Hepatitis B virus X protein downregulates expression of the miR-16 family in malignant hepatocytes in vitro

British Journal of Cancer

Volumn 105, Issue 1, 2011, Pages 146-153

  Wu, G ^a   Yu, F ^a   Xiao, Z ^a   Xu, K ^a   Xu, J ^a   Tang, W ^a   Wang, J ^a   Song, E ^a  

^a SUN YAT SEN UNIVERSITY   (China)

Author keywords

c Myc; HBx; hepatocellular carcinoma; miR 16 family; miRNAs

Indexed keywords

HEPATITIS B VIRUS X PROTEIN; LUCIFERASE; MESSENGER RNA; MICRORNA; MICRORNA 16; NOCODAZOLE; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL CYCLE; CELL CYCLE G1 PHASE; CELL PROLIFERATION; CLONOGENESIS; CONTROLLED STUDY; DOWN REGULATION; HUMAN; HUMAN CELL; IN VITRO STUDY; LIVER CELL; LIVER CELL CARCINOMA; MICROARRAY ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

APOPTOSIS; BLOTTING, WESTERN; CARCINOMA, HEPATOCELLULAR; CELL CYCLE; CELL PROLIFERATION; CELLS, CULTURED; DOWN-REGULATION; HEPATOCYTES; HUMANS; LIVER NEOPLASMS; LUCIFERASES; MICRORNAS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TRANS-ACTIVATORS;

EID: 79959702659     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2011.190     Document Type: Article

References (66)

