miR-106b-25/miR-17-92 clusters: Polycistrons with oncogenic roles in hepatocellular carcinoma

World Journal of Gastroenterology

Volumn 20, Issue 20, 2014, Pages 5962-5972

  Tan, Weiqi ^a   Li, Yang ^b   Lim, Seng Gee ^b   Tan, Theresa M C ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b Dept Medicine Endocrinol Diabet   (Singapore)

Author keywords

Hepatocellular carcinoma; Liver cirrhosis; Micrornas; miR 106b 25 cluster; miR 17 92 cluster

Indexed keywords

BETA CATENIN; BIM PROTEIN; FIBRONECTIN; HEPATITIS B VIRUS X PROTEIN; MICRORNA; MICRORNA 106B; MICRORNA 106B 25; MICRORNA 122; MICRORNA 124; MICRORNA 155; MICRORNA 17 5P; MICRORNA 17 92; MICRORNA 18A; MICRORNA 199; MICRORNA 19A; MICRORNA 19B; MICRORNA 19B 1; MICRORNA 200; MICRORNA 20A; MICRORNA 25; MICRORNA 29; MICRORNA 29B; MICRORNA 92A 1; MICRORNA 93; MYC PROTEIN; PHOSPHATIDYLINOSITOL 3, 4, 5 TRISPHOSPHATE 3 PHOSPHATASE; TRANSCRIPTION FACTOR E2F1; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; UNINDEXED DRUG; WNT PROTEIN; MCM7 PROTEIN, HUMAN; MINICHROMOSOME MAINTENANCE PROTEIN 7; MIRN106 MICRORNA, HUMAN; MIRN17-92 MICRORNA, HUMAN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PTEN PROTEIN, HUMAN;

APOPTOSIS; ARTICLE; CARCINOGENESIS; CELL ADHESION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; DOWN REGULATION; GENE CLUSTER; GENE EXPRESSION REGULATION; HEPATITIS B; HEPATITIS C; HUMAN; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; LIVER FIBROSIS; METASTASIS; PHASE 2 CLINICAL TRIAL (TOPIC); PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; TUMOR GROWTH; UPREGULATION; VIRUS REPLICATION; GENE SILENCING; GENETICS; LIVER TUMOR; METABOLISM; MULTIGENE FAMILY; SEQUENCE HOMOLOGY;

CARCINOMA, HEPATOCELLULAR; CELL SURVIVAL; E2F1 TRANSCRIPTION FACTOR; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; HUMANS; LIVER NEOPLASMS; MICRORNAS; MINICHROMOSOME MAINTENANCE COMPLEX COMPONENT 7; MULTIGENE FAMILY; NEOPLASM METASTASIS; PROTO-ONCOGENE PROTEINS C-MYC; PTEN PHOSPHOHYDROLASE; SEQUENCE HOMOLOGY, NUCLEIC ACID; SIGNAL TRANSDUCTION;

EID: 84901495059     PISSN: 10079327     EISSN: 22192840     Source Type: Journal    
DOI: 10.3748/wjg.v20.i20.5962     Document Type: Article

References (114)

1. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 2010; 127: 2893-2917. [PMID: 21351269 DOI: 10.1002/ijc.25516]
2. Della Corte C, Colombo M. Surveillance for hepatocellular carcinoma. Semin Oncol 2012; 39: 384-398. [PMID: 22846857 DOI: 10.1053/j.seminoncol.2012.05.002]
3. Mormone E, George J, Nieto N. Molecular pathogenesis of hepatic fibrosis and current therapeutic approaches. Chem Biol Interact 2011; 193: 225-231. [PMID: 21803030 DOI: 10.1016/j.cbi.2011.07.001]
4. Hernandez-Gea V, Friedman SL. Pathogenesis of liver fibrosis. Annu Rev Pathol 2011; 6: 425-456. [PMID: 21073339 DOI: 10.1146/annurev-pathol-011110-130246]
5. Rodriguez A, Griffiths-Jones S, Ashurst JL, Bradley A. Identification of mammalian microRNA host genes and transcription units. Genome Res 2004; 14: 1902-1910. [PMID: 15364901 DOI: 10.1101/gr.2722704]
6. Lee Y, Kim M, Han J, Yeom KH, Lee S, Baek SH, Kim VN. MicroRNA genes are transcribed by RNA polymerase II. EMBO J 2004; 23: 4051-4060. [PMID: 15372072 DOI: 10.1038/ sj.emboj.7600385]
7. Lee Y, Ahn C, Han J, Choi H, Kim J, Yim J, Lee J, Provost P, Rådmark O, Kim S, Kim VN. The nuclear RNase III Drosha initiates microRNA processing. Nature 2003; 425: 415-419. [PMID: 14508493 DOI: 10.1038/nature01957]
8. Han J, Lee Y, Yeom KH, Kim YK, Jin H, Kim VN. The Drosha-DGCR8 complex in primary microRNA processing. Genes Dev 2004; 18: 3016-3027. [PMID: 15574589 DOI: 10.1101/gad.1262504]
9. Lund E, Güttinger S, Calado A, Dahlberg JE, Kutay U. Nuclear export of microRNA precursors. Science 2004; 303: 95-98. [PMID: 14631048 DOI: 10.1126/science.1090599]
