Methylation of multiple genes as molecular markers for diagnosis of a small, well-differentiated hepatocellular carcinoma

International Journal of Cancer

Volumn 125, Issue 2, 2009, Pages 388-397

  Moribe, Toyoki ^a   Iizuka, Norio ^b   Miura, Toshiaki ^a   Kimura, Naoki ^a   Tamatsukuri, Shigeru ^a   Ishitsuka, Hideo ^a   Hamamoto, Yoshihiko ^c   Sakamoto, Kazuhiko ^b   Tamesa, Takao ^b   Oka, Masaaki ^b  

^a Research Group   (Japan)

^b YAMAGUCHI UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c YAMAGUCHI UNIVERSITY   (Japan)

Author keywords

Early hepatocellular carcinoma (HCC); Molecular marker; Multiple genes methylation; Well differentiated HCC

Indexed keywords

APC PROTEIN; CASPASE 8; CYCLIN D2; CYCLIN DEPENDENT KINASE INHIBITOR 2A; GLUTATHIONE TRANSFERASE P1; MOLECULAR MARKER; OCTAMER TRANSCRIPTION FACTOR 6; RAS ASSOCIATION DOMAIN FAMILY PROTEIN 1A; SERINE PROTEINASE INHIBITOR; TRANSCRIPTION FACTOR RUNX3; TRANSMEMBRANE CONDUCTANCE REGULATOR; TUMOR PROTEIN P73; UNCLASSIFIED DRUG; PRIMER DNA; TUMOR MARKER;

ADULT; AGED; ARTICLE; CANCER DIAGNOSIS; CLINICAL ARTICLE; COMPUTER MODEL; CONTROLLED STUDY; CPG ISLAND; DIAGNOSTIC ACCURACY; DNA METHYLATION; FEMALE; GENE SEQUENCE; HUMAN; HUMAN TISSUE; LIVER CELL CARCINOMA; MALE; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PYROSEQUENCING; SENSITIVITY AND SPECIFICITY; BLOOD; CASE CONTROL STUDY; CELL DIFFERENTIATION; GENETICS; LIVER TUMOR; PATHOLOGY; VALIDATION STUDY;

BASE SEQUENCE; CARCINOMA, HEPATOCELLULAR; CASE-CONTROL STUDIES; CELL DIFFERENTIATION; CPG ISLANDS; DNA METHYLATION; DNA PRIMERS; HUMANS; LIVER NEOPLASMS; POLYMERASE CHAIN REACTION; TUMOR MARKERS, BIOLOGICAL;

EID: 67449090372     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.24394     Document Type: Article

References (38)

