Circulating microRNAs: Emerging biomarkers of liver disease

Seminars in Liver Disease

Volumn 35, Issue 1, 2015, Pages 43-54

  Arrese, Marco ^a   Eguchi, Akiko ^b   Feldstein, Ariel E ^b,c  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^b RADY CHILDREN'S HOSPITAL   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

biomarkers; clinical applications; exosomes; extracellular vesicles; liver disease; liver injury; microparticles; microRNAs

Indexed keywords

BIOLOGICAL MARKER; MICRORNA;

ACUTE HEPATITIS; ACUTE LIVER FAILURE; ARTICLE; CHOLESTASIS; HEPATITIS C; HUMAN; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; LIVER DISEASE; LIVER INJURY; LIVER TRANSPLANTATION; NONALCOHOLIC FATTY LIVER; PATHOGENESIS; PATHOPHYSIOLOGY; PHYSIOLOGY; PRIORITY JOURNAL; TISSUE SPECIFICITY; TOXIC HEPATITIS; BLOOD; GENETICS;

BIOLOGICAL MARKERS; HUMANS; LIVER DISEASES; MICRORNAS;

EID: 84928538090     PISSN: 02728087     EISSN: 10988971     Source Type: Journal    
DOI: 10.1055/s-0034-1397348     Document Type: Article

References (102)

