Hepatitis B virus X protein prevents apoptosis of hepatocellular carcinoma cells by upregulating SATB1 and HURP expression

Biochemical Pharmacology

Volumn 80, Issue 7, 2010, Pages 1093-1102

  Kuo, Tzu Ching ^a   Chao, Chuck C K ^a  

^a CHANG GUNG UNIVERSITY   (Taiwan)

Author keywords

Apoptosis; HBx; HCC; HURP; SATB1

Indexed keywords

ADENOVIRUS VECTOR; CISPLATIN; HEPATITIS B VIRUS X PROTEIN; HEPATOMA UPREGULATED PROTEIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; ONCOPROTEIN; PROTEIN SATB1; SURVIVIN; UNCLASSIFIED DRUG; MICROTUBULE ASSOCIATED PROTEIN; TRANSACTIVATOR PROTEIN;

APOPTOSIS; ARTICLE; BREAST CANCER; CANCER GROWTH; CARCINOMA CELL; CELL STRAIN HEK293; CONTROLLED STUDY; DRUG CYTOTOXICITY; ENZYME ACTIVATION; GENE OVEREXPRESSION; HEPATITIS B VIRUS; HUMAN; HUMAN CELL; LIVER CELL CARCINOMA; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; UPREGULATION; DRUG EFFECTS; GENETICS; LIVER TUMOR; METABOLISM; NEOPLASM; PATHOLOGY; PHYSIOLOGY; PROTEIN PROCESSING;

APOPTOSIS; CARCINOMA, HEPATOCELLULAR; HEPATITIS B VIRUS; HUMANS; LIVER NEOPLASMS; MICROTUBULE-ASSOCIATED PROTEINS; NEOPLASMS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RNA, MESSENGER; TRANS-ACTIVATORS; UP-REGULATION;

EID: 77955655051     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2010.06.003     Document Type: Article

References (49)

