MicroRNA responses to environmental liver carcinogens: Biological and clinical significance

Clinica Chimica Acta

Volumn 445, Issue , 2015, Pages 25-33

  Nicolaidou, Vicky ^a,c   Koufaris, Costas ^b  

^a UNIVERSITY OF NICOSIA   (Cyprus)

^b CYPRUS INSTITUTE OF NEUROLOGY AND GENETICS   (Cyprus)

^c The Center for the Study of Haematological Malignancies   (Cyprus)

Author keywords

Aflatoxin; Alcohol; Carcinogen; Circulating; Hepatitis; Obesity

Indexed keywords

AFLATOXIN; BIOLOGICAL MARKER; CARCINOGEN; DIETHYLNITROSAMINE; ETHYLNITROSOUREA; MICRORNA; MICRORNA 122; MICRORNA 20A; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA AGONIST; PHENOBARBITAL; DNA METHYLTRANSFERASE; POLYCYCLIC AROMATIC HYDROCARBON;

ALCOHOL LIVER DISEASE; ALCOHOLISM; BIOGENESIS; ENVIRONMENTAL EXPOSURE; GENE EXPRESSION; HEPATITIS; HEPATITIS B; HEPATITIS C; HUMAN; LIVER CANCER; LIVER CARCINOGENESIS; NONALCOHOLIC FATTY LIVER; NONHUMAN; PRIORITY JOURNAL; REVIEW; RISK FACTOR; RNA SYNTHESIS; VIRUS HEPATITIS; ANIMAL; CHEMICALLY INDUCED; DRUG EFFECTS; FATTY LIVER; GENE EXPRESSION REGULATION; GENETICS; GENOTYPE ENVIRONMENT INTERACTION; HEPATITIS, VIRAL, HUMAN; LIVER; LIVER DISEASES, ALCOHOLIC; LIVER NEOPLASMS; METABOLISM; PATHOLOGY; RODENT;

AFLATOXINS; ANIMALS; CARCINOGENS, ENVIRONMENTAL; DNA MODIFICATION METHYLASES; FATTY LIVER; GENE EXPRESSION REGULATION; GENE-ENVIRONMENT INTERACTION; HEPATITIS, VIRAL, HUMAN; HUMANS; LIVER; LIVER DISEASES, ALCOHOLIC; LIVER NEOPLASMS; MICRORNAS; POLYCYCLIC HYDROCARBONS, AROMATIC; RISK FACTORS; RODENTIA;

EID: 84925134508     PISSN: 00098981     EISSN: 18733492     Source Type: Journal    
DOI: 10.1016/j.cca.2015.03.006     Document Type: Review

References (99)

