Hepatitis B virus inhibits apoptosis of hepatoma cells by sponging the MicroRNA 15a/16 cluster

Journal of Virology

Volumn 87, Issue 24, 2013, Pages 13370-13378

  Liu, Ningning ^a,b   Zhang, Jinfang ^a   Jiao, Tong ^a,b   Li, Zhiwei ^c   Peng, Jirun ^d   Cui, Zhuqingqing ^d   Ye, Xin ^a  

^a INSTITUTE OF MICROBIOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c BEIJING 302 HOSPITAL   (China)

^d PEKING UNIVERSITY PEOPLE S HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ETOPOSIDE; MICRORNA 15A; MICRORNA 16; NUCLEOTIDE; PROTEIN BCL 2;

ADULT; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CLINICAL ARTICLE; FEMALE; GENE CLUSTER; HEPATITIS B; HEPATITIS B VIRUS; HEPATOMA CELL; HUMAN; HUMAN TISSUE; LIVER CELL CARCINOMA; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN TARGETING; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; UPREGULATION;

ADULT; AGED; ANIMALS; ANTIVIRAL AGENTS; APOPTOSIS; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; DOWN-REGULATION; ETOPOSIDE; FEMALE; HEPATITIS B VIRUS; HOST-PATHOGEN INTERACTIONS; HUMANS; LIVER NEOPLASMS; MALE; MICE; MICE, INBRED BALB C; MICRORNAS; MIDDLE AGED; PROTO-ONCOGENE PROTEINS C-BCL-2; RNA, MESSENGER; RNA, VIRAL;

EID: 84888061942     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02130-13     Document Type: Article

References (35)

