CpG island hypermethylation of SOCS-1 gene is inversely associated with HBV infection in hepatocellular carcinoma

Cancer Letters

Volumn 271, Issue 2, 2008, Pages 240-250

  Ko, Eunkyung ^a   Kim, Sung Joo ^a   Joh, Jae Won ^a   Park, Cheol Keun ^a   Park, Joobae ^a,b   Kim, Duk Hwan ^a,b  

^a Sungkyunkwan University School of Medicine   (South Korea)

^b Samsung Medical Center   (South Korea)

Author keywords

Hepatic B virus; Hepatitis C virus; Hepatocellular carcinoma; Methylation; SOCS 1

Indexed keywords

SUPPRESSOR OF CYTOKINE SIGNALING 1;

ADULT; ARTICLE; CONTROLLED STUDY; CPG ISLAND; FEMALE; FROZEN SECTION; HEPATITIS B; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; MAJOR CLINICAL STUDY; MALE; METHYLATION; MULTIVARIATE LOGISTIC REGRESSION ANALYSIS; PREVALENCE; PRIORITY JOURNAL;

CARCINOMA, HEPATOCELLULAR; CPG ISLANDS; DNA METHYLATION; HEPATITIS B; HUMANS; IMMUNOHISTOCHEMISTRY; LIVER NEOPLASMS; MULTIVARIATE ANALYSIS; POLYMERASE CHAIN REACTION; PROPORTIONAL HAZARDS MODELS; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS;

CERCOPITHECINE HERPESVIRUS 1; HEPATITIS B VIRUS; HEPATITIS C VIRUS;

EID: 53249101337     PISSN: 03043835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.canlet.2008.06.009     Document Type: Article

References (48)

