MicroRNAs in hepatic pathophysiology

Hepatology Research

Volumn 47, Issue 1, 2017, Pages 60-69

  Murakami, Yoshiki ^a   Kawada, Norifumi ^a  

^a OSAKA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

biomarker; HBV; HCC; HCV; liver fibrosis; miRNA

Indexed keywords

ANTIVIRUS AGENT; ARC 520; MICRORNA; MICRORNA 122A; MICRORNA 125B; MICRORNA 130A; MICRORNA 139; MICRORNA 143; MICRORNA 145; MICRORNA 17 3P; MICRORNA 187; MICRORNA 18A; MICRORNA 199; MICRORNA 199A; MICRORNA 200A; MICRORNA 200B; MICRORNA 223; MICRORNA 27B; MICRORNA 30E; MICRORNA 326; MICRORNA 34B; MICRORNA 378; MICRORNA 422B; MICRORNA 652; MICRORNA 92; MICRORNA 99A; MIRAVIRSEN; NONSTRUCTURAL PROTEIN 5B; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; AUTOIMMUNE HEPATITIS; CELL DEATH; CHRONIC HEPATITIS B; CHRONIC LIVER DISEASE; CONTROLLED STUDY; FATTY ACID METABOLISM; GENE EXPRESSION REGULATION; GENE SILENCING; HEPATITIS B; HEPATITIS B VIRUS; HEPATITIS C VIRUS; HUMAN; HUMAN TISSUE; LIVER BIOPSY; LIVER CELL CARCINOMA; LIVER DISEASE; LIVER FIBROSIS; NONALCOHOLIC FATTY LIVER; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; RNA INTERFERENCE; UPREGULATION; VIRUS HEPATITIS; VIRUS REPLICATION;

EID: 84971613074     PISSN: 13866346     EISSN: 1872034X     Source Type: Journal    
DOI: 10.1111/hepr.12730     Document Type: Review

References (89)