1. Kamangar F., Dores G.M., Anderson W.F. Patterns of cancer incidence, mortality, and prevalence across five continents: defining priorities to reduce cancer disparities in different geographic regions of the world. J Clin Oncol Off J Am Soc Clin Oncol 2006, 24:2137-2150. 10.1200/JCO.2005.05.2308.
2. Farazi P.A., DePinho R.A. Hepatocellular carcinoma pathogenesis: from genes to environment. Nat Rev Cancer 2006, 6:674-687. 10.1038/nrc1934.
3. Hardisty J.F., Brix A.E. Comparative hepatic toxicity: prechronic/chronic liver toxicity in rodents. Toxicol Pathol 2005, 33:35-40. 10.1080/01926230590522077.
4. Fabbrini E., Sullivan S., Klein S. Obesity and nonalcoholic fatty liver disease: biochemical, metabolic, and clinical implications. Hepatology 2010, 51:679-689. 10.1002/hep.23280.
5. Hernández L.G., van Steeg H., Luijten M., van Benthem J. Mechanisms of non-genotoxic carcinogens and importance of a weight of evidence approach. Mutat Res 2009, 682:94-109. 10.1016/j.mrrev.2009.07.002.
6. Irigaray P., Belpomme D. Basic properties and molecular mechanisms of exogenous chemical carcinogens. Carcinogenesis 2010, 31:135-148. 10.1093/carcin/bgp252.
7. Uehara T., Hirode M., Ono A., et al. A toxicogenomics approach for early assessment of potential non-genotoxic hepatocarcinogenicity of chemicals in rats. Toxicology 2008, 250:15-26. 10.1016/j.tox.2008.05.013.
8. Neuveut C., Wei Y., Buendia M.A. Mechanisms of HBV-related hepatocarcinogenesis. J Hepatol 2010, 52:594-604. 10.1016/j.jhep.2009.10.033.
9. Lee S.J., Yum Y.N., Kim S.C., et al. Distinguishing between genotoxic and non-genotoxic hepatocarcinogens by gene expression profiling and bioinformatic pathway analysis. Sci Rep 2013, 3:2783. 10.1038/srep02783.
10. Altekruse S.F., McGlynn K.A., Reichman M.E. Hepatocellular carcinoma incidence, mortality, and survival trends in the United States from 1975 to 2005. J Clin Oncol Off J Am Soc Clin Oncol 2009, 27:1485-1491. 10.1200/JCO.2008.20.7753.
11. Friedländer M.R., Lizano E., Houben A.J.S., et al. Evidence for the biogenesis of more than 1,000 novel human microRNAs. Genome Biol 2014, 15:R57. 10.1186/gb-2014-15-4-r57.
12. Berezikov E., Chung W.-J., Willis J., Cuppen E., Lai E.C. Mammalian mirtron genes. Mol Cell 2007, 28:328-336. 10.1016/j.molcel.2007.09.028.
13. Lim L.P., Lau N.C., Garrett-Engele P., et al. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 2005, 433:769-773. 10.1038/nature03315.
14. Baek D., Villén J., Shin C., Camargo F.D., Gygi S.P., Bartel D.P. The impact of microRNAs on protein output. Nature 2008, 455:64-71. 10.1038/nature07242.
15. Selbach M., Schwanhäusser B., Thierfelder N., Fang Z., Khanin R., Rajewsky N. Widespread changes in protein synthesis induced by microRNAs. Nature 2008, 455:58-63. 10.1038/nature07228.
16. Bartel D.P. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233. 10.1016/j.cell.2009.01.002.
17. Jackson R.J., Hellen C.U.T., Pestova T.V. The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev Mol Cell Biol 2010, 11:113-127. 10.1038/nrm2838.
18. Pineau P., Volinia S., McJunkin K., et al. miR-221 overexpression contributes to liver tumorigenesis. Proc Natl Acad Sci U S A 2010, 107:264-269. 10.1073/pnas.0907904107.
19. Gramantieri L., Ferracin M., Fornari F., et al. Cyclin G1 is a target of miR-122a, a microRNA frequently down-regulated in human hepatocellular carcinoma. Cancer Res 2007, 67:6092-6099. 10.1158/0008-5472.CAN-06-4607.
20. Ladeiro Y., Couchy G., Balabaud C., et al. MicroRNA profiling in hepatocellular tumors is associated with clinical features and oncogene/tumor suppressor gene mutations. Hepatology 2008, 47:1955-1963. 10.1002/hep.22256.
21. Hou J., Lin L., Zhou W., et al. 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. 10.1016/j.ccr.2011.01.001.
