Systematic Reviews
Copyright ©The Author(s) 2015. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastroenterol. May 28, 2015; 21(20): 6317-6328
Published online May 28, 2015. doi: 10.3748/wjg.v21.i20.6317
Integrative analysis of aberrant Wnt signaling in hepatitis B virus-related hepatocellular carcinoma
Shan-Long Ding, Zi-Wei Yang, Jie Wang, Xiao-Lei Zhang, Xiang-Mei Chen, Feng-Min Lu
Shan-Long Ding, Zi-Wei Yang, Jie Wang, Xiao-Lei Zhang, Xiang-Mei Chen, Feng-Min Lu, Department of Microbiology and Infectious Disease Center, School of Basic Medical Sciences, Peking University Health Science Center, Beijing 100191, China
Author contributions: Wang J, Chen XM, and Lu FM designed the study; Ding SL, Yang ZW, and Zhang XL performed the majority of the experiments; Ding SL wrote the manuscript; and Lu FM edited the manuscript.
Supported by National Natural Science Foundation of China, No. 81372603; 973 Program, No. 2015CB554000; National S T Major Project for Infectious Diseases, No. 2012ZX10004-904; and The 111 Project, No. B07001.
Conflict-of-interest: The authors declare no conflicts of interest related to this manuscript.
Data sharing: No additional data are available.
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: Feng-Min Lu, PhD, Department of Microbiology and Infectious Disease Center, School of Basic Medical Sciences, Peking University Health Science Center, 38 Xueyuan Road, Beijing 100191, China. lu.fengmin@bjmu.edu.cn
Telephone: +86-10-82805136 Fax: +86-10-82805136
Received: December 21, 2014
Peer-review started: December 22, 2014
First decision: January 8, 2015
Revised: January 22, 2015
Accepted: March 12, 2015
Article in press: March 12, 2015
Published online: May 28, 2015
Processing time: 159 Days and 20 Hours
Abstract

AIM: To comprehensively understand the underlying molecular events accounting for aberrant Wnt signaling activation in hepatocellular carcinoma (HCC).

METHODS: This study was retrospective. The HCC tissue specimens used in this research were obtained from patients who underwent liver surgery. The Catalogue of Somatic Mutations in Cancer (COSMIC) database was searched for the mutation statuses of CTNNB1, TP53, and protein degradation regulator genes of CTNNB1. Dual-luciferase reporter assay was performed with TOP/FOP reporters to detect whether TP53 gain-of-function (GOF) mutations could enhance the transcriptional activity of Wnt signaling. Methylation sensitive restriction enzyme-quantitative PCR was used to explore the methylation status of CpG islands located in the promoters of APC, SFRP1, and SFRP5 in HCCs with different risk factors. Finally, nested-reverse transcription PCR was performed to examine the integration of HBx in front of LINE1 element and the existence of HBx-LINE1 chimeric transcript in Hepatitis B virus-related HCC. All results in this article were analyzed with the software SPSS version 19.0 for Windows, and different groups were compared by χ2 test as appropriate.

RESULTS: Based on the data from COSMIC database, compared with other solid tumors, mutation frequency of CTNNB1 was significantly higher in HCC (P < 0.01). The rate of CTNNB1 mutation was significantly less frequent in Hepatitis B virus-related HCC than in other etiologies (P < 0.01). Dual-luciferase reporter system and TOP/FOP reporter assays confirmed that TP53 GOF mutants were able to enhance the transcriptional ability of Wnt signaling. An exclusive relationship between the status of TP53 and CTNNB1 mutations was observed. However, according to the COSMIC database, TP53 GOF mutation is rare in HCC, which indicates that TP53 GOF mutation is not a reason for the aberrant activation of Wnt signaling in HCC. APC and AXIN1 were mutated in HCC. By using methylation sensitive restriction enzyme-quantitative PCR, hypermethylation of APC was detected in HCC with different risk factors, whereas SFRP1 and SFRP5 were not hypermethylated in any of the HCC etiologies, which indicates that the mutation of APC and AXIN1, together with the methylation of APC could take part in the overactivation of Wnt signaling. Nested-reverse transcription PCR failed to detect the integration of HBx before the LINE1 element, or the existence of an HBx-LINE1 chimeric transcript, suggesting that integration could not play a role in the aberrant activation of Wnt signaling in HCC.

CONCLUSION: In HCC, genetic/epigenetic aberration of CTNNB1 and its protein degradation regulators are the major cause of Wnt signaling overactivation.

Keywords: β-catenin; CTNNB1; Hepatitis B virus; Hepatocellular carcinoma; TP53; Wnt signaling

Core tip: Abnormal activation of Wnt/β-catenin signaling can be detected in approximately 50%-70% of hepatocellular carcinoma (HCC). It is necessary to take the analysis about the cause of Wnt/β-catenin signaling pathway aberration with the etiologic differences into consideration. In this review, the suggested genetic/epigenetic aberrations and their involvement in the abnormal Wnt/β-catenin overactivation in HCC were comprehensively analyzed, with focus on the cause of hepatitis B virus-related HCC. We suggest that genetic/epigenetic aberration of CTNNB1 and its protein degradation regulators are the major cause of Wnt signaling overactivation. TP53 gain-of-function mutation is seldom involved, and HBx-LINE1 chimeric transcripts created by viral integration may not be present.