10. Billy E, Brondani V, Zhang H, Müller U, Filipowicz W. Specific interference with gene expression induced by long, double-stranded RNA in mouse embryonal teratocarcinoma cell lines. Proc Natl Acad Sci USA 2001; 98: 14428-14433. [PMID: 11724966 DOI: 10.1073/pnas.261562698]
11. Hutvágner G, McLachlan J, Pasquinelli AE, Bálint E, Tuschl T, Zamore PD. A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science 2001; 293: 834-838. [PMID: 11452083 DOI: 10.1126/science.1062961]
12. Gregory RI, Chendrimada TP, Cooch N, Shiekhattar R. Human RISC couples microRNA biogenesis and posttranscriptional gene silencing. Cell 2005; 123: 631-640. [PMID: 16271387 DOI: 10.1016/j.cell.2005.10.022]
13. Maniataki E, Mourelatos Z. A human, ATP-independent, RISC assembly machine fueled by pre-miRNA. Genes Dev 2005; 19: 2979-2990. [PMID: 16357216 DOI: 10.1101/ gad.1384005]
14. Hutvágner G, Zamore PD. A microRNA in a multiple-turnover RNAi enzyme complex. Science 2002; 297: 2056-2060. [PMID: 12154197 DOI: 10.1126/science.1073827]
15. Yekta S, Shih IH, Bartel DP. MicroRNA-directed cleavage of HOXB8 mRNA. Science 2004; 304: 594-596. [PMID: 15105502 DOI: 10.1126/science.1097434]
16. Doench JG, Petersen CP, Sharp PA. siRNAs can function as miRNAs. Genes Dev 2003; 17: 438-442. [PMID: 12600936 DOI: 10.1101/gad.1064703]
17. Valencia-Sanchez MA, Liu J, Hannon GJ, Parker R. Control of translation and mRNA degradation by miRNAs and siRNAs. Genes Dev 2006; 20: 515-524. [PMID: 16510870 DOI: 10.1101/gad.1399806]
18. Lagos-Quintana M, Rauhut R, Lendeckel W, Tuschl T. Identification of novel genes coding for small expressed RNAs. Science 2001; 294: 853-858. [PMID: 11679670 DOI: 10.1126/science. 1064921]
19. Lau NC, Lim LP, Weinstein EG, Bartel DP. An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 2001; 294: 858-862. [PMID: 11679671 DOI: 10.1126/science.1065062]
20. Lee RC, Ambros V. An extensive class of small RNAs in Caenorhabditis elegans. Science 2001; 294: 862-864. [PMID: 11679672 DOI: 10.1126/science.1065329]
21. Calin GA, Dumitru CD, Shimizu M, Bichi R, Zupo S, Noch E, Aldler H, Rattan S, Keating M, Rai K, Rassenti L, Kipps T, Negrini M, Bullrich F, Croce CM. Frequent deletions and down-regulation of micro-RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc Natl Acad Sci USA 2002; 99: 15524-15529. [PMID: 12434020 DOI: 10.1073/ pnas.242606799]
22. Ota A, Tagawa H, Karnan S, Tsuzuki S, Karpas A, Kira S, Yoshida Y, Seto M. Identification and characterization of a novel gene, C13orf25, as a target for 13q31-q32 amplification in malignant lymphoma. Cancer Res 2004; 64: 3087-3095. [PMID: 15126345]
23. He L, Thomson JM, Hemann MT, Hernando-Monge E, Mu D, Goodson S, Powers S, Cordon-Cardo C, Lowe SW, Hannon GJ, Hammond SM. A microRNA polycistron as a potential human oncogene. Nature 2005; 435: 828-833. [PMID: 15944707 DOI: 10.1038/nature03552]
24. O'Donnell KA, Wentzel EA, Zeller KI, Dang CV, Mendell JT. c-Myc-regulated microRNAs modulate E2F1 expression. Nature 2005; 435: 839-843. [PMID: 15944709 DOI: 10.1038/nature03677]
25. Matsumura I, Tanaka H, Kanakura Y. E2F1 and c-Myc in cell growth and death. Cell Cycle 2003; 2: 333-338. [PMID: 12851485]
26. Hayashita Y, Osada H, Tatematsu Y, Yamada H, Yanagisawa K, Tomida S, Yatabe Y, Kawahara K, Sekido Y, Takahashi T. A polycistronic microRNA cluster, miR-17-92, is overexpressed in human lung cancers and enhances cell proliferation. Cancer Res 2005; 65: 9628-9632. [PMID: 16266980 DOI: 10.1158/0008-5472.CAN-05-2352]
27. Mourelatos Z, Dostie J, Paushkin S, Sharma A, Charroux B, Abel L, Rappsilber J, Mann M, Dreyfuss G. miRNPs: a novel class of ribonucleoproteins containing numerous microRNAs. Genes Dev 2002; 16: 720-728. [PMID: 11914277 DOI: 10.1101/gad.974702]
28. Lagos-Quintana M, Rauhut R, Meyer J, Borkhardt A, Tuschl T. New microRNAs from mouse and human. RNA 2003; 9: 175-179. [PMID: 12554859]
