Induction of Bcl-2 expression by hepatitis B virus pre-S2 mutant large surface protein resistance to 5-fluorouracil treatment in Huh-7 cells

PLoS ONE

Volumn 6, Issue 12, 2011, Pages

  Hung, Jui Hsiang ^a   Teng, Yen Ni ^b   WangLily, Lily Hui Ching ^c   Su, Ih Jen ^d   Wang, Clay C C ^e   Huang, Wenya ^f   Lee, Kuan Han ^a   Lu, Kuan Ying ^c   Wang, Lyu Han ^c  

^a CHIA NAN UNIVERSITY OF PHARMACY AND SCIENCE   (Taiwan)

^b NATIONAL UNIVERSITY OF TAINAN   (Taiwan)

^c NATIONAL TSING HUA UNIVERSITY   (Taiwan)

^d NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^e UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^f NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; FLUOROURACIL; GLUCOSE REGULATED PROTEIN 78; HEPATITIS B SURFACE ANTIGEN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN INHIBITOR; PROTEIN KINASE B; PROTEIN MCL 1; TRANSCRIPTION FACTOR RELA; UNCLASSIFIED DRUG; YC 137; ANTINEOPLASTIC ANTIMETABOLITE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PRESURFACE PROTEIN 2, HEPATITIS B SURFACE ANTIGEN; PRIMER DNA; PROTEIN KINASE; PROTEIN PRECURSOR;

ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL; CELL DEATH; CELL GROWTH; COLONY FORMATION; CONTROLLED STUDY; DRUG EFFICACY; DRUG POTENTIATION; DRUG RESISTANCE; HEPATITIS B VIRUS; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL CARCINOMA; MOUSE; MUTANT; NEWBORN; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; ANIMAL; GENETICS; IMMUNOHISTOCHEMISTRY; METABOLISM; MUTATION; NUCLEOTIDE SEQUENCE; PHOSPHORYLATION; POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE; TUMOR CELL LINE;

ANIMALS; ANTIMETABOLITES, ANTINEOPLASTIC; BASE SEQUENCE; CASPASE 3; CELL LINE, TUMOR; DNA PRIMERS; DRUG RESISTANCE, NEOPLASM; FLUOROURACIL; HEPATITIS B SURFACE ANTIGENS; IMMUNOHISTOCHEMISTRY; MICE; MICE, TRANSGENIC; MUTATION; NF-KAPPA B; PHOSPHORYLATION; POLYMERASE CHAIN REACTION; PROTEIN KINASES; PROTEIN PRECURSORS; PROTO-ONCOGENE PROTEINS C-BCL-2;

EID: 84055216950     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0028977     Document Type: Article

References (55)