22. Sekine S., Ogawa R., Ito R., et al. Disruption of Dicer1 induces dysregulated fetal gene expression and promotes hepatocarcinogenesis. Gastroenterology 2009, 136. [2304-15.e1-4]. 10.1053/j.gastro.2009.02.067.
23. Hsu S.H., Wang B., Kota J., et al. Essential metabolic, anti-inflammatory, and anti-tumorigenic functions of miR-122 in liver. J Clin Invest 2012, 122(8):2871-2883. 10.1172/JCI63539.
24. Callegari E., Elamin B.K., Giannone F., et al. Liver tumorigenicity promoted by microRNA-221 in a mouse transgenic model. Hepatology 2012, 56(3):1025-1033. 10.1002/hep.25747.
25. 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. 10.1053/j.gastro.2007.05.022.
26. Fornari F., Gramantieri L., Ferracin M., et al. MiR-221 controls CDKN1C/p57 and CDKN1B/p27 expression in human hepatocellular carcinoma. Oncogene 2008, 27:5651-5661. 10.1038/onc.2008.178.
27. Kutay H., Bai S., Datta J., et al. Downregulation of miR-122 in the rodent and human hepatocellular carcinomas. J Cell Biochem 2006, 99:671-678. 10.1002/jcb.20982.
28. Bala S., Marcos M., Szabo G. Emerging role of microRNAs in liver diseases. World J Gastroenterol 2009, 15:5633-5640.
29. Li R., Qian N., Tao K., You N., Wang X., Dou K. MicroRNAs involved in neoplastic transformation of liver cancer stem cells. J Exp Clin Cancer Res 23 2010, 29:169. 10.1186/1756-9966-29-169.
30. Ma S., Tang K.H., Chan Y.P., et al. miR-130b Promotes CD133(+) liver tumor-initiating cell growth and self-renewal via tumor protein 53-induced nuclear protein 1. Cell Stem Cell 3 2010, 7(6):694-707. 10.1016/j.stem.2010.11.010.
31. Tsuno S., Wang X., Shomori K., Hasegawa J., Miura N. Hsa-miR-520d induces hepatoma cells to form normal liver tissues via a stemness-mediated process. Sci Rep 24 2014, 4:3852. 10.1038/srep03852.
32. Parkin D.M. The global health burden of infection-associated cancers in the year 2002. Int J Cancer 2006, 118:3030-3044. 10.1002/ijc.21731.
33. Wang Y., Lu Y., Toh S.T., et al. 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. 10.1016/j.jhep.2009.12.043.
34. Wei X., Xiang T., Ren G., et al. miR-101 is down-regulated by the hepatitis B virus x protein and induces aberrant DNA methylation by targeting DNA methyltransferase 3A. Cell Signal 2013, 25:439-446. 10.1016/j.cellsig.2012.10.013.
35. Xu L., Beckebaum S., Iacob S., et al. MicroRNA-101 inhibits human hepatocellular carcinoma progression through EZH2 downregulation and increased cytostatic drug sensitivity. J Hepatol 2014, 60:590-598. 10.1016/j.jhep.2013.10.028.
36. 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. 10.1002/hep.23660.
37. Connolly E., Melegari M., Landgraf P., et al. 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. 10.2353/ajpath.2008.080096.
38. Liu Y., Zhao J.-J., Wang C., et al. Altered expression profiles of microRNAs in a stable hepatitis B virus-expressing cell line. Chin Med J (Engl) 2009, 122:10-14.
39. Zhang Y., Wei W., Cheng N., et al. Hepatitis C virus-induced up-regulation of microRNA-155 promotes hepatocarcinogenesis by activating Wnt signaling. Hepatology 2012, 56:1631-1640. 10.1002/hep.25849.
40. Bala S., Tilahun Y., Taha O., et al. Increased microRNA-155 expression in the serum and peripheral monocytes in chronic HCV infection. J Transl Med 2012, 10:151. 10.1186/1479-5876-10-151.
41. Wang B., Majumder S., Nuovo G., et al. Role of microRNA-155 at early stages of hepatocarcinogenesis induced by choline-deficient and amino acid-defined diet in C57BL/6 mice. Hepatology 2009, 50:1152-1161. 10.1002/hep.23100.
42. Jopling C.L., Schütz 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. 10.1016/j.chom.2008.05.013.
43. Qiu L., Fan H., Jin W., et al. miR-122-induced down-regulation of HO-1 negatively affects miR-122-mediated suppression of HBV. Biochem Biophys Res Commun 2010, 398:771-777. 10.1016/j.bbrc.2010.07.021.
