MicroRNAs as controlled systems and controllers in non-alcoholic fatty liver disease

World Journal of Gastroenterology

Volumn 20, Issue 41, 2014, Pages 15079-15086

  Panera, Nadia ^a   Gnani, Daniela ^a   Crudele, Annalisa ^a   Ceccarelli, Sara ^a   Nobili, Valerio ^a   Alisi, Anna ^a  

^a BAMBINO GESÙ CHILDREN S HOSPITAL   (Italy)

Author keywords

Fibrosis; Liver steatosis; MicroRNAs; Non alcoholic fatty liver disease; Non alcoholic steatohepatitis

Indexed keywords

MICRORNA; GENETIC MARKER;

ARTICLE; CONTROL SYSTEM; DISEASE COURSE; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LIVER INJURY; MOLECULAR PATHOLOGY; NONALCOHOLIC FATTY LIVER; NONHUMAN; PROGNOSIS; PROTEIN FUNCTION; ANIMAL; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETIC MARKER; GENETIC PREDISPOSITION; GENETICS; LIVER; LIVER CIRRHOSIS; METABOLISM; NON-ALCOHOLIC FATTY LIVER DISEASE; PATHOLOGY; PHENOTYPE; RISK ASSESSMENT; RISK FACTOR; SIGNAL TRANSDUCTION;

ANIMALS; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION; GENETIC MARKERS; GENETIC PREDISPOSITION TO DISEASE; HUMANS; LIVER; LIVER CIRRHOSIS; MICRORNAS; NON-ALCOHOLIC FATTY LIVER DISEASE; PHENOTYPE; PROGNOSIS; RISK ASSESSMENT; RISK FACTORS; SIGNAL TRANSDUCTION;

EID: 84912118983     PISSN: 10079327     EISSN: 22192840     Source Type: Journal    
DOI: 10.3748/wjg.v20.i41.15079     Document Type: Article

References (77)