1. Motola-Kuba D, Zamora-Valdés D, Uribe M, Méndez-Sánchez N, (2006) Hepatocellular carcinoma. An overview. Ann Hepatol 5 (1): 16-24.
2. Kao JH, Chen DS, (2005) Changing disease burden of hepatocellular carcinoma in the Far East and Southeast Asia. Liver Int 25 (4): 696-703.
3. Chen CJ, Wang LY, Lu SN, Wu MH, You SL, et al. (1996) Elevated aflatoxin exposure and increased risk of hepatocellular carcinoma. Hepatology 24 (1): 38-42.
4. Thorgeirsson SS, Grisham JW, (2002) Molecular pathogenesis of human hepatocellular carcinoma. Nat Genet 31 (4): 339-346.
5. Lee JW, Soung YH, Kim SY, Lee HW, Park WS, et al. (2005) PIK3CA gene is frequently mutated in breast carcinomas and hepatocellular carcinomas. Oncogene 24 (8): 1477-1480.
6. Feitelson MA, Sun B, Satiroglu Tufan NL, Liu J, Pan J, et al. (2002) Genetic mechanisms of hepatocarcinogenesis. Oncogene 21 (16): 2593-2604.
7. Suzuki K, Hayashi N, Yukinori Y, Yoshihara H, Miyamoto Y, et al. (1994) Expression of the c-met protooncogene in human hepatocellular carcinoma. Hepatology 20 (5): 1231-1236.
8. Parkin DM, Pisani P, Ferlay J, (1993) Prevalence of HPV in cytomorphologically normal cervical smears, as determined by the polymerase chain reaction, is age-dependent. Int J Cancer 53 (6): 919-923.
9. Arbuthnot P, Kew M, (2001) Hepatitis B virus and hepatocellular carcinoma. Int J Exp Pathol 82 (2): 77-100.
10. Chisari FV, Klopchin K, Moriyama T, Pasquinelli C, Dunsford HA, et al. (1989) Molecular pathogenesis of hepatocellular carcinoma in hepatitis B virus transgenic mice. Cell 59 (6): 1145-56.
11. Wang Y, Cui F, Lv Y, Li C, Xu X, et al. (2004) HBsAg and HBx knocked into the p21 locus causes hepatocellular carcinoma in mice. Hepatology 39 (2): 318-324.
12. Yang JC, Teng CF, Wu HC, Tsai HW, Chuang HC, et al. (2009) Enhanced expression of vascular endothelial growth factor-A in ground glass hepatocytes and its implication in hepatitis B virus hepatocarcinogenesis. Hepatology 49 (6): 1962-1971.
13. Chen CH, Hung CH, Lee CM, Hu TH, Wang JH, et al. (2007) Pre-S deletion and complex mutations of hepatitis B virus related to advanced liver disease in HBeAg-negative patients. Gastroenterology 133 (5): 1466-1474.
14. Sugauchi F, Ohno T, Orito E, Sakugawa H, Ichida T, et al. (2003) Influence of hepatitis B virus genotypes on the development of preS deletions and advanced liver disease. J Med Virol 70 (4): 537-544.
15. Fan YF, Lu CC, Chang YC, Chang TT, Lin PW, et al. (2000) Identification of a pre-S2 mutant in hepatocytes expressing a novel marginal pattern of surface antigen in advanced diseases of chronic hepatitis B virus infection. J Gastroenterol Hepatol 15 (5): 519-528.
16. Fan YF, Lu CC, Chen WC, Yao WJ, Wang HC, et al. (2001) Prevalence and significance of hepatitis B virus (HBV) pre-S mutants in serum and liver at different replicative stages of chronic HBV infection. Hepatology 33 (1): 277-286.
17. Abe K, Thung SN, Wu HC, Tran TT, Le Hoang P, et al. (2009) Pre-S2 deletion mutants of hepatitis B virus could have an important role in hepatocarcinogenesis in Asian children. Cancer Sci 100 (12): 2249-2254.
18. Wang HC, Wu HC, Chen CF, Fausto N, Lei HY, et al. (2003) Different types of ground glass hepatocytes in chronic hepatitis B virus infection contain specific pre-S mutants that may induce endoplasmic reticulum stress. Am J Pathol 163 (6): 2441-2449.
19. Huy TT, Ushijima H, Win KM, Luengrojanakul P, Shrestha PK, et al. (2003) High prevalence of hepatitis B virus pre-s mutant in countries where it is endemic and its relationship with genotype and chronicity. J Clin Microbiol 41 (12): 5449-5455.
