Distinct DNA methylation patterns in cirrhotic liver and hepatocellular carcinoma

International Journal of Cancer

Volumn 130, Issue 6, 2012, Pages 1319-1328

  Ammerpohl, Ole ^a   Pratschke, Johann ^b   Schafmayer, Clemens ^a   Haake, Andrea ^a   Faber, Wladimir ^b   Von Kampen, Oliver ^a   Brosch, Mario ^a   Sipos, Bence ^c   Von Schönfels, Witigo ^a   Balschun, Katharina ^a   Röcken, Christoph ^a   Arlt, Alexander ^a   Schniewind, Bodo ^a   Grauholm, Jonas ^d   Kalthoff, Holger ^a   Neuhaus, Peter ^e   Stickel, Felix ^f   Schreiber, Stefan ^a   Becker, Thomas ^a   Siebert, Reiner ^a   Hampe, Jochen ^a   more..

^a UNIVERSITY OF KIEL   (Germany)

^b UNIVERSITY OF INNSBRUCK   (Austria)

^c UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^d AROS Applied Biotechnology   (Denmark)

^e CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^f UNIVERSITY OF BERN   (Switzerland)

Author keywords

CpG island; hepatocellular carcinoma; liver cirrhosis; methylation

Indexed keywords

POLYCOMB GROUP PROTEIN; POLYCOMB REPRESSIVE COMPLEX 2; UNCLASSIFIED DRUG;

ADULT; AGED; ALOX12 GENE; ANGPTL7 GENE; ARTICLE; CELSR1 GENE; CONTROLLED STUDY; CPG ISLAND; CRMP1 GENE; DNA DETERMINATION; DNA METHYLATION; EPIGENETICS; FEMALE; GENE; GENE LOCUS; GNRH2 GENE; HUMAN; HUMAN TISSUE; LIVER CARCINOGENESIS; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; LOC55908 GENE; MALE; PRIORITY JOURNAL; PROMOTER REGION; SEQUENCE ANALYSIS; SPRR3 GENE; TNFSF15 GENE;

CARCINOMA, HEPATOCELLULAR; CPG ISLANDS; DNA METHYLATION; EMBRYONIC STEM CELLS; EPIGENESIS, GENETIC; HUMANS; LIVER CIRRHOSIS; LIVER NEOPLASMS; PRINCIPAL COMPONENT ANALYSIS; PROMOTER REGIONS, GENETIC; REPRESSOR PROTEINS; REPRODUCIBILITY OF RESULTS;

EID: 84856100724     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.26136     Document Type: Article

References (49)

