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

J Nutr. 2017 Oct;147(10):1900-1908. doi: 10.3945/jn.117.253955. Epub 2017 Aug 23.

Abstract

Background: The mechanism underlying transient increases in immunoglobulin (Ig) A concentrations in the cecal contents of rats fed fructo-oligosaccharide (FOS) is unclear.Objective: 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.Methods: 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).Results: The cecal IgA concentration in the FOS-fed rats was 15-fold higher than that of the rats fed FFP for 9 d (P < 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).Conclusions: 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.

Keywords: IgA; fructo-oligosaccharides; gut permeability; polymeric immunoglobulin receptor; rats.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bacterial Translocation
  • Cecum / drug effects
  • Cecum / metabolism*
  • Cecum / pathology
  • Cytokines / metabolism
  • Fructose / immunology
  • Fructose / pharmacology*
  • Immunoglobulin A / metabolism*
  • Inflammation / etiology
  • Inflammation / metabolism
  • Inflammation / pathology
  • Intestinal Mucosa / drug effects*
  • Intestinal Mucosa / immunology
  • Intestinal Mucosa / metabolism
  • Intestinal Mucosa / pathology
  • Lymph Nodes
  • Male
  • Mesentery
  • Mucositis / etiology
  • Mucositis / metabolism*
  • Mucositis / pathology
  • Oligosaccharides / immunology
  • Oligosaccharides / pharmacology*
  • Permeability
  • Peroxidase / metabolism
  • Prebiotics*
  • Rats, Wistar
  • Receptors, Polymeric Immunoglobulin / metabolism

Substances

  • Cytokines
  • Immunoglobulin A
  • Oligosaccharides
  • Prebiotics
  • Receptors, Polymeric Immunoglobulin
  • Fructose
  • Peroxidase