1. Neuveut C, Wei Y, Buendia MA. 2010. Mechanisms of HBV-related hepatocarcinogenesis. J. Hepatol. 52:594-604.
2. Rehermann B, Nascimbeni M. 2005. Immunology of hepatitis B virus and hepatitis C virus infection. Nat. Rev. Immunol. 5:215-229.
3. Kew MC. 2010. Epidemiology of chronic hepatitis B virus infection, hepatocellular carcinoma, and hepatitis B virus-induced hepatocellular carcinoma. Pathol. Biol. 58:273-277.
4. Beasley RP, Hwang LY, Lin CC, Chien CS. 1981. Hepatocellular carcinoma and hepatitis B virus. Lancet ii:1129-1133.
5. De Mitri MS, Cassini R, Bernardi M. 2010. Hepatitis B virus-related hepatocarcinogenesis:molecular oncogenic potential of clear or occult infections. Eur. J. Cancer 46:2178-2186.
6. Du J, Liang X, Liu Y, Qu Z, Gao L, Han L, Liu S, Cui M, Shi Y, Zhang Z, Yu L, Cao L, Ma C, Zhang L, Chen Y, Sun W. 2009. Hepatitis B virus core protein inhibits TRAIL-induced apoptosis of hepatocytes by blocking DR5 expression. Cell Death Differ. 16:219-229.
7. Wang XW, Gibson MK, Vermeulen W, Yeh H, Forrester K, Sturzbecher HW, Hoeijmakers JH, Harris CC. 1995. Abrogation of p53-induced apoptosis by the hepatitis B virus X gene. Cancer Res. 55:6012-6016.
8. Su F, Schneider RJ. 1997. Hepatitis B virus HBx protein sensitizes cells to apoptotic killing by tumor necrosis factor alpha. Proc. Natl. Acad. Sci. U.S.A. 94:8744-8749.
9. Diao J, Khine AA, Sarangi F, Hsu E, Iorio C, Tibbles LA, Woodgett JR, Penninger J, Richardson CD. 2001. X protein of hepatitis B virus inhibits Fas-mediated apoptosis and is associated with up-regulation of the SAPK/ JNK pathway. J. Biol. Chem. 276:8328-8340.
10. Krol J, Loedige I, Filipowicz W. 2010. The widespread regulation of microRNA biogenesis, function and decay. Nat. Rev. Genet. 11:597-610.
11. Bartel DP. 2004. MicroRNAs:genomics, biogenesis, mechanism, and function. Cell 116:281-297.
12. Care A, Catalucci D, Felicetti F, Bonci D, Addario A, Gallo P, Bang ML, Segnalini P, Gu Y, Dalton ND, Elia L, Latronico MV, Hoydal M, Autore C, Russo MA, Dorn GW, 2nd, Ellingsen O, Ruiz-Lozano P, Peterson KL, Croce CM, Peschle C, Condorelli G. 2007. MicroRNA-133 controls cardiac hypertrophy. Nat. Med. 13:613-618.
13. Su H, Yang JR, Xu T, Huang J, Xu L, Yuan Y, Zhuang SM. 2009. MicroRNA-101, down-regulated in hepatocellular carcinoma, promotes apoptosis and suppresses tumorigenicity. Cancer Res. 69:1135-1142.
14. Wang CM, Wang Y, Fan CG, Xu FF, Sun WS, Liu YG, Jia JH. 2011. miR-29c targets TNFAIP3, inhibits cell proliferation and induces apoptosis in hepatitis B virus-related hepatocellular carcinoma. Biochem. Biophys. Res. Commun. 411:586-592.
15. Lagos-Quintana M, Rauhut R, Lendeckel W, Tuschl T. 2001. Identification of novel genes coding for small expressed RNAs. Science 294:853-858.
16. Aqeilan RI, Calin GA, Croce CM. 2010. miR-15a and miR-16-1 in cancer:discovery, function and future perspectives. Cell Death Differ. 17:215-220.
17. Janumyan YM, Sansam CG, Chattopadhyay A, Cheng N, Soucie EL, Penn LZ, Andrews D, Knudson CM, Yang E. 2003. Bcl-xL/Bcl-2 coordinately regulates apoptosis, cell cycle arrest and cell cycle entry. EMBO J. 22:5459-5470.
18. Reed JC. 1994. Bcl-2 and the regulation of programmed cell death. J. Cell Biol. 124:1-6.
19. Vaux DL, Cory S, Adams JM. 1988. Bcl-2 gene promotes haemopoietic cell survival and cooperates with c-myc to immortalize pre-B cells. Nature 335:440-442.
20. Tsujimoto Y, Finger LR, Yunis J, Nowell PC, Croce CM. 1984. Cloning of the chromosome breakpoint of neoplastic B cells with the t(14;18) chromosome translocation. Science 226:1097-1099.
21. Marcinowski L, Tanguy M, Krmpotic A, Radle B, Lisnic VJ, Tuddenham L, Chane-Woon-Ming B, Ruzsics Z, Erhard F, Benkartek C, Babic M, Zimmer R, Trgovcich J, Koszinowski UH, Jonjic S, Pfeffer S, Dolken L. 2012. Degradation of cellular mir-27 by a novel, highly abundant viral transcript is important for efficient virus replication in vivo. PLoS Pathog. 8:e1002510. doi:10.1371/journal.ppat.1002510.
22. Li C, Wang Y, Wang S, Wu B, Hao J, Fan H, Ju Y, Ding Y, Chen L, Chu X, Liu W, Ye X, Meng S. 2013. Hepatitis B virus mRNA-mediated miR-122 inhibition upregulates PTTG1-binding protein, which promotes hepatocellular carcinoma tumor growth and cell invasion. J. Virol. 87:2193-2205.
23. Wu G, Yu F, Xiao Z, Xu K, Xu J, Tang W, Wang J, Song E. 2011. Hepatitis B virusXprotein downregulates expression of the miR-16 family in malignant hepatocytes in vitro. Br. J. Cancer 105:146-153.
24. 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. 122:10-14.
25. + T lymphocytes can produce gamma interferon without cytotoxicity. J. Virol. 79:5568-5576.
26. Ebert MS, Sharp PA. 2010. MicroRNA sponges:progress and possibilities. RNA 16:2043-2050.
27. Zhang L, Yang L, Liu X, Chen W, Chang L, Chen L, Loera S, Chu P, Huang WC, Liu YR, Yen Y. 2013. MicroRNA-657 promotes tumorigenesis in hepatocellular carcinoma by targeting transducin-like enhancer protein 1 through nuclear factor kappa B pathways. Hepatology 57:1919-1930.
28. Whittaker S, Marais R, Zhu AX. 2010. The role of signaling pathways in the development and treatment of hepatocellular carcinoma. Oncogene 29:4989-5005.
29. Wang Y, Jiang L, Ji X, Yang B, Zhang Y, Fu XD. 2013. Hepatitis B viral RNA directly mediates down-regulation of the tumor suppressor microRNA miR-15a/miR-16-1 in hepatocytes. J. Biol. Chem. 288:18484-18493.
30. Zhao X, Ogunwobi OO, Liu C. 2011. Survivin inhibition is critical for Bcl-2 inhibitor-induced apoptosis in hepatocellular carcinoma cells. PLoS One 6:e21980. doi:10.1371/journal.pone.0021980.
31. Kamesaki S, Kamesaki H, Jorgensen TJ, Tanizawa A, Pommier Y, Cossman J. 1993. Bcl-2 protein inhibits etoposide-induced apoptosis through its effects on events subsequent to topoisomerase II-induced DNA strand breaks and their repair. Cancer Res. 53:4251-4256.
32. Liu Q, Chen J, Liu L, Zhang J, Wang D, Ma L, He Y, Liu Y, Liu Z, Wu J. 2011. The X protein of hepatitis B virus inhibits apoptosis in hepatoma cells through enhancing the methionine adenosyltransferase 2A gene expression and reducing S-adenosylmethionine production. J. Biol. Chem. 286:17168-17180.
33. Elmore LW, Hancock AR, Chang SF, Wang XW, Chang S, Callahan CP, Geller DA, Will H, Harris CC. 1997. Hepatitis B virus X protein and p53 tumor suppressor interactions in the modulation of apoptosis. Proc. Natl. Acad. Sci. U.S.A. 94:14707-14712.
34. Marusawa H, Matsuzawa S, Welsh K, Zou H, Armstrong R, Tamm I, Reed JC. 2003. HBXIP functions as a cofactor of survivin in apoptosis suppression. EMBO J. 22:2729-2740.
35. Kuo TC, Chao CC. 2010. Hepatitis B virus X protein prevents apoptosis of hepatocellular carcinoma cells by upregulating SATB1 and HURP expression. Biochem. Pharmacol. 80:1093-1102.