miRNAs in non-alcoholic fatty liver disease

Frontiers of Medicine

Volumn 10, Issue 4, 2016, Pages 389-396

  He, Zhen ^a   Hu, Cheng ^a   Jia, Weiping ^a  

^a SHANGHAI JIAO TONG UNIVERSITY AFFILIATED SIXTH PEOPLE S HOSPITAL   (China)

Author keywords

hepatocellular carcinoma; miRNA; nonalcoholic fatty liver disease; nonalcoholic steatohepatitis

Indexed keywords

BIOLOGICAL MARKER; MICRORNA;

ANIMAL; BLOOD; CARCINOMA, HEPATOCELLULAR; DISEASE COURSE; ECHOGRAPHY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; LIVER; LIVER CIRRHOSIS; LIVER NEOPLASMS; MOUSE; NON-ALCOHOLIC FATTY LIVER DISEASE; PATHOLOGY; X-RAY COMPUTED TOMOGRAPHY;

ANIMALS; BIOMARKERS; CARCINOMA, HEPATOCELLULAR; DISEASE PROGRESSION; GENE EXPRESSION REGULATION; HUMANS; LIVER; LIVER CIRRHOSIS; LIVER NEOPLASMS; MICE; MICRORNAS; NON-ALCOHOLIC FATTY LIVER DISEASE; TOMOGRAPHY, X-RAY COMPUTED; ULTRASONOGRAPHY;

EID: 84988969187     PISSN: 20950217     EISSN: 20950225     Source Type: Journal    
DOI: 10.1007/s11684-016-0468-5     Document Type: Review

References (56)

