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Prebiotic effects of wheat Arabinoxylan related to the increase in Bifidobacteria, Roseburia and bacteroides/Prevotella in diet-induced obese mice

Audrey M Neyrinck, Sam Possemiers UGent, Celine Druart, Tom Van de Wiele UGent, Fabienne De Backer, Patrice D Cani, Yvan Larondelle and Nathalie M Delzenne (2011) PLOS ONE. 6(6).
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.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
ADIPOSE-TISSUE, IN-VITRO, HEALTH-BENEFITS, GLUCOSE-TOLERANCE, INSULIN-RESISTANCE, BACTERIAL COMMUNITY, CONJUGATED LINOLEIC-ACID, GUT MICROBIOTA, INTESTINAL BACTERIA, LIPID-METABOLISM
journal title
PLOS ONE
PLoS One
volume
6
issue
6
article_number
e20944
pages
12 pages
Web of Science type
Article
Web of Science id
000291612900042
JCR category
BIOLOGY
JCR impact factor
4.092 (2011)
JCR rank
12/84 (2011)
JCR quartile
1 (2011)
ISSN
1932-6203
DOI
10.1371/journal.pone.0020944
language
English
UGent publication?
yes
classification
A1
copyright statement
I have transferred the copyright for this publication to the publisher
id
1857853
handle
http://hdl.handle.net/1854/LU-1857853
date created
2011-07-13 09:28:16
date last changed
2011-08-03 13:52:48
@article{1857853,
  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.},
  articleno    = {e20944},
  author       = {Neyrinck, Audrey M and Possemiers, Sam and Druart, Celine and Van de Wiele, Tom and De Backer, Fabienne and Cani, Patrice D and Larondelle, Yvan and Delzenne, Nathalie M},
  issn         = {1932-6203},
  journal      = {PLOS ONE},
  keyword      = {ADIPOSE-TISSUE,IN-VITRO,HEALTH-BENEFITS,GLUCOSE-TOLERANCE,INSULIN-RESISTANCE,BACTERIAL COMMUNITY,CONJUGATED LINOLEIC-ACID,GUT MICROBIOTA,INTESTINAL BACTERIA,LIPID-METABOLISM},
  language     = {eng},
  number       = {6},
  pages        = {12},
  title        = {Prebiotic effects of wheat Arabinoxylan related to the increase in Bifidobacteria, Roseburia and bacteroides/Prevotella in diet-induced obese mice},
  url          = {http://dx.doi.org/10.1371/journal.pone.0020944},
  volume       = {6},
  year         = {2011},
}

Chicago
Neyrinck, Audrey M, Sam Possemiers, Celine Druart, Tom Van de Wiele, Fabienne De Backer, Patrice D Cani, Yvan Larondelle, and Nathalie M Delzenne. 2011. “Prebiotic Effects of Wheat Arabinoxylan Related to the Increase in Bifidobacteria, Roseburia and bacteroides/Prevotella in Diet-induced Obese Mice.” Plos One 6 (6).
APA
Neyrinck, A. M., Possemiers, S., Druart, C., Van de Wiele, T., De Backer, F., Cani, P. D., Larondelle, Y., et al. (2011). Prebiotic effects of wheat Arabinoxylan related to the increase in Bifidobacteria, Roseburia and bacteroides/Prevotella in diet-induced obese mice. PLOS ONE, 6(6).
Vancouver
1.
Neyrinck AM, Possemiers S, Druart C, Van de Wiele T, De Backer F, Cani PD, et al. Prebiotic effects of wheat Arabinoxylan related to the increase in Bifidobacteria, Roseburia and bacteroides/Prevotella in diet-induced obese mice. PLOS ONE. 2011;6(6).
MLA
Neyrinck, Audrey M, Sam Possemiers, Celine Druart, et al. “Prebiotic Effects of Wheat Arabinoxylan Related to the Increase in Bifidobacteria, Roseburia and bacteroides/Prevotella in Diet-induced Obese Mice.” PLOS ONE 6.6 (2011): n. pag. Print.