1. Arbuthnot P, Capovilla A, Kew M (2000) Putative role of hepatitis B virus X protein in hepatocarcinogenesis: effects on apoptosis, DNA repair, mitogen-activated protein kinase and JAK/STAT pathways. J Gastroenterol Hepatol 15(4): 357-368 (Pubitemid 30262201)
2. Balsano C, Avantaggiati ML, Natoli G, De Marzio E, Will H, Perricaudet M, Levrero M (1991) Full-length and truncated versions of the hepatitis B virus (HBV) X protein (pX) transactivate the cmyc protooncogene at the transcriptional level. Biochem Biophys Res Commun 176(3): 985-992
3. Bandi N, Zbinden S, Gugger M, Arnold M, Kocher V, Hasan L, Kappeler A, Brunner T, Vassella E (2009) miR-15a and miR-16 are implicated in cell cycle regulation in a Rb-dependent manner and are frequently deleted or down-regulated in non-small cell lung cancer. Cancer Res 69(13): 5553-5559
4. Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136(2): 215-233
5. Benn J, Schneider RJ (1995) Hepatitis B virus HBx protein deregulates cell cycle checkpoint controls. Proc Natl Acad Sci USA 92(24): 11215-11219
6. Bhattacharya R, Nicoloso M, Arvizo R, Wang E, Cortez A, Rossi S, Calin GA, Mukherjee P (2009) MiR-15a and MiR-16 control Bmi-1 expression in ovarian cancer. Cancer Res 69(23): 9090-9095
7. Blower PE, Chung JH, Verducci JS, Lin S, Park JK, Dai Z, Liu CG, Schmittgen TD, Reinhold WC, Croce CM, Weinstein JN, Sadee W (2008) MicroRNAs modulate the chemosensitivity of tumor cells. Mol Cancer Ther 7(1): 1-9
8. Bonci D, Coppola V, Musumeci M, Addario A, Giuffrida R, Memeo L, D'Urso L, Pagliuca A, Biffoni M, Labbaye C, Bartucci M, Muto G, Peschle C, De Maria R (2008) The miR-15a-miR-16-1 cluster controls prostate cancer by targeting multiple oncogenic activities. Nat Med 14(11): 1271-1277
9. Bottoni A, Piccin D, Tagliati F, Luchin A, Zatelli MC, degli Uberti EC (2005) miR-15a and miR-16-1 down-regulation in pituitary adenomas. J Cell Physiol 204(1): 280-285 (Pubitemid 40776831)
10. Braconi C, Valeri N, Gasparini P, Huang N, Taccioli C, Nuovo G, Suzuki T, Croce CM, Patel T (2010) Hepatitis C virus proteins modulate microRNA expression and chemosensitivity in malignant hepatocytes. Clin Cancer Res 16(3): 957-966
11. Budhu A, Jia HL, Forgues M, Liu CG, Goldstein D, Lam A, Zanetti KA, Ye QH, Qin LX, Croce CM, Tang ZY, Wang XW (2008) Identification of metastasis-related microRNAs in hepatocellular carcinoma. Hepatology (Baltimore, Md) 47(3): 897-907 (Pubitemid 351449681)
12. Bueno MJ, Gomez de Cedron M, Laresgoiti U, Fernandez-Piqueras J, Zubiaga AM, Malumbres M (2010) Multiple E2F-induced microRNAs prevent replicative stress in response to mitogenic signaling. Mol Cell Biol 30(12): 2983-2995
13. Calin GA, Croce CM (2006) MicroRNA signatures in human cancers. Nat Rev Cancer 6(11): 857-866 (Pubitemid 44629897)
14. Chang TC, Yu D, Lee YS, Wentzel EA, Arking DE, West KM, Dang CV, Thomas-Tikhonenko A, Mendell JT (2008) Widespread microRNA repression by Myc contributes to tumorigenesis. Nat Genet 40(1): 43-50
15. Chang TC, Zeitels LR, Hwang HW, Chivukula RR, Wentzel EA, Dews M, Jung J, Gao P, Dang CV, Beer MA, Thomas-Tikhonenko A, Mendell JT (2009) Lin-28B transactivation is necessary for Myc-mediated let-7 repression and proliferation. Proc Natl Acad Sci USA 106(9): 3384-3389
16. Chaudhry MA, Sachdeva H, Omaruddin RA (2010) Radiation-induced micro-RNA modulation in glioblastoma cells differing in DNA-repair pathways. DNA Cell Biol 29(9): 553-561
