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

Neyrinck AM, Possemiers S, Druart C, Van de Wiele T, De Backer F, Cani PD, Larondelle Y, Delzenne NM - PLoS ONE (2011)

Bottom Line: This effect was accompanied by improvement of gut barrier function and by a lower circulating inflammatory marker.Furthermore, AX treatment significantly decreased HF-induced adiposity, body weight gain, serum and hepatic cholesterol accumulation and insulin resistance.We postulate that hypocholesterolemic, anti-inflammatory and anti-obesity effects are related to changes in gut microbiota.

View Article: PubMed Central - PubMed

Affiliation: Metabolism and Nutrition Research Group, Louvain Drug Research Institute, Université catholique de Louvain, Brussels, Belgium.

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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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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pone-0020944-g006: 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.

Mentions: To determine whether modifications of the gut microbiota in mice fed AX were associated with an improvement in obesity and lipid metabolism, a correlation analysis was performed between bacteria and host metabolic parameters that were significantly affected through AX supplementation (Figure 6 and Table S3). The analysis revealed negative correlations (p<0.001) between Roseburia spp, and fat mass development, body weight gain, cholesterolemia, insulinoresistance index, and expression of several genes that mediate differentiation and/or fatty acid uptake (PPARγ, aP2, FAT/CD36, LPL, FIAF), fatty acid oxidation (CPT-1, ACO), short-chain fatty acid response (GPR43), and inflammation (IL6, F4/80) in the subcutaneous adipose tissue. Some of these metabolic parameters were also inversely correlated with the number of Bacteroides/Prevotella spp. (p<0.01) whereas none of these markers was significantly correlated with the number of total bifidobacteria. However, bifidobacteria levels were positively correlated with rumenic acid in the adipose tissue and with the mRNA levels of the tight junction proteins (ZO-1 and occludine) in the gut. The analysis revealed other interesting negative correlation with bifidobacteria such as the FAS activity/expression in the adipose tissue and circulating inflammatory markers (IL-6 and MCP-1).


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

Neyrinck AM, Possemiers S, Druart C, Van de Wiele T, De Backer F, Cani PD, Larondelle Y, Delzenne NM - PLoS ONE (2011)

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.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3111466&req=5

pone-0020944-g006: 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.
Mentions: To determine whether modifications of the gut microbiota in mice fed AX were associated with an improvement in obesity and lipid metabolism, a correlation analysis was performed between bacteria and host metabolic parameters that were significantly affected through AX supplementation (Figure 6 and Table S3). The analysis revealed negative correlations (p<0.001) between Roseburia spp, and fat mass development, body weight gain, cholesterolemia, insulinoresistance index, and expression of several genes that mediate differentiation and/or fatty acid uptake (PPARγ, aP2, FAT/CD36, LPL, FIAF), fatty acid oxidation (CPT-1, ACO), short-chain fatty acid response (GPR43), and inflammation (IL6, F4/80) in the subcutaneous adipose tissue. Some of these metabolic parameters were also inversely correlated with the number of Bacteroides/Prevotella spp. (p<0.01) whereas none of these markers was significantly correlated with the number of total bifidobacteria. However, bifidobacteria levels were positively correlated with rumenic acid in the adipose tissue and with the mRNA levels of the tight junction proteins (ZO-1 and occludine) in the gut. The analysis revealed other interesting negative correlation with bifidobacteria such as the FAS activity/expression in the adipose tissue and circulating inflammatory markers (IL-6 and MCP-1).

Bottom Line: This effect was accompanied by improvement of gut barrier function and by a lower circulating inflammatory marker.Furthermore, AX treatment significantly decreased HF-induced adiposity, body weight gain, serum and hepatic cholesterol accumulation and insulin resistance.We postulate that hypocholesterolemic, anti-inflammatory and anti-obesity effects are related to changes in gut microbiota.

View Article: PubMed Central - PubMed

Affiliation: Metabolism and Nutrition Research Group, Louvain Drug Research Institute, Université catholique de Louvain, Brussels, Belgium.

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.

Show MeSH
Related in: MedlinePlus