Non-coding RNAs in hepatitis B or C-associated hepatocellular carcinoma: Potential diagnostic and prognostic markers and therapeutic targets

Cancer Letters

Volumn 321, Issue 1, 2012, Pages 1-12

  Zhang, Qi ^a   Pu, Rui ^a   Du, Yan ^a   Han, Yifang ^a   Su, Tong ^a   Wang, Hongyang ^b   Cao, Guangwen ^a  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

^b Eastern Hepatobiliary Surgery Institute/Hospital   (China)

Author keywords

Biomarker; Hepatitis virus; Hepatocellular carcinoma; Non coding RNA; Therapeutic target

Indexed keywords

BIOLOGICAL MARKER; HOX TRANSCRIPT ANTISENSE RNA; LONG NON CODING RNA; MICRORNA; MICRORNA 122; MICRORNA 26A; ONCOGENE LIKE NON CODING RNA; SORAFENIB; TUMOR SUPPRESSOR LIKE NON CODING RNA; UNCLASSIFIED DRUG; UNTRANSLATED RNA;

CANCER DIAGNOSIS; CANCER INHIBITION; CANCER PREVENTION; CANCER PROGNOSIS; CANCER SURVIVAL; GENE EXPRESSION REGULATION; HEPATITIS B; HEPATITIS B VIRUS; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; LIVER CARCINOGENESIS; LIVER CELL CARCINOMA; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECURRENCE FREE SURVIVAL; SHORT SURVEY; VIRUS CARCINOGENESIS; VIRUS CELL INTERACTION; VIRUS REPLICATION;

HEPATITIS B VIRUS; HEPATITIS C VIRUS;

EID: 84860341483     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2012.03.011     Document Type: Review

References (154)

1. Stein L.D. Human genome: end of the beginning. Nature 2004, 431:915-916.
2. Costa F.F. Non-coding RNAs: meet thy masters. Bioessays 2010, 32:599-608.
3. Pauli A., Rinn J.L., Schier A.F. Non-coding RNAs as regulators of embryogenesis. Nat. Rev. Genet. 2011, 12:136-149.
4. Nana-Sinkam S.P., Croce C.M. Non-coding RNAs in cancer initiation and progression and as novel biomarkers. Mol. Oncol. 2011, 5:483-491.
5. Bartel D.P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116:281-297.
6. Lytle J.R., Yario T.A., Steitz J.A. Target mRNAs are repressed as efficiently by microRNA-binding sites in the 5' UTR as in the 3' UTR. Proc. Natl. Acad. Sci. USA 2007, 104:9667-9672.
7. Friedman R.C., Farh K.K., Burge C.B., Bartel D.P. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 2009, 19:92-105.
8. Esquela-Kerscher A., Slack F.J. Oncomirs - microRNAs with a role in cancer. Nat. Rev. Cancer 2006, 6:259-269.
9. Gibb E.A., Brown C.J., Lam W.L. The functional role of long non-coding RNA in human carcinomas. Mol. Cancer 2011, 10:38.
10. Ponting C.P., Oliver P.L., Reik W. Evolution and functions of long noncoding RNAs. Cell 2009, 136:629-641.
11. Wapinski O., Chang H.Y. Long noncoding RNAs and human disease. Trends Cell Biol. 2011, 21:354-361.
12. Braconi C., Kogure T., Valeri N., Huang N., Nuovo G., Costinean S., Negrini M., Miotto E., Croce C.M., Patel T. MicroRNA-29 can regulate expression of the long non-coding RNA gene MEG3 in hepatocellular cancer. Oncogene 2011, 30:4750-4756.
13. Huarte M., Guttman M., Feldser D., Garber M., Koziol M.J., Kenzelmann-Broz D., Khalil A.M., Zuk O., Amit I., Rabani M., Attardi L.D., Regev A., Lander E.S., Jacks T., Rinn J.L. A large intergenic noncoding RNA induced by p53 mediates global gene repression in the p53 response. Cell 2010, 142:409-419.
14. Gupta R.A., Shah N., Wang K.C., Kim J., Horlings H.M., Wong D.J., Tsai M.C., Hung T., Argani P., Rinn J.L., Wang Y., Brzoska P., Kong B., Li R., West R.B., van de Vijver M.J., Sukumar S., Chang H.Y. Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 2010, 464:1071-1076.
15. Bouchard M.J., Navas-Martin S. Hepatitis B and C virus hepatocarcinogenesis: lessons learned and future challenges. Cancer Lett. 2011, 305:123-143.
16. Huang S., He X. The role of microRNAs in liver cancer progression. Br. J. Cancer 2011, 104:235-240.
17. Jin W.B., Wu F.L., Kong D., Guo A.G. HBV-encoded microRNA candidate and its target. Comput. Biol. Chem. 2007, 31:124-126.
18. Zhang Z.Z., Liu X., Wang D.Q., Teng M.K., Niu L.W., Huang A.L., Liang Z. Hepatitis B virus and hepatocellular carcinoma at the miRNA level. World J. Gastroenterol. 2011, 17:3353-3358.
19. Liu Y., Zhao J.J., Wang C.M., Li M.Y., Han P., Wang L., Cheng Y.Q., Zoulim F., Ma X., Xu D.P. Altered expression profiles of microRNAs in a stable hepatitis B virus-expressing cell line. Chin. Med. J. (Engl.) 2009, 122:10-14.
20. Hsieh A., Kim H.S., Lim S.O., Yu D.Y., Jung G. Hepatitis B viral X protein interacts with tumor suppressor adenomatous polyposis coli to activate Wnt/beta-catenin signaling. Cancer Lett. 2011, 300:162-172.