1. De Guire V., Robitaille R., Tétreault N., et al. Circulating miRNAs as sensitive and specific biomarkers for the diagnosis and monitoring of human diseases: promises and challenges. Clin Biochem: 2013; 46 10-11 846 860
2. Srivastava S. K., Bhardwaj A., Leavesley S. J., Grizzle W. E., Singh S., Singh A. P. MicroRNAs as potential clinical biomarkers: emerging approaches for their detection. Biotech Histochem: 2013; 88 7 373 387
3. Chen X., Ba Y., Ma L., et al. Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res: 2008; 18 10 997 1006
4. Mitchell P. S., Parkin R. K., Kroh E. M., et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci U S A: 2008; 105 30 10513 10518
5. Szabo G., Bala S. MicroRNAs in liver disease. Nat Rev Gastroenterol Hepatol: 2013; 10 9 542 552
6. Hornby R. J., Starkey Lewis P., Dear J., Goldring C., Park B. K. MicroRNAs as potential circulating biomarkers of drug-induced liver injury: key current and future issues for translation to humans. Expert Rev Clin Pharmacol: 2014; 7 3 349 362
7. 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 5 1946 1957
8. Lakner A. M., Bonkovsky H. L., Schrum L. W. microRNAs: fad or future of liver disease. World J Gastroenterol: 2011; 17 20 2536 2542
9. Pogribny I. P., Beland F. A. Role of microRNAs in the regulation of drug metabolism and disposition genes in diabetes and liver disease. Expert Opin Drug Metab Toxicol: 2013; 9 6 713 724
10. Chen Y., Verfaillie C. M. MicroRNAs: the fine modulators of liver development and function. Liver Int: 2014; 34 7 976 990
11. Hsu S. H., Ghoshal K. MicroRNAs in liver health and disease. Curr Pathobiol Rep: 2013; 1 1 53 62
12. Takata A., Otsuka M., Yoshikawa T., Kishikawa T., Ohno M., Koike K. MicroRNAs and liver function. Minerva Gastroenterol Dietol: 2013; 59 2 187 203
13. Hulsmans M., Holvoet P. MicroRNA-containing microvesicles regulating inflammation in association with atherosclerotic disease. Cardiovasc Res: 2013; 100 1 7 18
14. Tsui N. B., Ng E. K., Lo Y. M. Stability of endogenous and added RNA in blood specimens, serum, and plasma. Clin Chem: 2002; 48 10 1647 1653
15. Turchinovich A., Samatov T. R., Tonevitsky A. G., Burwinkel B. Circulating miRNAs: cell-cell communication function? Front Genet: 2013; 4 119
16. Chen X., Liang H., Zhang J., Zen K., Zhang C. Y. Horizontal transfer of microRNAs: molecular mechanisms and clinical applications. Protein Cell: 2012; 3 1 28 37
17. Rani S. MicroRNA profiling of exosomes isolated from biofluids and conditioned media. Methods Mol Biol: 2014; 1182 131 144
18. Lemoinne S., Thabut D., Housset C., et al. The emerging roles of microvesicles in liver diseases. Nat Rev Gastroenterol Hepatol: 2014; 11 6 350 361
19. György B., Szabó T. G., Pásztói M., et al. Membrane vesicles, current state-of-the-art: emerging role of extracellular vesicles. Cell Mol Life Sci: 2011; 68 16 2667 2688
20. Raposo G., Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol: 2013; 200 4 373 383
21. Eguchi A., Dowdy S. F. siRNA delivery using peptide transduction domains. Trends Pharmacol Sci: 2009; 30 7 341 345
22. Vickers K. C., Palmisano B. T., Shoucri B. M., Shamburek R. D., Remaley A. T. MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat Cell Biol: 2011; 13 4 423 433
23. Arroyo J. D., Chevillet J. R., Kroh E. M., et al. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci U S A: 2011; 108 12 5003 5008
24. Pirola C. J., Fernández Gianotti T., Castaño G. O., et al. Circulating microRNA signature in non-alcoholic fatty liver disease: from serum non-coding RNAs to liver histology and disease pathogenesis. Gut: 2014
25. Povero D., Eguchi A., Niesman I. R., et al. Lipid-induced toxicity stimulates hepatocytes to release angiogenic microparticles that require Vanin-1 for uptake by endothelial cells. Sci Signal: 2013; 6 296 ra88
26. Esau C., Davis S., Murray S. F., et al. miR-122 regulation of lipid metabolism revealed by in vivo antisense targeting. Cell Metab: 2006; 3 2 87 98
27. Tsai W. C., Hsu S. D., Hsu C. S., et al. MicroRNA-122 plays a critical role in liver homeostasis and hepatocarcinogenesis. J Clin Invest: 2012; 122 8 2884 2897
28. Wang K., Zhang S., Marzolf B., et al. Circulating microRNAs, potential biomarkers for drug-induced liver injury. Proc Natl Acad Sci U S A: 2009; 106 11 4402 4407
