Hepatitis B virus mRNA-mediated miR-122 inhibition upregulates PTTG1-binding protein, which promotes hepatocellular carcinoma tumor growth and cell invasion

Journal of Virology

Volumn 87, Issue 4, 2013, Pages 2193-2205

  Li, Changfei ^a   Wang, Yanzhong ^a   Wang, Saifeng ^a   Wu, Bo ^a   Hao, Junli ^a   Fan, Hongxia ^a   Ju, Ying ^a   Ding, Yuping ^b   Chen, Lizhao ^a   Chu, Xiaoyu ^a   Liu, Wenjun ^a   Ye, Xin ^a   Meng, Songdong ^a  

^a INSTITUTE OF MICROBIOLOGY   (China)

^b Yantai Infectious Disease Hospital   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; MICRORNA 122; SECURIN; VIRUS MESSENGER RNA;

ADULT; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING AFFINITY; CANCER INHIBITION; CARCINOMA CELL; CELL INVASION; CELL PROLIFERATION; CHRONIC HEPATITIS; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; GENE; GENE OVEREXPRESSION; GENE REPRESSION; GENE SILENCING; GENE TRANSLOCATION; HEPATITIS B; HEPATITIS B VIRUS; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; LIVER CARCINOGENESIS; LIVER CELL CARCINOMA; MALE; MOUSE; NONHUMAN; PBF GENE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; PTTG1 GENE; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; UPREGULATION; VIRUS REPLICATION; VIRUS TRANSCRIPTION;

ADULT; AGED; ANIMALS; CARCINOMA, HEPATOCELLULAR; FEMALE; HEPATITIS B VIRUS; HEPATITIS B, CHRONIC; HUMANS; LIVER NEOPLASMS; MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; MICRORNAS; MIDDLE AGED; RNA, MESSENGER; RNA, VIRAL;

EID: 84873852453     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02831-12     Document Type: Article

References (48)