21. Wang Y., Lu Y., Toh S.T., Sung W.K., Tan P., Chow P., Chung A.Y., Jooi L.L., Lee C.G. Lethal-7 is down-regulated by the hepatitis B virus x protein and targets signal transducer and activator of transcription 3. J. Hepatol. 2010, 53:57-66.
22. Shan C., Zhang S., Cui W., You X., Kong G., Du Y., Qiu L., Ye L., Zhang X. Hepatitis B virus X protein activates CD59 involving DNA binding and let-7i in protection of hepatoma and hepatic cells from complement attack. Carcinogenesis 2011, 32:1190-1197.
23. Wu G., Yu F., Xiao Z., Xu K., Xu J., Tang W., Wang J., Song E. Hepatitis B virus X protein downregulates expression of the miR-16 family in malignant hepatocytes in vitro. Br. J. Cancer 2011, 105:146-153.
24. 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.
25. Wang Y., Lau S.H., Sham J.S., Wu M.C., Wang T., Guan X.Y. Characterization of HBV integrants in 14 hepatocellular carcinomas: association of truncated X gene and hepatocellular carcinogenesis. Oncogene 2004, 23:142-148.
26. Ma N.F., Lau S.H., Hu L., Xie D., Wu J., Yang J., Wang Y., Wu M.C., Fung J., Bai X., Tzang C.H., Fu L., Yang M., Su Y.A., Guan X.Y. COOH-terminal truncated HBV X protein plays key role in hepatocarcinogenesis. Clin. Cancer Res. 2008, 14:5061-5068.
27. Yip W.K., Cheng A.S., Zhu R., Lung R.W., Tsang D.P., Lau S.S., Chen Y., Sung J.G., Lai P.B., Ng E.K., Yu J., Wong N., To K.F., Wong V.W., Sung J.J., Chan H.L. Carboxyl-terminal truncated HBx regulates a distinct microRNA transcription program in hepatocellular carcinoma development. PLoS One 2011, 6:e22888.
28. Liu X., Wang T., Wakita T., Yang W. Systematic identification of microRNA and messenger RNA profiles in hepatitis C virus-infected human hepatoma cells. Virology 2010, 398:57-67.
29. Braconi C., Valeri N., Gasparini P., Huang N., Taccioli C., Nuovo G., Suzuki T., Croce C.M., Patel T. Hepatitis C virus proteins modulate microRNA expression and chemosensitivity in malignant hepatocytes. Clin. Cancer Res. 2010, 16:957-966.
30. Potenza N., Papa U., Mosca N., Zerbini F., Nobile V., Russo A. Human microRNA hsa-miR-125a-5p interferes with expression of hepatitis B virus surface antigen. Nucleic Acids Res. 2011, 39:5157-5163.
31. Wu F.L., Jin W.B., Li J.H., Guo A.G. Targets for human encoded microRNAs in HBV genes. Virus Genes 2011, 42:157-161.
32. Zhang X., Zhang E., Ma Z., Pei R., Jiang M., Schlaak J.F., Roggendorf M., Lu M. Modulation of hepatitis B virus replication and hepatocyte differentiation by MicroRNA-1. Hepatology 2011, 53:1476-1485.
33. Guo H., Liu H., Mitchelson K., Rao H., Luo M., Xie L., Sun Y., Zhang L., Lu Y., Liu R., Ren A., Liu S., Zhou S., Zhu J., Zhou Y., Huang A., Wei L., Guo Y., Cheng J. MicroRNAs-372/373 promote the expression of hepatitis B virus through the targeting of nuclear factor I/B. Hepatology 2011.
34. Zhang G.L., Li Y.X., Zheng S.Q., Liu M., Li X., Tang H. Suppression of hepatitis B virus replication by microRNA-199a-3p and microRNA-210. Antivir. Res. 2010, 88:169-175.
35. Chen Y., Shen A., Rider P.J., Yu Y., Wu K., Mu Y., Hao Q., Liu Y., Gong H., Zhu Y., Liu F., Wu J. 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. 2011, 25:4511-4521.
36. Qiu L., Fan H., Jin W., Zhao B., Wang Y., Ju Y., Chen L., Chen Y., Duan Z., Meng S. MiR-122-induced down-regulation of HO-1 negatively affects miR-122-mediated suppression of HBV. Biochem. Biophys. Res. Commun. 2010, 398:771-777.
37. Protzer U., Seyfried S., Quasdorff M., Sass G., Svorcova M., Webb D., Bohne F., Hosel M., Schirmacher P., Tiegs G. Antiviral activity and hepatoprotection by heme oxygenase-1 in hepatitis B virus infection. Gastroenterology 2007, 133:1156-1165.
38. Fan C.G., Wang C.M., Tian C., Wang Y., Li L., Sun W.S., Li R.F., Liu Y.G. MiR-122 inhibits viral replication and cell proliferation in hepatitis B virus-related hepatocellular carcinoma and targets NDRG3. Oncol. Rep. 2011, 26:1281-1286.
39. Wang S., Qiu L., Yan X., Jin W., Wang Y., Chen L., Wu E., Ye X., Gao G.F., Wang F., Chen Y., Duan Z., Meng S. Loss of MiR-122 expression in patients with hepatitis B enhances hepatitis B virus replication through cyclin G1 modulated P53 activity. Hepatology 2011, (Epub ahead of print). 10.1002/hep. 24809.
40. Ji F., Yang B., Peng X., Ding H., You H., Tien P. Circulating microRNAs in hepatitis B virus-infected patients. J. Viral Hepat. 2011, 18:e242-251.
41. Banaudha K., Kaliszewski M., Korolnek T., Florea L., Yeung M.L., Jeang K.T., Kumar A. MicroRNA silencing of tumor suppressor DLC-1 promotes efficient hepatitis C virus replication in primary human hepatocytes. Hepatology 2011, 53:53-61.