29. Köberle V., Pleli T., Schmithals C., et al. Differential stability of cell-free circulating microRNAs: implications for their utilization as biomarkers. PLoS ONE: 2013; 8 9 e75184
30. Cheng L., Sharples R. A., Scicluna B. J., Hill A. F. Exosomes provide a protective and enriched source of miRNA for biomarker profiling compared to intracellular and cell-free blood. J Extracell Vesicles: 2014; 3: 10.3402/jev.v3.23743
31. Wang Z., Yang B. MicroRNA Expression Detection Methods. Heidelberg, Germany Springer: 2010
32. Ramaiah S. K. Preclinical safety assessment: current gaps, challenges, and approaches in identifying translatable biomarkers of drug-induced liver injury. Clin Lab Med: 2011; 31 1 161 172
33. Aithal G. P., Guha N., Fallowfield J., Castera L., Jackson A. P. Biomarkers in liver disease: emerging methods and potential applications. Int J Hepatol: 2012; 2012 437508
34. Kim W. R., Flamm S. L., Di Bisceglie A. M., Bodenheimer H. C.; Public Policy Committee of the American Association for the Study of Liver Disease. Serum activity of alanine aminotransferase (ALT) as an indicator of health and disease. Hepatology: 2008; 47 4 1363 1370
35. Mofrad P., Contos M. J., Haque M., et al. Clinical and histologic spectrum of nonalcoholic fatty liver disease associated with normal ALT values. Hepatology: 2003; 37 6 1286 1292
36. Molleston J. P., Schwimmer J. B., Yates K. P., et al. NASH Clinical Research Network. Histological abnormalities in children with nonalcoholic fatty liver disease and normal or mildly elevated alanine aminotransferase levels. J Pediatr: 2014; 164 4 707 713.e3
37. Hong H., Tong W. Emerging efforts for discovering new biomarkers of liver disease and hepatotoxicity. Biomarkers Med: 2014; 8 2 143 146
38. Starkey Lewis P. J., Merz M., Couttet P., et al. Serum microRNA biomarkers for drug-induced liver injury. Clin Pharmacol Ther: 2012; 92 3 291 293
39. Fontana R. J. Pathogenesis of idiosyncratic drug-induced liver injury and clinical perspectives. Gastroenterology: 2014; 146 4 914 928
40. Björnsson E. S. Epidemiology and risk factors for idiosyncratic drug-induced liver injury. Semin Liver Dis: 2014; 34 2 115 122
41. Urban T. J., Daly A. K., Aithal G. P. Genetic basis of drug-induced liver injury: present and future. Semin Liver Dis: 2014; 34 2 123 133
42. Stephens C., Andrade R. J., Lucena M. I. Mechanisms of drug-induced liver injury. Curr Opin Allergy Clin Immunol: 2014; 14 4 286 292
43. Su Y. W., Chen X., Jiang Z. Z., et al. A panel of serum microRNAs as specific biomarkers for diagnosis of compound- and herb-induced liver injury in rats. PLoS ONE: 2012; 7 5 e37395
44. Starkey Lewis P. J., Dear J., Platt V., et al. Circulating microRNAs as potential markers of human drug-induced liver injury. Hepatology: 2011; 54 5 1767 1776
45. Antoine D. J., Dear J. W., Lewis P. S., et al. Mechanistic biomarkers provide early and sensitive detection of acetaminophen-induced acute liver injury at first presentation to hospital. Hepatology: 2013; 58 2 777 787
46. Dubin P. H., Yuan H., Devine R. K., Hynan L. S., Jain M. K., Lee W. M.; Acute Liver Failure Study Group. Micro-RNA-122 levels in acute liver failure and chronic hepatitis C. J Med Virol: 2014; 86 9 1507 1514
47. Qi R., Weiland M., Gao X. H., Zhou L., Mi Q. S. Identification of endogenous normalizers for serum microRNAs by microarray profiling: U6 small nuclear RNA is not a reliable normalizer. Hepatology: 2012; 55 5 1640 1642, author reply 1642-1643
48. Ward J., Kanchagar C., Veksler-Lublinsky I., et al. Circulating microRNA profiles in human patients with acetaminophen hepatotoxicity or ischemic hepatitis. Proc Natl Acad Sci U S A: 2014; 111 33 12169 12174
49. Angulo P. Nonalcoholic fatty liver disease. N Engl J Med: 2002; 346 16 1221 1231
50. Wong R. J., Cheung R., Ahmed A. Nonalcoholic steatohepatitis is the most rapidly growing indication for liver transplantation in patients with hepatocellular carcinoma in the U.S. Hepatology: 2014; 59 6 2188 2195
51. Wieckowska A., McCullough A. J., Feldstein A. E. Noninvasive diagnosis and monitoring of nonalcoholic steatohepatitis: present and future. Hepatology: 2007; 46 2 582 589
