Basic Study
Copyright ©The Author(s) 2018. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastroenterol. May 7, 2018; 24(17): 1901-1910
Published online May 7, 2018. doi: 10.3748/wjg.v24.i17.1901
Mitochondrial pathway mediated by reactive oxygen species involvement in α-hederin-induced apoptosis in hepatocellular carcinoma cells
Jiao Li, Dan-Dan Wu, Ji-Xiang Zhang, Jing Wang, Jing-Jing Ma, Xue Hu, Wei-Guo Dong
Jiao Li, Dan-Dan Wu, Ji-Xiang Zhang, Jing-Jing Ma, Xue Hu, Department of Gastroenterology, Renmin Hospital of Wuhan University, Central Laboratory of Renmin Hospital, Wuhan 430060, Hubei Province, China
Jing Wang, Department of Gastroenterology, Beijing Shijitan Hospital of Capital Medical University, Beijing 100038, China
Wei-Guo Dong, Department of Gastroenterology, Renmin Hospital of Wuhan University, Wuhan 430060, Hubei Province, China
Author contributions: Li J, Wu DD, Zhang JX, Wang J and Dong WG designed the research; Li J, Wu DD and Ma JJ performed the research; Zhang JX and Wang J contributed new reagents/analytical tools; Li J, Hu X and Ma JJ analyzed the data; Li J wrote the manuscript.
Supported by the National Natural Science Foundation of China, No. 81572426; and the Natural Science Foundation of Hubei Province, No. 2015CKB755.
Institutional animal care and use committee statement: All animal experiments were performed in accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of Wuhan University.
Conflict-of-interest statement: The authors declare that there are no conflicts-of-interest regarding the publication of this paper.
Data sharing statement: No additional data are available.
ARRIVE guidelines statement: The ARRIVE guidelines have been adopted.
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: Wei-Guo Dong, MD, PhD, Department of Gastroenterology, Renmin Hospital of Wuhan University, 238 Jiefang Road, Wuhan 430060, Hubei Province, China. dongweiguo@whu.edu.cn
Telephone: +86-13986167388
Received: March 1, 2018
Peer-review started: March 2, 2018
First decision: March 30, 2018
Revised: April 4, 2018
Accepted: April 9, 2018
Article in press: April 9, 2018
Published online: May 7, 2018
Processing time: 66 Days and 3 Hours
ARTICLE HIGHLIGHTS
Research background

Hepatocellular carcinoma (HCC) is a highly prevalent disease worldwide, with poor general prognosis. To develop highly effective natural treatments with limited toxicity for HCC is important. The α-hederin saponin is reported to have antitumor activity. However, the effect of α-hederin on HCC remains to be examined. We evaluated the effect and possible mechanism of α-hederin on HCC cells both in vitro and in vivo.

Research motivation

Developing new, effective and nontoxic chemotherapeutic drugs will contribute to the treatment and prognosis for HCC patients in clinic.

Research objectives

To investigate the antitumor activity of α-hederin in HCC cells and its underlying mechanisms in vitro and in vivo.

Research methods

Three HCC cells lines (SMMC-7721, HepG-2 and Huh-7 HCC cells) were used to detect the effect of α-hederin on HCC. Cell viability was detected by Cell Counting Kit-8 assay after cells were treated with α-hederin. (BSO) N-acetylcysteine (NAC) and DL-buthionine-S,R-sulfoximine (BSO) were used to interfere with the synthesis of glutathione (GSH) in the SMMC-7721 cells, then, the effects of α-hederin on cell proliferation, cell apoptosis, adenosine triphosphate (ATP) and reactive oxygen species (ROS) and mitochondrial membrane potential were detected. The protein levels of Bax, Bcl-2, cleaved caspase-3, cleaved caspase-9, apoptosis-inducing factor (AIF) and cytochrome C (Cyt C) were detected by western blotting. The antitumor efficacy of α-hederin on HCC was also evaluated in nude mice with xenograft tumor. The apoptosis of cancer cells in xenograft tumor were examined by TUNEL staining. In this research, as we used NAC and BSO to interfere with the synthesis of GSH, the mechanism we explored was more persuasive.

Research results

The α-hederin treatment inhibited cell growth of the three cell lines in a dose- and time-dependent manner. The IC50 values at 24 h for SMMC-7721, HepG-2 and Huh-7 cells were 13.88, 18.45 and 25.52 μmol/L, respectively, so we used SMMC-7721 cells for the on-going experiments. The results showed that the apoptosis rates in the control, low-dose α-hederin (5 μmol/L), mid-dose α-hederin (10 μmol/L) and high-dose α-hederin (20 μmol/L) groups were 0.90% ± 0.26%, 12% ± 2.05, 21% ± 2.15 and 37% ± 3.8%, respectively. In comparison to the control, after treatment with α-hederin, ROS increased significantly, while the ATP levels decreased. When SMMC-7721 cells were pretreated with BSO (2 mmol/L), compared with the mid-dose α-hederin group, the apoptosis rate increased to 27% ± 3.5% (P < 0.05); what’s more, the increase of ROS and the decrease of ATP were both enhanced. However, NAC pretreatment had a protective effect on SMMC-7721 cells and could alleviate the change of ROS and ATP. The proteins involving in the mitochondria-mediated pathway were detected by western blotting. The results showed α-hederin increased the levels of Bax, cleaved caspase-3 and cleaved caspase-9, and decreased Bcl-2 expression levels. Meanwhile, AIF and Cyt C in cytoplasm were up-regulated, but AIF and Cyt C in mitochondria were down-regulated. Subcutaneous xenografts were successfully constructed in 24 nude mice. After treatment with α-hederin for 3 wk, the weight of xenograft tumor was significantly reduced (P < 0.05). Compared to the control group, TUNEL staining showed a gradual increase in the proportion of apoptotic cells with the increase of α-hederin concentration (P < 0.05). There was no difference between the control mice and α-hederin-treated mic for the hepatic and renal functions. This research indicated that α-hederin could induce HCC cell apoptosis via mitochondria-mediated pathway by depleting GSH and accumulating ROS. But it did not explain how α-hederin changed the expression of GSH and ROS, and the effect of α-hederin on HCC cell invasion was not studied either. In addition, apoptosis involves multiple factors and multiple links, making it necessary to conduct in-depth research to clarify the specific mechanism.

Research conclusions

The α-hederin saponin induces apoptosis of HCC cells via the mitochondrial pathway mediated by increased intracellular ROS and may be an effective treatment for human HCC.

Research perspectives

It is of great value to discover natural anticancer compounds which have high efficacy and low toxicity in the treatment of HCC. In our study, we show that α-hederin could induce HCC cell apoptosis via mitochondria-mediated pathway by depleting GSH and accumulating ROS, which identifies α-hederin as a potential highly effective natural medicine with limited toxicity for HCC treatment. But some points remain unclear. How does α-hederin change the expression of ATP? The effect of α-hederin on HCC cell migration and invasion was not studied, either. In addition, apoptosis involves multiple factors and multiple links, and it’s necessary to conduct in-depth research to clarify specific mechanism. These results will facilitate the development of treatment for HCC.