1. De Minicis S, Day C, Svegliati-Baroni G. From NAFLD to NASH and HCC: pathogenetic mechanisms and therapeutic insights. Curr Pharm Des 2013; 19: 5239-5249 [PMID: 23394093 DOI: 10.2174/1381612811319290006]
2. Brunt EM. Pathology of nonalcoholic fatty liver disease. Nat Rev Gastroenterol Hepatol 2010; 7: 195-203 [PMID: 20195271 DOI: 10.1038/nrgastro.2010.21]
3. Browning JD, Szczepaniak LS, Dobbins R, Nuremberg P, Horton JD, Cohen JC, Grundy SM, Hobbs HH. Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. Hepatology 2004; 40: 1387-1395 [PMID: 15565570 DOI: 10.1002/hep.20466]
4. Bellentani S, Scaglioni F, Marino M, Bedogni G. Epidemiology of non-alcoholic fatty liver disease. Dig Dis 2010; 28: 155-161 [PMID: 20460905 DOI: 10.1159/000282080]
5. Milić S, Stimac D. Nonalcoholic fatty liver disease/steatohepatitis: epidemiology, pathogenesis, clinical presentation and treatment. Dig Dis 2012; 30: 158-162 [PMID: 22722431 DOI: 10.1159/000336669]
6. Barshop NJ, Francis CS, Schwimmer JB, Lavine JE. Nonalcoholic fatty liver disease as a comorbidity of childhood obesity. Ped Health 2009; 3: 271-281 [PMID: 20556232 DOI: 10.2217/phe.09.21]
7. Fabbrini E, Sullivan S, Klein S. Obesity and nonalcoholic fatty liver disease: biochemical, metabolic, and clinical implications. Hepatology 2010; 51: 679-689 [PMID: 20041406 DOI: 10.1002/hep.23280]
8. Williams KH, Shackel NA, Gorrell MD, McLennan SV, Twigg SM. Diabetes and nonalcoholic Fatty liver disease: a pathogenic duo. Endocr Rev 2013; 34: 84-129 [PMID: 23238855 DOI: 10.1210/er.2012-1009]
9. Day CP. Genetic and environmental susceptibility to nonalcoholic fatty liver disease. Dig Dis 2010; 28: 255-260 [PMID: 20460920 DOI: 10.1159/000282098]
10. Nobili V, Svegliati-Baroni G, Alisi A, Miele L, Valenti L, Vajro P. A 360-degree overview of paediatric NAFLD: recent insights. J Hepatol 2013; 58: 1218-1229 [PMID: 23238106 DOI: 10.1016/j.jhep.2012.12.003]
11. Corrado RL, Torres DM, Harrison SA. Review of treatment options for nonalcoholic fatty liver disease. Med Clin North Am 2014; 98: 55-72 [PMID: 24266914 DOI: 10.1016/j.mcna.2013.09.001]
12. Nobili V, Alisi A, Raponi M. Pediatric non-alcoholic fatty liver disease: preventive and therapeutic value of lifestyle intervention. World J Gastroenterol 2009; 15: 6017-6022 [PMID: 20027672 DOI: 10.3748/wjg.15.6017]
13. Sayed D, Abdellatif M. MicroRNAs in development and disease. Physiol Rev 2011; 91: 827-887 [PMID: 21742789 DOI: 10.1152/physrev.00006.2010]
14. Ul Hussain M. Micro-RNAs (miRNAs): genomic organisation, biogenesis and mode of action. Cell Tissue Res 2012; 349: 405-413 [PMID: 22622804 DOI: 10.1007/s00441-012-1438-0]
15. Vasudevan S, Steitz JA. AU-rich-element-mediated upregulation of translation by FXR1 and Argonaute 2. Cell 2007; 128: 1105-1118 [PMID: 17382880]
16. Vasudevan S, Tong Y, Steitz JA. Switching from repression to activation: microRNAs can up-regulate translation. Science 2007; 318: 1931-1934 [PMID: 18048652 DOI: 10.1126/science. 1149460]
17. Ørom UA, Nielsen FC, Lund AH. MicroRNA-10a binds the 5'UTR of ribosomal protein mRNAs and enhances their translation. Mol Cell 2008; 30: 460-471 [PMID: 18498749 DOI: 10.1016/j.molcel.2008.05.001]
18. Henke JI, Goergen D, Zheng J, Song Y, Schüttler CG, Fehr C, Jünemann C, Niepmann M. microRNA-122 stimulates translation of hepatitis C virus RNA. EMBO J 2008; 27: 3300-3310 [PMID: 19020517 DOI: 10.1038/emboj.2008.244]
19. Lee S, Vasudevan S. Post-transcriptional stimulation of gene expression by microRNAs. Adv Exp Med Biol 2013; 768: 97-126 [PMID: 23224967 DOI: 10.1007/978-1-4614-5107-5-7]
20. Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993; 75: 843-854 [PMID: 8252621 DOI: 10.1016/0092-8674(93)90529-Y]
21. Kozomara A, Griffiths-Jones S. miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res 2011; 39: D152-D157 [PMID: 21037258 DOI: 10.1093/nar/gkq1027]
22. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005; 120: 15-20 [PMID: 15652477 DOI: 10.1016/j.cell.2004.12.035]
23. Ghildiyal M, Zamore PD. Small silencing RNAs: an expanding universe. Nat Rev Genet 2009; 10: 94-108 [PMID: 19148191 DOI: 10.1038/nrg2504]
24. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004; 116: 281-297 [PMID: 14744438 DOI: 10.1016/S0092-8674(04)00045-5]
25. Cullen BR. Transcription and processing of human microRNA precursors. Mol Cell 2004; 16: 861-865 [PMID: 15610730 DOI: 10.1016/j.molcel.2004.12.002]
26. 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]
27. Berezikov E. Evolution of microRNA diversity and regulation in animals. Nat Rev Genet 2011; 12: 846-860 [PMID: 22094948 DOI: 10.1038/nrg3079]
28. Bracht J, Hunter S, Eachus R, Weeks P, Pasquinelli AE. Trans-splicing and polyadenylation of let-7 microRNA primary transcripts. RNA 2004; 10: 1586-1594 [PMID: 15337850 DOI: 10.1261/rna.7122604]
29. Cai X, Hagedorn CH, Cullen BR. Human microRNAs are processed from capped, polyadenylated transcripts that can also function as mRNAs. RNA 2004; 10: 1957-1966 [PMID: 15525708 DOI: 10.1261/rna.7135204]
30. 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]
31. Gregory RI, Yan KP, Amuthan G, Chendrimada T, Doratotaj B, Cooch N, Shiekhattar R. The Microprocessor complex mediates the genesis of microRNAs. Nature 2004; 432: 235-240 [PMID: 15531877 DOI: 10.1038/nature03120]
32. Landthaler M, Yalcin A, Tuschl T. The human DiGeorge syndrome critical region gene 8 and Its D. melanogaster homolog are required for miRNA biogenesis. Curr Biol 2004; 14: 2162-2167 [PMID: 15589161 DOI: 10.1016/j.cub.2004.11.001]
33. 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]
34. Winter J, Jung S, Keller S, Gregory RI, Diederichs S. Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat Cell Biol 2009; 11: 228-234 [PMID: 19255566 DOI: 10.1038/ncb0309-228]
35. Yi R, Qin Y, Macara IG, Cullen BR. Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev 2003; 17: 3011-3016 [PMID: 14681208 DOI: 10.1101/gad.1158803]
36. Bohnsack MT, Czaplinski K, Gorlich D. Exportin 5 is a RanGTP-dependent dsRNA-binding protein that mediates nuclear export of pre-miRNAs. RNA 2004; 10: 185-191 [PMID: 14730017 DOI: 10.1261/rna.5167604]
37. Berezikov E, Chung WJ, Willis J, Cuppen E, Lai EC. Mammalian mirtron genes. Mol Cell 2007; 28: 328-336 [PMID: 17964270 DOI: 10.1016/j.molcel.2007.09.028]
38. 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]
39. Ketting RF, Fischer SE, Bernstein E, Sijen T, Hannon GJ, Plasterk RH. Dicer functions in RNA interference and in synthesis of small RNA involved in developmental timing in C. elegans. Genes Dev 2001; 15: 2654-2659 [PMID: 11641272 DOI: 10.1101/gad.927801]
40. Provost P, Dishart D, Doucet J, Frendewey D, Samuelsson B, Rådmark O. Ribonuclease activity and RNA binding of recombinant human Dicer. EMBO J 2002; 21: 5864-5874 [PMID: 12411504 DOI: 10.1093/emboj/cdf578]
41. Zhang H, Kolb FA, Brondani V, Billy E, Filipowicz W. Human Dicer preferentially cleaves dsRNAs at their termini without a requirement for ATP. EMBO J 2002; 21: 5875-5885 [PMID: 12411505 DOI: 10.1093/emboj/cdf582]
