A micro-RNA expression signature for human NAFLD progression

Journal of Gastroenterology

Volumn 51, Issue 10, 2016, Pages 1022-1030

  Guo, Yan ^a   Xiong, Yanhua ^b   Sheng, Quanghu ^a   Zhao, Shilin ^a   Wattacheril, Julia ^c   Flynn, Charles Robb ^b  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY   (United States)

^c NONE   (United States)

Author keywords

HCC; Hepatocellular carcinoma; miRNA; NAFLD; NASH; Nonalcoholic fatty liver disease; Nonalcoholic steatohepatitis

Indexed keywords

ASPARTIC ACID TRANSFER RNA; LEUCINE TRANSFER RNA; MICRORNA; MICRORNA 10B 5P; MICRORNA 301A; MICRORNA 301A 3P; MICRORNA 34A 5P; MICRORNA 375; RIBOSOME RNA; SERINE TRANSFER RNA; SMALL NUCLEAR RNA; SMALL NUCLEOLAR RNA; TRANSFER RNA; TYROSINE TRANSFER RNA; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; MIRN34 MICRORNA, HUMAN; MIRN375 MICRORNA, HUMAN;

ADULT; ARTICLE; BARIATRIC SURGERY; BODY MASS; CLINICAL FEATURE; COMPARATIVE STUDY; CONTROLLED STUDY; DISEASE COURSE; DISEASE SEVERITY; ELECTIVE SURGERY; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION; HUMAN; LIVER BIOPSY; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; MALE; MIDDLE AGED; MOLECULAR PATHOLOGY; NEXT GENERATION SEQUENCING; NONALCOHOLIC FATTY LIVER; OBESITY; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; CHEMISTRY; COMPLICATION; GENETICS; LIVER TUMOR; METABOLISM; SEVERITY OF ILLNESS INDEX;

ADULT; BIOMARKERS; CARCINOMA, HEPATOCELLULAR; FEMALE; GENE EXPRESSION PROFILING; HUMANS; LIVER NEOPLASMS; MALE; MICRORNAS; MIDDLE AGED; NON-ALCOHOLIC FATTY LIVER DISEASE; OBESITY; RNA, RIBOSOMAL; RNA, SMALL NUCLEOLAR; RNA, TRANSFER; SEVERITY OF ILLNESS INDEX;

EID: 84957950070     PISSN: 09441174     EISSN: 14355922     Source Type: Journal    
DOI: 10.1007/s00535-016-1178-0     Document Type: Article

References (68)

