Original Article
Copyright ©2013 Baishideng Publishing Group Co., Limited. All rights reserved.
World J Gastroenterol. Mar 21, 2013; 19(11): 1718-1727
Published online Mar 21, 2013. doi: 10.3748/wjg.v19.i11.1718
Cancer detection by ubiquitin carboxyl-terminal esterase L1 methylation in pancreatobiliary fluids
Norihiro Kato, Hiroyuki Yamamoto, Yasushi Adachi, Hirokazu Ohashi, Hiroaki Taniguchi, Hiromu Suzuki, Mayumi Nakazawa, Hiroyuki Kaneto, Shigeru Sasaki, Kohzoh Imai, Yasuhisa Shinomura
Norihiro Kato, Hiroyuki Yamamoto, Yasushi Adachi, Hirokazu Ohashi, Mayumi Nakazawa, Shigeru Sasaki, Yasuhisa Shinomura, First Department of Internal Medicine, Sapporo Medical University School of Medicine, Sapporo 060-8543, Japan
Hiroaki Taniguchi, Kohzoh Imai, The Section of Antibody, Vaccine and Molecular Targeted Therapy Research, The Institute of Medical Science, The University of Tokyo, Tokyo 108-8639, Japan
Hiromu Suzuki, Department of Molecular Biology, Sapporo Medical University School of Medicine, Sapporo 060-8556, Japan
Hiroyuki Kaneto, Division of Gastroenterology, Muroran City General Hospital, Muroran 051-8512, Japan
Author contributions: Kato N and Taniguchi H performed experiments and analyzed the data; Yamamoto H designed the research, performed experiments, analyzed the data and wrote the manuscript; Adachi Y, Suzuki H, Kaneto H and Sasaki S analyzed the data; Ohashi H and Nakazawa M performed experiments; Imai K and Shinomura Y edited the manuscript.
Supported by Grants-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan (to Yamamoto H and Shinomura Y)
Correspondence to: Hiroyuki Yamamoto, MD, FJSIM, PhD, First Department of Internal Medicine, Sapporo Medical University School of Medicine, S-1, W-16, Chuo-ku, Sapporo 060-8543, Japan. h-yama@sapmed.ac.jp
Telephone: +81-11-6112111 Fax: +81-11-6112282
Received: September 14, 2012
Revised: January 11, 2013
Accepted: January 23, 2013
Published online: March 21, 2013
Processing time: 189 Days and 3.1 Hours
Abstract

AIM: To evaluate the utility of measuring epigenetic alterations in pancreatic and biliary fluids in determining molecular markers for pancreatobiliary cancers.

METHODS: DNA was extracted from undiluted pancreatic and biliary fluids. As a surrogate for a genome-wide hypomethylation assay, levels of long interspersed nuclear element-1 (LINE-1) methylation were analyzed using bisulfite pyrosequencing. CpG island hypermethylation of 10 tumor-associated genes, aryl-hydrocarbon receptor repressor, adenomatous polyposis coli, calcium channel, voltage dependent, T type α1G subunit, insulin-like growth factor 2, O-6-methyl-guanine-DNA methyltransferase, neurogenin 1, CDKN2A, runt-related transcription factor 3 (RUNX3), secreted frizzled-related protein 1, and ubiquitin carboxyl-terminal esterase L1 (UCHL1), was analyzed using MethyLight. To examine the role of CpG methylation and histone deacetylation in the silencing of UCHL1, human gallbladder carcinoma cell lines and pancreatic carcinoma cell lines were treated with 2 or 5 μmol/L 5-AZA-dC for 72 h or 100 nmol/L Trichostatin A for 24 h. After the treatment, UCHL1 expression was analyzed by real-time reverse transcription-polymerase chain reaction.

RESULTS: Pancreatobiliary cancers exhibited significantly lower LINE-1 methylation levels in pancreatic and biliary fluids than did noncancerous pancreatobiliary disease (58.7% ± 4.3% vs 61.7% ± 2.2%, P = 0.027; 53.8% ± 6.6% vs 57.5% ± 1.7%, P = 0.007); however, LINE-1 hypomethylation was more evident in pancreatic cancer tissues than in pancreatic fluids (45.4% ± 5.5% vs 58.7% ± 4.3%, P < 0.001). CpG island hypermethylation of tumor-associated genes was detected at various frequencies, but it was not correlated with LINE-1 hypomethylation. Hypermethylation of the UCHL1 gene was cancer-specific and most frequently detected in pancreatic (67%) or biliary (70%) fluids from patients with pancreatobiliary cancer. As a single marker, hypermethylation of the UCHL1 gene in pancreatic and biliary fluids was most useful for the detection of pancreatic and pancreatobiliary cancers, respectively (100% specificity). Hypermethylation of the UCHL1 and RUNX3 genes in pancreatic and biliary fluids was the most useful combined marker for pancreatic (87% sensitivity and 100% specificity) and pancreatobiliary (97% sensitivity and 100% specificity) cancers. Treatment with a demethylating agent, 5-AZA-2’-deoxycytidine, restored UCHL1 expression in pancreatobiliary cancer cell lines.

CONCLUSION: Our results suggest that hypermethylation of UCHL1 and RUNX3 in pancreatobiliary fluid might be useful for the diagnosis of pancreatobiliary cancers.

Keywords: Pancreatobiliary cancers; DNA methylation; Pancreatobiliary fluids; Ubiquitin carboxyl-terminal esterase L1; Runt-related transcription factor 3