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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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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.
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pone-0020944-g005: 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.

Mentions: Histological analysis revealed that the adipocyte size in subcutaneous adipose tissues were increased in the HF-fed mice versus controls, whereas the AX treatment normalized this parameter (Figure 4; adipocyte number per field: 339±49, 71±13* and 177±21*§ for CT, HF and HF-AX, respectively; ANOVA, * p<0.05 versus CT and §p<0.05 versus HF). HF feeding increased the expression of genes controlling inflammation (F4/80, IL-6, MCP-1), PPAR-α dependent-fatty acid oxidation (CPT-1, ACO), PPARγ-dependent differentiation and/or fatty acid uptake (C/EBPα, FAT/CD36, aP2, LPL), and lipolysis (MGL) (Figure 5). Furthermore, the mRNA content of GPR43 -a receptor activated by short-chain fatty acids and implicated in the regulation of lipolysis and adipocyte differentiation- was significantly increased upon HF feeding. Interestingly, the AX treatment hugely decreased the expression of the most of these genes in the subcutaneous tissue. Of particular interest, AX treatment decreased the serum concentrations of 2 inflammatory markers that were downregulated in the adipose tissue through AX treatment, namely IL6 (53.9±11.5 pg/ml and 21.9±7.7 pg/ml for HF and HF-AX groups, respectively; t test p<0.05) and MCP-1 (32.1±5.3 pg/ml and 12.3±2.4 pg/ml for HF and HF-AX groups, respectively; t test p<0.05). In addition, AX supplementation inhibited the expression of fatty acid synthase (FAS), a lipogenic enzyme that was already downregulated by the HF diet. In accordance with its expression, we confirmed that FAS activity was downregulated through AX supplementation in adipose tissue since its activity was significantly lower as compared to HF group (32.5±7.1, 25.5±7.5 and 7.1±1.3*§ for CT, HF and HF-AX respectively; ANOVA: *p<0.05 versus CT and §p<0.05 versus HF). By contrast, it did not affect the expression of the uncoupling protein UCP-2.


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)

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.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3111466&req=5

pone-0020944-g005: 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.
Mentions: Histological analysis revealed that the adipocyte size in subcutaneous adipose tissues were increased in the HF-fed mice versus controls, whereas the AX treatment normalized this parameter (Figure 4; adipocyte number per field: 339±49, 71±13* and 177±21*§ for CT, HF and HF-AX, respectively; ANOVA, * p<0.05 versus CT and §p<0.05 versus HF). HF feeding increased the expression of genes controlling inflammation (F4/80, IL-6, MCP-1), PPAR-α dependent-fatty acid oxidation (CPT-1, ACO), PPARγ-dependent differentiation and/or fatty acid uptake (C/EBPα, FAT/CD36, aP2, LPL), and lipolysis (MGL) (Figure 5). Furthermore, the mRNA content of GPR43 -a receptor activated by short-chain fatty acids and implicated in the regulation of lipolysis and adipocyte differentiation- was significantly increased upon HF feeding. Interestingly, the AX treatment hugely decreased the expression of the most of these genes in the subcutaneous tissue. Of particular interest, AX treatment decreased the serum concentrations of 2 inflammatory markers that were downregulated in the adipose tissue through AX treatment, namely IL6 (53.9±11.5 pg/ml and 21.9±7.7 pg/ml for HF and HF-AX groups, respectively; t test p<0.05) and MCP-1 (32.1±5.3 pg/ml and 12.3±2.4 pg/ml for HF and HF-AX groups, respectively; t test p<0.05). In addition, AX supplementation inhibited the expression of fatty acid synthase (FAS), a lipogenic enzyme that was already downregulated by the HF diet. In accordance with its expression, we confirmed that FAS activity was downregulated through AX supplementation in adipose tissue since its activity was significantly lower as compared to HF group (32.5±7.1, 25.5±7.5 and 7.1±1.3*§ for CT, HF and HF-AX respectively; ANOVA: *p<0.05 versus CT and §p<0.05 versus HF). By contrast, it did not affect the expression of the uncoupling protein UCP-2.

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