1. Friedman RC, Farh KK, Burge CB, Bartel DP. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 2009; 19: 92–105.
2. Ambros V. The functions of animal microRNAs. Nature 2004; 431: 350–5.
3. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004; 116: 281–97.
4. Landgraf P, Rusu M, Sheridan R et al. A mammalian microRNA expression atlas based on small RNA library sequencing. Cell 2007; 129: 1401–14.
5. Deng XG, Qiu RL, Wu YH et al. Overexpression of miR-122 promotes the hepatic differentiation and maturation of mouse ESCs through a miR-122/FoxA1/HNF4a-positive feedback loop. Liver int 2014; 34: 281–95.
6. Laudadio I, Manfroid I, Achouri Y et al. A feedback loop between the liver-enriched transcription factor network and miR-122 controls hepatocyte differentiation. Gastroenterology 2012; 142: 119–29.
7. Hsu SH, Wang B, Kota J et al. Essential metabolic, anti-inflammatory, and anti-tumorigenic functions of miR-122 in liver. J Clin Invest 2012; 122: 2871–83.
8. Tsai WC, Hsu SD, Hsu CS et al. MicroRNA-122 plays a critical role in liver homeostasis and hepatocarcinogenesis. J Clin Invest. 2012; 122: 2884–97.
9. Gatfield D, Le Martelot G, Vejnar CE et al. Integration of microRNA miR-122 in hepatic circadian gene expression. Genes Dev. 2009; 23: 1313–26.
10. Lanford RE, Hildebrandt-Eriksen ES, Petri A et al. Therapeutic silencing of microRNA-122 in primates with chronic hepatitis C virus infection. Science 2010; 327: 198–201.
11. Cheung O, Puri P, Eicken C et al. Nonalcoholic steatohepatitis is associated with altered hepatic MicroRNA expression. Hepatology 2008; 48: 1810–20.
12. 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: 730–41.
13. Sun X, Feinberg MW. MicroRNA-management of lipoprotein homeostasis. Circ Res 2014; 115: 2–6.
14. Ji J, Zhang J, Huang G, Qian J, Wang X, Mei S. Over-expressed microRNA-27a and 27b influence fat accumulation and cell proliferation during rat hepatic stellate cell activation. FEBS Lett 2009; 583: 759–66.
15. Carrer M, Liu N, Grueter CE et al. Control of mitochondrial metabolism and systemic energy homeostasis by microRNAs 378 and 378*. Proc Natl Acad Sci USA. 2012; 109: 15330–5.
16. 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: 12604–11.
17. Ahn J, Lee H, Jung CH, Ha T. Lycopene inhibits hepatic steatosis via microRNA-21-induced downregulation of fatty acid-binding protein 7 in mice fed a high-fat diet. Mol Nutr Food Res. 2012; 56: 1665–74.
18. Bhattacharyya SN, Habermacher R, Martine U, Closs EI, Filipowicz W. Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell. 2006; 125: 1111–24.
19. Patella F, Rainaldi G. MicroRNAs mediate metabolic stresses and angiogenesis. Cell Mol Life Sci. 2012; 69: 1049–65.
20. Jopling CL, Yi M, Lancaster AM, Lemon SM, Sarnow P. Modulation of hepatitis C virus RNA abundance by a liver-specific microRNA. Science. 2005; 309: 1577–81.
21. Henke JI, Goergen D, Zheng J et al. MicroRNA-122 stimulates translation of hepatitis C virus RNA. EMBO J. 2008; 27: 3300–10.
22. Norman KL, Sarnow P. Modulation of hepatitis C virus RNA abundance and the isoprenoid biosynthesis pathway by microRNA miR-122 involves distinct mechanisms. J Virol. 2010; 84: 666–70.
23. Nasheri N, Singaravelu R, Goodmurphy M, Lyn RK, Pezacki JP. Competing roles of microRNA-122 recognition elements in hepatitis C virus RNA. Virology. 2011; 410: 336–44.
24. Machlin ES, Sarnow P, Sagan SM. 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: 3193–8.
25. Murakami Y, Aly HH, Tajima A, Inoue I, Shimotohno K. Regulation of the hepatitis C virus genome replication by miR-199a. J Hepatol. 2009; 50: 453–60.
26. Pedersen IM, Cheng G, Wieland S et al. Interferon modulation of cellular microRNAs as an antiviral mechanism. Nature. 2007; 449: 919–22.
27. Cheng JC, Yeh YJ, Tseng CP et al. Let-7b is a novel regulator of hepatitis C virus replication. Cell Mol Life Sci. 2012; 69: 2621–33.
28. Bhanja Chowdhury J, Shrivastava S, Steele R, Di Bisceglie AM, Ray R, Ray RB. Hepatitis C virus infection modulates expression of interferon stimulatory gene IFITM1 by upregulating miR-130 A. J Virol. 2012; 86: 10221–5.
29. Murakami Y, Tanaka M, Toyoda H et al. Hepatic microRNA expression is associated with the response to interferon treatment of chronic hepatitis C. BMC Med Genomics. 2010; 3: 48.
30. Ura S, Honda M, Yamashita T et al. Differential microRNA expression between hepatitis B and hepatitis C leading disease progression to hepatocellular carcinoma. Hepatology. 2009; 49: 1098–112.
31. Janssen HL, Reesink HW, Lawitz EJ et al. Treatment of HCV infection by targeting microRNA. N Engl J Med. 2013; 368: 1685–94.
32. Lu JW, Liao CY, Yang WY et al. Overexpression of endothelin 1 triggers hepatocarcinogenesis in zebrafish and promotes cell proliferation and migration through the AKT pathway. PloS One. 2014; 9: e85318.
