Fructo-oligosaccharide-Induced Transient Increases in Cecal Immunoglobulin A Concentrations in Rats Are Associated with Mucosal Inflammation in Response to Increased Gut Permeability

Abstract

The mechanism underlying transient increases in immunoglobulin (Ig) A concentrations in the cecal contents of rats fed fructo-oligosaccharide (FOS) is unclear. This study was designed to test whether increased IgA concentrations represent one aspect of the inflammatory response to increased permeability induced by FOS in the cecum. Seven-week-old male Wistar rats were fed a fiber-free semipurified diet (FFP) with or without supplemental FOS (60 g/kg diet) for 9 or 58 d [experiment (expt.) 1], 7 d (expt. 2), or 7 or 56 d (expt. 3). In addition to measuring IgA concentrations in cecal content, we assessed gut permeability, inflammatory responses (expt. 1), the number of IgA plasma cells in the cecal lamina propria, polymeric Ig receptor (pIgR) expression in the cecal mucosa (expt. 2), and the condition of the cecal mucus layer (expt. 3). The cecal IgA concentration in the FOS-fed rats was 15-fold higher than that of the rats fed FFP for 9 d ( < 0.05). Gut permeability estimated by urinary chromium-EDTA excretion, bacterial translocation to mesenteric lymph nodes, myeloperoxidase activity, and expression of inflammatory cytokine genes in the cecal mucosa was greater in the FOS-fed rats than in the rats fed FFP for 9 d. These effects were not observed in the rats fed FOS for 58 d (expt. 1). Accompanying the higher cecal IgA concentration, pIgR protein and the number of IgA plasma cells in the cecal mucosa were higher in the FOS-fed rats than in the rats fed FFP for 7 d (expt. 2). Destruction of the mucus layer on the epithelial surface, as evidenced by Alcian blue staining in the cecal sections, was evident in the rats fed FOS for 7 d, but the mucus layer appeared normal in the rats fed FOS for 56 d (expt. 3). These findings suggest that transient increases in cecal IgA concentrations induced by FOS in rats are associated with mucosal inflammation in response to increased gut permeability; these are presumably evoked by disruption of the cecal mucus barrier. The observed responses could contribute to the maturation of the gut immune system.

The Impact of Fructo-Oligosaccharides on Gut Permeability and Inflammatory Responses in the Cecal Mucosa Quite Differs between Rats Fed Semi-Purified and Non-Purified Diets

“…Cecal fermentation in rats fed 6% FOS diet for 1 wk was characterized by a very low cecal pH (well below 6.0) accompanying the accumulation of lactate and succinate, which are stronger acids than short-chain fatty acids (SCFA) but are absorbed more slowly (12). In such a cecal environment, we found that the mucus layer on the epithelial surface in the cecum was completely destroyed, and this might be associated with the increased gut permeability (11). But in rats fed the same diet for 8 wk, at which time the cecal pH became almost neutral and SCFA were major fermentation products, the gut permeability returned to its nor-mal level (11).…”

“…Many factors could be involved in the above-mentioned different findings of FOS on gut permeability. Our recent study, however, showed that FOS-induced increase in the gut permeability in rats fed a SP was a transient phenomenon before adaptation of the gut bacteria to FOS (11). Cecal fermentation in rats fed 6% FOS diet for 1 wk was characterized by a very low cecal pH (well below 6.0) accompanying the accumulation of lactate and succinate, which are stronger acids than short-chain fatty acids (SCFA) but are absorbed more slowly (12).…”

Cholestyramine, a Bile Acid Sequestrant, Increases Cecal Short Chain Fatty Acids and Intestinal Immunoglobulin A in Mice

“…12) Fecal IgA was extracted using phosphate-buffered saline containing a protein inhibitor cocktail (cOmplete tablets; Roche, Manheim, Germany) as previously described. 13) Fecal IgA content was measured using a Mouse IgA kit (Bethyl Laboratories, Montgomery, TX, U.S.A.).…”

“…SCFAs in the cecal contents were analyzed as per our previous study. 13) The SCFA content in each sample was calculated using an internal standard method with 2-ethylbutyrate as the standard.…”

Resistant Starch‐Supplemented Udon Noodles Prevent Impaired Glucose Tolerance and Induce Intestinal Immunoglobulin‐A Secretion in Mice

“…IgA defends epithelial cells from infection and injury from pathogens and microbes in the intestines and improves intestinal conditions . Some polysaccharides and oligosaccharides can induce intestinal release of IgA, but transient induction of IgA release by polysaccharides and oligosaccharides might be caused by mucosal inflammation . We collected feces at 10 weeks and showed increased IgA levels in the HFD‐RS group, suggesting that induction of fecal IgA in the HFD‐RS group was not transient and not due to mucosal inflammation.…”