1. Bouchard M.J., Schneider R.J. The enigmatic X gene of hepatitis B virus. J Virol 2004, 78:12725-12734.
2. Tang H., Oishi N., Kaneko S., Murakami S. Molecular functions and biological roles of hepatitis B virus x protein. Cancer Sci 2006, 97:977-983.
3. Yen T.S. Hepadnaviral X protein: review of recent progress. J Biomed Sci 1996, 3:20-30.
4. Feitelson M. Hepatitis B virus infection and primary hepatocellular carcinoma. Clin Microbiol Rev 1992, 5:275-301.
5. Murakami S. Hepatitis B virus X protein: structure, function and biology. Intervirology 1999, 42:81-99.
6. Robinson W.S. Molecular events in the pathogenesis of hepadnavirus-associated hepatocellular carcinoma. Annu Rev Med 1994, 45:297-323.
7. Feitelson M.A., Zhu M., Duan L.X., London W.T. Hepatitis B x antigen and p53 are associated in vitro and in liver tissues from patients with primary hepatocellular carcinoma. Oncogene 1993, 8:1109-1117.
8. Lin Y., Nomura T., Yamashita T., Dorjsuren D., Tang H., Murakami S. The transactivation and p53-interacting functions of hepatitis B virus X protein are mutually interfering but distinct. Cancer Res 1997, 57:5137-5142.
9. Wang X.W., Forrester K., Yeh H., Feitelson M.A., Gu J.R., Harris C.C. Hepatitis B virus X protein inhibits p53 sequence-specific DNA binding, transcriptional activity, and association with transcription factor ERCC3. Proc Natl Acad Sci USA 1994, 91:2230-2234.
10. Becker S.A., Lee T.H., Butel J.S., Slagle B.L. Hepatitis B virus X protein interferes with cellular DNA repair. J Virol 1998, 72:266-272.
11. Lee T.H., Elledge S.J., Butel J.S. Hepatitis B virus X protein interacts with a probable cellular DNA repair protein. J Virol 1995, 69:1107-1114.
12. Bergametti F., Sitterlin D., Transy C. Turnover of hepatitis B virus X protein is regulated by damaged DNA-binding complex. J Virol 2002, 76:6495-6501.
13. Bontron S., Lin-Marq N., Strubin M. Hepatitis B virus X protein associated with UV-DDB1 induces cell death in the nucleus and is functionally antagonized by UV-DDB2. J Biol Chem 2002, 277:38847-38854.
14. Hu Z., Zhang Z., Doo E., Coux O., Goldberg A.L., Liang T.J. Hepatitis B virus X protein is both a substrate and a potential inhibitor of the proteasome complex. J Virol 1999, 73:7231-7240.
15. Zhang Z., Torii N., Furusaka A., Malayaman N., Hu Z., Liang T.J. Structural and functional characterization of interaction between hepatitis B virus X protein and the proteasome complex. J Biol Chem 2000, 275:15157-15165.
16. Kim H., Lee H., Yun Y. X-gene product of hepatitis B virus induces apoptosis in liver cells. J Biol Chem 1998, 273:381-385.
17. Shih W.L., Kuo M.L., Chuang S.E., Cheng A.L., Doong S.L. Hepatitis B virus X protein inhibits transforming growth factor-beta-induced apoptosis through the activation of phosphatidylinositol 3-kinase pathway. J Biol Chem 2000, 275:25858-25864.
18. Su F., Schneider R.J. Hepatitis B virus HBx protein sensitizes cells to apoptotic killing by tumor necrosis factor alpha. Proc Natl Acad Sci USA 1997, 94:8744-8749.
19. Kim S.Y., Kim J.K., Kim H.J., Ahn J.K. Hepatitis B virus X protein sensitizes UV-induced apoptosis by transcriptional transactivation of Fas ligand gene expression. IUBMB Life 2005, 57:651-658.
20. Koike K., Moriya K., Yotsuyanagi H., Iino S., Kurokawa K. Induction of cell cycle progression by hepatitis B virus HBx gene expression in quiescent mouse fibroblasts. J Clin Invest 1994, 94:44-49.
21. Lin N., Chen H.Y., Li D., Zhang S.J., Cheng Z.X., Wang X.Z. Apoptosis and its pathway in X gene-transfected HepG2 cells. World J Gastroenterol 2005, 11:4326-4331.
22. Miao J., Chen G.G., Chun S.Y., Lai P.P. Hepatitis B virus X protein induces apoptosis in hepatoma cells through inhibiting Bcl-xL expression. Cancer Lett 2006, 236:115-124.
23. Su F., Theodosis C.N., Schneider R.J. Role of NF-kappaB and myc proteins in apoptosis induced by hepatitis B virus HBx protein. J Virol 2001, 75:215-225.
24. Cheng A.S., Wong N., Tse A.M., Chan K.Y., Chan K.K., Sung J.J., et al. RNA interference targeting HBx suppresses tumor growth and enhances cisplatin chemosensitivity in human hepatocellular carcinoma. Cancer Lett 2007, 253:43-52.
25. Murata M., Matsuzaki K., Yoshida K., Sekimoto G., Tahashi Y., Mori S., et al. Hepatitis B virus X protein shifts human hepatic transforming growth factor (TGF)-beta signaling from tumor suppression to oncogenesis in early chronic hepatitis B. Hepatology 2009, 49:1203-1217.
26. Shih W.L., Kuo M.L., Chuang S.E., Cheng A.L., Doong S.L. Hepatitis B virus X protein activates a survival signaling by linking SRC to phosphatidylinositol 3-kinase. J Biol Chem 2003, 278:31807-31813.
27. Wu B.K., Li C.C., Chen H.J., Chang J.L., Jeng K.S., Chou C.K., et al. Blocking of G1/S transition and cell death in the regenerating liver of Hepatitis B virus X protein transgenic mice. Biochem Biophys Res Commun 2006, 340:916-928.