42. Hou W., Tian Q., Zheng J., Bonkovsky H.L. MicroRNA-196 represses Bach1 protein and hepatitis C virus gene expression in human hepatoma cells expressing hepatitis C viral proteins. Hepatology 2010, 51:1494-1504.
43. Jangra R.K., Yi M., Lemon S.M. Regulation of hepatitis C virus translation and infectious virus production by the microRNA miR-122. J. Virol. 2010, 84:6615-6625.
44. Machlin E.S., Sarnow P., Sagan S.M. Masking the 5' terminal nucleotides of the hepatitis C virus genome by an unconventional microRNA-target RNA complex. Proc. Natl. Acad. Sci. USA 2011, 108:3193-3198.
45. Wilson J.A., Zhang C., Huys A., Richardson C.D. Human Ago2 is required for efficient microRNA 122 regulation of hepatitis C virus RNA accumulation and translation. J. Virol. 2011, 85:2342-2350.
46. Shan Y., Zheng J., Lambrecht R.W., Bonkovsky H.L. Reciprocal effects of micro-RNA-122 on expression of heme oxygenase-1 and hepatitis C virus genes in human hepatocytes. Gastroenterology 2007, 133:1166-1174.
47. Pedersen I.M., Cheng G., Wieland S., Volinia S., Croce C.M., Chisari F.V., David M. Interferon modulation of cellular microRNAs as an antiviral mechanism. Nature 2007, 449:919-922.
48. Li Y.P., Gottwein J.M., Scheel T.K., Jensen T.B., Bukh J. MicroRNA-122 antagonism against hepatitis C virus genotypes 1-6 and reduced efficacy by host RNA insertion or mutations in the HCV 5' UTR. Proc. Natl. Acad. Sci. USA 2011, 108:4991-4996.
49. Lanford R.E., Hildebrandt-Eriksen E.S., Petri A., Persson R., Lindow M., Munk M.E., Kauppinen S., Orum H. Therapeutic silencing of microRNA-122 in primates with chronic hepatitis C virus infection. Science 2010, 327:198-201.
50. Sarasin-Filipowicz M., Krol J., Markiewicz I., Heim M.H., Filipowicz W. Decreased levels of microRNA miR-122 in individuals with hepatitis C responding poorly to interferon therapy. Nat. Med. 2009, 15:31-33.
51. Morita K., Taketomi A., Shirabe K., Umeda K., Kayashima H., Ninomiya M., Uchiyama H., Soejima Y., Maehara Y. Clinical significance and potential of hepatic microRNA-122 expression in hepatitis C. Liver Int. 2011, 31:474-484.
52. Bihrer V., Friedrich-Rust M., Kronenberger B., Forestier N., Haupenthal J., Shi Y., Peveling-Oberhag J., Radeke H.H., Sarrazin C., Herrmann E., Zeuzem S., Waidmann O., Piiper A. Serum miR-122 as a biomarker of necroinflammation in patients with chronic hepatitis C virus infection. Am. J. Gastroenterol. 2011, 106:1663-1669.
53. Cermelli S., Ruggieri A., Marrero J.A., Ioannou G.N., Beretta L. Circulating microRNAs in patients with chronic hepatitis C and non-alcoholic fatty liver disease. PLoS One 2011, 6:e23937.
54. Lan F.F., Wang H., Chen Y.C., Chan C.Y., Ng S.S., Li K., Xie D., He M.L., Lin M.C., Kung H.F. Hsa-let-7g inhibits proliferation of hepatocellular carcinoma cells by downregulation of c-Myc and upregulation of p16(INK4A). Int. J. Cancer 2011, 128:319-331.
55. Ji J., Zhao L., Budhu A., Forgues M., Jia H.L., Qin L.X., Ye Q.H., Yu J., Shi X., Tang Z.Y., Wang X.W. Let-7g targets collagen type I alpha2 and inhibits cell migration in hepatocellular carcinoma. J. Hepatol. 2010, 52:690-697.
56. Chung G.E., Yoon J.H., Myung S.J., Lee J.H., Lee S.H., Lee S.M., Kim S.J., Hwang S.Y., Lee H.S., Kim C.Y. High expression of microRNA-15b predicts a low risk of tumor recurrence following curative resection of hepatocellular carcinoma. Oncol. Rep. 2010, 23:113-119.
57. Zhang J., Yang Y., Yang T., Liu Y., Li A., Fu S., Wu M., Pan Z., Zhou W. MicroRNA-22, downregulated in hepatocellular carcinoma and correlated with prognosis, suppresses cell proliferation and tumourigenicity. Br. J. Cancer 2010, 103:1215-1220.
58. Kota J., Chivukula R.R., O'Donnell K.A., Wentzel E.A., Montgomery C.L., Hwang H.W., Chang T.C., Vivekanandan P., Torbenson M., Clark K.R., Mendell J.R., Mendell J.T. Therapeutic microRNA delivery suppresses tumorigenesis in a murine liver cancer model. Cell 2009, 137:1005-1017.
59. Ji J., Shi J., Budhu A., Yu Z., Forgues M., Roessler S., Ambs S., Chen Y., Meltzer P.S., Croce C.M., Qin L.X., Man K., Lo C.M., Lee J., Ng I.O., Fan J., Tang Z.Y., Sun H.C., Wang X.W. MicroRNA expression, survival, and response to interferon in liver cancer. New Engl. J. Med. 2009, 361:1437-1447.
60. Wang C.M., Wang Y., Fan C.G., Xu F.F., Sun W.S., Liu Y.G., Jia J.H. MiR-29c targets TNFAIP3, inhibits cell proliferation and induces apoptosis in hepatitis B virus-related hepatocellular carcinoma. Biochem. Biophys. Res. Commun. 2011, 411:586-592.