20. Chen BF, Liu CJ, Jow GM, Chen PJ, Kao JH, et al. (2006) High prevalence and mapping of pre-S deletion in hepatitis B virus carriers with progressive liver diseases. Gastroenterology 130 (4): 1153-1168.
21. Hung JH, Su IJ, Lei HY, Wang HC, Lin WC, et al. (2004) Endoplasmic reticulum stress stimulates the expression of cyclooxygenase-2 through activation of NF-kappaB and pp38 mitogen-activated protein kinase. J Biol Chem 279 (45): 46384-46392.
22. Pahl HL, Baeuerle PA, (1996) Activation of NF-kappa B by ER stress requires both Ca2+ and reactive oxygen intermediates as messengers. FEBS Lett 392 (2): 129-136.
23. Kaneko M, Niinuma Y, Nomura Y, (2003) Activation signal of nuclear factor-kappa B in response to endoplasmic reticulum stress is transduced via IRE1 and tumor necrosis factor receptor-associated factor 2. Biol Pharm Bull 26 (7): 931-935.
24. Kaneko M, Takahashi T, Niinuma Y, Nomura Y, (2004) Manganese superoxide dismutase is induced by endoplasmic reticulum stress through IRE1-mediated nuclear factor (NF)-kappaB and AP-1 activation. Biol Pharm Bull 27 (8): 1202-1206.
25. Hu P, Han Z, Couvillon AD, Kaufman RJ, Exton JH, (2006) Autocrine tumor necrosis factor alpha links endoplasmic reticulum stress to the membrane death receptor pathway through IRE1alpha-mediated NF-kappaB activation and down-regulation of TRAF2 expression. Mol Cell Biol 26 (8): 3071-3084.
26. Jiang HY, Wek SA, McGrath BC, Scheuner D, Kaufman RJ, et al. (2003) Phosphorylation of the alpha subunit of eukaryotic initiation factor 2 is required for activation of NF-kappaB in response to diverse cellular stresses. Mol Cell Biol 23 (16): 5651-5663.
27. Gavrielides MV, Frijhoff AF, Conti CJ, Kazanietz MG, (2004) Protein kinase C and prostate carcinogenesis: targeting the cell cycle and apoptotic mechanisms. Curr Drug Targets 5 (5): 431-443.
28. Hisaka T, Yano H, Haramaki M, Utsunomiya I, Kojiro M, (1999) Expressions of epidermal growth factor family and its receptor in hepatocellular carcinoma cell lines: relationship to cell proliferation. Int J Oncol 14 (3): 453-460.
29. Ross JS, Fletcher JA, (1999) HER-2/neu (c-erb-B2) gene and protein in breast cancer. Am J Clin Pathol 112 (1) Suppl 1: S53-67.
30. Fisher TC, Milner AE, Gregory CD, Jackman AL, Aherne GW, et al. (1993) bcl-2 modulation of apoptosis induced by anticancer drugs: resistance to thymidylate stress is independent of classical resistance pathways. Cancer Res 53 (14): 3321-3326.
31. Takehara T, Liu X, Fujimoto J, Friedman SL, Takahashi H, (2001) Expression and role of Bcl-xL in human hepatocellular carcinomas. Hepatology 34 (1): 55-61.
32. Watanabe J, Kushihata F, Honda K, Mominoki K, Matsuda S, et al. (2002) Bcl-xL overexpression in human hepatocellular carcinoma. Int J Oncol 21 (3): 515-519.
33. Adams JM, Cory S, (1998) The Bcl-2 protein family: arbiters of cell survival. Science 281 (5381): 1322-1326.
34. Gross A, McDonnell JM, Korsmeyer SJ, (1999) BCL-2 family members and the mitochondria in apoptosis. Genes Dev 13 (15): 1899-1911.
35. Yeo W, Mo FK, Chan SL, Leung NW, Hui P, et al. (2007) Hepatitis B viral load predicts survival of HCC patients undergoing systemic chemotherapy. Hepatology 45 (6): 1382-1389.
36. Yeo W, Chan PK, Ho WM, Zee B, Lam KC, et al. (2004) Lamivudine for the prevention of hepatitis B virus reactivation in hepatitis B s-antigen seropositive cancer patients undergoing cytotoxic chemotherapy. J Clin Oncol 22 (5): 927-934.
37. Nakopoulou L, Stefanaki K, Vourlakou C, Manolaki N, Gakiopoulou H, et al. (1999) Bcl-2 protein expression in acute and chronic hepatitis, cirrhosis and hepatocellular carcinoma. Pathol Res Pract 195 (1): 19-24.