42. Denli AM, Tops BB, Plasterk RH, Ketting RF, Hannon GJ. Processing of primary microRNAs by the Microprocessor complex. Nature 2004; 432: 231-235 [PMID: 15531879 DOI: 10.1038/nature03049]
43. Krol J, Loedige I, Filipowicz W. The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet 2010; 11: 597-610 [PMID: 20661255 DOI: 10.1038/nrg2843]
44. Ro S, Park C, Young D, Sanders KM, Yan W. Tissue-dependent paired expression of miRNAs. Nucleic Acids Res 2007; 35: 5944-5953 [PMID: 17726050 DOI: 10.1093/nar/gkm641]
45. Dostie J, Mourelatos Z, Yang M, Sharma A, Dreyfuss G. Numerous microRNPs in neuronal cells containing novel microRNAs. RNA 2003; 9: 180-186 [PMID: 12554860 DOI: 10.1101/gad.974702]
46. Chekulaeva M, Filipowicz W. Mechanisms of miRNAmediated post-transcriptional regulation in animal cells. Curr Opin Cell Biol 2009; 21: 452-460 [PMID: 19450959 DOI: 10.1016/j.ceb.2009.04.009]
47. Fabian MR, Sonenberg N, Filipowicz W. Regulation of mRNA translation and stability by microRNAs. Annu Rev Biochem 2010; 79: 351-379 [PMID: 20533884 DOI: 10.1146/annurev-biochem-060308-103103]
48. Eulalio A, Tritschler F, Izaurralde E. The GW182 protein family in animal cells: new insights into domains required for miRNA-mediated gene silencing. RNA 2009; 15: 1433-1442 [PMID: 19535464 DOI: 10.1261/rna.1703809]
49. Chekulaeva M, Filipowicz W, Parker R. Multiple independent domains of dGW182 function in miRNA-mediated repression in Drosophila. RNA 2009; 15: 794-803 [PMID: 19304924 DOI: 10.1261/rna.1364909]
50. Voinnet O. Origin, biogenesis, and activity of plant microRNAs. Cell 2009; 136: 669-687 [PMID: 19239888 DOI: 10.1016/j.cell.2009.01.046]
51. Rottiers V, Näär AM. MicroRNAs in metabolism and metabolic disorders. Nat Rev Mol Cell Biol 2012; 13: 239-250 [PMID: 22436747 DOI: 10.1038/nrm3313]
52. Lewis AP, Jopling CL. Regulation and biological function of the liver-specific miR-122. Biochem Soc Trans 2010; 38: 1553-1557 [PMID: 21118125 DOI: 10.1042/BST0381553]
53. Krützfeldt J, Rajewsky N, Braich R, Rajeev KG, Tuschl T, Manoharan M, Stoffel M. Silencing of microRNAs in vivo with 'antagomirs'. Nature 2005; 438: 685-689 [PMID: 16258535 DOI: 10.1038/nature04303]
54. Esau C, Davis S, Murray SF, Yu XX, Pandey SK, Pear M, Watts L, Booten SL, Graham M, McKay 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: 87-98 [PMID: 16459310 DOI: 10.1016/j.cmet.2006.01.005]
55. Elmén J, Lindow M, Schütz S, Lawrence M, Petri A, Obad S, Lindholm M, Hedtjärn M, Hansen HF, Berger U, Gullans S, Kearney P, Sarnow P, Straarup EM, Kauppinen S. LNAmediated microRNA silencing in non-human primates. Nature 2008; 452: 896-899 [PMID: 18368051 DOI: 10.1038/nature06783]
56. Stenvang J, Petri A, Lindow M, Obad S, Kauppinen S. Inhibition of microRNA function by antimiR oligonucleotides. Silence 2012; 3: 1 [PMID: 22230293 DOI: 10.1186/1758-907X-3-1]
57. 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: 1437-1446 [PMID: 20548288 DOI: 10.1038/labinvest.2010.113]
58. Alisi A, Da Sacco L, Bruscalupi G, Piemonte F, Panera N, De Vito R, Leoni S, Bottazzo GF, Masotti A, Nobili V. Mirnome analysis reveals novel molecular determinants in the pathogenesis of diet-induced nonalcoholic fatty liver disease. Lab Invest 2011; 91: 283-293 [PMID: 20956972 DOI: 10.1038/labinvest. 2010.166]
59. Vella S, Gnani D, Crudele A, Ceccarelli S, De Stefanis C, Gaspari S, Nobili V, Locatelli F, Marquez VE, Rota R, Alisi A. EZH2 down-regulation exacerbates lipid accumulation and inflammation in in vitro and in vivo NAFLD. Int J Mol Sci 2013; 14: 24154-24168 [PMID: 24351808 DOI: 10.3390/ijms141224154]