61. Chiang C.W., Huang Y., Leong K.W., Chen L.C., Chen H.C., Chen S.J., Chou C.K. PKCalpha mediated induction of miR-101 in human hepatoma HepG2 cells. J. Biomed. Sci. 2010, 17:35.
62. Fang J.H., Zhou H.C., Zeng C., Yang J., Liu Y., Huang X., Zhang J.P., Guan X.Y., Zhuang S.M. MicroRNA-29b suppresses tumor angiogenesis, invasion, and metastasis by regulating matrix metalloproteinase 2 expression. Hepatology 2011, 54:1729-1740.
63. Li D., Liu X., Lin L., Hou J., Li N., Wang C., Wang P., Zhang Q., Zhang P., Zhou W., Wang Z., Ding G., Zhuang S.M., Zheng L., Tao W., Cao X. MicroRNA-99a inhibits hepatocellular carcinoma growth and correlates with prognosis of patients with hepatocellular carcinoma. J. Biol. Chem. 2011, 286:36677-36685.
64. Su H., Yang J.R., Xu T., Huang J., Xu L., Yuan Y., Zhuang S.M. MicroRNA-101, down-regulated in hepatocellular carcinoma, promotes apoptosis and suppresses tumorigenicity. Cancer Res. 2009, 69:1135-1142.
65. Furuta M., Kozaki K.I., Tanaka S., Arii S., Imoto I., Inazawa J. MiR-124 and miR-203 are epigenetically silenced tumor-suppressive microRNAs in hepatocellular carcinoma. Carcinogenesis 2010, 31:766-776.
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.
67. Gao P., Wong C.C., Tung E.K., Lee J.M., Wong C.M., Ng I.O. Deregulation of microRNA expression occurs early and accumulates in early stages of HBV-associated multistep hepatocarcinogenesis. J. Hepatol. 2011, 54:1177-1184.
68. Shen Q., Cicinnati V.R., Zhang X., Iacob S., Weber F., Sotiropoulos G.C., Radtke A., Lu M., Paul A., Gerken G., Beckebaum S. Role of microRNA-199a-5p and discoidin domain receptor 1 in human hepatocellular carcinoma invasion. Mol. Cancer 2010, 9:227.
69. Hou J., Lin L., Zhou W., Wang Z., Ding G., Dong Q., Qin L., Wu X., Zheng Y., Yang Y., Tian W., Zhang Q., Wang C., Zhuang S.M., Zheng L., Liang A., Tao W., Cao X. Identification of miRNomes in human liver and hepatocellular carcinoma reveals miR-199a/b-3p as therapeutic target for hepatocellular carcinoma. Cancer Cell 2011, 19:232-243.
70. Fornari F., Milazzo M., Chieco P., Negrini M., Calin G.A., Grazi G.L., Pollutri D., Croce C.M., Bolondi L., Gramantieri L. MiR-199a-3p regulates mTOR and c-Met to influence the doxorubicin sensitivity of human hepatocarcinoma cells. Cancer Res. 2010, 70:5184-5193.
71. Huang J., Wang Y., Guo Y., Sun S. Down-regulated microRNA-152 induces aberrant DNA methylation in hepatitis B virus-related hepatocellular carcinoma by targeting DNA methyltransferase 1. Hepatology 2010, 52:60-70.
72. Ladeiro Y., Couchy G., Balabaud C., Bioulac-Sage P., Pelletier L., Rebouissou S., Zucman-Rossi J. MicroRNA profiling in hepatocellular tumors is associated with clinical features and oncogene/tumor suppressor gene mutations. Hepatology 2008, 47:1955-1963.
73. Liu A.M., Poon R.T., Luk J.M. MicroRNA-375 targets Hippo-signaling effector YAP in liver cancer and inhibits tumor properties. Biochem. Biophys. Res. Commun. 2010, 394:623-627.
74. Wong Q.W., Lung R.W., Law P.T., Lai P.B., Chan K.Y., To K.F., Wong N. MicroRNA-223 is commonly repressed in hepatocellular carcinoma and potentiates expression of Stathmin1. Gastroenterology 2008, 135:257-269.
75. Hou Y.Y., Cao W.W., Li L., Li S.P., Liu T., Wan H.Y., Liu M., Li X., Tang H. MicroRNA-519d targets MKi67 and suppresses cell growth in the hepatocellular carcinoma cell line QGY-7703. Cancer Lett. 2011, 307:182-190.
76. Zhang S., Shan C., Kong G., Du Y., Ye L., Zhang X. MicroRNA-520e suppresses growth of hepatoma cells by targeting the NF-kappaB-inducing kinase (NIK). Oncogene 2012, (Epub ahead of print). 10.1038/onc.2011.523.
77. 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.
78. Yao J., Liang L., Huang S., Ding J., Tan N., Zhao Y., Yan M., Ge C., Zhang Z., Chen T., Wan D., Yao M., Li J., Gu J., He X. MicroRNA-30d promotes tumor invasion and metastasis by targeting Galphai2 in hepatocellular carcinoma. Hepatology 2010, 51:846-856.
79. Zhang X., Liu S., Hu T., He Y., Sun S. Up-regulated microRNA-143 transcribed by nuclear factor kappa B enhances hepatocarcinoma metastasis by repressing fibronectin expression. Hepatology 2009, 50:490-499.
80. Pineau P., Volinia S., McJunkin K., Marchio A., Battiston C., Terris B., Mazzaferro V., Lowe S.W., Croce C.M., Dejean A. MiR-221 overexpression contributes to liver tumorigenesis. Proc. Natl. Acad. Sci. USA 2010, 107:264-269.