1. Younossi ZM, Koenig AB, Abdelatif D, Fazel Y, Henry L, Wymer M. Global epidemiology of non-alcoholic fatty liver disease-metaanalytic assessment of prevalence, incidence and outcomes. Hepatology 2015; 64(1): 73–84
2. Vernon G, Baranova A, Younossi ZM. Systematic review: the epidemiology and natural history of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis in adults. Aliment Pharmacol Ther 2011; 34(3): 274–285
3. Attar BM, Van Thiel DH. Current concepts and management approaches in nonalcoholic fatty liver disease. Sci World J 2013; 2013: 481893
4. Yki-Järvinen H. Non-alcoholic fatty liver disease as a cause and a consequence of metabolic syndrome. Lancet Diabetes Endocrinol 2014; 2(11): 901–910
5. Than NN, Newsome PN. A concise review of non-alcoholic fatty liver disease. Atherosclerosis 2015; 239(1): 192–202
6. Ul Hussain M. Micro-RNAs (miRNAs): genomic organisation, biogenesis and mode of action. Cell Tissue Res 2012; 349(2): 405–413
7. Wang XW, Heegaard NH, Orum H. MicroRNAs in liver disease. Gastroenterology 2012; 142(7): 1431–1443
8. Pirola CJ, Fernández Gianotti T, Castaño GO, Mallardi P, San Martino J, Mora Gonzalez Lopez Ledesma M, Flichman D, Mirshahi F, Sanyal AJ, Sookoian S. Circulating microRNA signature in non-alcoholic fatty liver disease: from serum non-coding RNAs to liver histology and disease pathogenesis. Gut 2015; 64(5): 800–812
9. Li S, Chen X, Zhang H, Liang X, Xiang Y, Yu C, Zen K, Li Y, Zhang CY. Differential expression of microRNAs in mouse liver under aberrant energy metabolic status. J Lipid Res 2009; 50(9): 1756–1765
10. Cheung O, Puri P, Eicken C, Contos MJ, Mirshahi F, Maher JW, Kellum JM, Min H, Luketic VA, Sanyal AJ. Nonalcoholic steatohepatitis is associated with altered hepatic microRNA expression. Hepatology 2008; 48(6): 1810–1820
11. Szabo G, Csak T. Role of microRNAs in NAFLD/NASH. Dig Dis Sci 2016; 61(5): 1314–1324
12. Tessitore A, Cicciarelli G, Del Vecchio F, Gaggiano A, Verzella D, Fischietti M, Mastroiaco V, Vetuschi A, Sferra R, Barnabei R, Capece D, Zazzeroni F, Alesse E. MicroRNA expression analysis in high fat diet-induced NAFLD-NASH-HCC progression: study on C57BL/6J mice. BMC Cancer 2016; 16(1): 3
13. Tsai WC, Hsu SD, Hsu CS, Lai TC, Chen SJ, Shen R, Huang Y, Chen HC, Lee CH, Tsai TF, Hsu MT, Wu JC, Huang HD, Shiao MS, Hsiao M, Tsou AP. MicroRNA-122 plays a critical role in liver homeostasis and hepatocarcinogenesis. J Clin Invest 2012; 122(8): 2884–2897
14. Moore KJ, Rayner KJ, Suárez Y, Fernández-Hernando C. The role of microRNAs in cholesterol efflux and hepatic lipid metabolism. Annu Rev Nutr 2011; 31(1): 49–63
15. Esau C, Davis S, Murray SF, Yu XX, Pandey SK, Pear M, Watts L, Booten SL, Graham M, Mc Kay R, Subramaniam A, Propp S, Lollo BA, Freier S, Bennett CF, Bhanot S, Monia BP. miR-122 regulation of lipid metabolism revealed by in vivo antisense targeting. Cell Metab 2006; 3(2): 87–98
16. Csak T, Bala S, Lippai D, Satishchandran A, Catalano D, Kodys K, Szabo G. microRNA-122 regulates hypoxia-inducible factor-1 and vimentin in hepatocytes and correlates with fibrosis in diet-induced steatohepatitis. Liver Int 2015; 35(2): 532–541
17. Horton JD, Goldstein JL, Brown MS. SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J Clin Invest 2002; 109(9): 1125–1131
18. Jeon TI, Osborne TF. SREBPs: metabolic integrators in physiology and metabolism. Trends Endocrinol Metab 2012; 23(2): 65–72
19. Najafi-Shoushtari SH, Kristo F, Li Y, Shioda T, Cohen DE, Gerszten RE, Näär AM. MicroRNA-33 and the SREBP host genes cooperate to control cholesterol homeostasis. Science 2010; 328 (5985): 1566–1569
20. Dávalos A, Goedeke L, Smibert P, Ramírez CM, Warrier NP, Andreo U, Cirera-Salinas D, Rayner K, Suresh U, Pastor-Pareja JC, Esplugues E, Fisher EA, Penalva LO, Moore KJ, Suárez Y, Lai EC, Fernández-Hernando C. miR-33a/b contribute to the regulation of fatty acid metabolism and insulin signaling. Proc Natl Acad Sci USA 2011; 108(22): 9232–9237
21. Rayner KJ, Esau CC, Hussain FN, McDaniel AL, Marshall SM, van Gils JM, Ray TD, Sheedy FJ, Goedeke L, Liu X, Khatsenko OG, Kaimal V, Lees CJ, Fernandez-Hernando C, Fisher EA, Temel RE, Moore KJ. Inhibition of miR-33a/b in non-human primates raises plasma HDL and lowers VLDL triglycerides. Nature 2011; 478 (7369): 404–407