1. Bosch FX, Ribes J, Borras J,. Epidemiology of primary liver cancer. Semin Liver Dis 1999; 19: 271-85. (Pubitemid 29488770)
2. Dufour JF, Johnson P,. Liver cancer: from molecular pathogenesis to new therapies: summary of the EASL single topic conference. J Hepatol 2010; 52: 296-304.
3. Schutte K, Bornschein J, Malfertheiner P,. Hepatocellular carcinoma-epidemiological trends and risk factors. Digest Dis (Basel, Switzerland) 2009; 27: 80-92.
4. El-Serag HB, Rudolph KL,. Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology 2007; 132: 2557-76. (Pubitemid 46890874)
5. Farazi PA, DePinho RA,. Hepatocellular carcinoma pathogenesis: from genes to environment. Nat Rev 2006; 6: 674-87. (Pubitemid 44286000)
6. Woo HG, Park ES, Lee JS, Lee YH, Ishikawa T, Kim YJ, Thorgeirsson SS,. Identification of potential driver genes in human liver carcinoma by genomewide screening. Cancer Res 2009; 69: 4059-66.
7. Schlaeger C, Longerich T, Schiller C, Bewerunge P, Mehrabi A, Toedt G, Kleeff J, Ehemann V, Eils R, Lichter P, Schirmacher P, Radlwimmer B,. Etiology-dependent molecular mechanisms in human hepatocarcinogenesis. Hepatology 2008; 47: 511-20. (Pubitemid 351280719)
8. Kaposi-Novak P, Libbrecht L, Woo HG, Lee YH, Sears NC, Coulouarn C, Conner EA, Factor VM, Roskams T, Thorgeirsson SS,. Central role of c-Myc during malignant conversion in human hepatocarcinogenesis. Cancer Res 2009; 69: 2775-82.
9. Ji J, Shi J, Budhu A, Yu Z, Forgues M, Roessler S, Ambs S, Chen Y, Meltzer PS, Croce CM, Qin LX, Man K, et al. MicroRNA expression, survival, and response to interferon in liver cancer. N Engl J Med 2009; 361: 1437-47.
10. Hoshida Y, Villanueva A, Kobayashi M, Peix J, Chiang DY, Camargo A, Gupta S, Moore J, Wrobel MJ, Lerner J, Reich M, Chan JA, et al. Gene expression in fixed tissues and outcome in hepatocellular carcinoma. N Engl J Med 2008; 359: 1995-2004.
11. Jones PA, Baylin SB,. The epigenomics of cancer. Cell 2007; 128: 683-92. (Pubitemid 46273572)
12. Gal-Yam EN, Saito Y, Egger G, Jones PA,. Cancer epigenetics: modifications, screening, and therapy. Annu Rev Med 2008; 59: 267-80. (Pubitemid 351287937)
13. Martin-Subero JI, Kreuz M, Bibikova M, Bentink S, Ammerpohl O, Wickham-Garcia E, Rosolowski M, Richter J, Lopez-Serra L, Ballestar E, Berger H, Agirre X, et al. New insights into the biology and origin of mature aggressive B-cell lymphomas by combined epigenomic, genomic, and transcriptional profiling. Blood 2009; 113: 2488-97.
14. Robertson KD, Wolffe AP,. DNA methylation in health and disease. Nat Rev Genet 2000; 1: 11-9.
15. Costello JF, Fruhwald MC, Smiraglia DJ, Rush LJ, Robertson GP, Gao X, Wright FA, Feramisco JD, Peltomaki P, Lang JC, Schuller DE, Yu L, et al. Aberrant CpG-island methylation has non-random and tumour-type-specific patterns. Nat Genet 2000; 24: 132-8. (Pubitemid 30094712)
16. Jones PA, Baylin SB,. The fundamental role of epigenetic events in cancer. Nat Rev Genet 2002; 3: 415-28. (Pubitemid 34587077)
17. Costello JF, Plass C, Cavenee WK,. Aberrant methylation of genes in low-grade astrocytomas. Brain Tumor Pathol 2000; 17: 49-56.
18. Faust C, Lawson KA, Schork NJ, Thiel B, Magnuson T,. The Polycomb-group gene eed is required for normal morphogenetic movements during gastrulation in the mouse embryo. Development (Cambridge, England) 1998; 125: 4495-506. (Pubitemid 28564293)
19. O'Carroll D, Erhardt S, Pagani M, Barton SC, Surani MA, Jenuwein T,. The polycomb-group gene Ezh2 is required for early mouse development. Mol Cell Biol 2001; 21: 4330-6. (Pubitemid 32565314)
20. Peng JC, Valouev A, Swigut T, Zhang J, Zhao Y, Sidow A, Wysocka J,. Jarid2/Jumonji coordinates control of PRC2 enzymatic activity and target gene occupancy in pluripotent cells. Cell 2009; 139: 1290-302.
21. Schlesinger Y, Straussman R, Keshet I, Farkash S, Hecht M, Zimmerman J, Eden E, Yakhini Z, Ben-Shushan E, Reubinoff BE, Bergman Y, Simon I, et al. Polycomb-mediated methylation on Lys27 of histone H3 pre-marks genes for de novo methylation in cancer. Nat Genet 2007; 39: 232-6. (Pubitemid 46184355)
22. Bracken AP, Helin K,. Polycomb group proteins: navigators of lineage pathways led astray in cancer. Nat Rev 2009; 9: 773-84.
23. Gal-Yam EN, Egger G, Iniguez L, Holster H, Einarsson S, Zhang X, Lin JC, Liang G, Jones PA, Tanay A,. Frequent switching of Polycomb repressive marks and DNA hypermethylation in the PC3 prostate cancer cell line. Proc Natl Acad Sci USA 2008; 105: 12979-84.
24. Ushijima T, Morimura K, Hosoya Y, Okonogi H, Tatematsu M, Sugimura T, Nagao M,. Establishment of methylation-sensitive-representational difference analysis and isolation of hypo- and hypermethylated genomic fragments in mouse liver tumors. Proc Natl Acad Sci USA 1997; 94: 2284-9. (Pubitemid 27136866)
