau³

et al. 2002

American Journal of Physiology-Gastrointestinal and Liver Physi

207

206

View full text Add to dashboard Cite

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“…In the field of gastrointestinal research, stress induces irritable bowel syndrome, gastric ulcers, or gastric hemorrhages (Bennett et al, 1998). It has been established that physical and psychological stressors can induce marked alterations in water and electrolyte transport across the epithelium in the small intestines of rats (Santos et al, 2001;Bonaz and Tache, 1994). In those experiments, WAS, as psychological stress, altered the barrier and transport properties of the small intestine.…”

Section: Discussionmentioning

confidence: 99%

“…Santos et al (2000) showed that water avoidance stress (WAS) was a good psychological stress model. They demonstrated that WAS caused an epithelial barrier defect and epithelial mitochondrial damage of the colon, in parallel with mucosal mast cell hyperplasia and activation (Santos et al, 2001).…”

Section: Introductionmentioning

confidence: 99%

Psychological Stress can Trigger Atopic Dermatitis in NC/Nga Mice: An Inhibitory Effect of Corticotropin-Releasing Factor

Amano

Negishi

Akiyama

et al. 2007

Neuropsychopharmacol

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Atopic dermatitis (AD) is one of the most common inflammatory diseases of the skin and is usually associated with a family history of atopic diathesis. It has been well established that many environmental or psychological factors aggravate AD. However, it is not clear whether psychological stress by itself can trigger AD. We examined the effect of psychological stress on the onset of AD, using an animal model, the NC/Nga mouse. The animals were exposed to the water avoidance stress (WAS) test to induce psychological stress. Additionally, we examined how corticotropin-releasing factor (CRF) affected the development of AD induced by psychological stress. Under specific pathogen-free (SPF) conditions, NC/Nga mice did not develop AD-like skin lesions. In contrast, NC/Nga mice exposed to psychological stress developed AD-like skin lesions along with elevated levels of serum immunoglobulin E even when kept under SPF conditions. The AD-like skin lesions induced by WAS were completely blocked by pretreating the animals with CRF. Our data indicate that a psychological factor is capable of eliciting AD-like skin lesions in NC/Nga mice. It is possible that the inhibitory effect of CRF may be mediated by the functional modification of various cells that have CRF receptors.

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“…Indeed, mast cells are involved in the regulation of intestinal permeability and the integrity of the epithelial barrier. [105][106][107] Studies focused on permeability assessment using urinary recovery of orally administered sugars or radioisotopes (Table 3) reported increased permeability in the small intestine, 22,108,109 with the exception of one study performed in children. 60 Several studies also highlighted an increased colonic permeability 60,71,[109][110][111] ; however, this result could not be consistently replicated by other groups.…”

Section: Intestinal Permeability In Ibs Patientsmentioning

confidence: 99%

Review article: associations between immune activation, intestinal permeability and the irritable bowel syndrome

Matricon

Méleine

Gelot

et al. 2012

Aliment Pharmacol Ther

183

178

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This uncommissioned review article was subject to full peer-review. SUMMARY BackgroundIrritable bowel syndrome (IBS), one of the most common gastrointestinal disorders, markedly impairing patients' quality of life. Drug development for IBS treatment has been hampered by the lack of understanding of IBS aetiology. In recent years, numerous data have emerged that suggest the involvement of immune activation in IBS, at least in a subset of patients. AimTo determine whether immune activation and intestinal permeabilisation are more frequently observed in IBS patients compared with healthy controls. MethodsThe scientific bibliography was searched using the following keywords: irritable bowel syndrome, inflammation, immune activation, permeabilisation, intestine, assay, histology and human. The retrieved studies, including blood, faecal and histological studies, were analysed to provide a comprehensive and structured overview of the available data including the type of assay, type of inflammatory marker investigated or intestinal segment studied. ResultsImmune activation was more frequently observed in IBS patients than in healthy controls. An increase in the number of mast cells and lymphocytes, an alteration in cytokine levels and intestinal permeabilisation were reported in IBS patients. No consistent changes in the numbers of B cells or enterochromaffin cells or in mucosal serotonin production were demonstrated. ConclusionsThe changes observed were modest and often heterogeneous among the studied population. Only appropriate interventions improving irritable bowel syndrome symptoms could highlight and confirm the role of immune activation in this pathophysiology.

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Role of mast cells in chronic stress induced colonic epithelial barrier dysfunction in the rat

Cited by 266 publications

References 45 publications

Neonatal maternal separation predisposes adult rats to colonic barrier dysfunction in response to mild stress

Neonatal maternal separation predisposes adult rats to colonic barrier dysfunction in response to mild stress

Psychological Stress can Trigger Atopic Dermatitis in NC/Nga Mice: An Inhibitory Effect of Corticotropin-Releasing Factor

Review article: associations between immune activation, intestinal permeability and the irritable bowel syndrome

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