29. Lai EC, Tomancak P, Williams RW, Rubin GM. Computational identification of Drosophila microRNA genes. Genome Biol 2003; 4: R42. [PMID: 12844358 DOI: 10.1186/gb-2003-47-r42]
30. Tanzer A, Stadler PF. Molecular evolution of a microRNA cluster. J Mol Biol 2004; 339: 327-335. [PMID: 15136036 DOI: 10.1016/j.jmb.2004.03.065]
31. Ventura A, Young AG, Winslow MM, Lintault L, Meissner A, Erkeland SJ, Newman J, Bronson RT, Crowley D, Stone JR, Jaenisch R, Sharp PA, Jacks T. Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters. Cell 2008; 132: 875-886. [PMID: 18329372 DOI: 10.1016/j.cell.2008.02.019]
32. Shan SW, Lee DY, Deng Z, Shatseva T, Jeyapalan Z, Du WW, Zhang Y, Xuan JW, Yee SP, Siragam V, Yang BB. MicroRNA MiR-17 retards tissue growth and represses fibronectin expression. Nat Cell Biol 2009; 11: 1031-1038. [PMID: 19633662 DOI: 10.1038/ncb1917]
33. Kan T, Sato F, Ito T, Matsumura N, David S, Cheng Y, Agarwal R, Paun BC, Jin Z, Olaru AV, Selaru FM, Hamilton JP, Yang J, Abraham JM, Mori Y, Meltzer SJ. The miR-106b-25 polycistron, activated by genomic amplification, functions as an oncogene by suppressing p21 and Bim. Gastroenterology 2009; 136: 1689-1700. [PMID: 19422085]
34. Li Y, Tan W, Neo TW, Aung MO, Wasser S, Lim SG, Tan TM. Role of the miR-106b-25 microRNA cluster in hepatocellular carcinoma. Cancer Sci 2009; 100: 1234-1242. [PMID: 19486339 DOI: 10.1111/j.1349-7006.2009.01164.x]
35. Poliseno L, Salmena L, Riccardi L, Fornari A, Song MS, Hobbs RM, Sportoletti P, Varmeh S, Egia A, Fedele G, Rameh L, Loda M, Pandolfi PP. Identification of the miR-106b~25 microRNA cluster as a proto-oncogenic PTENtargeting intron that cooperates with its host gene MCM7 in transformation. Sci Signal 2010; 3: ra29. [PMID: 20388916 DOI: 10.1126/scisignal.2000594]
36. Kim YK, Yu J, Han TS, Park SY, Namkoong B, Kim DH, Hur K, Yoo MW, Lee HJ, Yang HK, Kim VN. Functional links between clustered microRNAs: suppression of cell-cycle inhibitors by microRNA clusters in gastric cancer. Nucleic Acids Res 2009; 37: 1672-1681. [PMID: 19153141 DOI: 10.1093/ nar/gkp002]
37. Razumilava N, Bronk SF, Smoot RL, Fingas CD, Werneburg NW, Roberts LR, Mott JL. miR-25 targets TNF-related apoptosis inducing ligand (TRAIL) death receptor-4 and promotes apoptosis resistance in cholangiocarcinoma. Hepatology 2012; 55: 465-475. [PMID: 21953056 DOI: 10.1002/hep.24698]
38. Li Q, Zou C, Zou C, Han Z, Xiao H, Wei H, Wang W, Zhang L, Zhang X, Tang Q, Zhang C, Tao J, Wang X, Gao X. MicroRNA-25 functions as a potential tumor suppressor in colon cancer by targeting Smad7. Cancer Lett 2013; 335: 168-174. [PMID: 23435373 DOI: 10.1016/j.canlet.2013.02.029]
39. Yu XF, Zou J, Bao ZJ, Dong J. miR-93 suppresses proliferation and colony formation of human colon cancer stem cells. World J Gastroenterol 2011; 17: 4711-4717. [PMID: 22180714 DOI: 10.3748/wjg.v17.i42.4711]
40. El-Serag HB. Epidemiology of viral hepatitis and hepatocellular carcinoma. Gastroenterology 2012; 142: 1264-1273.e1. [PMID: 22537432 DOI: 10.1053/j.gastro.2011.12.061]
41. Zhang GL, Li YX, Zheng SQ, Liu M, Li X, Tang H. Suppression of hepatitis B virus replication by microRNA-199a-3p and microRNA-210. Antiviral Res 2010; 88: 169-175. [PMID: 20728471 DOI: 10.1016/j.antiviral.2010.08.008]
42. Fan CG, Wang CM, Tian C, Wang Y, Li L, Sun WS, Li RF, Liu YG. miR-122 inhibits viral replication and cell proliferation in hepatitis B virus-related hepatocellular carcinoma and targets NDRG3. Oncol Rep 2011; 26: 1281-1286. [PMID: 21725618 DOI: 10.3892/or.2011.1375]
43. Xu X, Fan Z, Kang L, Han J, Jiang C, Zheng X, Zhu Z, Jiao H, Lin J, Jiang K, Ding L, Zhang H, Cheng L, Fu H, Song Y, Jiang Y, Liu J, Wang R, Du N, Ye Q. Hepatitis B virus X protein represses miRNA-148a to enhance tumorigenesis. J Clin Invest 2013; 123: 630-645. [PMID: 23321675 DOI: 10.1172/ JCI64265]
