Original Article
Copyright ©2014 Baishideng Publishing Group Inc. All rights reserved.
World J Gastroenterol. May 21, 2014; 20(19): 5826-5838
Published online May 21, 2014. doi: 10.3748/wjg.v20.i19.5826
Identification of biomarkers for hepatocellular carcinoma by semiquantitative immunocytochemistry
Hong Mu, Kai-Xuan Lin, Hong Zhao, Shu Xing, Cong Li, Fang Liu, Hai-Zhen Lu, Ze Zhang, Yu-Lin Sun, Xi-Yun Yan, Jian-Qiang Cai, Xiao-Hang Zhao
Hong Mu, Fang Liu, Yu-Lin Sun, Xiao-Hang Zhao, State Key Laboratory of Molecular Oncology, Cancer Institute Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100021, China
Kai-Xuan Lin, Ze Zhang, Xiao-Hang Zhao, Center of Basic Medical Sciences, Navy General Hospital of Chinese PLA, Beijing 100048, China
Hong Zhao, Cong Li, Jian-Qiang Cai, Department of Abdominal Surgery, Cancer Institute Hospital, Chinese Academy of Medical Science and Peking Union Medical College, Beijing 100021, China
Hai-Zhen Lu, Department of Pathology, Cancer Institute Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100021, China
Shu Xing, Xi-Yun Yan, Key Laboratory of Protein and Peptide Pharmaceutical, National Laboratory of Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, China
Author contributions: Mu H and Lin KX performed the majority of the work and wrote the manuscript; Zhao H, Li C, Liu F, Lu HZ, Zhang Z, and Sun YL assisted in the experiments and data analysis; Xing S analyzed the three dimensional reconstructions; Zhao XH, Yan XY, and Cai JQ supervised this work; Zhao XH designed the study.
Supported by Grants from the National High-tech R and D Program No. 2012AA020206, the Key Project for the Infectious Diseases No. 2012ZX10002-017 and No. 2013ZX10002009-001-004, the State Key Projects for Basic Research No. 2011CB910703, the National Natural Science Foundation No. 81372591, and No. 81321091 of China and the Center for Marine Medicine and Rescue of Tsinghua University
Correspondence to: Xiao-Hang Zhao, MD, PhD, State Key Laboratory of Molecular Oncology, Cancer Institute Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Panjiayuan Nanli 17, Chaoyang District, Beijing 100021, China. zhaoxh@cicams.ac.cn
Telephone: +86-10-67709015 Fax: +86-10-87778360
Received: December 31, 2013
Revised: February 14, 2014
Accepted: April 5, 2014
Published online: May 21, 2014
Processing time: 137 Days and 19.9 Hours
Abstract

AIM: To investigate the expression of key biomarkers in hepatoma cell lines, tumor cells from patients’ blood samples, and tumor tissues.

METHODS: We performed the biomarker tests in two steps. First, cells plated on coverslips were used to assess biomarkers, and fluorescence intensities were calculated using the NIH Image J software. The measured values were analyzed using the SPSS 19.0 software to make comparisons among eight cell lines. Second, eighty-four individual samples were used to assess the biomarkers’ expression. Negative enrichment of the blood samples was performed, and karyocytes were isolated and dropped onto pre-treated glass slides for further analysis by immunofluorescence staining. Fluorescence intensities were compared among hepatocellular carcinoma (HCC) patients, chronic HBV-infected patients, and healthy controls following methods similar to those used for cell lines. The relationships between the expression of biomarkers and clinical pathological parameters were analyzed by Spearman rank correlation tests. In addition, we studied the distinct biomarkers’ expression with three-dimensional laser confocal microscopy reconstructions, and Kaplan-Meier survival analysis was performed to understand the clinical significance of these biomarkers.

RESULTS: Microscopic examination and fluorescence intensity calculations indicated that cytokeratin 8/18/19 (CK) expression was significantly higher in six of the seven HCC cell lines examined than in the control cells, and the expression levels of asialoglycoprotein receptor (ASGPR) and glypican-3 (GPC3) were higher in all seven HCC cell lines than in the control. Cells obtained from HCC patients’ blood samples also displayed significantly higher expression levels of ASGPR, GPC3, and CK than cells from chronic HBV-infected patients or healthy controls; these proteins may be valuable surface biomarkers for identifying HCC circulating tumor cells isolated and enriched from the blood samples. The stem cell-like and epithelial-mesenchymal transition-related biomarkers could be detected on the karyocyte slides. ASGPR and GPC3 were expressed at high levels, and thus three-dimensional reconstructions were used to observe their expression in detail. This analysis indicated that GPC3 was localized in the cytoplasm and membrane, but that ASGPR had a polar localization. Survival analyses showed that expression of GPC3 and ASGPR is associated with a patient’s overall survival (OS).

CONCLUSION: ASGPR, GPC3, and CK may be valuable HCC biomarkers for CTC detection; the expression of ASGPR and GPC3 might be helpful for understanding patients’ OS.

Keywords: Hepatocellular carcinoma; Biomarker; Immunocytochemistry; Semiquantitative analysis; Three-dimensional reconstruction

Core tip: We report a novel workflow to detect potentially valuable biomarkers for hepatocellular carcinoma (HCC). We measured immunofluorescence intensity and performed statistical analyses to assess the expression of biomarkers in cell lines and patient blood samples. Furthermore, we determined the expression of biomarkers via three-dimensional reconstructions. These analyses indicated that asialoglycoprotein receptor (ASGPR), glypican-3 (GPC3), and cytokeratin (CK) may be valuable HCC biomarkers for detecting circulating tumor cells (CTCs). In addition, the expression of ASGPR and GPC3 might correlate with patients’ prognoses, and our CTC detection method can include epithelial cell adhesion molecule- and vimentin-positive tumor cells, and will thus supplement previous studies and potentially help predict future tumor recurrence and metastasis.