1. Krol J, Loedige I, Filipowicz W. 2010. The widespread regulation of microRNA biogenesis, function and decay. Nat. Rev. Genet. 11:597- 610.
2. Girard M, Jacquemin E, Munnich A, Lyonnet S, Henrion-Caude A. 2008. miR-122, a paradigm for the role of microRNAs in the liver. J. Hepatol. 48:648-656.
3. Castoldi M, Vujic Spasic M, Altamura S, Elmén J, Lindow M, Kiss J, Stolte J, Sparla R, D'Alessandro LA, Klingmüller U, Fleming RE, Longerich T, Gröne HJ, Benes V, Kauppinen S, Hentze MW, Muckenthaler MU. 2011. The liver-specific microRNA miR-122 controls systemic iron homeostasis in mice. J. Clin. Investig. 121:1386 -1396.
4. Xu H, He JH, Xiao ZD, Zhang QQ, Chen YQ, Zhou H, Qu LH. 2010. Liver-enriched transcription factors regulate microRNA-122 that targets CUTL1 during liver development. Hepatology 52:1431-1442.
5. Bai S, Nasser MW, Wang B, Hsu SH, Datta J, Kutay H, Yadav A, Yadav A, Nuovo G, Kumar P, Ghoshal K. 2009. MicroRNA-122 inhibits tum-morigenic properties of hepatocellular carcinoma cells and sensitizes these cells to sorafenib. J. Biol. Chem. 284:32015-32027.
6. Fornari F, Gramantieri L, Giovannini C, Veronese A, Ferracin M, Sabbioni S, Calin GA, Grazi GL, Croce CM, Tavolari S, Chieco P, Negrini M, Bolondi L. 2009. miR-122/cyclin G1 interaction modulates p53 activity and affects doxorubicin sensitivity of human hepatocarcinoma cells. Cancer Res. 69:5761-5767.
7. Tsai WC, Hsu PW, Lai TC, Chau GY, Lin CW, Chen CM, Lin CD, Liao YL, Wang JL, Chau YP, Hsu MT, Hsiao M, Huang HD, Tsou AP. 2009. MicroRNA-122, a tumor suppressor microRNA that regulates intrahepatic metastasis of hepatocellular carcinoma. Hepatology 49:1571-1582.
8. Zeng C, Wang R, Li D, Lin XJ, Wei QK, Yuan Y, Wang Q, Chen W, Zhuang SM. 2010. A novel GSK-3 beta-C/EBP alpha-miR-122-insulinlike growth factor 1 receptor regulatory circuitry in human hepatocellular carcinoma. Hepatology 52:1702-1712.
9. Norman KL, Sarnow P. 2010. Modulation of hepatitis C virus RNA abundance and the isoprenoid biosynthesis pathway by microRNA miR-122 involves distinct mechanisms. J. Virol. 84:666-670.
10. O'Connell RM, Rao DS, Chaudhuri AA, Baltimore D. 2010. Physiological and pathological roles for microRNAs in the immune system. Nat. Rev. Immunol. 10:111-122.
11. Lanford RE, Hildebrandt-Eriksen ES, Petri A, Persson R, Lindow M, Munk ME, Kauppinen S, Orum H. 2010. Therapeutic silencing of microRNA-122 in primates with chronic hepatitis C virus infection. Science 327:198 -201.
12. Qiu L, Fan H, Jin W, Zhao B, Wang Y, Ju Y, Chen L, Chen Y, Duan Z, Meng S. 2010. miR-122-induced down-regulation of HO-1 negatively affects miR-122-mediated suppression of HBV. Biochem. Biophys. Res. Commun. 398:771-777.
13. Shimakami T, Yamane D, Jangra RK, Kempf BJ, Spaniel C, Barton DJ, Lemon SM. 2012. Stabilization of hepatitis C virus RNA by an Ago2-miR-122 complex. Proc. Natl. Acad. Sci. U. S. A. 10:941-946.
14. 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.
15. Neuveut C, Wei Y, Buendia MA. 2010. Mechanisms of HBV-related hepatocarcinogenesis. J. Hepatol. 52:594-604.
16. Rehermann B, Nascimbeni M. 2005. Immunology of hepatitis B virus and hepatitis C virus infection. Nat. Rev. Immunol. 5:215-229.
17. Beasley RP, Hwang LY, Lin CC, Chien CS. 1981. Hepatocellular carcinoma and hepatitis B virus. A prospective study of 22707 men in Taiwan. Lancet ii:1129 -1133.
18. Kew MC. 2010. Epidemiology of chronic hepatitis B virus infection, hepatocellular carcinoma, and hepatitis B virus-induced hepatocellular carcinoma. Pathol. Biol. (Paris) 58:273-277.
