Barley β-glucan improves metabolic condition via short-chain fatty acids produced by gut microbial fermentation in high fat diet fed mice.

Junki Miyamoto,Satsuki Taira,Keita Watanabe,Junichiro Irie,Hiroshi Itoh,Mayu Kasubuchi,Xuan Li,Ikuo Kimura,Pratibha V Nerurkar

doi:10.1371/journal.pone.0196579

Abstract

Dietary intake of barley β-glucan (BG) is known to affect energy metabolism. However, its underlying mechanism remains poorly understood because studies have presented inconsistent results, with both positive and negative effects reported in terms of satiety, energy intake, weight loss, and glycemic control. The objective of this study was to clarify the physiological role underlying the metabolic benefits of barley BG using a mouse model of high fat diet (HFD)-induced obesity. Male 4-wk-old C57BL/6J mice were fed an HFD with 20% barley flour containing either high BG (HBG; 2% BG) or low BG (LBG; 0.6% BG) levels under conventional and germ-free (GF) conditions for 12 wks. In addition, mice were fed either an HFD with 5% cellulose (HFC; high fiber cellulose) or 5% barley BG (HFB; high fiber β-glucan) for 12 wks. Then, metabolic parameters, gut microbial compositions, and the production of fecal short-chain fatty acids (SCFAs) were analyzed. The weight gain and fat mass of HBG-fed mice were lower than those of control mice at 16-wk-old. Moreover, the secretion of the gut hormones PYY and GLP-1 increased in HBG-fed mice, thereby reducing food intake and improving insulin sensitivity by changing the gut microbiota and increasing SCFAs (especially, butyrate) under conventional condition. These effects in HBG-fed mice were abolished under GF conditions. Moreover, the HFB diets also increased PYY and GLP-1 secretion, and decreased food intake compared with that in HFC-fed mice. These results suggest that the beneficial metabolic effects of barley BG are primary due to the suppression of appetite and improvement of insulin sensitivity, which are induced by gut hormone secretion promoted via gut microbiota-produced SCFAs.

Highlights

Diet is the most important energy resource for daily activities
We found that barley flour containing high levels of barley β-glucan (BG) was efficacious against weight gain and fat increases by reducing food intake and improving insulin sensitivity
These metabolic benefits of barley BG were associated with the short-chain fatty acids (SCFAs) produced by the gut microbiota and their promoting effects on gut hormone secretion

Summary

Introduction

Diet is the most important energy resource for daily activities. the dysregulation of energy homeostasis caused by excess and unbalanced diets leads to metabolic disorders, such as obesity and type 2 diabetes [1]. In epidemiological studies concerning the metabolic benefits of whole-grain foods, dietary fiber is considered to be the most important factor in explaining the health effects of the diet [5]. The laxative effect of dietary fiber arises from the mechanical irritation of the gut mucosa by some insoluble fiber and the consequent secretion of water and mucous. This mechanism requires that the fiber resists fermentation and remain relatively intact throughout the large bowel so as to increase stool water content and form bulky soft easy-to-pass stools. SCFAs, in addition to being involved in de novo synthesis of lipids and serving as energy sources for the host [12], play an essential role as signaling molecules in host energy homeostasis-related physiological functions, such as gut hormone secretion via the G protein-coupled receptors GPR41 or GPR43 [13,14,15,16,17,18]

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