60. Zhang Y, Cheng X, Lu Z, Wang J, Chen H, Fan W, Gao X, Lu D. Upregulation of miR-15b in NAFLD models and in the serum of patients with fatty liver disease. Diabetes Res Clin Pract 2013; 99: 327-334 [PMID: 23287814 DOI: 10.1016/j.diabres.2012.11.025]
61. Zheng L, Lv GC, Sheng J, Yang YD. Effect of miRNA-10b in regulating cellular steatosis level by targeting PPARalpha expression, a novel mechanism for the pathogenesis of NAFLD. J Gastroenterol Hepatol 2010; 25: 156-163 [PMID: 19780876 DOI: 10.1111/j.1440-1746.2009.05949.x]
62. 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: 1125-1131 [PMID: 11994399 DOI: 10.1172/JCI15593]
63. 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: 9232-9237 [PMID: 21576456 DOI: 10.1073/pnas.1102281108]
64. Näär AM. MiRs with a sweet tooth. Cell Metab 2011; 14: 149-150 [PMID: 21803284 DOI: 10.1016/j.cmet.2011.07.005]
65. Rayner KJ, Suárez Y, Dávalos A, Parathath S, Fitzgerald ML, Tamehiro N, Fisher EA, Moore KJ, Fernández-Hernando C. MiR-33 contributes to the regulation of cholesterol homeostasis. Science 2010; 328: 1570-1573 [PMID: 20466885 DOI: 10.1126/science.1189862]
66. Goedeke L, Vales-Lara FM, Fenstermaker M, Cirera-Salinas D, Chamorro-Jorganes A, Ramírez CM, Mattison JA, de Cabo R, Suárez Y, Fernández-Hernando C. A regulatory role for microRNA 33∗ in controlling lipid metabolism gene expression. Mol Cell Biol 2013; 33: 2339-2352 [PMID: 23547260 DOI: 10.1128/MCB.01714-12]
67. Kim HS, Xiao C, Wang RH, Lahusen T, Xu X, Vassilopoulos A, Vazquez-Ortiz G, Jeong WI, Park O, Ki SH, Gao B, Deng CX. Hepatic-specific disruption of SIRT6 in mice results in fatty liver formation due to enhanced glycolysis and triglyceride synthesis. Cell Metab 2010; 12: 224-236 [PMID: 20816089 DOI: 10.1016/j.cmet.2010.06.009]
68. Cantó C, Auwerx J. Targeting sirtuin 1 to improve metabolism: all you need is NAD(+)? Pharmacol Rev 2012; 64: 166-187 [PMID: 22106091 DOI: 10.1124/pr.110.003905]
69. Choi SE, Fu T, Seok S, Kim DH, Yu E, Lee KW, Kang Y, Li X, Kemper B, Kemper JK. Elevated microRNA-34a in obesity reduces NAD+ levels and SIRT1 activity by directly targeting NAMPT. Aging Cell 2013; 12: 1062-1072 [PMID: 23834033 DOI: 10.1111/acel.12135]
70. Fu T, Choi SE, Kim DH, Seok S, Suino-Powell KM, Xu HE, Kemper JK. Aberrantly elevated microRNA-34a in obesity attenuates hepatic responses to FGF19 by targeting a membrane coreceptor β-Klotho. Proc Natl Acad Sci USA 2012; 109: 16137-16142 [PMID: 22988100 DOI: 10.1073/pnas.1205951109]
71. Cortez MA, Bueso-Ramos C, Ferdin J, Lopez-Berestein G, Sood AK, Calin GA. MicroRNAs in body fluids - the mix of hormones and biomarkers. Nat Rev Clin Oncol 2011; 8: 467-477 [PMID: 21647195 DOI: 10.1038/nrclinonc.2011.76]
72. 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 [PMID: 23727030 DOI: 10.1016/j.cca.2013.05.021]
73. 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: e23937 [PMID: 21886843 DOI: 10.1371/journal.pone.0023937]
74. Hermeking H. The miR-34 family in cancer and apoptosis. Cell Death Differ 2010; 17: 193-199 [PMID: 19461653 DOI: 10.1038/cdd.2009.56]
75. 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: e302-e307 [PMID: 24313922 DOI: 10.1111/liv.12429]
76. Li J, Ghazwani M, Zhang Y, Lu J, Li J, Fan J, Gandhi CR, Li S. miR-122 regulates collagen production via targeting hepatic stellate cells and suppressing P4HA1 expression. J Hepatol 2013; 58: 522-528 [PMID: 23178710 DOI: 10.1016/j.jhep.2012.11.011]
77. 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: 1810-1820 [PMID: 19030170 DOI: 10.1002/hep.22569]