Basic Study
Copyright ©The Author(s) 2017. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastroenterol. Dec 14, 2017; 23(46): 8128-8139
Published online Dec 14, 2017. doi: 10.3748/wjg.v23.i46.8128
Structural shift of gut microbiota during chemo-preventive effects of epigallocatechin gallate on colorectal carcinogenesis in mice
Xin Wang, Tao Ye, Wen-Jie Chen, You Lv, Zong Hao, Jun Chen, Jia-Ying Zhao, Hui-Peng Wang, Yuan-Kun Cai
Xin Wang, Tao Ye, Wen-Jie Chen, You Lv, Zong Hao, Jun Chen, Jia-Ying Zhao, Hui-Peng Wang, Yuan-Kun Cai, Department of General Surgery, The 5th People’s Hospital of Shanghai, Fudan University, Shanghai 200240, China
Author contributions: All authors contributed to the manuscript; Wang HP and Cai YK contributed equally to the article.
Supported by Natural Science Foundation of Minhang District of Shanghai, No. 2012MHZ001.
Conflict-of-interest statement: The authors declare that there is no conflict of interest regarding the publication of this paper.
Open-Access: This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Correspondence to: Yuan-Kun Cai, MSc, Associate Professor, Chief Doctor, Surgeon of General Surgery, Department of General Surgery, The 5th People’s Hospital of Shanghai, Fudan University, 801 Heqing Road, Shanghai 200240, China. yuankun@medmail.com.cn
Telephone: +86-18918168583 Fax: +86-21-64307611
Received: February 23, 2017
Peer-review started: February 24, 2017
First decision: April 28, 2017
Revised: September 15, 2017
Accepted: November 2, 2017
Article in press: November 2, 2017
Published online: December 14, 2017
Processing time: 291 Days and 18.4 Hours
Abstract
AIM

To investigate the effect of epigallocatechin gallate (EGCG) on structural changes of gut microbiota in colorectal carcinogenesis.

METHODS

An azoxymethane (AOM)/dextran sodium sulfate (DSS)-induced colitis mouse model was established. Forty-two female FVB/N mice were randomly divided into the following three groups: group 1 (10 mice, negative control) was treated with vehicle, group 2 (16 mice, positive control) was treated with AOM plus vehicle, and group 3 (16 mice, EG) was treated with AOM plus EGCG. For aberrant crypt foci (ACF) evaluation, the colons were rapidly took out after sacrifice, rinsed with saline, opened longitudinally, laid flat on a polystyrene board, and fixed with 10% buffered formaldehyde solution before being stained with 0.2% methylene blue in saline. For tumor evaluation, the colon was macroscopically inspected and photographed, then the total number of tumors was enumerated and tumor size measured. For histological examination, the fixed tissues were paraffin-embedded and sectioned at 5 mm thickness. Microbial genomic DNA was extracted from fecal and intestinal content samples using a commercial kit. The V4 hypervariable regions of 16S rRNA were PCR-amplified with the barcoded fusion primers. Using the best hit classification option, the sequences from each sample were aligned to the RDP 16S rRNA training set to classify the taxonomic abundance in QIIME. Statistical analyses were then performed.

RESULTS

Treatment of mice with 1% EGCG caused a significant decrease in the mean number of ACF per mouse, when compared with the model mice treated with AOM/DSS (5.38 ± 4.24 vs 13.13 ± 3.02, P < 0.01). Compared with the positive control group, 1% EGCG treatment dependently decreased tumor load per mouse by 85% (33.96 ± 6.10 vs 2.96 ± 2.86, respectively, P < 0.01). All revealed that EGCG could inhibit colon carcinogenesis by decreasing the number of precancerous lesions as well as solid tumors, with reduced tumor load and delayed histological progression of CRC. During the cancerization, the diversity of gut microbiota increased, potential carcinogenic bacteria such as Bacteroides were enriched, and the abundance of butyrate-producing bacteria (Clostridiaceae, Ruminococcus, etc.) decreased continuously. In contrast, the structure of gut microbiota was relatively stable during the intervention of EGCG on colon carcinogenesis. Enrichment of probiotics (Bifidobacterium, Lactobacillu, etc.) might be a potential mechanism for EGCG’s effects on tumor suppression. Via bioinformatics analysis, principal coordinate analysis and cluster analysis of the tumor formation process, we found that the diversity of gut microbiota increased in the tumor model group while that in the EGCG interfered group (EG) remained relatively stable.

CONCLUSION

Gut microbiota imbalance might be a potential mechanism for the prevention of malignant transformation by EGCG, which is significant for diagnosis, treatment, prognosis evaluation, and prevention of colorectal cancer.

Keywords: Epigallocatechin gallate; Gut microbiota; Colorectal cancer; High throughput sequencing; Chemoprevention; Animal experiment

Core tip: Our study revealed the protective effect of epigallocatechin gallate (EGCG) on colorectal carcinogenesis and structural changes of intestinal flora in an animal model of colorectal cancer. EGCG was detected for its roles through azoxymethane/dextran sulfate sodium induced tumor (aberrant crypt foci) formation. The microbial population was compared among groups at different developmental stages by pyrosequencing of V4 regions of 16S rRNA genes. Results suggested that intestinal flora imbalance might be a potential mechanism for the prevention of malignant transformation by the green tea extract EGCG, which is significant for the diagnosis, treatment, prognosis evaluation, and prevention of colorectal cancer.