44. Jung YJ, Kim JW, Park SJ, Min BY, Jang ES, Kim NY, Jeong SH, Shin CM, Lee SH, Park YS, Hwang JH, Kim N, Lee DH. c-Myc-mediated overexpression of miR-17-92 suppresses replication of hepatitis B virus in human hepatoma cells. J Med Virol 2013; 85: 969-978. [PMID: 23532756 DOI: 10.1002/ jmv.23534]
45. Liu Y, Zhang Y, Wen J, Liu L, Zhai X, Liu J, Pan S, Chen J, Shen H, Hu Z. A genetic variant in the promoter region of miR-106b-25 cluster and risk of HBV infection and hepatocellular carcinoma. PLoS One 2012; 7: e32230. [PMID: 22393390 DOI: 10.1371/journal.pone.0032230]
46. Kumar V, Kato N, Urabe Y, Takahashi A, Muroyama R, Hosono N, Otsuka M, Tateishi R, Omata M, Nakagawa H, Koike K, Kamatani N, Kubo M, Nakamura Y, Matsuda K. Genome-wide association study identifies a susceptibility locus for HCV-induced hepatocellular carcinoma. Nat Genet 2011; 43: 455-458. [PMID: 21499248 DOI: 10.1038/ng.809]
47. Kumar V, Yi Lo PH, Sawai H, Kato N, Takahashi A, Deng Z, Urabe Y, Mbarek H, Tokunaga K, Tanaka Y, Sugiyama M, Mizokami M, Muroyama R, Tateishi R, Omata M, Koike K, Tanikawa C, Kamatani N, Kubo M, Nakamura Y, Matsuda K. Soluble MICA and a MICA variation as possible prognostic biomarkers for HBV-induced hepatocellular carcinoma. PLoS One 2012; 7: e44743. [PMID: 23024757 DOI: 10.1371/journal. pone.0044743]
48. Kishikawa T, Otsuka M, Yoshikawa T, Ohno M, Takata A, Shibata C, Kondo Y, Akanuma M, Yoshida H, Koike K. Regulation of the expression of the liver cancer susceptibility gene MICA by microRNAs. Sci Rep 2013; 3: 2739. [PMID: 24061441 DOI: 10.1038/srep02739]
49. Jopling CL, Yi M, Lancaster AM, Lemon SM, Sarnow P. Modulation of hepatitis C virus RNA abundance by a liverspecific MicroRNA. Science 2005; 309: 1577-1581. [PMID: 16141076 DOI: 10.1126/science.1113329]
50. Janssen HL, Reesink HW, Lawitz EJ, Zeuzem S, Rodriguez-Torres M, Patel K, van der Meer AJ, Patick AK, Chen A, Zhou Y, Persson R, King BD, Kauppinen S, Levin AA, Hodges MR. Treatment of HCV infection by targeting microRNA. N Engl J Med 2013; 368: 1685-1694. [PMID: 23534542 DOI: 10.1056/NEJMoa1209026]
51. Singaravelu R, Chen R, Lyn RK, Jones DM, O'Hara S, Rouleau Y, Cheng J, Srinivasan P, Nasheri N, Russell RS, Tyrrell DL, Pezacki JP. Hepatitis C virus induced up-regulation of microRNA-27: a novel mechanism for hepatic steatosis. Hepatology 2014; 59: 98-108. [PMID: 23897856 DOI: 10.1002/ hep.26634]
52. Shrivastava S, Petrone J, Steele R, Lauer GM, Di Bisceglie AM, Ray RB. Up-regulation of circulating miR-20a is correlated with hepatitis C virus-mediated liver disease progression. Hepatology 2013; 58: 863-871. [PMID: 23390075 DOI: 10.1002/hep.26296]
53. Fleming KM, Aithal GP, Solaymani-Dodaran M, Card TR, West J. Incidence and prevalence of cirrhosis in the United Kingdom, 1992-2001: a general population-based study. J Hepatol 2008; 49: 732-738. [PMID: 18667256 DOI: 10.1016/ j.jhep.2008.05.023]
54. Schuppan D, Afdhal NH. Liver cirrhosis. Lancet 2008; 371: 838-851. [PMID: 18328931 DOI: 10.1016/S0140-6736(08)60383-9]
55. Roderburg C, Urban GW, Bettermann K, Vucur M, Zimmermann H, Schmidt S, Janssen J, Koppe C, Knolle P, Castoldi M, Tacke F, Trautwein C, Luedde T. Micro-RNA profiling reveals a role for miR-29 in human and murine liver fibrosis. Hepatology 2011; 53: 209-218. [PMID: 20890893 DOI: 10.1002/ hep.23922]
56. Murakami Y, Toyoda H, Tanaka M, Kuroda M, Harada Y, Matsuda F, Tajima A, Kosaka N, Ochiya T, Shimotohno K. The progression of liver fibrosis is related with overexpression of the miR-199 and 200 families. PLoS One 2011; 6: e16081. [PMID: 21283674 DOI: 10.1371/journal.pone.0016081]
57. Shu J, Kren BT, Xia Z, Wong PY, Li L, Hanse EA, Min MX, Li B, Albrecht JH, Zeng Y, Subramanian S, Steer CJ. Genomewide microRNA down-regulation as a negative feedback mechanism in the early phases of liver regeneration. Hepatology 2011; 54: 609-619. [PMID: 21574170 DOI: 10.1002/ hep.24421]
