Increased antigen and bacterial uptake in follicle associated epithelium induced by chronic psychological stress in rats

Abstract

Background: Chronic stress affects the course of inflammatory bowel disease and experimental colitis, and may also initiate intestinal inflammation in rats. Aim: To investigate the effects of stress on the M cell containing follicle associated epithelium, specialised in antigen uptake. Subjects and methods: Wistar rats were submitted to acute water avoidance stress for one hour or chronic water avoidance stress for 1 hour/day for 10 consecutive days. Permeability to 51 Cr-EDTA, horseradish peroxidase, and chemically killed Escherichia coli K-12 was studied in both villus and follicle associated epithelium in Ussing chambers. Segments were further examined by light, electron, and confocal microscopy. Results: Acute stress increased horseradish peroxidase flux in villus as well as in follicle associated epithelium. Chronic stress further increased permeability to horseradish peroxidase in villus and follicle associated epithelium, in the latter by almost fourfold. Moreover, chronic stress induced over 30 times increased E coli passage in follicle associated epithelium whereas there was no significant increase in villus epithelium. Bacterial uptake was confirmed by confocal microscopy showing fluorescent bacteria penetrating and passing through the epithelial surface. Conclusions: These results show that the barrier function of follicle associated epithelium can be modulated, and that chronic stress enhances the uptake of luminal antigens and bacteria via the follicle associated epithelium. This can increase antigen exposure in Peyer's patches thereby having implications in the initiation of proinflammatory immune responses within the intestinal mucosa.

Characterization of antigen and bacterial transport in the follicle-associated epithelium of human ileum

“…In the FAE we found a high transmucosal flux of the protein antigen, HRP, whereas 51 Cr-EDTA flux and conductance did not significantly differ between VE and FAE. These findings are in line with our previous studies in rat FAE, 8 and point to an enhanced uptake of antigens in the human FAE compared with VE, but equal paracellular permeability. Analogous to the enhanced antigen uptake, a notably higher transmucosal passage of both chemically killed K-12 and live HB101 E. coli was found, which further implies that the human FAE is prone to uptake and transport of antigens and bacteria.…”

“…8 In brief, serosal samples were diluted and transferred to microtitre plates. QuantaBlut Working Solution was added and plates were incubated at 300 r.p.m.…”

“…4,5 Unfortunately, the histochemical properties of FAE and microfold cell (M cells) vary according to species and location 6 and yet no universal human M-cell marker has been established. 7 Previous animal studies have examined uptake and transport of antigens and bacteria in FAE; 5,8,9 however, to date there are no reports quantifying barrier function of human FAE. The main objective of the present study was, consequently, to characterize the barrier properties of human FAE and compare it with regular villus epithelium (VE).…”

Modulatory Effects of Gut Microbiota on the Central Nervous System: How Gut Could Play a Role in Neuropsychiatric Health and Diseases

“…[48][49][50][51][52][53][54] Additionally, stress can change the function of mucosalassociated immune cells and cause increased antigenic and bacterial uptake. 55,56 Multiple studies have been published that have shown that the composition of gut microbiota is changed in the face of acute or chronic stress, and this in turn can subsequently change the function of intestinal barrier as explained above. [57][58][59][60] There is limited data regarding the changes in intestinal barrier or GI physiology and the underlying mechanisms of it in neuropsychiatric disorders.…”

Manning the Barricades: Role of the Gut Epithelium in Crohn’s Disease

“…The SAMP1/Yit mouse strain develops spontaneous ileal inflammation (Matsumoto et al, 1998). In this model, as well as in a water avoidance stress-induced rat model, early inflammatory lesions were observed in the FAE (Kosiewicz et al, 2001;Velin et al, 2004). Very recently, the FAE and M cells were shown to be targeted specifically by adhesiveinvasive E. coli bacteria associated with Crohn's disease (Chassaing et al, 2011).…”