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. 2011;6(6):e20944.
doi: 10.1371/journal.pone.0020944. Epub 2011 Jun 9.

Prebiotic effects of wheat arabinoxylan related to the increase in bifidobacteria, Roseburia and Bacteroides/Prevotella in diet-induced obese mice

Affiliations

Prebiotic effects of wheat arabinoxylan related to the increase in bifidobacteria, Roseburia and Bacteroides/Prevotella in diet-induced obese mice

Audrey M Neyrinck et al. PLoS One. 2011.

Abstract

Background: Alterations in the composition of gut microbiota--known as dysbiosis--has been proposed to contribute to the development of obesity, thereby supporting the potential interest of nutrients targeting the gut with beneficial effect for host adiposity. We test the ability of a specific concentrate of water-extractable high molecular weight arabinoxylans (AX) from wheat to modulate both the gut microbiota and lipid metabolism in high-fat (HF) diet-induced obese mice.

Methodology/principal findings: Mice were fed either a control diet (CT) or a HF diet, or a HF diet supplemented with AX (10% w/w) during 4 weeks. AX supplementation restored the number of bacteria that were decreased upon HF feeding, i.e. Bacteroides-Prevotella spp. and Roseburia spp. Importantly, AX treatment markedly increased caecal bifidobacteria content, in particular Bifidobacterium animalis lactis. This effect was accompanied by improvement of gut barrier function and by a lower circulating inflammatory marker. Interestingly, rumenic acid (C18:2 c9,t11) was increased in white adipose tissue due to AX treatment, suggesting the influence of gut bacterial metabolism on host tissue. In parallel, AX treatment decreased adipocyte size and HF diet-induced expression of genes mediating differentiation, fatty acid uptake, fatty acid oxidation and inflammation, and decreased a key lipogenic enzyme activity in the subcutaneous adipose tissue. Furthermore, AX treatment significantly decreased HF-induced adiposity, body weight gain, serum and hepatic cholesterol accumulation and insulin resistance. Correlation analysis reveals that Roseburia spp. and Bacteroides/Prevotella levels inversely correlate with these host metabolic parameters.

Conclusions/significance: Supplementation of a concentrate of water-extractable high molecular weight AX in the diet counteracted HF-induced gut dysbiosis together with an improvement of obesity and lipid-lowering effects. We postulate that hypocholesterolemic, anti-inflammatory and anti-obesity effects are related to changes in gut microbiota. These data support a role for wheat AX as interesting nutrients with prebiotic properties related to obesity prevention.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Caecum weight, DGGE fingerprints and PCA analysis in the caecal content.
Caecal content (A) and caecal tissue (B) weight. Denaturing gradient gel electrophoresis (DGGE) fingerprint patterns of the caecal microbial community; the DGGE profiles were constructed using primers for total bacteria (C). Principal Coordinate Analysis (PCA) was used to explore the similarity within a composite data set consisting of DGGE fingerprints of total bacteria, bifidobacteria, lactobacilli and the Bacteroides-Prevotella spp. cluster (D). Mice were fed a standard (CT, green symbols), a high fat diet (HF, red symbols) or a high fat diet supplemented with 10% arabinoxylan (HF-AX, blue symbols) for 4 weeks. *p<0.05 versus CT and §p<0.05 versus HF (ANOVA).
Figure 2
Figure 2. Bacterial quantification per gram of caecal content.
Caecal bacterial content of total bacteria (A), Bifidobacterium spp. (B), Bacteroides-Prevotella spp. (C), Roseburia spp. (D). Bacterial quantities are expressed as Log10 (bacterial cells/ g caecal content wet weight). Mice were fed a standard (CT), a high fat diet (HF) or a high fat diet supplemented with 10% arabinoxylan (HF-AX) for 4 weeks. *p<0.05 versus CT and §p<0.05 versus HF (ANOVA).
Figure 3
Figure 3. Body weight and fat mass.
Body weight evolution (A), body weight gain (B), visceral (C), epididymal (D), and subcutaneous (E) adipose tissue weight (% versus body weight) of mice fed a standard (CT), a high fat diet (HF) or a high fat diet supplemented with 10% arabinoxylan (HF-AX) for 4 weeks. *p<0.05 versus CT and §p<0.05 versus HF (ANOVA).
Figure 4
Figure 4. Histological pictures of subcutaneous adipose tissue.
Mice were fed a standard diet (CT), a high fat diet (HF) or a high fat diet supplemented with 10% arabinoxylan (HF-AX) for 4 weeks.
Figure 5
Figure 5. mRNA levels of key factors and metabolic network in the subcutaneous adipose tissue.
Expression of genes involved in subcutaneous adipose tissue metabolism (A). Mice were fed a standard (CT), a high fat diet (HF) or a high fat diet supplemented with 10% arabinoxylan (HF-AX) for 4 weeks. Values are expressed relative to CT group (set at 1). *p<0.05 versus CT and §p<0.05 versus HF (ANOVA). Genes that regulate metabolic processes in white adipose tissue (B); some of them are dependent on PPARα (blue) or PPARγ (orange) activation by an endogenous ligand. PPARγ, peroxisome proliferator-activated receptor γ; aP2, adipocyte fatty acid binding protein; C/EBPα, CCAAT enhancer binding protein α; GPR43, G protein-coupled receptor 43; LPL, lipoprotein lipase; CD-36, cluster of differenciation 36; FAS, Fatty acid synthase; ACC, AcylCoa carboxylase; PPARα, peroxisome proliferator-activated receptor-alpha ; CPT-1, carnitine palmitoyl transferase-1 ; ACO, AcylCoA oxydase; MGL, monoacylglycerol lipase; UCP-2, uncoupling protein-2; VLDL, very low density lipoprotein; CM, chylomicron; FA, fatty acids; TG, triglycerides.
Figure 6
Figure 6. Interrelationship between gut microbiota composition and host metabolic parameters significantly modified by arabinoxylan supplementation.
Green connections indicate a positive correlation (Pearson r>0.5), while red connections show correlations that are inverse (Pearson r<0.5). Solid lines represent significance with p<0.001 and shared lines represent significance with p<0.01. aP2, adipocyte fatty acid binding protein; GPR43, G protein-coupled receptor 43; IL6, interleukin 6; LPL, lipoprotein lipase; FAS, Fatty acid synthase; CPT-1, carnitine palmitoyl transferase-1 ; MCP-1, monocyte chemoattractant protein-1; MGL, monoacylglycerol lipase; SCFA, short chain fatty acid.

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