33. Wu G, Huang P, Ju X, Li Z, Wang Y. Lin28B over-expression mediates the repression of let-7 by hepatitis B virus X protein in hepatoma cells. Int J Clin Exp Med 2015; 8: 15108–16.
34. Wang Y, Lu Y, Toh ST 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.
35. Hu XM, Yan XH, Hu YW et al. MicroRNA-548p suppresses hepatitis B virus X protein associated hepatocellular carcinoma by downregulating oncoprotein HBXIP. Hepatol Res 2015. doi: 10.1111/hepr.12618.
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.
37. Dai X, Zhang W, Zhang H et al. Modulation of HBV replication by microRNA-15b through targeting hepatocyte nuclear factor 1α. Nucleic Acids Res. 2014; 42: 6578–90.
38. Liu WH, Yeh SH, Lu CC et al. MicroRNA-18a prevents estrogen receptor-α expression, promoting proliferation of hepatocellular carcinoma cells. Gastroenterology. 2009; 136: 683–93.
39. Fan CG, Wang CM, Tian C et al. miR-122 inhibits viral replication and cell proliferation in hepatitis B virus-related hepatocellular carcinoma and targets NDRG3. Oncol Rep. 2011; 26: 1281–6.
40. Li C, Wang Y, Wang S et al. Hepatitis B virus mRNA-mediated miR-122 inhibition upregulates PTTG1-binding protein, which promotes hepatocellular carcinoma tumor growth and cell invasion. J Virol. 2013; 87: 2193–205.
41. Hu W, Wang X, Ding X et al. MicroRNA-141 represses HBV replication by targeting PPARA. PloS One. 2012; 7: e34165.
42. Guo H, Liu H, Mitchelson K et al. MicroRNAs-372/373 promote the expression of hepatitis B virus through the targeting of nuclear factor I/B. Hepatology. 2011; 54: 808–19.
43. Wang Y, Jiang L, Ji X, Yang B, Zhang Y, Fu XD. Hepatitis B viral RNA directly mediates down-regulation of the tumor suppressor microRNA miR-15a/miR-16-1 in hepatocytes. J Biol Chem. 2013; 288: 18484–93.
44. Chen Y, Shen A, Rider PJ et al. 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: 4511–21.
45. 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: 5157–63.
46. 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: 169–75.
47. Kohno T, Tsuge M, Murakami E et al. Human microRNA hsa-miR-1231 suppresses hepatitis B virus replication by targeting core mRNA. J Viral Hepat. 2014; 21: e89–97.
48. Gish RG, Yuen MF, Chan HL et al. Synthetic RNAi triggers and their use in chronic hepatitis B therapies with curative intent. Antiviral Res. 2015; 121: 97–108.
49. Friedman SL. Hepatic stellate cells: protean, multifunctional, and enigmatic cells of the liver. Physiol Rev. 2008; 88: 125–72.
50. Friedman SL. Evolving challenges in hepatic fibrosis. Nat Rev Gastroenterol Hepatol. 2010; 7: 425–36.
51. Yin C, Evason KJ, Asahina K, Stainier DY. Hepatic stellate cells in liver development, regeneration, and cancer. J Clin Invest. 2013; 123: 1902–10.
52. 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: 847–55.
53. Mann J, Chu DC, Maxwell A et al. MeCP2 controls an epigenetic pathway that promotes myofibroblast transdifferentiation and fibrosis. Gastroenterology 2010; 138: 705–14, 14 e1-4.
54. Lee YA, Wallace MC, Friedman SL. Pathobiology of liver fibrosis: a translational success story. Gut. 2015; 64: 830–41.
55. Zhang Z, Zha Y, Hu W et al. The autoregulatory feedback loop of microRNA-21/programmed cell death protein 4/activation protein-1 (MiR-21/PDCD4/AP-1) as a driving force for hepatic fibrosis development. J Biol Chem. 2013; 288: 37082–93.
56. He X, Xie J, Zhang D et al. Recombinant adeno-associated virus-mediated inhibition of microRNA-21 protects mice against the lethal schistosome infection by repressing both IL-13 and transforming growth factor β 1 pathways. Hepatology. 2015; 61: 2008–17.
57. 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: 27526–39.
58. Roderburg C, Urban GW, Bettermann K et al. Micro-RNA profiling reveals a role for miR-29 in human and murine liver fibrosis. Hepatology. 2011; 53: 209–18.
59. Sekiya Y, Ogawa T, Yoshizato K, Ikeda K, Kawada N. Suppression of hepatic stellate cell activation by microRNA-29b. Biochem Biophys Res Commun. 2011; 412: 74–9.
60. Zhang Y, Ghazwani M, Li J et al. MiR-29b inhibits collagen maturation in hepatic stellate cells through down-regulating the expression of HSP47 and lysyl oxidase. Biochem Biophys Res Commun. 2014; 446: 940–4.
61. Knabel MK, Ramachandran K, Karhadkar S et al. Systemic delivery of scAAV8-encoded niR-29a ameliorates hepatic fibrosis in carbon tetrachloride-treated mice. PloS One. 2015; 10: e0124411.
62. Kwiecinski M, Noetel A, Elfimova N et al. Hepatocyte growth factor (HGF) inhibits collagen I and IV synthesis in hepatic stellate cells by miRNA-29 induction. PloS One. 2011; 6: e24568.