44. Shimakami T., Yamane D., Jangra R.K., et al. Stabilization of hepatitis C virus RNA by an Ago2-miR-122 complex. Proc Natl Acad Sci U S A 2012, 109:941-946. 10.1073/pnas.1112263109.
45. Conrad K.D., Giering F., Erfurth C., et al. MicroRNA-122 dependent binding of Ago2 protein to hepatitis C virus RNA is associated with enhanced RNA stability and translation stimulation. PLoS One 2013, 8:e56272. 10.1371/journal.pone.0056272.
46. Wang S., Qiu L., Yan X., et al. Loss of microRNA 122 expression in patients with hepatitis B enhances hepatitis B virus replication through cyclin G(1) -modulated P53 activity. Hepatology 2012, 55:730-741. 10.1002/hep.24809.
47. Bai S., Nasser M.W., Wang B., et al. MicroRNA-122 inhibits tumorigenic properties of hepatocellular carcinoma cells and sensitizes these cells to sorafenib. J Biol Chem 2009, 284:32015-32027. 10.1074/jbc.M109.016774.
48. 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. 10.1038/onc.2009.211.
49. Tsai W.-C., Hsu P.W.-C., Lai T.-C., et al. MicroRNA-122, a tumor suppressor microRNA that regulates intrahepatic metastasis of hepatocellular carcinoma. Hepatology 2009, 49:1571-1582. 10.1002/hep.22806.
50. Hsu S.-H., Wang B., Kota J., et al. Essential metabolic, anti-inflammatory, and anti-tumorigenic functions of miR-122 in liver. J Clin Invest 2012, 122:2871-2883. 10.1172/JCI63539.
51. Rottiers V., Näär A.M. MicroRNAs in metabolism and metabolic disorders. Nat Rev Mol Cell Biol 2012, 13:239-250. 10.1038/nrm3313.
52. Gori M., Arciello M., Balsano C. MicroRNAs in nonalcoholic fatty liver disease: novel biomarkers and prognostic tools during the transition from steatosis to hepatocarcinoma. Biomed Res Int 2014, 2014:741465. 10.1155/2014/741465.
53. Cheung O., Puri P., Eicken C., et al. Nonalcoholic steatohepatitis is associated with altered hepatic MicroRNA expression. Hepatology 2008, 48:1810-1820. 10.1002/hep.22569.
54. Lee J., Padhye A., Sharma A., et al. A pathway involving farnesoid X receptor and small heterodimer partner positively regulates hepatic sirtuin 1 levels via microRNA-34a inhibition. J Biol Chem 2010, 285:12604-12611. 10.1074/jbc.M109.094524.
55. Castro R.E., Ferreira D.M.S., Afonso M.B., et al. miR-34a/SIRT1/p53 is suppressed by ursodeoxycholic acid in the rat liver and activated by disease severity in human non-alcoholic fatty liver disease. J Hepatol 2013, 58:119-125. 10.1016/j.jhep.2012.08.008.
56. Alisi A., Da Sacco L., Bruscalupi G., et al. Mirnome analysis reveals novel molecular determinants in the pathogenesis of diet-induced nonalcoholic fatty liver disease. Lab Invest J Tech Methods Pathol 2011, 91:283-293. 10.1038/labinvest.2010.166.
57. Pogribny I.P., Starlard-Davenport A., Tryndyak V.P., et al. Difference in expression of hepatic microRNAs miR-29c, miR-34a, miR-155, and miR-200b is associated with strain-specific susceptibility to dietary nonalcoholic steatohepatitis in mice. Lab Investig J Tech Methods Pathol 2010, 90:1437-1446. 10.1038/labinvest.2010.113.
58. Sharma H., Estep M., Birerdinc A., et al. Expression of genes for microRNA-processing enzymes is altered in advanced non-alcoholic fatty liver disease. J Gastroenterol Hepatol 2013, 28:1410-1415. 10.1111/jgh.12268.
59. Schütze M., Boeing H., Pischon T., et al. Alcohol attributable burden of incidence of cancer in eight European countries based on results from prospective cohort study. BMJ 2011, 342:d1584.
60. Dippold R.P., Vadigepalli R., Gonye G.E., Patra B., Hoek J.B. Chronic ethanol feeding alters miRNA expression dynamics during liver regeneration. Alcohol Clin Exp Res 2013, 37(Suppl. 1):E59-E69. 10.1111/j.1530-0277.2012.01852.x.