17. Chung GE, Yoon JH, Myung SJ, Lee JH, Lee SH, Lee SM, Kim SJ, Hwang SY, Lee HS, Kim CY (2010) High expression of microRNA-15b predicts a low risk of tumor recurrence following curative resection of hepatocellular carcinoma. Oncol Rep 23(1): 113-119
18. Cimmino A, Calin GA, Fabbri M, Iorio MV, Ferracin M, Shimizu M, Wojcik SE, Aqeilan RI, Zupo S, Dono M, Rassenti L, Alder H, Volinia S, Liu CG, Kipps TJ, Negrini M, Croce CM (2005) miR-15 and miR-16 induce apoptosis by targeting BCL2. Proc Natl Acad Sci USA 102(39): 13944-13949 (Pubitemid 41377683)
19. Cittelly DM, Das PM, Salvo VA, Fonseca JP, Burow ME, Jones FE (2010) Oncogenic HER2\{Delta\}16 suppresses miR-15a/16 and d. Carcinogenesis 31(12): 2049-2057
20. Cohen EE, Zhu H, Lingen MW, Martin LE, Kuo WL, Choi EA, Kocherginsky M, Parker JS, Chung CH, Rosner MR (2009) A feed-forward loop involving protein kinase C alpha and microRNAs regulates tumor cell cycle. Cancer Res 69(1): 65-74
21. Costa FF (2005) Non-coding RNAs: new players in eukaryotic biology. Gene 357(2): 83-94 (Pubitemid 41297574)
22. Dewantoro O, Gani RA, Akbar N (2006) Hepatocarcinogenesis in viral Hepatitis B infection: the role of HBx and p53. Acta Med Indones 38(3): 154-159
23. El-Serag HB, Rudolph KL (2007) Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology 132(7): 2557-2576 (Pubitemid 46890874)
24. Feitelson MA, Lee J (2007) Hepatitis B virus integration, fragile sites, and hepatocarcinogenesis. Cancer Lett 252(2): 157-170 (Pubitemid 46809787)
25. Guo CJ, Pan Q, Jiang B, Chen GY, Li DG (2009a) Effects of upregulated expression of microRNA-16 on biological properties of culture-activated hepatic stellate cells. Apoptosis 14(11): 1331-1340
26. Guo CJ, Pan Q, Li DG, Sun H, Liu BW (2009b) miR-15b and miR-16 are implicated in activation of the rat hepatic stellate cell: An essential role for apoptosis. J Hepatol 50(4): 766-778
27. Gupta RA, Shah N, Wang KC, Kim J, Horlings HM, Wong DJ, Tsai MC, Hung T, Argani P, Rinn JL, Wang Y, Brzoska P, Kong B, Li R, West RB, van de Vijver MJ, Sukumar S, Chang HY (2010) Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 464(7291): 1071-1076
28. Huang XH, Wang Q, Chen JS, Fu XH, Chen XL, Chen LZ, Li W, Bi J, Zhang LJ, Fu Q, Zeng WT, Cao LQ, Tan HX, Su Q (2009) Bead-based microarray analysis of microRNA expression in hepatocellular carcinoma: miR-338 is downregulated. Hepatol Res 39(8): 786-794
29. Jung JK, Arora P, Pagano JS, Jang KL (2007) Expression of DNA methyltransferase 1 is activated by hepatitis B virus X protein via a regulatory circuit involving the p16INK4a-cyclin D1-CDK 4/6-pRb-E2F1 pathway. Cancer Res 67(12): 5771-5778 (Pubitemid 46985010)
30. Kalra N, Kumar V (2006) The X protein of hepatitis B virus binds to the F box protein Skp2 and inhibits the ubiquitination and proteasomal degradation of c-Myc. FEBS Lett 580(2): 431-436 (Pubitemid 43089667)
31. Kaposi-Novak P, Libbrecht L, Woo HG, Lee YH, Sears NC, Coulouarn C, Conner EA, Factor VM, Roskams T, Thorgeirsson SS (2009) Central role of c-Myc during malignant conversion in human hepatocarcinogenesis. Cancer Res 69(7): 2775-2782
32. Kim CM, Koike K, Saito I, Miyamura T, Jay G (1991) HBx gene of hepatitis B virus induces liver cancer in transgenic mice. Nature 351(6324): 317-320 (Pubitemid 21896589)
33. Kim VN (2005) MicroRNA biogenesis: coordinated cropping and dicing. Nat Rev 6(5): 376-385 (Pubitemid 40637855)