1. El-Serag HB, Mason AC. Rising incidence of hepatocellular carcinoma in the United States. N Engl J Med 1999;340:745-50.
2. Okuda K. Hepatocellular carcinoma. J Hepatol 2000;32:225-37.
3. Bruix J, Sherman M, Llovet JM, Beaugrand M, Lencioni R, Burroughs AK, Christensen E, Pagliaro L, Colombo M, Rodés J; EASL Panel of Experts on HCC. Clinical management of hepatocellular carcinoma. Conclusions of the Barcelona-2000 EASL conference. European Association for the Study of the Liver. J Hepatol 2001;35:421-30.
4. Kojiro M. Focus on dysplastic nodules and early hepatocellular carcinoma: an Eastern point of view. Liver Transpl 2004;10 (2 Suppl 1):S3-S8.
5. Esteller M, Corn PG, Baylin SB, Herman JG. A gene hypermethylation profile of human cancer. Cancer Res 2001;61:3225-9.
6. Jones PA, Baylin SB. The fundamental role of epigenetic events in cancer. Nat Rev Genet 2002;3:415-28.
7. Herman JG, Baylin SB. Gene silencing in cancer in association with promoter hypermethylation. N Engl J Med 2003;349:2042-54.
8. Dammann R, Li C, Yoon JH, Chin PL, Bates S, Pfeifer GP. Epigenetic inactivation of a RAS association domain family protein from the lung tumour suppressor locus 3p21.3. Nat Genet 2000;25:315-9.
9. Jin Z, Tamura G, Tsuchiya T, Sakata K, Kashiwaba M, Osakabe M, Motoyama T. Adenomatous polyposis coli (APC) gene promoter hypermethylation in primary breast cancers. Br J Cancer 2001;85:69-73.
10. Song JZ, Stirzaker C, Harrison J, Melki JR, Clark SJ. Hypermethylation trigger of the glutathione-S-transferase gene (GSTP1) in prostate cancer cells. Oncogene 2002;21:1048-61.
11. Ku JL, Kang SB, Shin YK, Kang HC, Hong SH, Kim IJ, Shin JH, Han IO, Park JG. Promoter hypermethylation downregulates RUNX3 gene expression in colorectal cancer cell lines. Oncogene 2004;23:6736-42.
12. Sakuma M, Akahira J, Ito K, Niikura H, Moriya T, Okamura K, Sasano H, Yaegashi N. Promoter methylation status of the Cyclin D2 gene is associated with poor prognosis in human epithelial ovarian cancer. Cancer Sci 2007;98:380-6.
13. Kanai Y, Hui AM, Sun L, Ushijima S, Sakamoto M, Tsuda H, Hirohashi S. DNA hypermethylation at the D17S5 locus and reduced HIC-1 mRNA expression are associated with hepatocarcinogenesis. Hepatology 1999;29:703-9.
14. Tchou JC, Lin X, Freije D, Isaacs WB, Brooks JD, Rashid A, De Marzo AM, Kanai Y, Hirohashi S, Nelson WG. GSTP1 CpG island DNA hypermethylation in hepatocellular carcinomas. Int J Oncol 2000;16:663-76.
15. Kaneto H, Sasaki S, Yamamoto H, Itoh F, Toyota M, Suzuki H, Ozeki I, Iwata N, Ohmura T, Satoh T, Karino Y, Satoh T, et al. Detection of hypermethylation of the p16(INK4A) gene promoter in chronic hepatitis and cirrhosis associated with hepatitis B or C virus. Gut 2001;48:372-7.
16. Yu J, Ni M, Xu J, Zhang H, Gao B, Gu J, Chen J, Zhang L, Wu M, Zhen S, Zhu J. Methylation profiling of twenty promoter-CpG islands of genes which may contribute to hepatocellular carcinogenesis. BMC Cancer 2002;2:29.
17. Yu J, Zhang HY, Ma ZZ, Lu W, Wang YF, Zhu JD. Methylation profiling of twenty four genes and the concordant methylation behaviours of nineteen genes that may contribute to hepatocellular carcinogenesis. Cell Res 2003;13:319-33.
18. Fukai K, Yokosuka O, Chiba T, Hirasawa Y, Tada M, Imazeki F, Kataoka H, Saisho H. Hepatocyte growth factor activator inhibitor 2/placental bikunin (HAI-2/PB) gene is frequently hypermethylated in human hepatocellular carcinoma. Cancer Res 2003;63:8674-9.
19. Ding S, Gong BD, Yu J, Gu J, Zhang HY, Shang ZB, Fei Q, Wang P, Zhu JD. Methylation profile of the promoter CpG islands of 14 "drug- resistance" genes in hepatocellular carcinoma. World J Gastroenterol 2004;10:3433-40.
20. Mori T, Nomoto S, Koshikawa K, Fujii T, Sakai M, Nishikawa Y, Inoue S, Takeda S, Kaneko T, Nakao A. Decreased expression and frequent allelic inactivation of the RUNX3 gene at 1p36 in human hepatocellular carcinoma. Liver Int 2005;25:380-8.