52. Eguchi A., Povero D., Alkhouri N., Feldstein A. E. Novel therapeutic targets for nonalcoholic fatty liver disease. Expert Opin Ther Targets: 2013; 17 7 773 779
53. Clarke J. D., Sharapova T., Lake A. D., Blomme E., Maher J., Cherrington N. J. Circulating microRNA 122 in the methionine and choline-deficient mouse model of non-alcoholic steatohepatitis. J Appl Toxicol: 2014; 34 6 726 732
54. 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
55. Longchamps R. J., Abey S. K., Martino A. C., Henderson W. A. Letter: gender-associated cell-free microRNA profiles in non-alcoholic fatty liver disease. Aliment Pharmacol Ther: 2014; 39 9 997 998
56. Vincent R., Sanyal A. Recent advances in understanding of NASH: MicroRNAs as both biochemical markers and players. Curr Pathobiol Rep: 2014; 2 109 116
57. Shrivastava S., Mukherjee A., Ray R. B. Hepatitis C virus infection, microRNA and liver disease progression. World J Hepatol: 2013; 5 9 479 486
58. Singaravelu R., Russell R. S., Tyrrell D. L., Pezacki J. P. Hepatitis C virus and microRNAs: miRed in a host of possibilities. Curr Opin Virol: 2014; 7 1 10
59. Randall G., Panis M., Cooper J. D., et al. Cellular cofactors affecting hepatitis C virus infection and replication. Proc Natl Acad Sci U S A: 2007; 104 31 12884 12889
60. Shwetha S., Gouthamchandra K., Chandra M., Ravishankar B., Khaja M. N., Das S. Circulating miRNA profile in HCV infected serum: novel insight into pathogenesis. Sci Rep: 2013; 3 1555
61. Bihrer V., Friedrich-Rust M., Kronenberger B., et al. Serum miR-122 as a biomarker of necroinflammation in patients with chronic hepatitis C virus infection. Am J Gastroenterol: 2011; 106 9 1663 1669
62. van der Meer A. J., Farid W. R., Sonneveld M. J., et al. Sensitive detection of hepatocellular injury in chronic hepatitis C patients with circulating hepatocyte-derived microRNA-122. J Viral Hepat: 2013; 20 3 158 166
63. 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 3 863 871
64. Abdalla M. A., Haj-Ahmad Y. Promising candidate urinary MicroRNA biomarkers for the early detection of hepatocellular carcinoma among high-risk hepatitis C virus Egyptian patients. J Cancer: 2012; 3 19 31
65. Thirion M., Ochiya T. Roles of microRNAs in the hepatitis B virus infection and related diseases. Viruses: 2013; 5 11 2690 2703
66. Wei Y. F., Cui G. Y., Ye P., Chen J. N., Diao H. Y. MicroRNAs may solve the mystery of chronic hepatitis B virus infection. World J Gastroenterol: 2013; 19 30 4867 4876
67. Zhang X., Hou J., Lu M. Regulation of hepatitis B virus replication by epigenetic mechanisms and microRNAs. Front Genet: 2013; 4 202
68. Novellino L., Rossi R. L., Bonino F., et al. Circulating hepatitis B surface antigen particles carry hepatocellular microRNAs. PLoS ONE: 2012; 7 3 e31952
69. Ji F., Yang B., Peng X., Ding H., You H., Tien P. Circulating microRNAs in hepatitis B virus-infected patients. J Viral Hepat: 2011; 18 7 e242 e251
70. Zhang H., Li Q. Y., Guo Z. Z., et al. Serum levels of microRNAs can specifically predict liver injury of chronic hepatitis B. World J Gastroenterol: 2012; 18 37 5188 5196
71. Arataki K., Hayes C. N., Akamatsu S., et al. Circulating microRNA-22 correlates with microRNA-122 and represents viral replication and liver injury in patients with chronic hepatitis B. J Med Virol: 2013; 85 5 789 798
72. Waidmann O., Bihrer V., Pleli T., et al. Serum microRNA-122 levels in different groups of patients with chronic hepatitis B virus infection. J Viral Hepat: 2012; 19 2 e58 e65
73. Winther T. N., Heiberg I. L., Bang-Berthelsen C. H., Pociot F., Hogh B. Hepatitis B surface antigen quantity positively correlates with plasma levels of microRNAs differentially expressed in immunological phases of chronic hepatitis B in children. PLoS ONE: 2013; 8 11 e80384
74. Forner A., Llovet J. M., Bruix J. Hepatocellular carcinoma. Lancet: 2012; 379 9822 1245 1255
75. Singal A. G., Marrero J. A., Yopp A. Screening process failures for hepatocellular carcinoma. J Natl Compr Canc Netw: 2014; 12 3 375 382
76. Forner A., Bruix J. Biomarkers for early diagnosis of hepatocellular carcinoma. Lancet Oncol: 2012; 13 8 750 751
77. Li X., Yang W., Lou L., Chen Y., Wu S., Ding G. microRNA: a promising diagnostic biomarker and therapeutic target for hepatocellular carcinoma. Dig Dis Sci: 2014; 59 6 1099 1107