22. Goedeke L, Salerno A, Ramírez CM, Guo L, Allen RM, Yin X, Langley SR, Esau C, Wanschel A, Fisher EA, Suárez Y, Baldán A, Mayr M, Fernández-Hernando C. Long-term therapeutic silencing of miR-33 increases circulating triglyceride levels and hepatic lipid accumulation in mice. EMBO Mol Med 2014; 6(9): 1133–1141
23. Vega-Badillo J, Gutiérrez-Vidal R, Hernández-Pérez HA, Villamil-Ramírez H, León-Mimila P, Sánchez-Muñoz F, Morán-Ramos S, Larrieta-Carrasco E, Fernández-Silva I, Méndez-Sánchez N, Tovar AR, Campos-Pérez F, Villarreal-Molina T, Hernández-Pando R, Aguilar-Salinas CA, Canizales-Quinteros S. Hepatic miR-33a/miR-144 and their target gene ABCA1 are associated with steatohepatitis in morbidly obese subjects. Liver Int 2016 Mar 4. [Epub ahead of print] doi: 10.1111/liv.13109
24. Cirera-Salinas D, Pauta M, Allen RM, Salerno AG, Ramírez CM, Chamorro-Jorganes A, Wanschel AC, Lasuncion MA, Morales-Ruiz M, Suarez Y, Baldan Á, Esplugues E, Fernández-Hernando C. mir-33 regulates cell proliferation and cell cycle progression. Cell Cycle 2012; 11(5): 922–933
25. Ding J, Li M, Wan X, Jin X, Chen S, Yu C, Li Y. Effect of miR-34a in regulating steatosis by targeting PPARa expression in nonalcoholic fatty liver disease. Sci Rep 2015; 5: 13729
26. Derdak Z, Villegas KA, Harb R, Wu AM, Sousa A, Wands JR. Inhibition of p53 attenuates steatosis and liver injury in a mouse model of non-alcoholic fatty liver disease. J Hepatol 2013; 58(4): 785–791
27. Xu Y, Zalzala M, Xu J, Li Y, Yin L, Zhang Y. A metabolic stressinducible miR-34a-HNF4a pathway regulates lipid and lipoprotein metabolism. Nat Commun 2015; 6: 7466
28. Hayhurst GP, Lee YH, Lambert G, Ward JM, Gonzalez FJ. Hepatocyte nuclear factor 4a (nuclear receptor 2A1) is essential for maintenance of hepatic gene expression and lipid homeostasis. Mol Cell Biol 2001; 21(4): 1393–1403
29. Yin L, Ma H, Ge X, Edwards PA, Zhang Y. Hepatic hepatocyte nuclear factor 4a is essential for maintaining triglyceride and cholesterol homeostasis. Arterioscler Thromb Vasc Biol 2011; 31 (2): 328–336
30. Shan W, Gao L, Zeng W, Hu Y, Wang G, Li M, Zhou J, Ma X, Tian X, Yao J.Activation of the SIRT1/p66shc antiapoptosis pathway via carnosic acid-induced inhibition of miR-34a protects rats against nonalcoholic fatty liver disease. Cell Death Dis 2015; 6: e1833
31. Sun C, Huang F, Liu X, Xiao X, Yang M, Hu G, Liu H, Liao L. miR-21 regulates triglyceride and cholesterol metabolism in nonalcoholic fatty liver disease by targeting HMGCR. Int J Mol Med 2015; 35(3): 847–853
32. 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 (11): 1665–1674
33. Loyer X, Paradis V, Hénique C, Vion AC, Colnot N, Guerin CL, Devue C, On S, Scetbun J, Romain M, Paul JL, Rothenberg ME, Marcellin P, Durand F, Bedossa P, Prip-Buus C, Baugé E, Staels B, Boulanger CM, Tedgui A, Rautou PE. Liver microRNA-21 is overexpressed in non-alcoholic steatohepatitis and contributes to the disease in experimental models by inhibiting PPARa expression. Gut 2015 Sep 3. [Epub ahead of print] doi: 10.1136/gutjnl-2014-308883
34. Reddy JK, Rao MS. Lipid metabolism and liver inflammation. II. Fatty liver disease and fatty acid oxidation. Am J Physiol Gastrointest Liver Physiol 2006; 290(5): G852–G858
35. Yang L, Roh YS, Song J, Zhang B, Liu C, Loomba R, Seki E. Transforming growth factor beta signaling in hepatocytes participates in steatohepatitis through regulation of cell death and lipid metabolism in mice. Hepatology 2014; 59(2): 483–495
36. Dattaroy D, Pourhoseini S, Das S, Alhasson F, Seth RK, Nagarkatti M, Michelotti GA, Diehl AM, Chatterjee S. MicroRNA 21 inhibition of SMAD7 enhances fibrogenesis via leptin-mediated NADPH oxidase in experimental and human nonalcoholic steatohepatitis. Am J Physiol Gastrointest Liver Physiol 2015; 308(4): G298–G312
37. Wu H, Ng R, Chen X, Steer CJ, Song G. MicroRNA-21 is a potential link between non-alcoholic fatty liver disease and hepatocellular carcinoma via modulation of the HBP1-p53-Srebp1c pathway. Gut 2015 Aug 17. [Epub ahead of print] doi: 10.1136/gutjnl-2014-308430