58. Lakner AM, Steuerwald NM, Walling TL, Ghosh S, Li T, McKillop IH, Russo MW, Bonkovsky HL, Schrum LW. Inhibitory effects of microRNA 19b in hepatic stellate cellmediated fibrogenesis. Hepatology 2012; 56: 300-310. [PMID: 22278637 DOI: 10.1002/hep.25613]
59. Pineau P, Volinia S, McJunkin K, Marchio A, Battiston C, Terris B, Mazzaferro V, Lowe SW, Croce CM, Dejean A. miR-221 overexpression contributes to liver tumorigenesis. Proc Natl Acad Sci USA 2010; 107: 264-269. [PMID: 20018759 DOI: 10.1073/pnas.0907904107]
60. Chen YJ, Zhu JM, Wu H, Fan J, Zhou J, Hu J, Yu Q, Liu TT, Yang L, Wu CL, Guo XL, Huang XW, Shen XZ. Circulating microRNAs as a Fingerprint for Liver Cirrhosis. PLoS One 2013; 8: e66577. [PMID: 23805240 DOI: 10.1371/journal. pone.0066577]
61. Bandrés E, Cubedo E, Agirre X, Malumbres R, Zárate R, Ramirez N, Abajo A, Navarro A, Moreno I, Monzó M, García-Foncillas J. Identification by Real-time PCR of 13 mature microRNAs differentially expressed in colorectal cancer and non-tumoral tissues. Mol Cancer 2006; 5: 29. [PMID: 16854228 DOI: 10.1186/1476-4598-5-29]
62. Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F, Visone R, Iorio M, Roldo C, Ferracin M, Prueitt RL, Yanaihara N, Lanza G, Scarpa A, Vecchione A, Negrini M, Harris CC, Croce CM. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA 2006; 103: 2257-2261. [PMID: 16461460 DOI: 10.1073/ pnas.0510565103]
63. Murakami Y, Yasuda T, Saigo K, Urashima T, Toyoda H, Okanoue T, Shimotohno K. Comprehensive analysis of microRNA expression patterns in hepatocellular carcinoma and non-tumorous tissues. Oncogene 2006; 25: 2537-2545. [PMID: 16331254 DOI: 10.1038/sj.onc.1209283]
64. Kutay H, Bai S, Datta J, Motiwala T, Pogribny I, Frankel W, Jacob ST, Ghoshal K. Downregulation of miR-122 in the rodent and human hepatocellular carcinomas. J Cell Biochem 2006; 99: 671-678. [PMID: 16924677 DOI: 10.1002/jcb.20982]
65. Huang YS, Dai Y, Yu XF, Bao SY, Yin YB, Tang M, Hu CX. Microarray analysis of microRNA expression in hepatocellular carcinoma and non-tumorous tissues without viral hepatitis. J Gastroenterol Hepatol 2008; 23: 87-94. [PMID: 18171346 DOI: 10.1111/j.1440-1746.2007.05223.x]
66. Li W, Xie L, He X, Li J, Tu K, Wei L, Wu J, Guo Y, Ma X, Zhang P, Pan Z, Hu X, Zhao Y, Xie H, Jiang G, Chen T, Wang J, Zheng S, Cheng J, Wan D, Yang S, Li Y, Gu J. Diagnostic and prognostic implications of microRNAs in human hepatocellular carcinoma. Int J Cancer 2008; 123: 1616-1622. [PMID: 18649363 DOI: 10.1002/ijc.23693]
67. Connolly E, Melegari M, Landgraf P, Tchaikovskaya T, Tennant BC, Slagle BL, Rogler LE, Zavolan M, Tuschl T, Rogler CE. Elevated expression of the miR-17-92 polycistron and miR-21 in hepadnavirus-associated hepatocellular carcinoma contributes to the malignant phenotype. Am J Pathol 2008; 173: 856-864. [PMID: 18688024 DOI: 10.2353/ajpath. 2008.080096]
68. Su H, Yang JR, Xu T, Huang J, Xu L, Yuan Y, Zhuang SM. MicroRNA-101, down-regulated in hepatocellular carcinoma, promotes apoptosis and suppresses tumorigenicity. Cancer Res 2009; 69: 1135-1142. [PMID: 19155302 DOI: 10.1158/0008-5472.CAN-08-2886]
69. Chen L, Jiang M, Yuan W, Tang H. miR-17-5p as a novel prognostic marker for hepatocellular carcinoma. J Invest Surg 2012; 25: 156-161. [PMID: 22583011 DOI: 10.3109/08941939.20 11.618523]
70. Shen G, Jia H, Tai Q, Li Y, Chen D. miR-106b downregulates adenomatous polyposis coli and promotes cell proliferation in human hepatocellular carcinoma. Carcinogenesis 2013; 34: 211-219. [PMID: 23087084 DOI: 10.1093/carcin/bgs320]
71. Yau WL, Lam CS, Ng L, Chow AK, Chan ST, Chan JY, Wo JY, Ng KT, Man K, Poon RT, Pang RW. Over-expression of miR-106b promotes cell migration and metastasis in hepatocellular carcinoma by activating epithelial-mesenchymal transition process. PLoS One 2013; 8: e57882. [PMID: 23483935 DOI: 10.1371/journal.pone.0057882]