21. Lehmann U, Berg-Ribbe I, Wingen LU, Brakensiek K, Becker T, Klempnauer J, Schlegelberger B, Kreipe H, Flemming P. Distinct methylation patterns of benign and malignant liver tumors revealed by quantitative methylation profiling. Clin Cancer Res 2005;11:3654-60.
22. Sobin LH, Wittekind C. TNM classification of malignant tumors, 6th edn. UICC: Wiley-Liss, 2002.81-3.
23. Moribe T, Iizuka N, Miura T, Stark M, Tamatsukuri S, Ishitsuka H, Hamamoto Y, Sakamoto K, Tamesa T, Oka M. Identification of novel aberrant methylation of BASP1 and SRD5A2 for early diagnosis of hepatocellular carcinoma by genome-wide search. Int J Oncol 2008;33:949-58.
24. Monroe JJ, Manjanatha MG, Skopek TR. Extent of CpG methylation is not proportional to the in vivo spontaneous mutation frequency at transgenic loci in Big BlueTM rodents. Mutat Res 2001;476:1-11.
25. Tost J, Schatz P, Schuster M, Berlin K, Gut IG. Analysis and accurate quantification of CpG methylation by MALDI mass spectrometry. Nucleic Acids Res 2003;31:e50.
26. Iizuka N, Sakaida I, Moribe T, Fujita N, Miura T, Stark M, Tamatsukuri S, Ishitsuka H, Uchida K, Terai S, Sakamoto K, Tamesa T, et al. Elevated levels of circulating cell-free DNA in the blood of patients with hepatitis C virus-associated hepatocellular carcinoma. Anticancer Res 2006;26:4713-9.
27. Colella S, Shen L, Baggerly KA, Issa JP, Krahe R. Sensitive and quantitative universal pyrosequencing methylation analysis of CpG sites. Biotechniques 2003;35:146-50.
28. Iizuka N, Oka M, Yamada-Okabe H, Mori N, Tamesa T, Okada T, Takemoto N, Tangoku A, Hamada K, Nakayama H, Miyamoto T, Uchimura S, et al. Comparison of gene expression profiles between hepatitis B virus- and hepatitis C virus-infected hepatocellular carcinoma by oligonucleotide microarray data on the basis of a supervised learning method. Cancer Res 2002;62:3939-44.
29. Narimatsu T, Tamori A, Koh N, Kubo S, Hirohashi K, Yano Y, Arakawa T, Otani S, Nishiguchi S. p16 Promoter hypermethylation in human hepatocellular carcinoma with or without hepatitis virus infection. Intervirology 2004;47:26-31.
30. Saito Y, Kanai Y, Sakamoto M, Saito H, Ishii H, Hirohashi S. Expression of mRNA for DNA methyltransferases and methyl-CpG-binding proteins and DNA methylation status on CpG islands and pericentromeric satellite regions during human hepatocarcinogenesis. Hepatology 2001;33:561-8.
31. Fukai K, Yokosuka O, Imazeki F, Tada M, Mikata R, Miyazaki M, Ochiai T, Saisho H. Methylation status of p14ARF, p15INK4b, and p16INK4a genes in human hepatocellular carcinoma. Liver Int 2005;25:1209-16.
32. Harder J, Opitz OG, Brabender J, Olschewski M, Blum HE, Nomoto S, Usadel H. Quantitative promoter methylation analysis of hepatocellular carcinoma, cirrhotic and normal liver. Int J Cancer 2008;122: 2800-4.
33. Herman JG, Graff JR, Myöhänen S, Nelkin BD, Baylin SB. Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. Proc Natl Acad Sci USA 1996;93:9821-6.
34. Kondo Y, Shen L, Suzuki S, Kurokawa T, Masuko K, Tanaka Y, Kato H, Mizuno Y, Yokoe M, Sugauchi F, Hirashima N, Orito E, et al. Alterations of DNA methylation and histone modifications contribute to gene silencing in hepatocellular carcinomas. Hepatol Res 2007;37:974-83.
35. Nishida N, Nagasaka T, Nishimura T, Ikai I, Boland CR, Goel A. Aberrant methylation of multiple tumor suppressor genes in aging liver, chronic hepatitis, and hepatocellular carcinoma. Hepatology 2008;47:908-18.
36. Morris MR, Gentle D, Abdulrahman M, Maina EN, Gupta K, Banks RE, Wiesener MS, Kishida T, Yao M, Teh B, Latif F, Maher ER. Tumor suppressor activity and epigenetic inactivation of hepatocyte growth factor activator inhibitor type 2/SPINT2 in papillary and clear cell renal cell carcinoma. Cancer Res 2005;65:4598-606.
37. Yoshikawa H, Matsubara K, Qian GS, Jackson P, Groopman JD, Manning JE, Harris CC, Herman JG. SOCS-1, a negative regulator of the JAK/STAT pathway, is silenced by methylation in human hepatocellular carcinoma and shows growth-suppression activity. Nat Genet 2001;28:29-35.
38. Bruix J, Boix L, Sala M, Llovet JM. Focus on hepatocellular carcinoma. Cancer Cell 2004;5:215-19.