81. Gramantieri L., Fornari F., Ferracin M., Veronese A., Sabbioni S., Calin G.A., Grazi G.L., Croce C.M., Bolondi L., Negrini M. MicroRNA-221 targets Bmf in hepatocellular carcinoma and correlates with tumor multifocality. Clin. Cancer Res. 2009, 15:5073-5081.
82. Fornari F., Gramantieri L., Ferracin M., Veronese A., Sabbioni S., Calin G.A., Grazi G.L., Giovannini C., Croce C.M., Bolondi L., Negrini M. MiR-221 controls CDKN1C/p57 and CDKN1B/p27 expression in human hepatocellular carcinoma. Oncogene 2008, 27:5651-5661.
83. Wong Q.W., Ching A.K., Chan A.W., Choy K.W., To K.F., Lai P.B., Wong N. MiR-222 overexpression confers cell migratory advantages in hepatocellular carcinoma through enhancing AKT signaling. Clin. Cancer Res. 2010, 16:867-875.
84. Lin J., Huang S., Wu S., Ding J., Zhao Y., Liang L., Tian Q., Zha R., Zhan R., He X. MicroRNA-423 promotes cell growth and regulates G(1)/S transition by targeting p21Cip1/Waf1 in hepatocellular carcinoma. Carcinogenesis 2011, 32:1641-1647.
85. Yang L., Ma Z., Wang D., Zhao W., Chen L., Wang G. MicroRNA-602 regulating tumor suppressive gene RASSF1A is overexpressed in hepatitis B virus-infected liver and hepatocellular carcinoma. Cancer Biol. Ther. 2010, 9:803-808.
86. Lin R., Maeda S., Liu C., Karin M., Edgington T.S. A large noncoding RNA is a marker for murine hepatocellular carcinomas and a spectrum of human carcinomas. Oncogene 2007, 26:851-858.
87. Lai M.C., Yang Z., Zhou L., Zhu Q.Q., Xie H.Y., Zhang F., Wu L.M., Chen L.M., Zheng S.S. Long non-coding RNA MALAT-1 overexpression predicts tumor recurrence of hepatocellular carcinoma after liver transplantation. Med. Oncol. 2012, (Epub ahead of print). 10.1007/s12032-011-0004-z.
88. Rinn J.L., Kertesz M., Wang J.K., Squazzo S.L., Xu X., Brugmann S.A., Goodnough L.H., Helms J.A., Farnham P.J., Segal E., Chang H.Y. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 2007, 129:1311-1323.
89. Yang Z., Zhou L., Wu L.M., Lai M.C., Xie H.Y., Zhang F., Zheng S.S. Overexpression of long non-coding RNA HOTAIR predicts tumor recurrence in hepatocellular carcinoma patients following liver transplantation. Ann. Surg. Oncol. 2011, 18:1243-1250.
90. Matouk I.J., Abbasi I., Hochberg A., Galun E., Dweik H., Akkawi M. Highly upregulated in liver cancer noncoding RNA is overexpressed in hepatic colorectal metastasis. Eur. J. Gastroenterol. Hepatol. 2009, 21:688-692.
91. Panzitt K., Tschernatsch M.M., Guelly C., Moustafa T., Stradner M., Strohmaier H.M., Buck C.R., Denk H., Schroeder R., Trauner M., Zatloukal K. Characterization of HULC, a novel gene with striking up-regulation in hepatocellular carcinoma, as noncoding RNA. Gastroenterology 2007, 132:330-342.
92. Gabory A., Ripoche M.A., Yoshimizu T., Dandolo L. The H19 gene: regulation and function of a non-coding RNA. Cytogenet. Genome Res. 2006, 113:188-193.
93. Matouk I.J., DeGroot N., Mezan S., Ayesh S., Abu-lail R., Hochberg A., Galun E. The H19 non-coding RNA is essential for human tumor growth. PLoS One 2007, 2:e845.
94. Yang F., Zhang L., Huo X.S., Yuan J.H., Xu D., Yuan S.X., Zhu N., Zhou W.P., Yang G.S., Wang Y.Z., Shang J.L., Gao C.F., Zhang F.R., Wang F., Sun S.H. Long noncoding RNA high expression in hepatocellular carcinoma facilitates tumor growth through enhancer of zeste homolog 2 in humans. Hepatology 2011, 54:1679-1689.
95. Liu A.M., Zhang C., Burchard J., Fan S.T., Wong K.F., Dai H., Poon R.T., Luk J.M. Global regulation on microRNA in hepatitis B virus-associated hepatocellular carcinoma. OMICS 2011, 15:187-191.
96. Kim T., Veronese A., Pichiorri F., Lee T.J., Jeon Y.J., Volinia S., Pineau P., Marchio A., Palatini J., Suh S.S., Alder H., Liu C.G., Dejean A., Croce C.M. P53 regulates epithelial-mesenchymal transition through microRNAs targeting ZEB1 and ZEB2. J. Exp. Med. 2011, 208:875-883.
97. Scisciani C., Vossio S., Guerrieri F., Schinzari V., De Iaco R., Cervello M., Montalto G., Pollicino T., Raimondo G., Levrero M., Pediconi N. Transcriptional regulation of mir-224 upregulated in human HCCs by NFkB inflammatory pathways. J. Hepatol. 2012, (Epub ahead of print). 10.1016/j.jhep. 2011.11.017.
98. Calin G.A., Sevignani C., Dumitru C.D., Hyslop T., Noch E., Yendamuri S., Shimizu M., Rattan S., Bullrich F., Negrini M., Croce C.M. Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers. Proc. Natl. Acad. Sci. USA 2004, 101:2999-3004.
99. Feitelson M.A., Lee J. Hepatitis B virus integration, fragile sites, and hepatocarcinogenesis. Cancer Lett. 2007, 252:157-170.