72. Schlaeger C, Longerich T, Schiller C, Bewerunge P, Mehrabi A, Toedt G, Kleeff J, Ehemann V, Eils R, Lichter P, Schirmacher P, Radlwimmer B. Etiology-dependent molecular mechanisms in human hepatocarcinogenesis. Hepatology 2008; 47: 511-520. [PMID: 18161050 DOI: 10.1002/hep.22033]
73. Nevzorova YA, Hu W, Cubero FJ, Haas U, Freimuth J, Tacke F, Trautwein C, Liedtke C. Overexpression of c-myc in hepatocytes promotes activation of hepatic stellate cells and facilitates the onset of liver fibrosis. Biochim Biophys Acta 2013; 1832: 1765-1775. [PMID: 23770341 DOI: 10.1016/ j.bbadis.2013.06.001]
74. Yoshida K, Matsuzaki K. Differential Regulation of TGF-β/ Smad Signaling in Hepatic Stellate Cells between Acute and Chronic Liver Injuries. Front Physiol 2012; 3: 53. [PMID: 22457652 DOI: 10.3389/fphys.2012.00053]
75. Buendia MA, Bourre L, Cairo S. Myc target miRs and liver cancer: small molecules to get Myc sick. Gastroenterology 2012; 142: 214-218. [PMID: 22178210 DOI: 10.1053/j.gastro.2011.12.023]
76. Ambs S, Prueitt RL, Yi M, Hudson RS, Howe TM, Petrocca F, Wallace TA, Liu CG, Volinia S, Calin GA, Yfantis HG, Stephens RM, Croce CM. Genomic profiling of microRNA and messenger RNA reveals deregulated microRNA expression in prostate cancer. Cancer Res 2008; 68: 6162-6170. [PMID: 18676839 DOI: 10.1158/0008-5472.CAN-08-0144]
77. Petrocca F, Visone R, Onelli MR, Shah MH, Nicoloso MS, de Martino I, Iliopoulos D, Pilozzi E, Liu CG, Negrini M, Cavazzini L, Volinia S, Alder H, Ruco LP, Baldassarre G, Croce CM, Vecchione A. E2F1-regulated microRNAs impair TGFbeta-dependent cell-cycle arrest and apoptosis in gastric cancer. Cancer Cell 2008; 13: 272-286. [PMID: 18328430 DOI: 10.1016/j.ccr.2008.02.013]
78. Tsuruga H, Yabuta N, Hashizume K, Ikeda M, Endo Y, Nojima H. Expression, nuclear localization and interactions of human MCM/P1 proteins. Biochem Biophys Res Commun 1997; 236: 118-125. [PMID: 9223437 DOI: 10.1006/ bbrc.1997.6865]
79. Fernandez PC, Frank SR, Wang L, Schroeder M, Liu S, Greene J, Cocito A, Amati B. Genomic targets of the human c-Myc protein. Genes Dev 2003; 17: 1115-1129. [PMID: 12695333 DOI: 10.1101/gad.1067003]
80. Zhao ZN, Bai JX, Zhou Q, Yan B, Qin WW, Jia LT, Meng YL, Jin BQ, Yao LB, Wang T, Yang AG. TSA suppresses miR-106b-93-25 cluster expression through downregulation of MYC and inhibits proliferation and induces apoptosis in human EMC. PLoS One 2012; 7: e45133. [PMID: 23028803 DOI: 10.1371/journal.pone.0045133]
81. Sylvestre Y, De Guire V, Querido E, Mukhopadhyay UK, Bourdeau V, Major F, Ferbeyre G, Chartrand P. An E2F/ miR-20a autoregulatory feedback loop. J Biol Chem 2007; 282: 2135-2143. [PMID: 17135249 DOI: 10.1074/jbc.M608939200]
82. Woods K, Thomson JM, Hammond SM. Direct regulation of an oncogenic micro-RNA cluster by E2F transcription factors. J Biol Chem 2007; 282: 2130-2134. [PMID: 17135268 DOI: 10.1074/jbc.C600252200]
83. Shiraha H, Yamamoto K, Namba M. Human hepatocyte carcinogenesis (review). Int J Oncol 2013; 42: 1133-1138. [PMID: 23426905 DOI: 10.3892/ijo.2013.1829]
84. Xiao C, Srinivasan L, Calado DP, Patterson HC, Zhang B, Wang J, Henderson JM, Kutok JL, Rajewsky K. Lymphoproliferative disease and autoimmunity in mice with increased miR-17-92 expression in lymphocytes. Nat Immunol 2008; 9: 405-414. [PMID: 18327259 DOI: 10.1038/ni1575]
85. Shan SW, Fang L, Shatseva T, Rutnam ZJ, Yang X, Du W, Lu WY, Xuan JW, Deng Z, Yang BB. Mature miR-17-5p and passenger miR-17-3p induce hepatocellular carcinoma by targeting PTEN, GalNT7 and vimentin in different signal pathways. J Cell Sci 2013; 126: 1517-1530. [PMID: 23418359 DOI: 10.1242/jcs.122895]
