Decaffeinated green and black tea polyphenols decrease weight gain and alter microbiome populations and function in diet-induced obese mice

Abstract

Purpose: Decaffeinated green tea (GT) and black tea (BT) polyphenols inhibit weight gain in mice fed an obesogenic diet. Since the intestinal microflora is an important contributor to obesity, it was the objective of this study to determine whether the intestinal microflora plays a role in the anti-obesogenic effect of GT and BT.

Methods: C57BL/6J mice were fed a high-fat/high-sucrose diet (HF/HS, 32% energy from fat; 25% energy from sucrose) or the same diet supplemented with 0.25% GTP or BTP or a low-fat/high-sucrose (LF/HS, 10.6% energy from fat, 25% energy from sucrose) diet for 4 weeks. Bacterial composition was assessed by MiSeq sequencing of the 16S rRNA gene.

Results: GTP and BTP diets resulted in a decrease of cecum Firmicutes and increase in Bacteroidetes. The relative proportions of Blautia, Bryantella, Collinsella, Lactobacillus, Marvinbryantia, Turicibacter, Barnesiella, and Parabacteroides were significantly correlated with weight loss induced by tea extracts. BTP increased the relative proportion of Pseudobutyrivibrio and intestinal formation of short-chain fatty acids (SCFA) analyzed by gas chromatography. Cecum propionic acid content was significantly correlated with the relative proportion of Pseudobutyrivibrio. GTP and BTP induced a significant increase in hepatic 5'adenosylmonophosphate-activated protein kinase (AMPK) phosphorylation by 70 and 289%, respectively (P < 0.05) determined by Western blot.

Conclusion: In summary, both BTP and GTP induced weight loss in association with alteration of the microbiota and increased hepatic AMPK phosphorylation. We hypothesize that BTP increased pAMPK through increased intestinal SCFA production, while GTPs increased hepatic AMPK through GTP present in the liver.

Keywords: AMPK phosphorylation; Black tea; Green tea; Microflora; Obesity; Polyphenols; Short-chain fatty acids.

Fig. 1

Effects of tea extracts on (a) body weight, (b) % subcutaneous fat, (c) % mesenteric fat, (d) % epididymal fat normalized to body weight, (e) food intake, and (f) energy intake in male C57BL/6J mice fed an HF/HS, LF/HS, HF/HS-GTP, or HF/HS-BTP diet for 4 weeks. Data are mean ± SEM (n = 11–12). Labeled means of dietary interventions without a common letter differ by diet; P < 0.05

Fig. 2

Beta-diversity analysis of the microbiome of cecum content from mice fed the HF/HS, LF/HS, HF/HS-GTP, or HF/HS-BTP diet for 4 weeks. Three-dimensional principal coordinate analyses (PCoA) based on the unweighted UniFrac distance between samples were performed using QIIME (n = 9)

Fig. 3

Effects of tea extracts on cecum bacteria relative proportion in male C57BL/6J mice fed an HF/HS, LF/HS, HF/HS-GTP, HF/HSOTP, or HF/HS-BTP diet for 4 weeks. Data are means (n = 9). Wilcoxon rank sum test was utilized to evaluate the differences in bacterial relative proportion comparing each tea and LF/HS intervention with HF/HS control diet. Labeled means are different from the HF/HS group with *P ≤ 0.05, **P ≤ 0.01, ***P ≤ 0.001

Fig. 4

Correlation of body weight and bacteria relative proportion of a Bacteroidetes and b Firmicutes phyla including data from all intervention groups. The correlation was evaluated using the GraphPad Prism6 software (San Diego, CA, USA)

Fig. 5

Effects of tea extracts on microbiome on the genus level in cecum content from male C57BL/6J mice fed an HF/HS, LF/HS, HF/HS-GTP, or HF/HS-BTP diet for 4 weeks. Comparison of relative proportion of bacteria between a HF/HS to HF/HS-GTP, b HF/HS to HF/HS-BTP, and c HF/HS to LF/HS fed mice. Data are mean ± SD; N = 9. The difference in relative proportion compared to mice fed the HF/HS control diet was significant for all bacteria included in the figure (P < 0.05)

Fig. 6

Effects of tea extracts on protein expression of hepatic AMPK phosphorylation in liver from male C57BL/6J mice fed an HF/HS, LF/HS, HF/HS-GTP, or HF/HS-BTP diet for 4 weeks. Data are mean ± SEM (n = 5). Data were analyzed by one-way ANOVA, followed by Tukey–Kramer multiple comparison procedure. Labeled means without a common letter differ, P < 0.05