100. Lagana A., Russo F., Sismeiro C., Giugno R., Pulvirenti A., Ferro A. Variability in the incidence of miRNAs and genes in fragile sites and the role of repeats and CpG islands in the distribution of genetic material. PLoS One 2010, 5:e11166.
101. Datta J., Kutay H., Nasser M.W., Nuovo G.J., Wang B., Majumder S., Liu C.G., Volinia S., Croce C.M., Schmittgen T.D., Ghoshal K., Jacob S.T. Methylation mediated silencing of MicroRNA-1 gene and its role in hepatocellular carcinogenesis. Cancer Res. 2008, 68:5049-5058.
102. Xu T., Zhu Y., Wei Q.K., Yuan Y., Zhou F., Ge Y.Y., Yang J.R., Su H., Zhuang S.M. A functional polymorphism in the miR-146a gene is associated with the risk for hepatocellular carcinoma. Carcinogenesis 2008, 29:2126-2131.
103. Akkiz H., Bayram S., Bekar A., Akgollu E., Uskudar O., Sandikci M. No association of pre-microRNA-146a rs2910164 polymorphism and risk of hepatocellular carcinoma development in Turkish population: a case-control study. Gene 2011, 486:104-109.
104. Xu Y., Liu L., Liu J., Zhang Y., Zhu J., Chen J., Liu S., Liu Z., Shi H., Shen H., Hu Z. A potentially functional polymorphism in the promoter region of miR-34b/c is associated with an increased risk for primary hepatocellular carcinoma. Int. J. Cancer 2011, 128:412-417.
105. Qi P., Dou T.H., Geng L., Zhou F.G., Gu X., Wang H., Gao C.F. Association of a variant in MIR 196A2 with susceptibility to hepatocellular carcinoma in male Chinese patients with chronic hepatitis B virus infection. Hum. Immunol. 2010, 71:621-626.
106. Akkiz H., Bayram S., Bekar A., Akgollu E., Ulger Y. A functional polymorphism in pre-microRNA-196a-2 contributes to the susceptibility of hepatocellular carcinoma in a Turkish population: a case-control study. J. Viral. Hepat. 2011, 18:e399-407.
107. Guo Z., Wu C., Wang X., Wang C., Zhang R., Shan B. A polymorphism at the miR-502 binding site in the 3' untranslated region of the histone methyltransferase SET8 is associated with hepatocellular carcinoma outcome. Int. J. Cancer 2012, (Epub ahead of print). 10.1002/ijc.27352.
108. Xiang Y., Fan S., Cao J., Huang S., Zhang L.P. Association of the microRNA-499 variants with susceptibility to hepatocellular carcinoma in a Chinese population. Mol. Biol. Rep. 2012, (Epub ahead of print). 10.1007/s11033-012-1532-0.
109. 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.
110. Chen X., Ba Y., Ma L., Cai X., Yin Y., Wang K., Guo J., Zhang Y., Chen J., Guo X., Li Q., Li X., Wang W., Wang J., Jiang X., Xiang Y., Xu C., Zheng P., Zhang J., Li R., Zhang H., Shang X., Gong T., Ning G., Zen K., Zhang C.Y. Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res. 2008, 18:997-1006.
111. Li L.M., Hu Z.B., Zhou Z.X., Chen X., Liu F.Y., Zhang J.F., Shen H.B., Zhang C.Y., Zen K. Serum microRNA profiles serve as novel biomarkers for HBV infection and diagnosis of HBV-positive hepatocarcinoma. Cancer Res. 2010, 70:9798-9807.
112. Zhou J., Yu L., Gao X., Hu J., Wang J., Dai Z., Wang J.F., Zhang Z., Lu S., Huang X., Wang Z., Qiu S., Wang X., Yang G., Sun H., Tang Z., Wu Y., Zhu H., Fan J. Plasma microRNA panel to diagnose hepatitis B virus-related hepatocellular carcinoma. J. Clin. Oncol. 2011, 29:4781-4788.
113. Xu J., Wu C., Che X., Wang L., Yu D., Zhang T., Huang L., Li H., Tan W., Wang C., Lin D. Circulating microRNAs, miR-21, miR-122, and miR-223, in patients with hepatocellular carcinoma or chronic hepatitis. Mol. Carcinogen. 2011, 50:136-142.
114. Qi P., Cheng S.Q., Wang H., Li N., Chen Y.F., Gao C.F. Serum microRNAs as biomarkers for hepatocellular carcinoma in Chinese patients with chronic hepatitis B virus infection. PLoS One 2011, 6:e28486.
115. Qu K.Z., Zhang K., Li H., Afdhal N.H., Albitar M. Circulating microRNAs as biomarkers for hepatocellular carcinoma. J. Clin. Gastroenterol. 2011, 45:355-360.
116. Li J., Wang Y., Yu W., Chen J., Luo J. Expression of serum miR-221 in human hepatocellular carcinoma and its prognostic significance. Biochem. Biophys. Res. Commun. 2011, 406:70-73.
117. Shigoka M., Tsuchida A., Matsudo T., Nagakawa Y., Saito H., Suzuki Y., Aoki T., Murakami Y., Toyoda H., Kumada T., Bartenschlager R., Kato N., Ikeda M., Takashina T., Tanaka M., Suzuki R., Oikawa K., Takanashi M., Kuroda M. Deregulation of miR-92a expression is implicated in hepatocellular carcinoma development. Pathol. Int. 2010, 60:351-357.
118. Zhu H.T., Dong Q.Z., Wang G., Zhou H.J., Ren N., Jia H.L., Ye Q.H., Qin L.X. Identification of suitable reference genes for qRT-PCR analysis of circulating microRNAs in hepatitis B virus-infected patients. Mol. Biotechnol. 2012, 50:49-56.