1. Parkin D.M., Bray F., Ferlay J., and Pisani P. Global cancer statistics, 2002. CA. Cancer J. Clin. 55 (2005) 74-108
2. Poon R.T., Fan S.T., and Wong J. Risk factors, prevention, and management of postoperative recurrence after resection of hepatocellular carcinoma. Ann. Surg. 232 (2000) 10-24
3. Naka T., Fujimoto M., and Kishimoto T. Negative regulation of cytokine signaling: STAT-induced STAT inhibitor. Trends Biochem. Sci. 24 (1999) 394-398
4. Ruff-Jamison S., Chen K., and Cohen S. Epidermal growth factor induces the tyrosine phosphorylation and nuclear translocation of Stat 5 in mouse liver. Proc. Natl. Acad. Sci. USA 92 (1995) 4215-4218
5. Cressman D.E., Diamond R.H., and Jaub R. Rapid activation of the stat3 transcription complex in liver regeneration. Hepatology 21 (1995) 1443-1449
6. Ram P.A., Park S.-H., Choi H.K., and Waxman D.J. Growth hormone activation of stat 1, stat 3, and stat 5 in rat liver. J. Biol. Chem. 271 (1996) 5929-5940
7. Endo T.A., Masuhara M., Yokouchi M., Suzuki R., Sakamoto H., Mitsui K., Matsumoto A., Tanimura S., Ohtsubo M., Misawa H., Miyazaki T., Leonor N., Taniguchi T., Fujita T., Kanakura Y., Komiya S., and Yoshimura A. A new protein containing an SH2 domain that inhibits JAK kinases. Nature 387 (1997) 921-924
8. Naka T., Narazaki M., Hirata M., Matsumoto T., Minamoto S., Aono A., Nishimoto N., Kajita T., Taga T., Yoshizaki K., Akira S., and Kishimoto T. Structure and function of a new STAT-induced STAT inhibitor. Nature 387 (1997) 924-929
9. Starr R., Willson T.A., Viney E.M., Starr R., Willson T.A., Viney E.M., Murray L.J., Rayner J.R., Jenkins B.J., Gonda T.J., Alexander W.S., Metcalf D., Nicola N.A., and Hilton D.J. A family of cytokine-inducible inhibitors of signaling. Nature 387 (1997) 917-921
10. Naka T., Matsumoto T., Narazaki M., Fujimoto M., Morita Y., Ohsawa Y., Saito H., Nagasawa T., Uchiyama Y., and Kishimoto T. Three distinct domains of SSI-1/SOCS-1/JAB protein are required for its suppression of interleukin 6 signaling. Proc. Natl. Acad. Sci. USA 95 (1998) 13130-13134
11. Yasukawa H., Sakamoto H., Masuhara M., Sasaki A., Wakioka T., Ohtsuka S., and Imaizumi T. The JAK-binding protein JAB inhibits Janus tyrosine kinase activity through binding in the activation loop. EMBO J. 18 (1999) 1309-1320
12. Rottapel R., Ilangumaran S., Neale C., La Rose J., Ho J.M., Nguyen M.H., Barber D., Dubreuil P., and de Sepulveda P. The tumor suppressor activity of SOCS-1. Oncogene 21 (2002) 4351-4362
13. Ilangumaran S., and Rottapel R. Regulation of cytokine receptor signaling by SOCS1. Immunol. Rev. 192 (2003) 196-211
14. Kishimoto T., and Kikutani H. Knocking the SOCS off a tumor suppressor. Nat. Genet. 28 (2001) 4-5
15. Yoshikawa H., Matsubara K., Qian G.S., Jackson P., Groopman J.D., Manning J.E., and Harris C.C. 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. 28 (2001) 29-35
16. Nagai H., Kim Y.S., Konishi N., Baba M., Kubota T., Yoshimura A., and Emi M. Combined hypermethylation and chromosome loss associated with inactivation of SSI-1/SOCS-1/JAB gene in human hepatocellular carcinoma. Cancer Lett. 186 (2002) 59-65
17. Okochi O., Hibi K., Sakai M., Inoue S., Takeda S., Kaneko T., and Nakao A. Methylation-mediated silencing of SOCS-1 gene in hepatocellular carcinoma derived from cirrhosis. Clin. Cancer Res. 9 (2003) 5295-5298
18. Yang B., Guo M., Herman J., and Clark D.P. Aberrant CpG island methylation profiles of tumor suppressor genes in hepatocellular carcinoma. Am. J. Pathol. 163 (2003) 1101-1107
19. Miyoshi H., Fujie H., Moriya K., Shintani Y., Tsutsumi T., Makuuchi M., Kimura S., and Koike K. Methylation status of suppressor of cytokine signaling-1 gene in hepatocellular carcinoma. J. Gastroenterol. 39 (2004) 563-569
20. Calvisi D.F., Ladu S., Gorden A., Farina M., Conner E.A., Lee J.S., Factor V.M., and Thorgeirsson S.S. Ubiquitous activation of Ras and Jak/Stat pathways in human HCC. Gastroenterology 130 (2006) 1117-1128
21. Morgan T.R., Mandayam S., and Jamal M.M. Alcohol and hepatocellular carcinoma. Gastroenterology 127 (2004) S87-S96
22. Greence F.L., Page F.L., and Fleming I.D. AJCC Cancer Staging Manual. sixth ed. (2002), Springer, New York pp. 132
23. Seeger C., and Mason W.S. Hepatitis B virus boil. Microbiol. Mol. Biol. Rev. 64 (2000) 51-68
24. Kim C.M., Koike K., Saito I., Miyamura T., and Jay G. HBx gene of hepatitis B virus induces liver cancer in transgenic mice. Nature 351 (1991) 317-320
25. Yu D.Y., Moon H.B., Son J.K., Jeong S., Yu S.L., Yoon H., Han Y.M., Lee C.S., Park J.S., Lee C.H., Hyun B.H., Murakami S., and Lee K.K. Incidence of hepatocellular carcinoma in transgenic mice expressing the hepatitis B virus X-protein. J. Hepatol. 31 (1999) 123-132
