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Chinese Propolis Prevents Obesity and Metabolism Syndromes Induced by a High Fat Diet and Accompanied by an Altered Gut Microbiota Structure in Mice - PubMed

  • ️Wed Jan 01 2020

Chinese Propolis Prevents Obesity and Metabolism Syndromes Induced by a High Fat Diet and Accompanied by an Altered Gut Microbiota Structure in Mice

Yufei Zheng et al. Nutrients. 2020.

Abstract

The increasing incidence of obesity poses a great threat to public health worldwide. Recent reports also indicate the relevance of obesity in metabolic diseases. Chinese propolis (CP), as a well-studied natural nutraceutical, has shown a beneficial effect on alleviating diabetes mellitus. However, few studies have investigated the effect of CP on weight management and energy balance. We examined the beneficial effects of dietary CP on weight in high-fat diet-fed female and male mice and determined whether CP alters gut microbiota. In this study, dietary CP supplementation reduces body weight and improves insulin resistance in high-fat diet (HFD)-fed mice in a dose-dependent manner. CP treatment also reverses liver weight loss and triglyceride accumulation in association with hepatic steatosis. The 16S rRNA analysis of gut microbiota demonstrated that CP treatment modulates the composition in HFD-fed mice. Our study also suggests that male mice were more sensitive to CP treatment than female mice. Taken together, CP supplementation reduces weight gain and reverses gut microbiome dysbiosis induced by HFD. Further, the effects of CP treatment on metabolic biomarkers and microbiome structure differ by gender.

Keywords: Chinese propolis (CP), obesity; high-fat diet; metabolic syndromes; microbiome.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1

Chinese propolis (CP) prevented body weight gain and fat accumulation in both female and male high-fat diet (HFD)-fed mice. (A) The mean weight gain and weight of each group of both genders. (B) The weight of parametrial white adipose tissue (Par-WAT), mesenteric white adipose tissue (Mes-WAT), inguinal subcutaneous adipose tissue (Ing-SAT) and perirenal white adipose tissue (Per-WAT) and their ratios to body weight of female mice. (C) The weight of Par-WAT, Mes-WAT, Ing-SAT and Per-WAT as well as their ratios to body weight of male mice.

Figure 1
Figure 1

Chinese propolis (CP) prevented body weight gain and fat accumulation in both female and male high-fat diet (HFD)-fed mice. (A) The mean weight gain and weight of each group of both genders. (B) The weight of parametrial white adipose tissue (Par-WAT), mesenteric white adipose tissue (Mes-WAT), inguinal subcutaneous adipose tissue (Ing-SAT) and perirenal white adipose tissue (Per-WAT) and their ratios to body weight of female mice. (C) The weight of Par-WAT, Mes-WAT, Ing-SAT and Per-WAT as well as their ratios to body weight of male mice.

Figure 1
Figure 1

Chinese propolis (CP) prevented body weight gain and fat accumulation in both female and male high-fat diet (HFD)-fed mice. (A) The mean weight gain and weight of each group of both genders. (B) The weight of parametrial white adipose tissue (Par-WAT), mesenteric white adipose tissue (Mes-WAT), inguinal subcutaneous adipose tissue (Ing-SAT) and perirenal white adipose tissue (Per-WAT) and their ratios to body weight of female mice. (C) The weight of Par-WAT, Mes-WAT, Ing-SAT and Per-WAT as well as their ratios to body weight of male mice.

Figure 2
Figure 2

CP administration improved insulin sensitivity and lipid metabolism in HFD-fed mice. Oral glucose tolerance tests (A) and insulin tolerance test (B) (n = 10) were measured in the 8th and 9th week during the experiment, respectively. (C) Curves of blood glucose levels and the calculated area under curve (AUC) (inner graph). Values are expressed as the mean ± SEM. (D) Serum concentrations of alanine aminotransferase (ALT), aspartate aminotransferase (AST), cholesterol (CHOL), high-density lipoprotein (HDL), low-density lipoprotein (LDL), and triglycerides (TGs) in mice (n ≥ 8). (E) Plasma concentrations of transforming growth factor alpha (TGF-α), interleukin-6 (IL-6) and lipopolysaccharide (LPS) in mice. Values are presented as the mean ± SEM.