63. Murakami Y, Toyoda H, Tanaka M et al. The progression of liver fibrosis is related with overexpression of the miR-199 and 200 families. PloS One. 2011; 6: e16081.
64. Sun X, He Y, Ma TT, Huang C, Zhang L, Li J. Participation of miR-200a in TGF-β1-mediated hepatic stellate cell activation. Mol Cell Biochem. 2014; 388: 11–23.
65. Ogawa T, Enomoto M, Fujii H et al. MicroRNA-221/222 upregulation indicates the activation of stellate cells and the progression of liver fibrosis. Gut. 2012; 61: 1600–9.
66. Shen WJ, Dong R, Chen G, Zheng S. MicroRNA-222 modulates liver fibrosis in a murine model of biliary atresia. Biochem Biophys Res Commun. 2014; 446: 155–9.
67. Dong R, Zheng Y, Chen G, Zhao R, Zhou Z, Zheng S. miR-222 overexpression may contribute to liver fibrosis in biliary atresia by targeting PPP2R2A. J Pediatr Gastroenterol Nutr. 2015; 60: 84–90.
68. Du J, Niu X, Wang Y et al. MiR-146a-5p suppresses activation and proliferation of hepatic stellate cells in nonalcoholic fibrosing steatohepatitis through directly targeting Wnt1 and Wnt5a. Sci Rep. 2015; 5: 16163.
69. Povero D, Panera N, Eguchi A et al. Lipid-induced hepatocyte-derived extracellular vesicles regulate hepatic stellate cell via microRNAs targeting PPAR-γ. Cell Mol Gastroenterol Hepatol 2015; 1: 646–63 e4.
70. Castera L, Pinzani M. Biopsy and non-invasive methods for the diagnosis of liver fibrosis: does it take two to tango? Gut. 2010; 59: 861–6.
71. Li LM, Hu ZB, Zhou ZX et al. Serum microRNA profiles serve as novel biomarkers for HBV infection and diagnosis of HBV-positive hepatocarcinoma. Cancer Res. 2010; 70: 9798–807.
72. Dhayat SA, Husing A, Senninger N et al. Circulating microRNA-200 family as diagnostic marker in hepatocellular carcinoma. PLoS One. 2015; 10: e0140066.
73. Lin XJ, Chong Y, Guo ZW et al. A serum microRNA classifier for early detection of hepatocellular carcinoma: a multicentre, retrospective, longitudinal biomarker identification study with a nested case–control study. Lancet Oncol. 2015; 16: 804–15.
74. Wen Y, Han J, Chen J et al. Plasma miRNAs as early biomarkers for detecting hepatocellular carcinoma. Int J Cancer. 2015; 137: 1679–90.
75. Miyaaki H, Ichikawa T, Kamo Y et al. Significance of serum and hepatic microRNA-122 levels in patients with non-alcoholic fatty liver disease. Liver Int. 2014; 34: e302–7.
76. Pirola CJ, Fernandez Gianotti T, Castano GO et al. Circulating microRNA signature in non-alcoholic fatty liver disease: from serum non-coding RNAs to liver histology and disease pathogenesis. Gut. 2015; 64: 800–12.
77. Becker PP, Rau M, Schmitt J et al. Performance of serum microRNAs-122, -192 and -21 as biomarkers in patients with non-alcoholic steatohepatitis. PLoS One. 2015; 10: e0142661.
78. Tan Y, Pan T, Ye Y et al. Serum microRNAs as potential biomarkers of primary biliary cirrhosis. PLoS One. 2014; 9: e111424.
79. Migita K, Komori A, Kozuru H et al. Circulating microRNA profiles in patients with type-1 autoimmune hepatitis. PloS One. 2015; 10: e0136908.
80. Ninomiya M, Kondo Y, Funayama R et al. Distinct microRNAs expression profile in primary biliary cirrhosis and evaluation of miR 505-3p and miR197-3p as novel biomarkers. PloS One. 2013; 8: e66086.
81. Okada H, Honda M, Campbell JS et al. Inhibition of microRNA-214 ameliorates hepatic fibrosis and tumor incidence in platelet-derived growth factor C transgenic mice. Cancer Sci. 2015; 106: 1143–52.
82. Zhang J, Jiao J, Cermelli S et al. miR-21 inhibition reduces liver fibrosis and prevents tumor development by inducing apoptosis of CD24+ progenitor cells. Cancer Res. 2015; 75: 1859–67.
83. Welch C, Chen Y, Stallings RL. MicroRNA-34a functions as a potential tumor suppressor by inducing apoptosis in neuroblastoma cells. Oncogene. 2007; 26: 5017–22.
84. Akao Y, Nakagawa Y, Naoe T. let-7 microRNA functions as a potential growth suppressor in human colon cancer cells. Biol Pharm Bull. 2006; 29: 903–6.
85. Calin GA, Ferracin M, Cimmino A et al. A microRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. N Engl J Med. 2005; 353: 1793–801.
86. He L, He X, Lim LP et al. A microRNA component of the p53 tumour suppressor network. Nature. 2007; 447: 1130–4.
87. Liu C, Kelnar K, Liu B et al. The microRNA miR-34a inhibits prostate cancer stem cells and metastasis by directly repressing CD44. Nat Med. 2011; 17: 211–5.
88. Trang P, Wiggins JF, Daige CL et al. Systemic delivery of tumor suppressor microRNA mimics using a neutral lipid emulsion inhibits lung tumors in mice. Mol Ther. 2011; 19: 1116–22.
89. Liu YM, Xia Y, Dai W et al. Cholesterol-conjugated let-7a mimics: antitumor efficacy on hepatocellular carcinoma in vitro and in a preclinical orthotopic xenograft model of systemic therapy. BMC Cancer. 2014; 14: 889.