Hepatitis B virus X protein represses miRNA-148a to enhance tumorigenesis

Journal of Clinical Investigation

Volumn 123, Issue 2, 2013, Pages 630-645

  Xu, Xiaojie ^a,b   Fan, Zhongyi ^a,c   Kang, Lei ^a,d   Han, Juqiang ^a,c   Jiang, Chengying ^a,c   Zheng, Xiaofei ^e   Zhu, Ziman ^c   Jiao, Huabo ^c   Lin, Jing ^c   Jiang, Kai ^a   Ding, Lihua ^a   Zhang, Hao ^a   Cheng, Long ^a   Fu, Hanjiang ^e   Song, Yi ^e   Jiang, Ying ^e   Liu, Jiahong ^a,c   Wang, Rongfu ^d   Du, Nan ^c   Ye, Qinong ^a,b  

^a BEIJING INSTITUTE OF BIOTECHNOLOGY   (China)

^b DALIAN MEDICAL UNIVERSITY   (China)

^c CHINESE PLA GENERAL HOSPITAL   (China)

^d PEKING UNIVERSITY FIRST HOSPITAL   (China)

^e BEIJING INSTITUTE OF RADIATION MEDICINE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

HEPATITIS B VIRUS X PROTEIN; MICRORNA; MIRNA 148A; TRANSCRIPTION FACTOR PBX1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER GROWTH; CANCER INVASION; CARCINOGENESIS; CELL CULTURE; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; GENE REPRESSION; HEPATITIS B VIRUS; HEPATOMA CELL; HUMAN; HUMAN CELL; LIVER CELL CARCINOMA; METASTASIS; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; ORTHOHEPADNAVIRUS; PRIORITY JOURNAL; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION; TUMOR XENOGRAFT;

ANIMALS; BASE SEQUENCE; CARCINOMA, HEPATOCELLULAR; DOWN-REGULATION; EPITHELIAL-MESENCHYMAL TRANSITION; HEP G2 CELLS; HEPATITIS B VIRUS; HUMANS; LIVER NEOPLASMS; LIVER NEOPLASMS, EXPERIMENTAL; MALE; MICE; MICE, NUDE; MICRORNAS; NEOPLASM INVASIVENESS; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSPLANTATION, HETEROLOGOUS;

EID: 84873344263     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI64265     Document Type: Article

References (59)