19. Wang WH, Studach LL, Andrisani OM. 2011. Proteins ZNF198 and SUZ12 are down-regulated in hepatitis B virus (HBV)Xprotein-mediated hepatocyte transformation and in HBV replication. Hepatology 53:1137- 1147.
20. Yang HI, Yeh SH, Chen PJ, Iloeje UH, Jen CL, Su J, Wang LY, Lu SN, You SL, Chen DS, Liaw YF, Chen CJ, Study Group REVEALHBV. 2008. Associations between hepatitis B virus genotype and mutants and the risk of hepatocellular carcinoma. J. Natl. Cancer Inst. 100:1134 -1143.
21. Barash H, Gross RE, Edrei Y, Ella E, Israel A, Cohen I, Corchia N, Ben-Moshe T, Pappo O, Pikarsky E, Goldenberg D, Shiloh Y, Galun E, Abramovitch R. 2010. Accelerated carcinogenesis following liver regeneration is associated with chronic inflammation-induced double-strand DNA breaks. Proc. Natl. Acad. Sci. U. S. A. 107:2207-2212.
22. Yang JC, Teng CF, Wu HC, Tsai HW, Chuang HC, Tsai TF, Hsu YH, Huang W, Wu LW, Su IJ. 2009. Enhanced expression of vascular endothelial growth factor-A in ground glass hepatocytes and its implication in hepatitis B virus hepatocarcinogenesis. Hepatology 49:1962-1971.
23. Zhao J, Wu G, Bu F, Lu B, Liang A, Cao L, Tong X, Lu X, Wu M, Guo Y. 2010. Epigenetic silence of ankyrin-repeat-containing, SH3-domaincontaining, and proline-rich-region-containing protein 1 (ASPP1) and ASPP2 genes promotes tumor growth in hepatitis B virus-positive hepatocellular carcinoma. Hepatology 51:142-153.
24. Zhang H, Zhai Y, Hu Z, Wu C, Qian J, Jia W, Ma F, Huang W, Yu L, Yue W, Wang Z, Li P, Zhang Y, Liang R, Wei Z, Cui Y, Xie W, Cai M, Yu X, Yuan Y, Xia X, Zhang X, Yang H, Qiu W, Yang J, Gong F, Chen M, Shen H, Lin D, Zeng YX, He F, Zhou G. 2010. Genome-wide association study identifies 1p36.22 as a new susceptibility locus for hepatocellular carcinoma in chronic hepatitis B virus carriers. Nat. Genet. 42:755-758.
25. Wang S, Qiu L, Yan X, Jin W, Wang Y, Chen L, Wu E, Ye X, Gao GF, Wang F, Chen Y, Duan Z, Meng S. 2012. Loss of miR-122 expression in patients with hepatitis B enhances hepatitis B virus replication through cyclin G1 modulated P53 activity. Hepatology 55:730 -741.
26. Coulouarn C, Factor VM, Andersen JB, Durkin ME, Thorgeirsson SS. 2009. Loss of miR-122 expression in liver cancer correlates with suppression of the hepatic phenotype and gain of metastatic properties. Oncogene 28:3526 -3536.
27. Fu J, Xu D, Liu Z, Shi M, Zhao P, Fu B, Zhang Z, Yang H, Zhang H, Zhou C, Yao J, Jin L, Wang H, Yang Y, Fu YX, Wang FS. 2007. Increased regulatory T cells correlate with CD8 T-cell impairment and poor survival in hepatocellular carcinoma patients. Gastroenterology 132: 2328-2339.
28. Wang S, Qiu L, Liu G, Li Y, Zhang X, Jin W, Gao GF, Kong X, Meng S. 2011. Heat shock protein gp96 enhances humoral and T cell responses, decreases Treg frequency and potentiates the anti-HBV activity in BALB/c and transgenic mice. Vaccine 29:6342- 6351.
29. Li C, Cao S, Liu Z, Ye X, Chen L, Meng S. 2010. RNAi-mediated downregulation of uPAR synergizes with targeting of HER2 through the ERK pathway in breast cancer cells. Int. J. Cancer 127:1507-1516.
30. Kelly EJ, Hadac EM, Cullen BR, Russell SJ. 2010. MicroRNA antagonism of the picornaviral life cycle: alternative mechanisms of interference. PLoS Pathog. 6:e1000820. doi:10.1371/journal.ppat.1000820.
31. Ebert MS, Sharp PA. 2010. MicroRNA sponges: progress and possibilities. RNA 16:2043-2050.
32. Jeong JH, Kwak DS, Rho HM, Jung G. 1996. The catalytic properties of human hepatitis B virus polymerase. Biochem. Biophys. Res. Commun. 223:264 -271.