38. Vinciguerra M, Sgroi A, Veyrat-Durebex C, Rubbia-Brandt L, Buhler LH, Foti M. Unsaturated fatty acids inhibit the expression of tumor suppressor phosphatase and tensin homolog (PTEN) via microRNA-21 up-regulation in hepatocytes. Hepatology 2009; 49 (4): 1176–1184
39. He Y, Huang C, Lin X, Li J. MicroRNA-29 family, a crucial therapeutic target for fibrosis diseases. Biochimie 2013; 95(7): 1355–1359
40. Pogribny IP, Starlard-Davenport A, Tryndyak VP, Han T, Ross SA, Rusyn I, Beland FA. 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 Invest 2010; 90(10): 1437–1446
41. Mattis AN, Song G, Hitchner K, Kim RY, Lee AY, Sharma AD, Malato Y, McManus MT, Esau CC, Koller E, Koliwad S, Lim LP, Maher JJ, Raffai RL, Willenbring H. A screen in mice uncovers repression of lipoprotein lipase by microRNA-29a as a mechanism for lipid distribution away from the liver. Hepatology 2015; 61(1): 141–152
42. Ahn J, Lee H, Chung CH, Ha T. High fat diet induced downregulation of microRNA-467b increased lipoprotein lipase in hepatic steatosis. Biochem Biophys Res Commun 2011; 414(4): 664–669
43. Kurtz CL, Fannin EE, Toth CL, Pearson DS, Vickers KC, Sethupathy P. Inhibition of miR-29 has a significant lipid-lowering benefit through suppression of lipogenic programs in liver. Sci Rep 2015; 5: 12911
44. Xiao J, Bei Y, Liu J, Dimitrova-Shumkovska J, Kuang D, Zhou Q, Li J, Yang Y, Xiang Y, Wang F, Yang C, Yang W. miR-212 downregulation contributes to the protective effect of exercise against non-alcoholic fatty liver via targeting FGF-21. J Cell Mol Med 2016; 20(2): 204–216
45. Zhang ZC, Liu Y, Xiao LL, Li SF, Jiang JH, Zhao Y, Qian SW, Tang QQ, Li X. Upregulation of miR-125b by estrogen protects against non-alcoholic fatty liver in female mice. J Hepatol 2015; 63 (6): 1466–1475
46. Ng R, Wu H, Xiao H, Chen X, Willenbring H, Steer CJ, Song G. Inhibition of microRNA-24 expression in liver prevents hepatic lipid accumulation and hyperlipidemia. Hepatology 2014; 60(2): 554–564
47. Wang B, Majumder S, Nuovo G, Kutay H, Volinia S, Patel T, Schmittgen TD, Croce C, Ghoshal K, Jacob ST. Role of microRNA-155 at early stages of hepatocarcinogenesis induced by cholinedeficient and amino acid-defined diet in C57BL/6 mice. Hepatology 2009; 50(4): 1152–1161
48. Lee SS, Park SH. Radiologic evaluation of nonalcoholic fatty liver disease. World J Gastroenterol 2014; 20(23): 7392–7402
49. Povero D, Eguchi A, Li H, Johnson CD, Papouchado BG, Wree A, Messer K, Feldstein AE. Circulating extracellular vesicles with specific proteome and liver microRNAs are potential biomarkers for liver injury in experimental fatty liver disease. PLoS ONE 2014; 9 (12): e113651
50. Yamada H, Suzuki K, Ichino N, Ando Y, Sawada A, Osakabe K, Sugimoto K, Ohashi K, Teradaira R, Inoue T, Hamajima N, Hashimoto S. 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
51. Yamada H, Ohashi K, Suzuki K, Munetsuna E, Ando Y, Yamazaki M, Ishikawa H, Ichino N, Teradaira R, Hashimoto S. Longitudinal study of circulating miR-122 in a rat model of non-alcoholic fatty liver disease. Clin Chim Acta 2015; 446: 267–271
52. Clarke JD, Sharapova T, Lake AD, Blomme E, Maher J, Cherrington NJ. Circulating microRNA 122 in the methionine and choline-deficient mouse model of non-alcoholic steatohepatitis. J Appl Toxicol 2014; 34(6): 726–732
53. Miyaaki H, Ichikawa T, Kamo Y, Taura N, Honda T, Shibata H, Milazzo M, Fornari F, Gramantieri L, Bolondi L, Nakao K. Significance of serum and hepatic microRNA-122 levels in patients with non-alcoholic fatty liver disease. Liver Int 2014; 34(7): e302–e307
54. Cermelli S, Ruggieri A, Marrero JA, Ioannou GN, Beretta L. Circulating microRNAs in patients with chronic hepatitis C and non-alcoholic fatty liver disease. PLoS ONE 2011; 6(8): e23937
55. Celikbilek M, Baskol M, Taheri S, Deniz K, Dogan S, Zararsiz G, Gursoy S, Guven K, Ozbakir O, Dundar M, Yucesoy M. Circulating microRNAs in patients with non-alcoholic fatty liver disease. World J Hepatol 2014; 6(8): 613–620
56. Tan Y, Ge G, Pan T, Wen D, Gan J. A pilot study of serum microRNAs panel as potential biomarkers for diagnosis of nonalcoholic fatty liver disease. PLoS ONE 2014; 9(8): e105192