Lactobacilli Degrade Wheat Amylase Trypsin Inhibitors to Reduce Intestinal Dysfunction Induced by Immunogenic Wheat Proteins

Gastroenterology. 2019 Jun;156(8):2266-2280. doi: 10.1053/j.gastro.2019.02.028. Epub 2019 Feb 22.

Abstract

Background & aims: Wheat-related disorders, a spectrum of conditions induced by the ingestion of gluten-containing cereals, have been increasing in prevalence. Patients with celiac disease have gluten-specific immune responses, but the contribution of non-gluten proteins to symptoms in patients with celiac disease or other wheat-related disorders is controversial.

Methods: C57BL/6 (control), Myd88-/-, Ticam1-/-, and Il15-/- mice were placed on diets that lacked wheat or gluten, with or without wheat amylase trypsin inhibitors (ATIs), for 1 week. Small intestine tissues were collected and intestinal intraepithelial lymphocytes (IELs) were measured; we also investigated gut permeability and intestinal transit. Control mice fed ATIs for 1 week were gavaged daily with Lactobacillus strains that had high or low ATI-degrading capacity. Nonobese diabetic/DQ8 mice were sensitized to gluten and fed an ATI diet, a gluten-containing diet or a diet with ATIs and gluten for 2 weeks. Mice were also treated with Lactobacillus strains that had high or low ATI-degrading capacity. Intestinal tissues were collected and IELs, gene expression, gut permeability and intestinal microbiota profiles were measured.

Results: In intestinal tissues from control mice, ATIs induced an innate immune response by activation of Toll-like receptor 4 signaling to MD2 and CD14, and caused barrier dysfunction in the absence of mucosal damage. Administration of ATIs to gluten-sensitized mice expressing HLA-DQ8 increased intestinal inflammation in response to gluten in the diet. We found ATIs to be degraded by Lactobacillus, which reduced the inflammatory effects of ATIs.

Conclusions: ATIs mediate wheat-induced intestinal dysfunction in wild-type mice and exacerbate inflammation to gluten in susceptible mice. Microbiome-modulating strategies, such as administration of bacteria with ATI-degrading capacity, may be effective in patients with wheat-sensitive disorders.

Keywords: Bacterial Metabolism; Food Allergy; HLA; Microbiome.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amylases / antagonists & inhibitors
  • Animals
  • Celiac Disease / diet therapy
  • Celiac Disease / immunology*
  • Celiac Disease / physiopathology
  • Diet, Gluten-Free / methods*
  • Disease Models, Animal
  • Gastrointestinal Microbiome / immunology
  • Gliadin / adverse effects*
  • Gliadin / immunology
  • Humans
  • Immunity, Innate / drug effects
  • Lactobacillus / immunology*
  • Lactobacillus / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Random Allocation
  • Reference Values
  • Sensitivity and Specificity
  • Triticum / adverse effects*
  • Triticum / immunology
  • Trypsin Inhibitors / immunology
  • Trypsin Inhibitors / pharmacology

Substances

  • Trypsin Inhibitors
  • Gliadin
  • Amylases