25. Calvisi DF, Ladu S, Gorden A, Farina M, Lee JS, Conner EA, Schroeder I, Factor VM, Thorgeirsson SS,. Mechanistic and prognostic significance of aberrant methylation in the molecular pathogenesis of human hepatocellular carcinoma. J Clin Invest 2007; 117: 2713-22. (Pubitemid 47494371)
26. Chaubert P, Gayer R, Zimmermann A, Fontolliet C, Stamm B, Bosman F, Shaw P,. Germ-line mutations of the p16INK4(MTS1) gene occur in a subset of patients with hepatocellular carcinoma. Hepatology 1997; 25: 1376-81. (Pubitemid 27250757)
27. 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. (Pubitemid 38420864)
28. Zhang YJ, Ahsan H, Chen Y, Lunn RM, Wang LY, Chen SY, Lee PH, Chen CJ, Santella RM,. High frequency of promoter hypermethylation of RASSF1A and p16 and its relationship to aflatoxin B1-DNA adduct levels in human hepatocellular carcinoma. Mol Carcinog 2002; 35: 85-92.
29. 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. (Pubitemid 32405812)
30. Okochi O, Hibi K, Sakai M, Inoue S, Takeda S, Kaneko T, Nakao A,. Methylation-mediated silencing of SOCS-1 gene in hepatocellular carcinoma derived from cirrhosis. Clin Cancer Res 2003; 9: 5295-8. (Pubitemid 37413582)
31. Schagdarsurengin U, Wilkens L, Steinemann D, Flemming P, Kreipe HH, Pfeifer GP, Schlegelberger B, Dammann R,. Frequent epigenetic inactivation of the RASSF1A gene in hepatocellular carcinoma. Oncogene 2003; 22: 1866-71. (Pubitemid 36513145)
32. Tischoff I, Tannapfe A,. DNA methylation in hepatocellular carcinoma. World J Gastroenterol 2008; 14: 1741-8. (Pubitemid 351493380)
33. Huang J,. Current progress in epigenetic research for hepatocarcinomagenesis. Sci China 2009; 52: 31-42.
34. Huang J, Zheng DL, Qin FS, Cheng N, Chen H, Wan BB, Wang YP, Xiao HS, Han ZG,. Genetic and epigenetic silencing of SCARA5 may contribute to human hepatocellular carcinoma by activating FAK signaling. J Clin Invest 2010; 120: 223-41.
35. Lee TI, Jenner RG, Boyer LA, Guenther MG, Levine SS, Kumar RM, Chevalier B, Johnstone SE, Cole MF, Isono K, Koseki H, Fuchikami T, et al. Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 2006; 125: 301-13. (Pubitemid 44313811)
36. Weber M, Hellmann I, Stadler MB, Ramos L, Paabo S, Rebhan M, Schubeler D,. Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nat Genet 2007; 39: 457-66. (Pubitemid 46514772)
37. Martin-Subero JI, Ammerpohl O, Bibikova M, Wickham-Garcia E, Agirre X, Alvarez S, Bruggemann M, Bug S, Calasanz MJ, Deckert M, Dreyling M, Du MQ, et al. A comprehensive microarray-based DNA methylation study of 367 hematological neoplasms. PLoS One 2009; 4: e6986.
38. Richter J, Ammerpohl O, Martin-Subero JI, Montesinos-Rongen M, Bibikova M, Wickham-Garcia E, Wiestler OD, Deckert M, Siebert R,. Array-based DNA methylation profiling of primary lymphomas of the central nervous system. BMC Cancer 2009; 9: 455.
39. Cho RJ, Campbell MJ,. Transcription, genomes, function. Trends Genet 2000; 16: 409-15. (Pubitemid 30665374)
40. Bibikova M, Lin Z, Zhou L, Chudin E, Garcia EW, Wu B, Doucet D, Thomas NJ, Wang Y, Vollmer E, Goldmann T, Seifart C, et al. High-throughput DNA methylation profiling using universal bead arrays. Genome Res 2006; 16: 383-93. (Pubitemid 43327509)
41. Sherman M,. Hepatocellular carcinoma: epidemiology, surveillance, and diagnosis. Semin Liver Dis 2010; 30: 3-16.
42. Gao W, Kondo Y, Shen L, Shimizu Y, Sano T, Yamao K, Natsume A, Goto Y, Ito M, Murakami H, Osada H, Zhang J, et al. Variable DNA methylation patterns associated with progression of disease in hepatocellular carcinomas. Carcinogenesis 2008; 29: 1901-10.
43. Esteller M,. Cancer epigenomics: DNA methylomes and histone-modification maps. Nat Rev Genet 2007; 8: 286-98. (Pubitemid 46439286)
44. Ting AH, McGarvey KM, Baylin SB,. The cancer epigenome-components and functional correlates. Genes Dev 2006; 20: 3215-31.
45. Antequera F, Boyes J, Bird A,. High levels of de novo methylation and altered chromatin structure at CpG islands in cell lines. Cell 1990; 62: 503-14.
46. Ohm JE, McGarvey KM, Yu X, Cheng L, Schuebel KE, Cope L, Mohammad HP, Chen W, Daniel VC, Yu W, Berman DM, Jenuwein T, et al. A stem cell-like chromatin pattern may predispose tumor suppressor genes to DNA hypermethylation and heritable silencing. Nat Genet 2007; 39: 237-42. (Pubitemid 46184356)
47. Widschwendter M, Fiegl H, Egle D, Mueller-Holzner E, Spizzo G, Marth C, Weisenberger DJ, Campan M, Young J, Jacobs I, Laird PW,. Epigenetic stem cell signature in cancer. Nat Genet 2007; 39: 157-8. (Pubitemid 46184343)
48. de Lima VM, Oliveira CP, Alves VA, Chammas MC, Oliveira EP, Stefano JT, de Mello ES, Cerri GG, Carrilho FJ, Caldwell SH,. A rodent model of NASH with cirrhosis, oval cell proliferation and hepatocellular carcinoma. J Hepatol 2008; 49: 1055-61.
49. Spee B, Carpino G, Schotanus BA, Katoonizadeh A, Vander Borght S, Gaudio E, Roskams T,. Characterisation of the liver progenitor cell niche in liver diseases: potential involvement of Wnt and Notch signalling. Gut 2010; 59: 247-57.