1. Bartel D. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004;116(2):281-297.
2. Calin GA, Croce CM. MicroRNA signatures in human cancers. Nat Rev Cancer. 2006;6(11):857-866.
3. Croce CM. Causes and consequences of micro-RNA dysregulation in cancer. Nat Rev Genet. 2009;10(10):704-714.
4. Zhang B, Pan X, Cobb GP, Anderson TA. micro-RNAs as oncogenes and tumor suppressors. Dev Biol. 2007;302(1):1-12.
5. Guertin DA, Sabatini DM. Defining the role of mTOR in cancer. Cancer Cell. 2007;12(1):9-22.
6. Dazert E, Hall MN. mTOR signaling in disease. Curr Opin Cell Biol. 2011;23(6):744-755.
7. Mendoza MC, Er EE, Blenis J. The Ras-ERK and PI3K-mTOR pathways: cross-talk and compensation. Trends Biochem Sci. 2011;36(6):320-328.
8. Moore PS, Chang Y. Why do viruses cause cancer? Highlights of the first century of human tumour virology. Nat Rev Cancer. 2010;10(12):878-889.
9. Saha A, Kaul R, Murakami M, Robertson ES. Tumor viruses and cancer biology: Modulating signaling pathways for therapeutic intervention. Cancer Biol Ther. 2010;10(10):961-978.
10. Lin Z, Flemington EK. miRNAs in the pathogenesis of oncogenic human viruses. Cancer Lett. 2011;305(2):186-199.
11. Zhang ZZ, et al. Hepatitis B virus and hepatocellular carcinoma at the miRNA level. World J Gastroenterol. 2011;17(28):3353-3358.
12. Wang X, et al. The estrogen receptor-interacting protein HPIP increases estrogen-responsive gene expression through activation of MAPK and AKT. Biochim Biophys Acta. 2008;1783(6):1220-1228.
13. Manavathi B, Acconcia F, Rayala SK, Kumar R. An inherent role of microtubule network in the action of nuclear receptor. Proc Natl Acad Sci U S A. 2006;103(43):15981-15986.
14. Abramovich C, et al. Functional cloning and characterization of a novel nonhomeodomain protein that inhibits the binding of PBX1-HOX complexes to DNA. J Biol Chem. 2000;275(34):26172-26177.
15. Cheng L, et al. PES1 promotes breast cancer by differentially regulating ERα and ERβ. J Clin Invest. 2012;122(8):2857-2870.
16. Chen Y, et al. Altered expression of MiR-148a and MiR-152 in gastrointestinal cancers and its clinical significance. J Gastrointest Surg. 2010;14(7):1170-1179.
17. Liffers ST, et al. MicroRNA-148a is down-regulated in human pancreatic ductal adenocarcinomas and regulates cell survival by targeting CDC25B. Lab Invest. 2011;91(10):1472-1479.
18. Neuveut C, Wei Y, Buendia MA. Mechanisms of HBV-related hepatocarcinogenesis. J Hepatol. 2010;52(4):594-604.
19. Ng SA, Lee C. Hepatitis B virus X gene and hepatocarcinogenesis. J Gastroenterol. 2011;46(8):974-990.
20. Pópulo H, Lopes JM, Soares P. The mTOR signalling pathway in human cancer. Int J Mol Sci. 2012;13(2):1886-1918.
21. Toschi A, Lee E, Xu L, Garcia A, Gadir N, Foster DA. Regulation of mTORC1 and mTORC2 complex assembly by phosphatidic acid: competition with rapamycin. Mol Cell Biol. 2009;29(6):1411-1420.
22. Sheng Z, Ma L, Sun JE, Zhu LJ, Green MR. BCR-ABL suppresses autophagy through ATF5-mediated regulation of mTOR transcription. Blood. 2011;118(10):2840-2848.
23. Roy SK, Srivastava RK, Shankar S. Inhibition of PI3K/AKT and MAPK/ERK pathways causes activation of FOXO transcription factor, leading to cell cycle arrest and apoptosis in pancreatic cancer. J Mol Signal. 2010;5:10.
24. Zhang H, et al. MiR-148a promotes apoptosis by targeting Bcl-2 in colorectal cancer. Cell Death Differ. 2011;18(11):1702-1710.
25. Dewantoro O, Gani RA, Akbar N. Hepatocarcinogenesis in viral Hepatitis B infection: the role of HBx and p53. Acta Med Indones. 2006;38(3):154-159.
26. Elmore LW, et al. Hepatitis B virus X protein and p53 tumor suppressor interactions in the modulation of apoptosis. Proc Natl Acad Sci U S A. 1997;94(26):14707-14712.
27. Staib F, Hussain SP, Hofseth LJ, Wang XW, Harris CC. TP53 and liver carcinogenesis. Hum Mutat. 2003;21(3):201-216.
28. Wong KB, De Decker BS, Freund SM, Proctor MR, Bycroft M, Fersht AR. Hot-spot mutants of p53 core domain evince characteristic local structural changes. Proc Natl Acad Sci U S A. 1999;96(15):8438-8442.
29. Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell. 2009;139(5):871-890.
30. Moreno-Bueno G, Portillo F, Cano A. Transcriptional regulation of cell polarity in EMT and cancer. Oncogene. 2008;27(55):6958-6969.
31. Christiansen JJ, Rajasekaran AK. Reassessing epithelial to mesenchymal transition as a prerequisite for carcinoma invasion and metastasis. Cancer Res. 2006;66(17):8319-8326.
32. Yuan K, Lian Z, Sun B, Clayton MM, Ng IO, Feitelson MA. Role of miR-148a in hepatitis B associated hepatocellular carcinoma. PLoS One. 2012;7(4):e35331.