33. Chien W, Pei L. 2000. A novel binding factor facilitates PTTG1 translocation and transcriptional activation. J. Biol. Chem. 275:19422-19427.
34. Smith VE, Franklyn JA, McCabe CJ. 2010. Pituitary tumor-transforming gene and its binding factor in endocrine cancer. Expert Rev. Mol. Med. 12:e38.
35. Tong Y, Eigler T. 2009. Transcriptional targets for pituitary tumortransforming gene-1. J. Mol. Endocrinol. 43:179 -185.
36. Chen Y, Shen A, Rider PJ, Yu Y, Wu K, Mu Y, Hao Q, Liu Y, Gong H, Zhu Y, Liu F, Wu J. 2011. A liver-specific microRNA binds to a highly conserved RNA sequence of hepatitis B virus and negatively regulates viral gene expression and replication. FASEB J. 25:4511- 4521.
37. Fan CG, Wang CM, Tian C, Wang Y, Li L, Sun WS, Li RF, Liu YG. 2011. miR-122 inhibits viral replication and cell proliferation in hepatitis B virus-related hepatocellular carcinoma and targets NDRG3. Oncol. Rep. 26:1281-1286.
38. Ma F, Xu S, Liu X, Zhang Q, Xu X, Liu M, Hua M, Li N, Yao H, Cao X. 2011. The microRNA miR-29 controls innate and adaptive immune responses to intracellular bacterial infection by targeting interferon-. Nat. Immunol. 12:861- 869.
39. Sarasin-Filipowicz M, Krol J, Markiewicz I, Heim MH, Filipowicz W. 2009. Decreased levels of microRNA miR-122 in individuals with hepatitis C responding poorly to interferon therapy. Nat. Med. 15:31-33.
40. Cermelli S, Ruggieri A, Marrero JA, Ioannou GN, Beretta L. 2011. Circulating microRNAs in patients with chronic hepatitis C and nonalcoholic fatty liver disease. PLoS One 6:e23937. doi:10.1371/journal.pone .0023937.
41. Zhang X, Zhang E, Ma Z, Pei R, Jiang M, Schlaak JF, Roggendorf M, Lu M. 2011. Modulation of hepatitis B virus replication and hepatocyte differentiation by microRNA-1. Hepatology 53:1476 -1485.
42. Stiffler JD, Nguyen M, Sohn JA, Liu C, Kaplan D, Seeger C. 2009. Focal distribution of hepatitis C virus RNA in infected livers. PLoS One 4:e6661. doi:10.1371/journal.pone.0006661.
43. Filipowicz W, Grosshans H. 2011. The liver-specific microRNA miR-122: biology and therapeutic potential. Prog. Drug Res. 67:221-238.
44. Quasdorff M, Protzer U. 2010. Control of hepatitis B virus at the level of transcription. J. Viral Hepat. 17:527-536.
45. Smith VE, Franklyn JA, McCabe CJ. 2011. Expression and function of the novel proto-oncogene PBF in thyroid cancer-a new target for augmenting radioiodine uptake. J. Endocrinol. 210:157-163.
46. Watkins RJ, Read ML, Smith VE, Sharma N, Reynolds GM, Buckley L, Doig C, Campbell MJ, Lewy G, Eggo MC, Loubiere LS, Franklyn JA, Boelaert K, McCabe CJ. 2010. Pituitary tumor transforming gene binding factor: a new gene in breast cancer. Cancer Res. 70:3739 -3749.
47. Molina-Jiménez F, Benedicto I, Murata M, Martín-Vílchez S, Seki T, Antonio Pintor-Toro J, Tortolero M, Moreno-Otero R, Okazaki K, Koike K, Barbero JL, Matsuzaki K, Majano PL, López-Cabrera M. 2010. Expression of pituitary tumor-transforming gene 1 (PTTG1)/securin in hepatitis B virus (HBV)-associated liver diseases: evidence for an HBV X protein-mediated inhibition of PTTG1 ubiquitination and degradation. Hepatology 51:777-787.
48. Mizuguchi Y, Mishima T, Yokomuro S, Arima Y, Kawahigashi Y, Shigehara K, Kanda T, Yoshida H, Uchida E, Tajiri T, Takizawa T. 2011. Sequencing and bioinformatics-based analyses of the microRNA transcriptome in hepatitis B-related hepatocellular carcinoma. PLoS One 6:e15304. doi:10.1371/journal.pone.0015304.