86. Zhao B, Zhu Y, Cui K, Gao J, Yu F, Chen L, Li S. Expression and significance of PTEN and miR-92 in hepatocellular carcinoma. Mol Med Rep 2013; 7: 1413-1416. [PMID: 23546593 DOI: 10.3892/mmr.2013.1406]
87. Peyrou M, Bourgoin L, Foti M. PTEN in liver diseases and cancer. World J Gastroenterol 2010; 16: 4627-4633. [PMID: 20872961 DOI: 10.3748/wjg.v16.i37.4627]
88. Watanabe S, Horie Y, Kataoka E, Sato W, Dohmen T, Ohshima S, Goto T, Suzuki A. Non-alcoholic steatohepatitis and hepatocellular carcinoma: lessons from hepatocyte-specific phosphatase and tensin homolog (PTEN)-deficient mice. J Gastroenterol Hepatol 2007; 22 Suppl 1: S96-S100. [PMID: 17567478 DOI: 10.1111/j.1440-1746.2006.04665.x]
89. Hao LS, Zhang XL, An JY, Karlin J, Tian XP, Dun ZN, Xie SR, Chen S. PTEN expression is down-regulated in liver tissues of rats with hepatic fibrosis induced by biliary stenosis. APMIS 2009; 117: 681-691. [PMID: 19703128 DOI: 10.1111/ j.1600-0463.2009.02515.x]
90. Takashima M, Parsons CJ, Ikejima K, Watanabe S, White ES, Rippe RA. The tumor suppressor protein PTEN inhibits rat hepatic stellate cell activation. J Gastroenterol 2009; 44: 847-855. [PMID: 19436944 DOI: 10.1007/s00535-009-0073-3]
91. Cai K, Wang Y, Bao X. MiR-106b promotes cell proliferation via targeting RB in laryngeal carcinoma. J Exp Clin Cancer Res 2011; 30: 73. [PMID: 21819631 DOI: 10.1186/1756-9966-30-73]
92. Mayhew CN, Carter SL, Fox SR, Sexton CR, Reed CA, Srinivasan SV, Liu X, Wikenheiser-Brokamp K, Boivin GP, Lee JS, Aronow BJ, Thorgeirsson SS, Knudsen ES. RB loss abrogates cell cycle control and genome integrity to promote liver tumorigenesis. Gastroenterology 2007; 133: 976-984. [PMID: 17854601 DOI: 10.1053/j.gastro.2007.06.025]
93. Miao J, Chen GG, Yun JP, Chun SY, Zheng ZZ, Ho RL, Chak EC, Xia NS, Lai PB. Identification and characterization of BH3 domain protein Bim and its isoforms in human hepatocellular carcinomas. Apoptosis 2007; 12: 1691-1701. [PMID: 17503221 DOI: 10.1007/s10495-007-0093-5]
94. Johnstone RW, Frew AJ, Smyth MJ. The TRAIL apoptotic pathway in cancer onset, progression and therapy. Nat Rev Cancer 2008; 8: 782-798. [PMID: 18813321 DOI: 10.1038/ nrc2465]
95. Hirano S, Kimoto N, Shimoyama Y, Hirohashi S, Takeichi M. Identification of a neural alpha-catenin as a key regulator of cadherin function and multicellular organization. Cell 1992; 70: 293-301. [PMID: 1638632]
96. Chen ZL, Zhao XH, Wang JW, Li BZ, Wang Z, Sun J, Tan FW, Ding DP, Xu XH, Zhou F, Tan XG, Hang J, Shi SS, Feng XL, He J. microRNA-92a promotes lymph node metastasis of human esophageal squamous cell carcinoma via E-cadherin. J Biol Chem 2011; 286: 10725-10734. [PMID: 21148309 DOI: 10.1074/jbc.M110.165654]
97. Xu X, Chen Z, Zhao X, Wang J, Ding D, Wang Z, Tan F, Tan X, Zhou F, Sun J, Sun N, Gao Y, Shao K, Li N, Qiu B, He J. MicroRNA-25 promotes cell migration and invasion in esophageal squamous cell carcinoma. Biochem Biophys Res Commun 2012; 421: 640-645. [PMID: 22450326 DOI: 10.1016/ j.bbrc.2012.03.048]
98. Zhai B, Yan HX, Liu SQ, Chen L, Wu MC, Wang HY. Reduced expression of E-cadherin/catenin complex in hepatocellular carcinomas. World J Gastroenterol 2008; 14: 5665-5673. [PMID: 18837082]
99. Kong G, Zhang J, Zhang S, Shan C, Ye L, Zhang X. Upregulated microRNA-29a by hepatitis B virus X protein enhances hepatoma cell migration by targeting PTEN in cell culture model. PLoS One 2011; 6: e19518. [PMID: 21573166 DOI: 10.1371/journal.pone.0019518]
100. Liu S, Guo W, Shi J, Li N, Yu X, Xue J, Fu X, Chu K, Lu C, Zhao J, Xie D, Wu M, Cheng S, Liu S. MicroRNA-135a contributes to the development of portal vein tumor thrombus by promoting metastasis in hepatocellular carcinoma. J Hepatol 2012; 56: 389-396. [PMID: 21888875 DOI: 10.1016/ j.jhep.2011.08.008]