34. Klein A, Guhl E, Tzeng YJ, Fuhrhop J, Levrero M, Graessmann M, Graessmann A (2003) HBX causes cyclin D1 overexpression and development of breast cancer in transgenic animals that are heterozygous for p53. Oncogene 22(19): 2910-2919 (Pubitemid 36648917)
35. Klein U, Lia M, Crespo M, Siegel R, Shen Q, Mo T, Ambesi-Impiombato A, Califano A, Migliazza A, Bhagat G, Dalla-Favera R (2010) The DLEU2/ miR-15a/16-1 cluster controls B cell proliferation and its deletion leads to chronic lymphocytic leukemia. Cancer Cell 17(1): 28-40
36. Kumar MS, Lu J, Mercer KL, Golub TR, Jacks T (2007) Impaired microRNA processing enhances cellular transformation and tumorigenesis. Nat Genet 39(5): 673-677 (Pubitemid 46676103)
37. Lee SG, Rho HM (2000) Transcriptional repression of the human p53 gene by hepatitis B viral X protein. Oncogene 19(3): 468-471 (Pubitemid 30077349)
38. Lee YS, Dutta A (2009) MicroRNAs in cancer. Annu Rev Pathol 4: 199-227
39. Li W, Miao X, Qi Z, Zeng W, Liang J, Liang Z (2010) Hepatitis B virus X protein upregulates HSP90alpha expression via activation of c-Myc in human hepatocarcinoma cell line, HepG2. Virol J 7: 45
40. Linsley PS, Schelter J, Burchard J, Kibukawa M, Martin MM, Bartz SR, Johnson JM, Cummins JM, Raymond CK, Dai H, Chau N, Cleary M, Jackson AL, Carleton M, Lim L (2007) Transcripts targeted by the microRNA-16 family cooperatively regulate cell cycle progression. Mol Cell Biol 27(6): 2240-2252 (Pubitemid 46418479)
41. Liu Q, Fu H, Sun F, Zhang H, Tie Y, Zhu J, Xing R, Sun Z, Zheng X (2008) miR-16 family induces cell cycle arrest by regulating multiple cell cycle genes. Nucleic Acids Res 36(16): 5391-5404
42. Liu Y, Zhao JJ, Wang CM, Li MY, Han P, Wang L, Cheng YQ, Zoulim F, Ma X, Xu DP (2009) Altered expression profiles of microRNAs in a stable hepatitis B virus-expressing cell line. Chin Med J 122(1): 10-14
43. Martin-Vilchez S, Sanz-Cameno P, Rodriguez-Munoz Y, Majano PL, Molina-Jimenez F, Lopez-Cabrera M, Moreno-Otero R, Lara-Pezzi E (2008) The hepatitis B virus X protein induces paracrine activation of human hepatic stellate cells. Hepatology (Baltimore, Md) 47(6): 1872-1883 (Pubitemid 351945555)
44. Matouk IJ, DeGroot N, Mezan S, Ayesh S, Abu-lail R, Hochberg A, Galun E (2007) The H19 non-coding RNA is essential for human tumor growth. PLoS One 2(9): e845
45. Mercer TR, Dinger ME, Mattick JS (2009) Long non-coding RNAs: insights into functions. Nat Rev Genet 10(3): 155-159
46. Meyer-Rochow GY, Jackson NE, Conaglen JV, Whittle DE, Kunnimalaiyaan M, Chen H, Westin G, Sandgren J, Stalberg P, Khanafshar E, Shibru D, Duh QY, Clark OH, Kebebew E, Gill AJ, Clifton-Bligh R, Robinson BG, Benn DE, Sidhu SB (2010) MicroRNA profiling of benign and malignant pheochromocytomas identifies novel diagnostic and therapeutic targets. Endocr Relat Cancer 17(3): 835-846
47. Motsch N, Pfuhl T, Mrazek J, Barth S, Grasser FA (2007) Epstein-Barr virus-encoded latent membrane protein 1 (LMP1) induces the expression of the cellular microRNA miR-146a. RNA Biol 4(3): 131-137 (Pubitemid 351237914)
48. Park SG, Chung C, Kang H, Kim JY, Jung G (2006) Up-regulation of cyclin D1 by HBx is mediated by NF-kappaB2/BCL3 complex through kappaB site of cyclin D1 promoter. J Biol Chem 281(42): 31770-31777 (Pubitemid 46041442)