61. Francis H., McDaniel K., Han Y., et al. Regulation of the extrinsic apoptotic pathway by microRNA-21 in alcoholic liver injury. J Biol Chem 2014, 289:27526-27539. 10.1074/jbc.M114.602383.
62. Meng F., Glaser S.S., Francis H., et al. Epigenetic regulation of miR-34a expression in alcoholic liver injury. Am J Pathol 2012, 181:804-817. 10.1016/j.ajpath.2012.06.010.
63. Tang Y., Banan A., Forsyth C.B., et al. Effect of alcohol on miR-212 expression in intestinal epithelial cells and its potential role in alcoholic liver disease. Alcohol Clin Exp Res 2008, 32:355-364. 10.1111/j.1530-0277.2007.00584.x.
64. Yeligar S., Tsukamoto H., Kalra V.K. Ethanol-induced expression of ET-1 and ET-BR in liver sinusoidal endothelial cells and human endothelial cells involves hypoxia-inducible factor-1alpha and microrNA-199. J Immunol 2009, 183:5232-5243. 10.4049/jimmunol.0901084.
65. Liu Y., Wu F. Global burden of aflatoxin-induced hepatocellular carcinoma: a risk assessment. Environ Health Perspect 2010, 118:818-824. 10.1289/ehp.0901388.
66. Kew M.C. Aflatoxins as a cause of hepatocellular carcinoma. J Gastrointestin Liver Dis 2013, 22:305-310.
67. Zeng C., Wang R., Li D., et al. A novel GSK-3 beta-C/EBP alpha-miR-122-insulin-like growth factor 1 receptor regulatory circuitry in human hepatocellular carcinoma. Hepatology 2010, 52:1702-1712. 10.1002/hep.23875.
68. Fang Y., Feng Y., Wu T., et al. Aflatoxin B1 negatively regulates Wnt/β-catenin signaling pathway through activating miR-33a. PLoS One 2013, 8:e73004. 10.1371/journal.pone.0073004.
69. 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. 10.1002/hep.23660.
70. Liu Y.-X., Long X.-D., Xi Z.-F., et al. MicroRNA-24 modulates aflatoxin B1-related hepatocellular carcinoma prognosis and tumorigenesis. Biomed Res Int 2014, 2014:482926. 10.1155/2014/482926.
71. Pogribny I.P. MicroRNA dysregulation during chemical carcinogenesis. Epigenomics 2009, 1:281-290. 10.2217/epi.09.17.
72. Gooderham N.J., Koufaris C. Using microRNA profiles to predict and evaluate hepatic carcinogenic potential. Toxicol Lett 2014, 228:127-132. 10.1016/j.toxlet.2014.04.015.
73. Marrone A.K., Beland F.A., Pogribny I.P. Noncoding RNA response to xenobiotic exposure: an indicator of toxicity and carcinogenicity. Expert Opin Drug Metab Toxicol 2014, 10:1409-1422. 10.1517/17425255.2014.954312.
74. Moffat I.D., Boutros P.C., Celius T., Lindén J., Pohjanvirta R., Okey A.B. microRNAs in adult rodent liver are refractory to dioxin treatment. Toxicol Sci Off J Soc Toxicol 2007, 99:470-487. 10.1093/toxsci/kfm189.
75. Li Z., Branham W.S., Dial S.L., et al. Genomic analysis of microRNA time-course expression in liver of mice treated with genotoxic carcinogen N-ethyl-N-nitrosourea. BMC Genomics 2010, 11:609. 10.1186/1471-2164-11-609.
76. Yauk C.L., Jackson K., Malowany M., Williams A. Lack of change in microRNA expression in adult mouse liver following treatment with benzo(a)pyrene despite robust mRNA transcriptional response. Mutat Res 2011, 722:131-139. 10.1016/j.mrgentox.2010.02.012.
77. Koufaris C., Wright J., Osborne M., Currie R.A., Gooderham N.J. Time and dose-dependent effects of phenobarbital on the rat liver miRNAome. Toxicology 2013, 314:247-253. 10.1016/j.tox.2013.10.004.
78. Pogribny I.P., Muskhelishvili L., Tryndyak V.P., Beland F.A. The tumor-promoting activity of 2-acetylaminofluorene is associated with disruption of the p53 signaling pathway and the balance between apoptosis and cell proliferation. Toxicol Appl Pharmacol 2009, 235:305-311. 10.1016/j.taap.2008.12.021.
79. Chen T., Mally A., Ozden S., Chipman J.K. Low doses of the carcinogen furan alter cell cycle and apoptosis gene expression in rat liver independent of DNA methylation. Environ Health Perspect 2010, 118:1597-1602. 10.1289/ehp.1002153.