101. Han ZB, Chen HY, Fan JW, Wu JY, Tang HM, Peng ZH. Upregulation of microRNA-155 promotes cancer cell invasion and predicts poor survival of hepatocellular carcinoma following liver transplantation. J Cancer Res Clin Oncol 2012; 138: 153-161. [PMID: 22071603 DOI: 10.1007/s00432-011-1076-z]
102. Zheng F, Liao YJ, Cai MY, Liu YH, Liu TH, Chen SP, Bian XW, Guan XY, Lin MC, Zeng YX, Kung HF, Xie D. The putative tumour suppressor microRNA-124 modulates hepatocellular carcinoma cell aggressiveness by repressing ROCK2 and EZH2. Gut 2012; 61: 278-289. [PMID: 21672940 DOI: 10.1136/gut.2011.239145]
103. Fang JH, Zhou HC, Zeng C, Yang J, Liu Y, Huang X, Zhang JP, Guan XY, Zhuang SM. MicroRNA-29b suppresses tumor angiogenesis, invasion, and metastasis by regulating matrix metalloproteinase 2 expression. Hepatology 2011; 54: 1729-1740. [PMID: 21793034 DOI: 10.1002/hep.24577]
104. Yang F, Yin Y, Wang F, Wang Y, Zhang L, Tang Y, Sun S. miR-17-5p Promotes migration of human hepatocellular carcinoma cells through the p38 mitogen-activated protein kinase-heat shock protein 27 pathway. Hepatology 2010; 51: 1614-1623. [PMID: 20209605 DOI: 10.1002/hep.23566]
105. Budhu A, Jia HL, Forgues M, Liu CG, Goldstein D, Lam A, Zanetti KA, Ye QH, Qin LX, Croce CM, Tang ZY, Wang XW. Identification of metastasis-related microRNAs in hepatocellular carcinoma. Hepatology 2008; 47: 897-907. [PMID: 18176954 DOI: 10.1002/hep.22160]
106. Wong CM, Wong CC, Lee JM, Fan DN, Au SL, Ng IO. Sequential alterations of microRNA expression in hepatocellular carcinoma development and venous metastasis. Hepatology 2012; 55: 1453-1461. [PMID: 22135159 DOI: 10.1002/hep.25512]
107. Lin YH, Liao CJ, Huang YH, Wu MH, Chi HC, Wu SM, Chen CY, Tseng YH, Tsai CY, Chung IH, Wu TI, Tsai MM, Lin CD, Lin KH. Thyroid hormone receptor represses miR-17 expression to enhance tumor metastasis in human hepatoma cells. Oncogene 2013; 32: 4509-4518. [PMID: 23912452 DOI: 10.1038/ onc.2013.309]
108. Smith AL, Iwanaga R, Drasin DJ, Micalizzi DS, Vartuli RL, Tan AC, Ford HL. The miR-106b-25 cluster targets Smad7, activates TGF-β signaling, and induces EMT and tumor initiating cell characteristics downstream of Six1 in human breast cancer. Oncogene 2012; 31: 5162-5171. [PMID: 22286770 DOI: 10.1038/onc.2012.11]
109. Xu D, He XX, Chang Y, Sun SZ, Xu CR, Lin JS. Downregulation of MiR-93 expression reduces cell proliferation and clonogenicity of HepG2 cells. Hepatogastroenterology 2012; 59: 2367-2373. [PMID: 22773266 DOI: 10.5754/hge12458]
110. Wang H, Liu J, Zong Y, Xu Y, Deng W, Zhu H, Liu Y, Ma C, Huang L, Zhang L, Qin C. miR-106b aberrantly expressed in a double transgenic mouse model for Alzheimer's disease targets TGF-β type II receptor. Brain Res 2010; 1357: 166-174. [PMID: 20709030 DOI: 10.1016/j.brainres.2010.08.023]
111. Mamiya T, Yamazaki K, Masugi Y, Mori T, Effendi K, Du W, Hibi T, Tanabe M, Ueda M, Takayama T, Sakamoto M. Reduced transforming growth factor-beta receptor II expression in hepatocellular carcinoma correlates with intrahepatic metastasis. Lab Invest 2010; 90: 1339-1345. [PMID: 20531292 DOI: 10.1038/labinvest.2010.105]
112. Shahbazi J, Lock R, Liu T. Tumor Protein 53-Induced Nuclear Protein 1 Enhances p53 Function and Represses Tumorigenesis. Front Genet 2013; 4: 80. [PMID: 23717325 DOI: 10.3389/fgene.2013.00080]
113. Wang M, Gu H, Qian H, Zhu W, Zhao C, Zhang X, Tao Y, Zhang L, Xu W. miR-17-5p/20a are important markers for gastric cancer and murine double minute 2 participates in their functional regulation. Eur J Cancer 2013; 49: 2010-2021. [PMID: 23333058 DOI: 10.1016/j.ejca.2012.12.017]
114. Ma S, Tang KH, Chan YP, Lee TK, Kwan PS, Castilho A, Ng I, Man K, Wong N, To KF, Zheng BJ, Lai PB, Lo CM, Chan KW, Guan XY. miR-130b Promotes CD133(+) liver tumorinitiating cell growth and self-renewal via tumor protein 53-induced nuclear protein 1. Cell Stem Cell 2010; 7: 694-707. [PMID: 21112564 DOI: 10.1016/j.stem.2010.11.010]