38. Kanda T, Yokosuka O, Nagao K, Saisho H, (2006) State of hepatitis C viral replication enhances activation of NF-κB- and AP-1-signaling induced by hepatitis B virus X. Cancer Lett 234 (2): 143-148.
39. Li S, Ye L, Yu X, Xu B, Li K, et al. (2009) Hepatitis C virus NS4B induces unfolded protein response and endoplasmic reticulum overload response-dependent NF-kappaB activation. Virology 391 (2): 257-264.
40. Ghosh S, Karin M, (2002) Missing pieces in the NF-kappaB puzzle. Cell 109 (Suppl): S81-96.
41. Pikarsky E, Porat RM, Stein I, Abramovitch R, Amit S, et al. (2004) NF-kappaB functions as a tumour promoter in inflammation-associated cancer. Nature 431 (7007): 461-466.
42. Karin M, Greten FR, (2005) NF-kappaB: linking inflammation and immunity to cancer development and progression. Nat Rev Immunol 5 (10): 749-759.
43. Ravi R, Bedi A, (2004) NF-kappaB in cancer-a friend turned foe. Drug Resist Updat 7 (1): 53-67.
44. Matsusaka T, Fujikawa K, Nishio Y, Mukaida N, Matsushima K, et al. (1993) Transcription factors NF-IL6 and NF-kappa B synergistically activate transcription of the inflammatory cytokines, interleukin 6 and interleukin 8. Proc Natl Acad Sci U S A 90 (21): 10193-10197.
45. Huang S, Robinson JB, Deguzman A, Bucana CD, Fidler IJ, (2000) Blockade of nuclear factor-kappaB signaling inhibits angiogenesis and tumorigenicity of human ovarian cancer cells by suppressing expression of vascular endothelial growth factor and interleukin 8. Cancer Res 60 (19): 5334-5339.
46. Guttridge DC, Albanese C, Reuther JY, Pestell RG, Baldwin AS, (1999) NF-kappaB controls cell growth and differentiation through transcriptional regulation of cyclin D1. Mol Cell Biol 19 (8): 5785-5799.
47. Bourguignon LY, Xia W, Wong G, (2009) Hyaluronan-mediated CD44 interaction with p300 and SIRT1 regulates beta-catenin signaling and NFkappaB-specific transcription activity leading to MDR1 and Bcl-xL gene expression and chemoresistance in breast tumor cells. J Biol Chem 284 (5): 2657-2671.
48. Wang W, Cassidy J, O'Brien V, Ryan KM, Collie-Duguid E, (2004) Mechanistic and predictive profiling of 5-Fluorouracil resistance in human cancer cells. Cancer Res 64 (22): 8167-8176.
49. Hsieh YH, Su IJ, Wang HC, Chang WW, Lei HY, et al. (2004) Pre-S mutant surface antigens in chronic hepatitis B virus infection induce oxidative stress and DNA damage. Carcinogenesis 25 (10): 2023-2032.
50. Wang HC, Chang WT, Chang WW, Wu HC, Huang W, et al. (2005) Hepatitis B virus pre-S2 mutant upregulates cyclin A expression and induces nodular proliferation of hepatocytes. Hepatology 41 (4): 761-70.
51. Hsieh YH, Su IJ, Wang HC, Tsai JH, Huang YJ, Chang WW, et al. (2007) Hepatitis B virus pre-S2 mutant surface antigen induces degradation of cyclin-dependent kinase inhibitor p27Kip1 through c-Jun activation domain-binding protein 1. Mol Cancer Res 5 (10): 1063-1072.
52. Hung JH, Yan CW, Su IJ, Wang HC, Lei HY, Lin WC, et al. (2010) Hepatitis B virus surface antigen interacts with acid alpha-glucosidase and alters glycogen metabolism. Hepatol Res 40 (6): 633-640.
53. Chang YS, Tsai CT, Huangfu CA, Huang WY, Lei HY, et al. (2011) ACSL3 and GSK-3β are essential for lipid upregulation induced by endoplasmic reticulum stress in liver cells. J Cell Biochem 2011 112 (3): 881-893.
54. Henderson S, Rowe M, Gregory C, Croom-Carter D, Wang F, et al. (1991) Induction of bcl-2 expression by Epstein-Barr virus latent membrane protein 1 protects infected B cells from programmed cell death. Cell 65 (7): 1107-1115.
55. Xia L, Zhang D, Du R, Pan Y, Zhao L, et al. (2008) miR-15b and miR-16 modulate multidrug resistance by targeting BCL2 in human gastric cancer cells. Int J Cancer 123 (2): 372-379.