80. Koufaris C., Wright J., Currie R.A., Gooderham N.J. Hepatic microRNA profiles offer predictive and mechanistic insights after exposure to genotoxic and epigenetic hepatocarcinogens. Toxicol Sci Off J Soc Toxicol 2012, 128:532-543. 10.1093/toxsci/kfs170.
81. Malik A.I., Williams A., Lemieux C.L., White P.A., Yauk C.L. Hepatic mRNA, microRNA, and miR-34a-target responses in mice after 28days exposure to doses of benzo(a)pyrene that elicit DNA damage and mutation. Environ Mol Mutagen 2012, 53:10-21. 10.1002/em.20668.
82. Hermeking H. MiR-34a and p53. Cell Cycle Georget Tex 2009, 8:1308.
83. Korpal M., Kang Y. The emerging role of miR-200 family of microRNAs in epithelial-mesenchymal transition and cancer metastasis. RNA Biol 2008, 5:115-119.
84. Luan Y., Qi X., Xu L., Ren J., Chen T. Absence of mature microRNAs inactivates the response of gene expression to carcinogenesis induced by N-ethyl-N-nitrosourea in mouse liver. J Appl Toxicol 2014, 34:1409-1417. 10.1002/jat.2973.
85. Koufaris C., Gooderham N.J. Are differences in microRNA regulation implicated in species-dependent response to toxicological exposures?. Toxicol Sci Off J Soc Toxicol 2013, 131:337-342. 10.1093/toxsci/kfs302.
86. Shah Y.M., Morimura K., Yang Q., Tanabe T., Takagi M., Gonzalez F.J. Peroxisome proliferator-activated receptor alpha regulates a microRNA-mediated signaling cascade responsible for hepatocellular proliferation. Mol Cell Biol 2007, 27:4238-4247. 10.1128/MCB. 00317-07.
87. Weiland M., Gao X.-H., Zhou L., Mi Q.-S. Small RNAs have a large impact: circulating microRNAs as biomarkers for human diseases. RNA Biol 2012, 9:850-859. 10.4161/rna.20378.
88. Zhang Y., Jia Y., Zheng R., et al. Plasma microRNA-122 as a biomarker for viral-, alcohol-, and chemical-related hepatic diseases. Clin Chem 2010, 56:1830-1838. 10.1373/clinchem.2010.147850.
89. Bala S., Petrasek J., Mundkur S., et al. Circulating microRNAs in exosomes indicate hepatocyte injury and inflammation in alcoholic, drug-induced, and inflammatory liver diseases. Hepatology 2012, 56:1946-1957. 10.1002/hep.25873.
90. 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. 10.1371/journal.pone.0023937.
91. Shrivastava S., Petrone J., Steele R., Lauer G.M., Di Bisceglie A.M., Ray R.B. Up-regulation of circulating miR-20a is correlated with hepatitis C virus-mediated liver disease progression. Hepatology 2013, 58:863-871. 10.1002/hep.26296.
92. Sukata T., Sumida K., Kushida M., et al. Circulating microRNAs, possible indicators of progress of rat hepatocarcinogenesis from early stages. Toxicol Lett 2011, 200:46-52. 10.1016/j.toxlet.2010.10.013.
93. Leung A.K.L., Sharp P.A. MicroRNA functions in stress responses. Mol Cell 2010, 40:205-215. 10.1016/j.molcel.2010.09.027.
94. Mendell J.T., Olson E.N. MicroRNAs in stress signaling and human disease. Cell 2012, 148:1172-1187. 10.1016/j.cell.2012.02.005.
95. Drakaki A., Hatziapostolou M., Iliopoulos D. Therapeutically targeting microRNAs in liver cancer. Curr Pharm Des 2013, 19:1180-1191.
96. Kota J., Chivukula R.R., O'Donnell K.A., et al. Therapeutic microRNA delivery suppresses tumorigenesis in a murine liver cancer model. Cell 2009, 137:1005-1017. 10.1016/j.cell.2009.04.021.
97. Janssen H.L.A., Reesink H.W., Lawitz E.J., et al. Treatment of HCV infection by targeting microRNA. N Engl J Med 2013, 368:1685-1694. 10.1056/NEJMoa1209026.
98. Qi P., Cheng S., Wang H., Li N., Chen Y., Gao C. Serum microRNAs as biomarkers for hepatocellular carcinoma in Chinese patients with chronic hepatitis B virus infection. PLoS One 2011, 6:e28486. 10.1371/journal.pone.0028486.
99. Yamada H., Suzuki K., Ichino N., et al. Associations between circulating microRNAs (miR-21, miR-34a, miR-122 and miR-451) and non-alcoholic fatty liver. Clin Chim Acta 2013, 424:99-103. 10.1016/j.cca.2013.05.021.