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Interactions Between Diet and the Intestinal Microbiota Alter Intestinal Permeability and Colitis Severity in Mice.

ABSTRACT: BACKGROUND & AIMS:It is not clear how the complex interactions between diet and the intestinal microbiota affect development of mucosal inflammation or inflammatory bowel disease. We investigated interactions between dietary ingredients, nutrients, and the microbiota in specific pathogen-free (SPF) and germ-free (GF) mice given more than 40 unique diets; we quantified individual and synergistic effects of dietary macronutrients and the microbiota on intestinal health and development of colitis. METHODS:C56BL/6J SPF and GF mice were placed on custom diets containing different concentrations and sources of protein, fat, digestible carbohydrates, and indigestible carbohydrates (fiber). After 1 week, SPF and GF mice were given dextran sulfate sodium (DSS) to induce colitis. Disease severity was determined based on the percent weight change from baseline, and modeled as a function of the concentration of each macronutrient in the diet. In unchallenged mice, we measured intestinal permeability by feeding mice labeled dextran and measuring levels in blood. Feces were collected and microbiota were analyzed by 16S rDNA sequencing. We collected colons from mice and performed transcriptome analyses. RESULTS:Fecal microbiota varied with diet; the concentration of protein and fiber had the strongest effect on colitis development. Among 9 fiber sources tested, psyllium, pectin, and cellulose fiber reduced the severity of colitis in SPF mice, whereas methylcellulose increased severity. Increasing dietary protein increased the density of the fecal microbiota and the severity of colitis in SPF mice, but not in GF mice or mice given antibiotics. Psyllium fiber reduced the severity of colitis through microbiota-dependent and microbiota-independent mechanisms. Combinatorial perturbations to dietary casein protein and psyllium fiber in parallel accounted for most variation in gut microbial density and intestinal permeability in unchallenged mice, as well as the severity of DSS-induced colitis; changes in 1 ingredient could be offset by changes in another. CONCLUSIONS:In an analysis of the effects of different dietary components and the gut microbiota on mice with and without DSS-induced colitis, we found complex mixtures of nutrients affect intestinal permeability, gut microbial density, and development of intestinal inflammation.

SUBMITTER: Llewellyn SR

PROVIDER: S-EPMC5847454 | biostudies-literature | 2018 Mar

REPOSITORIES: biostudies-literature

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Interactions Between Diet and the Intestinal Microbiota Alter Intestinal Permeability and Colitis Severity in Mice.

Llewellyn Sean R SR Britton Graham J GJ Contijoch Eduardo J EJ Vennaro Olivia H OH Mortha Arthur A Colombel Jean-Frederic JF Grinspan Ari A Clemente Jose C JC Merad Miriam M Faith Jeremiah J JJ

Gastroenterology 20171123 4

<h4>Background & aims</h4>It is not clear how the complex interactions between diet and the intestinal microbiota affect development of mucosal inflammation or inflammatory bowel disease. We investigated interactions between dietary ingredients, nutrients, and the microbiota in specific pathogen-free (SPF) and germ-free (GF) mice given more than 40 unique diets; we quantified individual and synergistic effects of dietary macronutrients and the microbiota on intestinal health and development of c ...[more]

PMID: 29174952

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Project description:Increasing evidence suggests that maternal diet during pregnancy modifies an offspring's microbiota composition and intestinal development in a long-term manner. However, the effects of maternal soluble fiber diet during pregnancy on growth traits and the developing intestine are still underexplored. Sows were allocated to either a control or 2.0% pregelatinized waxy maize starch plus guar gum (SF) dietary treatment during gestation. Growth performance, diarrhea incidence, gut microbiota composition and metabolism, and gut permeability and inflammation status of 14-day-old suckling piglets were analyzed. The maternal SF diet improved the growth rate and decreased the incidence of diarrhea in the piglets. Next-generation sequencing analysis revealed that the intestinal microbiota composition was altered by a maternal SF diet. The fecal and plasma levels of acetate and butyrate were also increased. Furthermore, a maternal SF diet reduced the levels of plasma zonulin and fecal lipocalin-2 but increased the plasma concentrations of interleukin 10 (IL-10) and transforming growth factor β (TGF-β). Additionally, the increased relative abundances of Lactobacillus spp. in SF piglets were positively correlated with growth rate, while the decreased abundances of Bilophila spp. were positively correlated with fecal lipocalin-2 levels. Our data reveal that a maternal SF diet during pregnancy has remarkable effects on an offspring's growth traits and intestinal permeability and inflammation, perhaps by modulating the composition and metabolism of gut microbiota.IMPORTANCE Although the direct effects of dietary soluble fiber on gut microbiota have been extensively studied, the more indirect effects of maternal nutrition solely during pregnancy on the development of the offspring's intestine are until now largely unexplored. Our data show that a maternal soluble fiber diet during pregnancy is independently associated with changes in the intestinal microbiota composition and metabolism of suckling piglets. These findings have direct implications for refining dietary recommendations in pregnancy. Moreover, a maternal soluble fiber diet reduces intestinal permeability and prevents intestinal inflammation and an excessive systemic immune response of suckling piglets. Therefore, the suckling piglets' resistance to disease was enhanced, diarrhea was reduced, and weight gain was raised. Additionally, the changes in gut microbiota in response to a maternal soluble fiber diet may also be directly correlated with the offspring's growth and gut development.

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Interactions Between Diet and the Intestinal Microbiota Alter Intestinal Permeability and Colitis Severity in Mice.

Publications

Interactions Between Diet and the Intestinal Microbiota Alter Intestinal Permeability and Colitis Severity in Mice.

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