119. Xiong Y., Fang J.H., Yun J.P., Yang J., Zhang Y., Jia W.H., Zhuang S.M. Effects of microRNA-29 on apoptosis, tumorigenicity, and prognosis of hepatocellular carcinoma. Hepatology 2010, 51:836-845.
120. Fornari F., Gramantieri L., Giovannini C., Veronese A., Ferracin M., Sabbioni S., Calin G.A., Grazi G.L., Croce C.M., Tavolari S., Chieco P., Negrini M., Bolondi L. MiR-122/cyclin G1 interaction modulates p53 activity and affects doxorubicin sensitivity of human hepatocarcinoma cells. Cancer Res. 2009, 69:5761-5767.
121. Luk J.M., Burchard J., Zhang C., Liu A.M., Wong K.F., Shek F.H., Lee N.P., Fan S.T., Poon R.T., Ivanovska I., Philippar U., Cleary M.A., Buser C.A., Shaw P.M., Lee C.N., Tenen D.G., Dai H., Mao M. DLK1-DIO3 genomic imprinted microRNA cluster at 14q32.2 defines a stemlike subtype of hepatocellular carcinoma associated with poor survival. J. Biol. Chem. 2011, 286:30706-30713.
122. Sato F., Hatano E., Kitamura K., Myomoto A., Fujiwara T., Takizawa S., Tsuchiya S., Tsujimoto G., Uemoto S., Shimizu K. MicroRNA profile predicts recurrence after resection in patients with hepatocellular carcinoma within the Milan Criteria. PLoS One 2011, 6:e16435.
123. Utsunomiya T., Shimada M., Imura S., Morine Y., Ikemoto T., Mori M. Molecular signatures of noncancerous liver tissue can predict the risk for late recurrence of hepatocellular carcinoma. J. Gastroenterol. 2010, 45:146-152.
124. Chuma M., Hige S., Kamiyama T., Meguro T., Nagasaka A., Nakanishi K., Yamamoto Y., Nakanishi M., Kohara T., Sho T., Yamamoto K., Horimoto H., Kobayashi T., Yokoo H., Matsushita M., Todo S., Asaka M. The influence of hepatitis B DNA level and antiviral therapy on recurrence after initial curative treatment in patients with hepatocellular carcinoma. J. Gastroenterol. 2009, 44:991-999.
125. Lee Y.S., Dutta A. MicroRNAs in cancer. Annu. Rev. Pathol. 2009, 4:199-227.
126. Bai S., Nasser M.W., Wang B., Hsu S.H., Datta J., Kutay H., Yadav A., Nuovo G., Kumar P., Ghoshal K. MicroRNA-122 inhibits tumorigenic properties of hepatocellular carcinoma cells and sensitizes these cells to sorafenib. J. Biol. Chem. 2009, 284:32015-32027.
127. Xu Y., Xia F., Ma L., Shan J., Shen J., Yang Z., Liu J., Cui Y., Bian X., Bie P., Qian C. MicroRNA-122 sensitizes HCC cancer cells to adriamycin and vincristine through modulating expression of MDR and inducing cell cycle arrest. Cancer Lett. 2011, 310:160-169.
128. Su C., Hou Z., Zhang C., Tian Z., Zhang J. Ectopic expression of microRNA-155 enhances innate antiviral immunity against HBV infection in human hepatoma cells. Virol. J. 2011, 8:354.
129. Bandyopadhyay S., Friedman R.C., Marquez R.T., Keck K., Kong B., Icardi M.S., Brown K.E., Burge C.B., Schmidt W.N., Wang Y., McCaffrey A.P. Hepatitis C virus infection and hepatic stellate cell activation downregulate miR-29: miR-29 overexpression reduces hepatitis C viral abundance in culture. J. Infect. Dis. 2011, 203:1753-1762.
130. Jopling C.L., Yi M., Lancaster A.M., Lemon S.M., Sarnow P. Modulation of hepatitis C virus RNA abundance by a liver-specific MicroRNA. Science 2005, 309:1577-1581.
131. Jopling C.L., Schutz S., Sarnow P. Position-dependent function for a tandem microRNA miR-122-binding site located in the hepatitis C virus RNA genome. Cell Host Microbe 2008, 4:77-85.
132. Henke J.I., Goergen D., Zheng J., Song Y., Schuttler C.G., Fehr C., Junemann C., Niepmann M. MicroRNA-122 stimulates translation of hepatitis C virus RNA. EMBO J. 2008, 27:3300-3310.
133. Ishida H., Tatsumi T., Hosui A., Nawa T., Kodama T., Shimizu S., Hikita H., Hiramatsu N., Kanto T., Hayashi N., Takehara T. Alterations in microRNA expression profile in HCV-infected hepatoma cells: involvement of miR-491 in regulation of HCV replication via the PI3 kinase/Akt pathway. Biochem. Biophys. Res. Commun. 2011, 412:92-97.
134. Murakami Y., Aly H.H., Tajima A., Inoue I., Shimotohno K. Regulation of the hepatitis C virus genome replication by miR-199a. J. Hepatol. 2009, 50:453-460.
135. Salvi A., Sabelli C., Moncini S., Venturin M., Arici B., Riva P., Portolani N., Giulini S.M., De Petro G., Barlati S. MicroRNA-23b mediates urokinase and c-met downmodulation and a decreased migration of human hepatocellular carcinoma cells. FEBS J. 2009, 276:2966-2982.
136. Li N., Fu H., Tie Y., Hu Z., Kong W., Wu Y., Zheng X. MiR-34a inhibits migration and invasion by down-regulation of c-Met expression in human hepatocellular carcinoma cells. Cancer Lett. 2009, 275:44-53.