26. Chen H.S., Kaneko S., Girones R., Anderson R.W., Hornbuckle W.E., Tennant B.C., Cote P.J., Gerin J.L., Purcell R.H., and Miller R.H. The woodchuck hepatitis virus X gene is important for establishment of virus infection in woodchucks. J. Virol. 67 (1993) 1218-1226
27. Lee H., Lee Y.M., Huh Y.S., and Moon H. Y. X-gene product antagonizes the p53-mediated inhibition of hepatitis B virus replication through regulation of the pregenomic/core promoter. J. Biol. Chem. 270 (1995) 31405-31412
28. Bouchard M.J., and Schneider R.J. The enigmatic X gene of hepatitis B virus. J. Virol. 78 (2004) 12725-12734
29. Lee Y.-H., and Yun Y. HBx protein of hepatitis B virus activates Jak1-STAT signaling. J. Biol. Chem. 273 (1998) 25510-25515
30. Moriya K., Fujie H., Shintani Y., Yotsuyanagi H., Tsutsumi T., Ishibashi K., Matsuura Y., Kimura S., and Miyamura T. K. The core protein of hepatitis C virus induces hepatocellular carcinoma in transgenic mice. Nat. Med. 4 (1998) 1065-1067
31. Farazi P.A., and Dephino R.A. Hepatocellular carcinoma pathogenesis: from genes to environment. Nat. Rev. Cancer 6 (2006) 674-687
32. Yoshida T., Hanada T., Tokuhisa T., Kosai K., Sata M., and Kohara M. A. Activation of STAT3 by the hepatitis C virus core protein leads to cellular transformation of STAT3 by the hepatitis C virus core protein leads to cellular transformation. J. Exp. Med. 196 (2002) 641-653
33. Hosui A., Ohkawa K., Ishida H., Sato A., Nakanishi F., Ueda K., Takehara T., Kasahara A., Sasaki Y., and Hori M. Hepatitis C virus core protein differently regulates the JAK-STAT signaling pathway under interleukin-6 and interferon-gamma stimuli. J. Biol. Chem. 278 (2003) 28562-28571
34. Miyoshi H., Fujie H., Shintani Y., Tsutsumi T., Shinzawa S., Makuuchi M., Kokudo N., Matsuura Y., Suzuki T., Miyamura T., and Moriya K. Hepatitis C virus core protein exerts an inhibitory effect on suppressor of cytokine signaling (SOCS)-1 gene expression. J. Hepatol. 43 (2005) 757-763
35. Wieland S.F., and Chisari F.V. Stealth and cunning: hepatitis B and hepatitis C viruses. J. Virol. 79 (2005) 9369-9380
36. Sun L., Hui A.M., Kanai Y., Sakamoto M., and Hirohashi S. Increased DNA methyltransferase expression is associated with an early stage of human hepatocarcinogenesis. Jpn. J. Cancer Res. 88 (1997) 1165-1170
37. Lin C.-H., Hsieh S.-Y., Shen I.-S., Lee W.-C., Chen T.-C., Shyu W.-C., and Liaw Y.-F. Genome-wide hypomethylation in hepatocellular carcinogenesis. Cancer Res. 61 (2001) 4238-4243
38. Saito Y., Kanai Y., Sakamoto M., Saito H., Ishii H., and 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 33 (2001) 561-568
39. Saito Y., Kanai Y., Nakagawa T., Sakamoto M., Saito H., Ishii H., and Hirohashi S. Increased protein expression of DNA methyltransferase (DNMT) 1 is significantly correlated with the malignant potential and poor prognosis of human hepatocellular carcinomas. Int. J. Cancer 105 (2003) 527-532
40. Zhong S., Tang M.W., Yeo W., Liu C., Lo Y.M., and Johnson P.J. Silencing of GSTP1 gene by CpG island DNA hypermethylation in HBV-associated hepatocellular carcinomas. Clin. Cancer Res. 8 (2002) 1087-1092
41. Su P.F., Lee T.C., Lin P.J., Lee P.H., Jeng Y.M., Chen C.H., Liang J.D., Chiou L.L., Huang G.T., and Lee H.S. Differential DNA methylation associated with hepatitis B virus infection in hepatocellular carcinoma. Int. J. Cancer 121 (2007) 1257-1264
42. INK4A Hypermethylation is associated with hepatitis virus infection, age, and gender in hepatocellular carcinoma. Clin. Cancer Res. 10 (2004) 7484-7489
43. Fahrner J.A., Eguchi S., Herman J.G., and Baylin S.B. Dependence of histone modifications and gene expression on DNA hypermethylation in cancer. Cancer Res. 62 (2002) 7213-7218
44. Nguyen C.T., Weisenberger D.J., Velicescu M., Gonzales F.A., Lin J.C., Liang G., and Jones P. Histone H3-lysine 9 methylation is associated with aberrant gene silencing in cancer cells and is rapidly reversed by 5-aza-2′-deoxycytidine. Cancer Res. 62 (2002) 6456-6461
45. Bachman K.E., Park B.H., Rhee I., Rajagopalan H., Herman J.G., Baylin S.B., Kinzler K.W., and Vogelstein B. Histone modifications and silencing prior to DNA methylation of a tumor suppressor gene. Cancer Cell 3 (2003) 89-95
46. Nielsen S.J., Schneider R., Bauer U.M., Bannister A.J., Morrison A., O'Carroll D., Firestein R., Cleary M., Jenuwein T., and Herrera R.E. Rb targets histone H3 methylation and HP1 to promoters. Nature 412 (2001) 561-565
47. Fuks F., Hurd P.J., Deplus R., and Kouzarides T. The DNA methyltransferases associate with HP1 and the SUV39H1 histone methyltransferase. Nucleic Acids Res. 31 (2003) 2305-2312
48. Yoshida T., Ogata H., Kamio M., Yoshida T., Ogata H., Kamio M., Joo A., Shiraishi H., Tokunaga Y., Sata M., Nagai H., and Yoshimura A. SOCS-1 is a suppressor of liver fibrosis and hepatitis-induced carcinogenesis. J. Exp. Med. 199 (2004) 1701-1707