1. Charlton M. Nonalcoholic fatty liver disease: a review of current understanding and future impact. Clin Gastroenterol Hepatol Off Clin Pract J Am Gastroenterol Assoc. 2004;2(12):1048–58.
2. Chalasani N, Younossi Z, Lavine JE, et al. The diagnosis and management of non-alcoholic fatty liver disease: practice guideline by the American Association for the Study of Liver Diseases, American College of Gastroenterology, and the American Gastroenterological Association. Hepatology. 2012;55(6):2005–23.
3. Ekstedt M, Franzen LE, Mathiesen UL, et al. Long-term follow-up of patients with NAFLD and elevated liver enzymes. Hepatology. 2006;44(4):865–73.
4. Cheung O, Puri P, Eicken C, et al. Nonalcoholic steatohepatitis is associated with altered hepatic MicroRNA expression. Hepatology. 2008;48(6):1810–20.
5. Vickers KC, Roteta LA, Hucheson-Dilks H, Han L, Guo Y. Mining diverse small RNA species in the deep transcriptome. Trends Biochem Sci. 2015;40(1):4–7.
6. Han L, Vickers KC, Samuels DC, Guo Y. Alternative applications for distinct RNA sequencing strategies. Brief Bioinform. 2014;16(4):629–39.
7. Frye M, Watt FM. The RNA methyltransferase Misu (NSun2) mediates Myc-induced proliferation and is upregulated in tumors. Curr Biol. 2006;16(10):971–81.
8. Berg M, Agesen TH, Thiis-Evensen E, et al. Distinct high resolution genome profiles of early onset and late onset colorectal cancer integrated with gene expression data identify candidate susceptibility loci. Mol Cancer. 2010;9:100.
9. Bartlett JM, Thomas J, Ross DT, et al. Mammostrat as a tool to stratify breast cancer patients at risk of recurrence during endocrine therapy. Breast Cancer Res. 2010;12(4):R47.
10. Wei FY, Suzuki T, Watanabe S, et al. Deficit of tRNA(Lys) modification by Cdkal1 causes the development of type 2 diabetes in mice. J Clin Invest. 2011;121(9):3598–608.
11. Kirchhoff K, Machicao F, Haupt A, et al. Polymorphisms in the TCF7L2, CDKAL1 and SLC30A8 genes are associated with impaired proinsulin conversion. Diabetologia. 2008;51(4):597–601.
12. Omori S, Tanaka Y, Takahashi A, et al. Association of CDKAL1, IGF2BP2, CDKN2A/B, HHEX, SLC30A8, and KCNJ11 with susceptibility to type 2 diabetes in a Japanese population. Diabetes. 2008;57(3):791–5.
13. Yasukawa T, Suzuki T, Ueda T, Ohta S, Watanabe K. Modification defect at anticodon wobble nucleotide of mitochondrial tRNAs(Leu)(UUR) with pathogenic mutations of mitochondrial myopathy, encephalopathy, lactic acidosis, and stroke-like episodes. J Biol Chem. 2000;275(6):4251–7.
14. Yasukawa T, Kirino Y, Ishii N, et al. Wobble modification deficiency in mutant tRNAs in patients with mitochondrial diseases. FEBS Lett. 2005;579(13):2948–52.
15. Kirino Y, Goto Y, Campos Y, Arenas J, Suzuki T. Specific correlation between the wobble modification deficiency in mutant tRNAs and the clinical features of a human mitochondrial disease. Proc Natl Acad Sci USA. 2005;102(20):7127–32.
16. Kleiner DE, Brunt EM, Van Natta M, et al. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology. 2005;41(6):1313–21.
17. Fujii M, Shibazaki Y, Wakamatsu K, et al. A murine model for non-alcoholic steatohepatitis showing evidence of association between diabetes and hepatocellular carcinoma. Med Mol Morphol. 2013;46(3):141–52.
18. Guo Y, Bosompem A, Mohan S, et al. Transfer RNA detection by small RNA deep sequencing and disease association with myelodysplastic syndromes. BMC Genom. 2015;16:727.
19. Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. 2011;17:10–2.
20. Guo Y, Zhao S, Sheng Q, et al. Multi-perspective quality control of Illumina exome sequencing data using QC3. Genomics. 2014;103(5–6):322–8.
21. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009;10(3):R25.
22. Berezikov E, Robine N, Samsonova A, et al. Deep annotation of Drosophila melanogaster microRNAs yields insights into their processing, modification, and emergence. Genome Res. 2011;21(2):203–15.
23. Rajagopalan R, Vaucheret H, Trejo J, Bartel DP. A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Gene Dev. 2006;20(24):3407–25.
24. Westholm JO, Ladewig E, Okamura K, Robine N, Lai EC. Common and distinct patterns of terminal modifications to mirtrons and canonical microRNAs. RNA. 2012;18(2):177–92.
25. Larter CZ, Yeh MM. Animal models of NASH: getting both pathology and metabolic context right. J Gastroenterol Hepatol. 2008;23(11):1635–48.
26. Chan PP, Lowe TM. GtRNAdb: a database of transfer RNA genes detected in genomic sequence. Nucleic Acids Res. 2009;37(Database issue):D93–7.
27. Flicek P, Amode MR, Barrell D, et al. Ensembl 2014. Nucleic Acids Res. 2014;42(Database issue):D749–55.
28. Guo Y, Zhao S, Ye F, Sheng Q, Shyr Y. MultiRankSeq: multiperspective approach for RNAseq differential expression analysis and quality control. Biomed Res Int. 2014;2014:248090.
29. Zou H, Hastie T. Regularization and variable selection via the elastic net. J R Stat Soc B. 2005;67:301–20.
30. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15(12):550.
31. Tibshirani R. Regression shrinkage and selection via the Lasso. J Roy Stat Soc B Met. 1996;58(1):267–88.
32. Domencich TA, McFadden D, Charles River Associates. Urban travel demand: a behavioral analysis: a Charles River Associates research study. New York: American Elsevier; 1975. vol xv, p. 215.
33. Hirsch RM, Slack JR, Smith RA. Techniques of trend analysis for monthly water-quality data. Water Resour Res. 1982;18(1):107–21.
34. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25(4):402–8.
35. Wattacheril J, Seeley EH, Angel P, et al. Differential intrahepatic phospholipid zonation in simple steatosis and nonalcoholic steatohepatitis. PLoS One. 2013;8(2):e57165.
36. Guo Y, Bosompem A, Zhong X, Clark T, Shyr Y, Kim AS. A comparison of microRNA sequencing reproducibility and noise reduction using mirVana and TrIzol isolation methods. Int J Comput Biol Drug Des. 2014;7(2–3):102–12.
37. Odiase EO. The risk level of liver cancer cases among smokers in developing countries. Eur J Cancer. 2012;48:S13.
38. Varnholt H. The role of microRNAs in primary liver cancer. Ann Hepatol. 2008;7(2):104–13.
39. Jiang J, Gusev Y, Aderca I, et al. Association of microRNA expression in hepatocellular carcinomas with hepatitis infection, cirrhosis, and patient survival. Clin Cancer Res. 2008;14(2):419–27.
40. 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(6):1955–63.
41. Wong QWL, Lung RWM, Law PTY, et al. MicroRNA-223 is commonly repressed in hepatocellular carcinoma and potentiates expression of Stathmin1. Gastroenterology. 2008;135(1):257–69.
42. Li WQ, Chen C, Xu MD, et al. The rno-miR-34 family is upregulated and targets ACSL1 in dimethylnitrosamine-induced hepatic fibrosis in rats. FEBS J. 2011;278(9):1522–32.
43. Concepcion CP, Han YC, Mu P, et al. Intact p53-dependent responses in miR-34-deficient mice. PLoS Genet. 2012;8(7):e1002797.
44. Chang Y, Yan W, He XX, et al. miR-375 inhibits autophagy and reduces viability of hepatocellular carcinoma cells under hypoxic conditions. Gastroenterology. 2012;143(1):177-U357.
45. Liu AM, Poon RTP, Luk JM. MicroRNA-375 targets Hippo-signaling effector YAP in liver cancer and inhibits tumor properties. Biochem Bioph Res Co. 2010;394(3):623–7.
46. Ascha MS, Hanouneh IA, Lopez R, Tamimi TA, Feldstein AF, Zein NN. The incidence and risk factors of hepatocellular carcinoma in patients with nonalcoholic steatohepatitis. Hepatology. 2010;51(6):1972–8.
47. Takuma Y, Nouso K. Nonalcoholic steatohepatitis-associated hepatocellular carcinoma: our case series and literature review. World J Gastroenterol. 2010;16(12):1436–41.
48. Yasui K, Hashimoto E, Komorizono Y, et al. Characteristics of patients with nonalcoholic steatohepatitis who develop hepatocellular carcinoma. Clin Gastroenterol Hepatol. 2011;9(5):428–33 (e50).
49. 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(5):800–12.
50. 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.
51. 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.
52. 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.
53. Celikbilek M, Baskol M, Taheri S, et al. Circulating microRNAs in patients with non-alcoholic fatty liver disease. World J Hepatol. 2014;6(8):613–20.
54. Estep M, Armistead D, Hossain N, et al. Differential expression of miRNAs in the visceral adipose tissue of patients with non-alcoholic fatty liver disease. Aliment Pharmacol Ther. 2010;32(3):487–97.
55. 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(8):1410–5.
56. Jiang ZC, Tang XM, Zhao YR, Zheng L. A functional variant at miR-34a binding site in toll-like receptor 4 gene alters susceptibility to hepatocellular carcinoma in a Chinese Han population. Tumour Biol. 2014;35(12):12345–52.
57. Li W, Xie L, He X, et al. Diagnostic and prognostic implications of microRNAs in human hepatocellular carcinoma. Int J Cancer. 2008;123(7):1616–22.
58. Castro RE, Ferreira DM, Afonso MB, 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(1):119–25.
59. Min HK, Kapoor A, Fuchs M, et al. Increased hepatic synthesis and dysregulation of cholesterol metabolism is associated with the severity of nonalcoholic fatty liver disease. Cell Metab. 2012;15(5):665–74.
60. Streba LA, Vere CC, Rogoveanu I, Streba CT. Nonalcoholic fatty liver disease, metabolic risk factors, and hepatocellular carcinoma: an open question. World J Gastroenterol. 2015;21(14):4103–10.
61. Zhou P, Jiang W, Wu L, Chang R, Wu K, Wang Z. miR-301a is a candidate oncogene that targets the homeobox gene Gax in human hepatocellular carcinoma. Dig Dis Sci. 2012;57(5):1171–80.
62. Chang Y, Yan W, He X, et al. miR-375 inhibits autophagy and reduces viability of hepatocellular carcinoma cells under hypoxic conditions. Gastroenterology. 2012;143(1):177–87.
63. Li N, Fu H, Tie Y, et al. miR-34a inhibits migration and invasion by down-regulation of c-Met expression in human hepatocellular carcinoma cells. Cancer Lett. 2009;275(1):44–53.
64. Yang P, Li QJ, Feng Y, et al. TGF-beta-miR-34a-CCL22 signaling-induced Treg cell recruitment promotes venous metastases of HBV-positive hepatocellular carcinoma. Cancer Cell. 2012;22(3):291–303.
65. He XX, Chang Y, Meng FY, et al. MicroRNA-375 targets AEG-1 in hepatocellular carcinoma and suppresses liver cancer cell growth in vitro and in vivo. Oncogene. 2012;31(28):3357–69.
66. Liu AM, Poon RT, Luk JM. MicroRNA-375 targets Hippo-signaling effector YAP in liver cancer and inhibits tumor properties. Biochem Biophys Res Commun. 2010;394(3):623–7.
67. Robertson CL, Srivastava J, Siddiq A, et al. Astrocyte elevated gene-1 (AEG-1) regulates lipid homeostasis. J Biol Chem. 2015;290(29):18227–36.
68. Septer S, Edwards G, Gunewardena S, et al. Yes-associated protein is involved in proliferation and differentiation during postnatal liver development. Am J Physiol Gastrointest Liver Physiol. 2012;302(5):G493–503.