137. Li S., Fu H., Wang Y., Tie Y., Xing R., Zhu J., Sun Z., Wei L., Zheng X. MicroRNA-101 regulates expression of the v-fos FBJ murine osteosarcoma viral oncogene homolog (FOS) oncogene in human hepatocellular carcinoma. Hepatology 2009, 49:1194-1202.
138. Gramantieri L., Ferracin M., Fornari F., Veronese A., Sabbioni S., Liu C.G., Calin G.A., Giovannini C., Ferrazzi E., Grazi G.L., Croce C.M., Bolondi L., Negrini M. Cyclin G1 is a target of miR-122a, a microRNA frequently down-regulated in human hepatocellular carcinoma. Cancer Res. 2007, 67:6092-6099.
139. Coulouarn C., Factor V.M., Andersen J.B., Durkin M.E., Thorgeirsson S.S. Loss of miR-122 expression in liver cancer correlates with suppression of the hepatic phenotype and gain of metastatic properties. Oncogene 2009, 28:3526-3536.
140. Lin C.J., Gong H.Y., Tseng H.C., Wang W.L., Wu J.L. MiR-122 targets an anti-apoptotic gene, Bcl-w, in human hepatocellular carcinoma cell lines. Biochem. Biophys. Res. Commun. 2008, 375:315-320.
141. Ma L., Liu J., Shen J., Liu L., Wu J., Li W., Luo J., Chen Q., Qian C. Expression of miR-122 mediated by adenoviral vector induces apoptosis and cell cycle arrest of cancer cells. Cancer Biol. Ther. 2010, 9:554-561.
142. Tsai W.C., Hsu P.W., Lai T.C., Chau G.Y., Lin C.W., Chen C.M., Lin C.D., Liao Y.L., Wang J.L., Chau Y.P., Hsu M.T., Hsiao M., Huang H.D., Tsou A.P. MicroRNA-122, a tumor suppressor microRNA that regulates intrahepatic metastasis of hepatocellular carcinoma. Hepatology 2009, 49:1571-1582.
143. Xu T., Zhu Y., Xiong Y., Ge Y.Y., Yun J.P., Zhuang S.M. MicroRNA-195 suppresses tumorigenicity and regulates G1/S transition of human hepatocellular carcinoma cells. Hepatology 2009, 50:113-121.
144. Henry J.C., Park J.K., Jiang J., Kim J.H., Nagorney D.M., Roberts L.R., Banerjee S., Schmittgen T.D. MiR-199a-3p targets CD44 and reduces proliferation of CD44 positive hepatocellular carcinoma cell lines. Biochem. Biophys. Res. Commun. 2010, 403:120-125.
145. Liu W.H., Yeh S.H., Lu C.C., Yu S.L., Chen H.Y., Lin C.Y., Chen D.S., Chen P.J. MicroRNA-18a prevents estrogen receptor-alpha expression, promoting proliferation of hepatocellular carcinoma cells. Gastroenterology 2009, 136:683-693.
146. Meng F., Henson R., Wehbe-Janek H., Ghoshal K., Jacob S.T., Patel T. MicroRNA-21 regulates expression of the PTEN tumor suppressor gene in human hepatocellular cancer. Gastroenterology 2007, 133:647-658.
147. Li Y., Tan W., Neo T.W., Aung M.O., Wasser S., Lim S.G., Tan T.M. Role of the miR-106b-25 microRNA cluster in hepatocellular carcinoma. Cancer Sci. 2009, 100:1234-1242.
148. Ding J., Huang S., Wu S., Zhao Y., Liang L., Yan M., Ge C., Yao J., Chen T., Wan D., Wang H., Gu J., Yao M., Li J., Tu H., He X. Gain of miR-151 on chromosome 8q24.3 facilitates tumour cell migration and spreading through downregulating RhoGDIA. Nat. Cell Biol. 2010, 12:390-399.
149. Garofalo M., Di Leva G., Romano G., Nuovo G., Suh S.S., Ngankeu A., Taccioli C., Pichiorri F., Alder H., Secchiero P., Gasparini P., Gonelli A., Costinean S., Acunzo M., Condorelli G., Croce C.M. MiR-221&222 regulate TRAIL resistance and enhance tumorigenicity through PTEN and TIMP3 downregulation. Cancer Cell 2009, 16:498-509.
150. Wang Y., Lee A.T., Ma J.Z., Wang J., Ren J., Yang Y., Tantoso E., Li K.B., Ooi L.L., Tan P., Lee C.G. Profiling microRNA expression in hepatocellular carcinoma reveals microRNA-224 up-regulation and apoptosis inhibitor-5 as a microRNA-224-specific target. J. Biol. Chem. 2008, 283:13205-13215.
151. Yamamoto Y., Kosaka N., Tanaka M., Koizumi F., Kanai Y., Mizutani T., Murakami Y., Kuroda M., Miyajima A., Kato T., Ochiya T. MicroRNA-500 as a potential diagnostic marker for hepatocellular carcinoma. Biomarkers 2009, 14:529-538.
152. Ariel I., Miao H.Q., Ji X.R., Schneider T., Roll D., de Groot N., Hochberg A., Ayesh S. Imprinted H19 oncofetal RNA is a candidate tumour marker for hepatocellular carcinoma. Mol. Pathol. 1998, 51:21-25.
153. Yamamoto Y., Nishikawa Y., Tokairin T., Omori Y., Enomoto K. Increased expression of H19 non-coding mRNA follows hepatocyte proliferation in the rat and mouse. J. Hepatol. 2004, 40:808-814.
154. Gui J., Tian Y., Wen X., Zhang W., Zhang P., Gao J., Run W., Tian L., Jia X., Gao Y. Serum microRNA characterization identifies miR-885-5p as a potential marker for detecting liver pathologies. Clin. Sci. (Lond.) 2011, 120:183-193.