33. Gao P, Wong CC, Tung EK, Lee JM, Wong CM, Ng IO. Deregulation of microRNA expression occurs early and accumulates in early stages of HBV-associated multistep hepatocarcinogenesis. J Hepatol. 2011;54(6):1177-1184.
34. Yip WK, et al. Carboxyl-terminal truncated HBx regulates a distinct microRNA transcription program in hepatocellular carcinoma development. PLoS. One. 2011;6(8):e22888.
35. Kruse JP, Gu W. Modes of p53 regulation. Cell. 2009;137(4):609-622.
36. Soussi T, Wiman KG. Shaping genetic alterations in human cancer: the p53 mutation paradigm. Cancer Cell. 2007;12(4):303-312.
37. Levine AJ, Momand J, Finlay CA. The p53 tumour suppressor gene. Nature. 1991;351(6326):453-456.
38. Lujambio A, et al. A microRNA DNA methylation signature for human cancer metastasis. Proc Natl Acad Sci U S A. 2008;105(36):13556-13561.
39. Pavicic W, Perkio E, Kaur S, Peltomaki P. Altered methylation at microRNA-associated CpG islands in hereditary and sporadic carcinomas: a methylation-specific multiplex ligation-dependent probe amplification (MS-MLPA)-based approach. Mol Med. 2011;17(7-8):726-735.
40. Hanoun N, et al. The silencing of microRNA 148a production by DNA hypermethylation is an early event in pancreatic carcinogenesis. Clin Chem. 2010;56(7):1107-1118.
41. Zheng B, et al. MicroRNA-148a suppresses tumor cell invasion and metastasis by downregulating ROCK1 in gastric cancer. Clin Cancer Res. 2011;17(24):7574-7583.
42. Grille SJ, et al. The protein kinase Akt induces epithelial mesenchymal transition and promotes enhanced motility and invasiveness of squamous cell carcinoma lines. Cancer Res. 2003;63(9):2172-2178.
43. Ellenrieder V, et al. Transforming growth factor beta1 treatment leads to an epithelial-mesenchymal transdifferentiation of pancreatic cancer cells requiring extracellular signal-regulated kinase 2 activation. Cancer Res. 2001;61(10):4222-4228.
44. Shin SY, Rath O, Zebisch A, Choo SM, Kolch W, Cho KH. Functional roles of multiple feedback loops in extracellular signal-regulated kinase and Wnt signaling pathways that regulate epithelial-mesenchymal transition. Cancer Res. 2010;70(17):6715-6724.
45. Lamouille S, Derynck R. Cell size and invasion in TGF-beta-induced epithelial to mesenchymal transition is regulated by activation of the mTOR pathway. J Cell Biol. 2007;178(3):437-451.
46. Pon YL, Zhou HY, Cheung AN, Ngan HY, Wong AS. p70 S6 kinase promotes epithelial to mesenchymal transition through snail induction in ovarian cancer cells. Cancer Res. 2008;68(16):6524-6532.
47. Smith AP, et al. A positive role for Myc in TGFβ-induced Snail transcription and epithelial-to-mesenchymal transition. Oncogene. 2009;28(3):422-430.
48. Manning BD, Cantley LC. AKT/PKB signaling: navigating downstream. Cell. 2007;129(7):1261-1274.
49. Sebolt-Leopold JS, Herrera R. Targeting the mitogen-activated protein kinase cascade to treat cancer. Nat Rev Cancer. 2004;4(12):937-947.
50. Ford J, Jiang M, Milner J. Cancer-specific functions of SIRT1 enable human epithelial cancer cell growth and survival. Cancer Res. 2005;65(22):10457-10463.
51. Sheng Z, et al. A genome-wide RNA interference screen reveals an essential CREB3L2-ATF5-MCL1 survival pathway in malignant glioma with therapeutic implications. Nat Med. 2010;16(6):671-677.
52. Kim DH, et al. mTOR interacts with raptor to form a nutrient-sensitive complex that signals to the cell growth machinery. Cell. 2002;110(2):163-175.
53. Busch S, Renaud SJ, Schleussner E, Graham CH, Markert UR. mTOR mediates human trophoblast invasion through regulation of matrixremodeling enzymes and is associated with serine phosphorylation of STAT3. Exp Cell Res. 2009;315(10):1724-1733.
54. Zhang F, et al. mTOR complex component Rictor interacts with PKC? and regulates cancer cell metastasis. Cancer Res. 2010;70(22):9360-9370.
55. Han J, et al. Hepatitis B virus X protein and the estrogen receptor variant lacking exon 5 inhibit estrogen receptor signaling in hepatoma cells. Nucleic Acids Res. 2006;34(10):3095-3106.
56. Li Y, et al. Establishment of cell clones with different metastatic potential from the metastatic hepatocellular carcinoma cell line MHCC97. World J Gastroenterol. 2001;7(5):630-636.
57. Ding L, et al. Ligand-independent activation of estrogen receptor alpha by XBP-1. Nucleic Acids Res. 2003;31(18):5266-5274.
58. Ding L, et al. Human four-and-a-half LIM family members suppress tumor cell growth through a TGF-β-like signaling pathway. J Clin Invest. 2009;119(2):349-361.
59. Ding L, et al. FHL1 interacts with oestrogen receptors and regulates breast cancer cell growth. J Cell Mol Med. 2011;15(1):72-85.