49. Pichler K, Schneider G, Grassmann R (2008) MicroRNA miR-146a and further oncogenesis-related cellular microRNAs are dysregulated in HTLV-1-transformed T lymphocytes. Retrovirology 5: 100
50. Seifer M, Hohne M, Schaefer S, Gerlich WH (1991) In vitro tumorigenicity of hepatitis B virus DNA and HBx protein. J Hepatol 13(Suppl 4): S61-S65
51. Sells MA, Chen ML, Acs G (1987) Production of hepatitis B virus particles in Hep G2 cells transfected with cloned hepatitis B virus DNA. Proc Natl Acad Sci USA 84(4): 1005-1009 (Pubitemid 17031557)
52. Skawran B, Steinemann D, Becker T, Buurman R, Flik J, Wiese B, Flemming P, Kreipe H, Schlegelberger B, Wilkens L (2008) Loss of 13q is associated with genes involved in cell cycle and proliferation in dedifferentiated hepatocellular carcinoma. Mod Pathol 21(12): 1479-1489
53. Suzuki HI, Yamagata K, Sugimoto K, Iwamoto T, Kato S, Miyazono K (2009) Modulation of microRNA processing by p53. Nature 460(7254): 529-533
54. Terradillos O, Billet O, Renard CA, Levy R, Molina T, Briand P, Buendia MA (1997) The hepatitis B virus X gene potentiates c-myc-induced liver oncogenesis in transgenic mice. Oncogene 14(4): 395-404 (Pubitemid 27087102)
55. Terradillos O, Pollicino T, Lecoeur H, Tripodi M, Gougeon ML, Tiollais P, Buendia MA (1998) p53-independent apoptotic effects of the hepatitis B virus HBx protein in vivo and in vitro. Oncogene 17(16): 2115-2123 (Pubitemid 28499338)
56. Wagner-Ecker M, Schwager C, Wirkner U, Abdollahi A, Huber PE (2010) MicroRNA expression after ionizing radiation in human endothelial cells. Radiat Oncol 5: 25
57. Wang Y, Lu Y, Toh ST, Sung WK, Tan P, Chow P, Chung AY, Jooi LL, Lee CG (2010) Lethal-7 is down-regulated by the hepatitis B virus x protein and targets signal transducer and activator of transcription 3. J Hepatol 53(1): 57-66
58. Wilusz JE, Sunwoo H, Spector DL (2009) Long noncoding RNAs: functional surprises from the RNA world. Genes Dev 23(13): 1494-1504
59. Wong CM, Lee JM, Lau TC, Fan ST, Ng IO (2002) Clinicopathological significance of loss of heterozygosity on chromosome 13q in hepatocel-lular carcinoma. Clin Cancer Res 8(7): 2266-2272 (Pubitemid 34753600)
60. Xia L, Zhang D, Du R, Pan Y, Zhao L, Sun S, Hong L, Liu J, Fan D (2008) miR-15b and miR-16 modulate multidrug resistance by targeting BCL2 in human gastric cancer cells. Int J Cancer 123(2): 372-379 (Pubitemid 351842022)
61. Xu T, Zhu Y, Xiong Y, Ge YY, Yun JP, Zhuang SM (2009) MicroRNA-195 suppresses tumorigenicity and regulates G1/S transition of human hepatocellular carcinoma cells. Hepatology (Baltimore, Md) 50(1): 113-121
62. Yu F, Yao H, Zhu P, Zhang X, Pan Q, Gong C, Huang Y, Hu X, Su F, Lieberman J, Song E (2007) let-7 regulates self renewal and tumor-igenicity of breast cancer cells. Cell 131(6): 1109-1123 (Pubitemid 350235025)
63. Yue J, Tigyi G (2010) Conservation of miR-15a/16-1 and miR-15b/16-2 clusters. Mamm Genome 21(1-2): 88-94
64. Zhang X, Wan G, Mlotshwa S, Vance V, Berger FG, Chen H, Lu X (2010) Oncogenic Wip1 phosphatase is inhibited by miR-16 in the DNA damage signaling pathway. Cancer Res 70(18): 7176-7186
65. Zhao H, Kalota A, Jin S, Gewirtz AM (2009) The c-myb proto-oncogene and microRNA-15a comprise an active autoregulatory feedback loop in human hematopoietic cells. Blood 113(3): 505-516
66. Zhu JY, Pfuhl T, Motsch N, Barth S, Nicholls J, Grasser F, Meister G (2009) Identification of novel Epstein-Barr virus microRNA genes from nasopharyngeal carcinomas. J Virol 83(7): 3333-3341