78. Otsuka M., Kishikawa T., Yoshikawa T., et al. The role of microRNAs in hepatocarcinogenesis: current knowledge and future prospects. J Gastroenterol: 2014; 49 2 173 184
79. Braconi C., Henry J. C., Kogure T., Schmittgen T., Patel T. The role of microRNAs in human liver cancers. Semin Oncol: 2011; 38 6 752 763
80. Qi P., Cheng S. Q., Wang H., Li N., Chen Y. F., Gao C. F. Serum microRNAs as biomarkers for hepatocellular carcinoma in Chinese patients with chronic hepatitis B virus infection. PLoS ONE: 2011; 6 12 e28486
81. Qu K. Z., Zhang K., Li H., Afdhal N. H., Albitar M. Circulating microRNAs as biomarkers for hepatocellular carcinoma. J Clin Gastroenterol: 2011; 45 4 355 360
82. Zhang Z. Q., Meng H., Wang N., et al. Serum microRNA 143 and microRNA 215 as potential biomarkers for the diagnosis of chronic hepatitis and hepatocellular carcinoma. Diagn Pathol: 2014; 9 135
83. Liu A. M., Yao T. J., Wang W., et al. Circulating miR-15b and miR-130b in serum as potential markers for detecting hepatocellular carcinoma: a retrospective cohort study. BMJ Open: 2012; 2 2 e000825
84. Li L. M., Hu Z. B., Zhou Z. X., et al. Serum microRNA profiles serve as novel biomarkers for HBV infection and diagnosis of HBV-positive hepatocarcinoma. Cancer Res: 2010; 70 23 9798 9807
85. Zhou J., Yu L., Gao X., et al. Plasma microRNA panel to diagnose hepatitis B virus-related hepatocellular carcinoma. J Clin Oncol: 2011; 29 36 4781 4788
86. Yang Y., Zhu R. Diagnostic value of circulating microRNAs for hepatocellular carcinoma. Mol Biol Rep: 2014; 41 10 6919 6929
87. Wang H., Hou L., Li A., Duan Y., Gao H., Song X. Expression of serum exosomal microRNA-21 in human hepatocellular carcinoma. Biomed Res Int: 2014; 2014 864894
88. Köberle V., Kronenberger B., Pleli T., et al. Serum microRNA-1 and microRNA-122 are prognostic markers in patients with hepatocellular carcinoma. Eur J Cancer: 2013; 49 16 3442 3449
89. Marin J. J., Bujanda L., Banales J. M. MicroRNAs and cholestatic liver diseases. Curr Opin Gastroenterol: 2014; 30 3 303 309
90. Wang X. W., Heegaard N. H., Orum H. MicroRNAs in liver disease. Gastroenterology: 2012; 142 7 1431 1443
91. Shen W. J., Dong R., Chen G., Zheng S. microRNA-222 modulates liver fibrosis in a murine model of biliary atresia. Biochem Biophys Res Commun: 2014; 446 1 155 159
92. Yamaura Y., Nakajima M., Takagi S., Fukami T., Tsuneyama K., Yokoi T. Plasma microRNA profiles in rat models of hepatocellular injury, cholestasis, and steatosis. PLoS ONE: 2012; 7 2 e30250
93. Woolbright B. L., Antoine D. J., Jenkins R. E., Bajt M. L., Park B. K., Jaeschke H. Plasma biomarkers of liver injury and inflammation demonstrate a lack of apoptosis during obstructive cholestasis in mice. Toxicol Appl Pharmacol: 2013; 273 3 524 531
94. 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 6 e66086
95. Qin B., Huang F., Liang Y., Yang Z., Zhong R. Analysis of altered microRNA expression profiles in peripheral blood mononuclear cells from patients with primary biliary cirrhosis. J Gastroenterol Hepatol: 2013; 28 3 543 550
96. Katsushima F., Takahashi A., Sakamoto N., Kanno Y., Abe K., Ohira H. Expression of micro-RNAs in peripheral blood mononuclear cells from primary biliary cirrhosis patients. Hepatol Res: 2014; 44 10 E189 E197
97. Zahm A. M., Hand N. J., Boateng L. A., Friedman J. R. Circulating microRNA is a biomarker of biliary atresia. J Pediatr Gastroenterol Nutr: 2012; 55 4 366 369
98. O'Hara S. P., Gradilone S. A., Masyuk T. V., Tabibian J. H., LaRusso N. F. MicroRNAs in cholangiopathies. Curr Pathobiol Rep: 2014; 2 3 133 142
99. Elfimova N., Schlattjan M., Sowa J. P., Dienes H. P., Canbay A., Odenthal M. Circulating microRNAs: promising candidates serving as novel biomarkers of acute hepatitis. Front Phys: 2012; 3 476
100. Waidmann O., Köberle V., Brunner F., Zeuzem S., Piiper A., Kronenberger B. Serum microRNA-122 predicts survival in patients with liver cirrhosis. PLoS ONE: 2012; 7 9 e45652
101. Chen Y. J., Zhu J. M., Wu H., et al. Circulating microRNAs as a fingerprint for liver cirrhosis. PLoS ONE: 2013; 8 6 e66577
102. Gehrau R. C., Mas V. R., Maluf D. G. Hepatic disease biomarkers and liver transplantation: what is the potential utility of microRNAs? Expert Rev Gastroenterol Hepatol: 2013; 7 2 157 170