28. Tsou A.P., Yang C.W., Huang C.Y., Yu R.C., Lee Y.C., Chang C.W., et al. Identification of a novel cell cycle regulated gene, HURP, overexpressed in human hepatocellular carcinoma. Oncogene 2003, 22:298-307.
29. Gudmundsson K.O., Thorsteinsson L., Sigurjonsson O.E., Keller J.R., Olafsson K., Egeland T., et al. Gene expression analysis of hematopoietic progenitor cells identifies Dlg7 as a potential stem cell gene. Stem Cells 2007, 25:1498-1506.
30. Yu C.T., Hsu J.M., Lee Y.C., Tsou A.P., Chou C.K., Huang C.Y. Phosphorylation and stabilization of HURP by Aurora-A: implication of HURP as a transforming target of Aurora-A. Mol Cell Biol 2005, 25:5789-5800.
31. Betz M.J., Beuschlein F. Diagnosis: Novel molecular signatures for adrenocortical carcinoma. Nat Rev Endocrinol 2009, 5:297-299.
32. de Reynies A., Assie G., Rickman D.S., Tissier F., Groussin L., Rene-Corail F., et al. Gene expression profiling reveals a new classification of adrenocortical tumors and identifies molecular predictors of malignancy and survival. J Clin Oncol 2009, 27:1108-1115.
33. Kumar P.P., Bischof O., Purbey P.K., Notani D., Urlaub H., Dejean A., et al. Functional interaction between PML and SATB1 regulates chromatin-loop architecture and transcription of the MHC class I locus. Nat Cell Biol 2007, 9:45-56.
34. Zweyer M., Riederer B.M., Ochs R.L., Fackelmayer F.O., Kohwi-Shigematsu T., Bareggi R., et al. Association of nuclear matrix proteins with granular and threaded nuclear bodies in cell lines undergoing apoptosis. Exp Cell Res 1997, 230:325-336.
35. Pavan Kumar P., Purbey P.K., Sinha C.K., Notani D., Limaye A., Jayani R.S., et al. Phosphorylation of SATB1, a global gene regulator, acts as a molecular switch regulating its transcriptional activity in vivo. Mol Cell 2006, 22:231-243.
36. Tan J.A., Sun Y., Song J., Chen Y., Krontiris T.G., Durrin L.K. SUMO conjugation to the matrix attachment region-binding protein, special AT-rich sequence-binding protein-1 (SATB1), targets SATB1 to promyelocytic nuclear bodies where it undergoes caspase cleavage. J Biol Chem 2008, 283:18124-18134.
37. Han H.J., Russo J., Kohwi Y., Kohwi-Shigematsu T. SATB1 reprogrammes gene expression to promote breast tumour growth and metastasis. Nature 2008, 452:187-193.
38. Li Q.Q., Chen Z.Q., Xu J.D., Cao X.X., Chen Q., Liu X.P., et al. Overexpression and involvement of special AT-rich sequence binding protein 1 in multidrug resistance in human breast carcinoma cells. Cancer Sci 2009.
39. Kamarajan P., Sun N.K., Sun C.L., Chao C.C. Apaf-1 overexpression partially overcomes apoptotic resistance in a cisplatin-selected HeLa cell line. FEBS Lett 2001, 505:206-212.
40. He T.C., Zhou S., da Costa L.T., Yu J., Kinzler K.W., Vogelstein B. A simplified system for generating recombinant adenoviruses. Proc Natl Acad Sci USA 1998, 95:2509-2514.
41. Sun C.L., Chao C.C. Cross-resistance to death ligand-induced apoptosis in cisplatin-selected HeLa cells associated with overexpression of DDB2 and subsequent induction of cFLIP. Mol Pharmacol 2005, 67:1307-1314.
42. Tsai S.Y., Sun N.K., Lu H.P., Cheng M.L., Chao C.C. Involvement of reactive oxygen species in multidrug resistance of a vincristine-selected lymphoblastoma. Cancer Sci 2007, 98:1206-1214.
43. Schek N., Bartenschlager R., Kuhn C., Schaller H. Phosphorylation and rapid turnover of hepatitis B virus X-protein expressed in HepG2 cells from a recombinant vaccinia virus. Oncogene 1991, 6:1735-1744.
44. Kim J.H., Sohn S.Y., Benedict Yen T.S., Ahn B.Y. Ubiquitin-dependent and -independent proteasomal degradation of hepatitis B virus X protein. Biochem Biophys Res Commun 2008, 366:1036-1042.
45. Wiesenauer C.A., Yip-Schneider M.T., Wang Y., Schmidt C.M. Multiple anticancer effects of blocking MEK-ERK signaling in hepatocellular carcinoma. J Am Coll Surg 2004, 198:410-421.
46. Terradillos O., de La Coste A., Pollicino T., Neuveut C., Sitterlin D., Lecoeur H., et al. The hepatitis B virus X protein abrogates Bcl-2-mediated protection against Fas apoptosis in the liver. Oncogene 2002, 21:377-386.
47. Jung J.K., Kwun H.J., Lee J.O., Arora P., Jang K.L. Hepatitis B virus X protein differentially affects the ubiquitin-mediated proteasomal degradation of beta-catenin depending on the status of cellular p53. J Gen Virol 2007, 88:2144-2154.
48. Cha M.Y., Kim C.M., Park Y.M., Ryu W.S. Hepatitis B virus X protein is essential for the activation of Wnt/beta-catenin signaling in hepatoma cells. Hepatology 2004, 39:1683-1693.
49. Wen Y., Golubkov V.S., Strongin A.Y., Jiang W., Reed J.C. Interaction of hepatitis B viral oncoprotein with cellular target HBXIP dysregulates centrosome dynamics and mitotic spindle formation. J Biol Chem 2008, 283:2793-2803.