Figure 2
Figure 2

CP administration improved insulin sensitivity and lipid metabolism in HFD-fed mice. Oral glucose tolerance tests (A) and insulin tolerance test (B) (n = 10) were measured in the 8th and 9th week during the experiment, respectively. (C) Curves of blood glucose levels and the calculated area under curve (AUC) (inner graph). Values are expressed as the mean ± SEM. (D) Serum concentrations of alanine aminotransferase (ALT), aspartate aminotransferase (AST), cholesterol (CHOL), high-density lipoprotein (HDL), low-density lipoprotein (LDL), and triglycerides (TGs) in mice (n ≥ 8). (E) Plasma concentrations of transforming growth factor alpha (TGF-α), interleukin-6 (IL-6) and lipopolysaccharide (LPS) in mice. Values are presented as the mean ± SEM.

Figure 3
Figure 3

CP application prevented liver steatosis and promoted liver lipid metabolism in HFD-fed mice. (A) Liver Oil Red O staining of each group in both female and male mice. Each bar: 50 μm in original photo; 20 μm in enlarged photo. (B) Liver TG concentration and liver weight were changed according to the diet. (C) The relative expression of PGC1, ACC1, SREBP1/2, and PPARɑ/γ mRNA in liver, and were normalized with GADPH (n = 8). Values are presented as the mean ± SD.

Figure 3
Figure 3

CP application prevented liver steatosis and promoted liver lipid metabolism in HFD-fed mice. (A) Liver Oil Red O staining of each group in both female and male mice. Each bar: 50 μm in original photo; 20 μm in enlarged photo. (B) Liver TG concentration and liver weight were changed according to the diet. (C) The relative expression of PGC1, ACC1, SREBP1/2, and PPARɑ/γ mRNA in liver, and were normalized with GADPH (n = 8). Values are presented as the mean ± SD.

Figure 4
Figure 4

Effects of CP on adipose tissue (BAT & WAT) formation in HFD-fed mice. (A) Hematoxylin and eosin (H&E) staining of brown adipose tissue section. Each bar: 50 μm in original photo; 20 μm in enlarged photo. (B) The relative mRNA expression of adipose browning-related genes (CD36, CPT1β, DIO2, FABP, PGC1, UCP1, and UCP3) in BAT. (C) H&E staining of epididymal and parametrial white adipose tissue sections. Scale: 100 μm.

Figure 5
Figure 5

CP application altered microbial diversity and structure in HFD-fed mice. The operational taxonomic unit (OTU) rarefaction curve and the rank curve of microbial diversity responded to dietary change and CP treatment in female mice (A–C) and male mice (F–H). (D,I) show the Shannon, Chao1, Simpson and ACE indexes in both genders. (E,J) Principal coordinate analysis PCoA score plot based on a binary Jaccard, non-metric multidimensional scaling (NMDS) score plot based on an unweighted, and principal component analysis (PCA) score plot based on weights.

Figure 5
Figure 5

CP application altered microbial diversity and structure in HFD-fed mice. The operational taxonomic unit (OTU) rarefaction curve and the rank curve of microbial diversity responded to dietary change and CP treatment in female mice (A–C) and male mice (F–H). (D,I) show the Shannon, Chao1, Simpson and ACE indexes in both genders. (E,J) Principal coordinate analysis PCoA score plot based on a binary Jaccard, non-metric multidimensional scaling (NMDS) score plot based on an unweighted, and principal component analysis (PCA) score plot based on weights.

Figure 6
Figure 6

Differences in the bacterial community induced by diet and treatment according to the relative abundances of gut microbiota at the genus level and LEfSe analysis. (A,B,F,G) The relative abundance of intestinal microbiota at the genus level in the four groups of both genders. (C,D,H,I) LEfSe results showed the change in microbiota under HFD and HP administration. The LDA significant threshold was 4.0. Red, green, and blue represented HFD, HP, ND, respectively. (E,J) Heat maps of taxons that were most significantly different in abundance between the four groups at the genus level generated by LEfSe analysis.

Figure 6
Figure 6

Differences in the bacterial community induced by diet and treatment according to the relative abundances of gut microbiota at the genus level and LEfSe analysis. (A,B,F,G) The relative abundance of intestinal microbiota at the genus level in the four groups of both genders. (C,D,H,I) LEfSe results showed the change in microbiota under HFD and HP administration. The LDA significant threshold was 4.0. Red, green, and blue represented HFD, HP, ND, respectively. (E,J) Heat maps of taxons that were most significantly different in abundance between the four groups at the genus level generated by LEfSe analysis.

Figure 7
Figure 7

The modulation of main colon short-chain fatty acid (SCFA) concentrations responded to HFD and CP administration in female mice (A,B) and male mice (C,D). Data are presented as the mean ± SD.

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