Circulating RNA molecules as biomarkers in liver disease

International Journal of Molecular Sciences

Volumn 15, Issue 10, 2014, Pages 17644-17666

  Enache, Liviu S ^a,b,c   Enache, Elena L ^b   Ramière, Christophe ^a,d,e,f,g   Diaz, Olivier ^a,d,e,f   Bancu, Ligia ^b,c   Sin, Anca ^b,c   André, Patrice ^a,d,e,f,g  

^a UNIVERSITÉ LYON 1   (France)

^b UNIVERSITY OF MEDICINE AND PHARMACY   (Romania)

^c Emergency Clinical Hospital   (Romania)

^d CENTRE INTERNATIONAL DE RECHERCHE EN INFECTIOLOGIE   (France)

^e UNIVERSITÉ DE LYON   (France)

^f CNRS   (France)

^g CROIX ROUSSE HOSPITAL   (France)

Author keywords

Biomarker; Cell free RNA; Diagnostic; Liver disease; miRNA; Preanalytical variable

Indexed keywords

ALANINE AMINOTRANSFERASE; ALBUMIN; ARGONAUTE 1 PROTEIN; ARGONAUTE 2 PROTEIN; BETA2 GLYCOPROTEIN 1; BIOLOGICAL MARKER; CD81 ANTIGEN; CELL FREE RNA; FAMILIAL HIGH DENSITY LIPOPROTEIN DEFICIENCY USE: FAMILIAL HYPOALPHALIPOPROTEINEMIA; GALACTOSAMINE; HAPTOGLOBIN; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MICRORNA; MICRORNA 122; MICRORNA 125B; MICRORNA 223; MICRORNA 375; PHOSPHATIDYLINOSITOL 3, 4, 5 TRISPHOSPHATE 3 PHOSPHATASE; RNA; SCAVENGER RECEPTOR BI; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; TUMOR NECROSIS FACTOR ALPHA CONVERTING ENZYME; UNCLASSIFIED DRUG; VITAMIN D BINDING PROTEIN;

APOPTOSIS; CARCINOGENESIS; CELL COMMUNICATION; DNA RNA HYBRIDIZATION; DRUG INTOXICATION; GENE EXPRESSION; HEPATITIS B; HEPATITIS C; HUMAN; IMMUNOSUPPRESSIVE TREATMENT; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; LIVER DISEASE; LIVER FIBROSIS; LIVER INJURY; LIVER TOXICITY; LIVER TRANSPLANTATION; NECROSIS; NONALCOHOLIC FATTY LIVER; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION; REVIEW; RNA SEQUENCE; SENSITIVITY AND SPECIFICITY; VIRUS HEPATITIS; BLOOD; LIVER DISEASES; LUNG TUMOR; PATHOLOGY; PROGNOSIS;

BIOLOGICAL MARKERS; HUMANS; LIVER DISEASES; LUNG NEOPLASMS; MICRORNAS; NON-ALCOHOLIC FATTY LIVER DISEASE; PROGNOSIS; RNA;

EID: 84907834010     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms151017644     Document Type: Review

References (97)

1. European Association for the Study of the Liver. EASL clinical practice guidelines: Management of chronic hepatitis B virus infection. J. Hepatol. 2012, 57, 167-185.
2. EASL Recommendations on Treatment of Hepatitis C. Available online: http://files. easl. eu/easl-recommendations-on-treatment-of-hepatitis-C. pdf (accessed on 22 August 2014).
3. El-Serag, H. B. Epidemiology of viral hepatitis and hepatocellular carcinoma. Gastroenterology 2012, 142, 1264-1273. e1.
4. European Association for the Study of the Liver; European Organisation for Research and Treatment of Cancer. EASL-EORTC Clinical Practice Guidelines: management of hepatocellular carcinoma. J. Hepatol. 2012, 56, 908-943.
5. Tsang, J. C. H.; Lo, Y. M. D. Circulating nucleic acids in plasma/serum. Pathology 2007, 39, 197-207.
6. Weber, J. A.; Baxter, D. H.; Zhang, S.; Huang, D. Y.; Huang, K. H.; Lee, M. J.; Galas, D. J.; Wang, K. The microRNA spectrum in 12 body fluids. Clin. Chem. 2010, 56, 1733-1741.
7. Tsui, N. B. Y.; Ng, E. K. O.; Lo, Y. M. D. Stability of endogenous and added RNA in blood specimens, serum, and plasma. Clin. Chem. 2002, 48, 1647-1653.
8. El-Hefnawy, T.; Raja, S.; Kelly, L.; Bigbee, W. L.; Kirkwood, J. M.; Luketich, J. D.; Godfrey, T. E. Characterization of amplifiable, circulating RNA in plasma and its potential as a tool for cancer diagnostics. Clin. Chem. 2004, 50, 564-573.
9. Wetmore, B. A.; Brees, D. J.; Singh, R.; Watkins, P. B.; Andersen, M. E.; Loy, J.; Thomas, R. S. Quantitative analyses and transcriptomic profiling of circulating messenger RNAs as biomarkers of rat liver injury. Hepatol. Baltim. Md. 2010, 51, 2127-2139.
10. Halicka, H. D.; Bedner, E.; Darzynkiewicz, Z. Segregation of RNA and separate packaging of DNA and RNA in apoptotic bodies during apoptosis. Exp. Cell Res. 2000, 260, 248-256.
11. Cocucci, E.; Racchetti, G.; Meldolesi, J. Shedding microvesicles: Artefacts no more. Trends Cell Biol. 2009, 19, 43-51.
12. García, J. M.; García, V.; Peña, C.; Domínguez, G.; Silva, J.; Diaz, R.; Espinosa, P.; Citores, M. J.; Collado, M.; Bonilla, F. Extracellular plasma RNA from colon cancer patients is confined in a vesicle-like structure and is mRNA-enriched. RNA 2008, 14, 1424-1432.
13. Bolukbasi, M. F.; Mizrak, A.; Ozdener, G. B.; Madlener, S.; Ströbel, T.; Erkan, E. P.; Fan, J.-B.; Breakefield, X. O.; Saydam, O. miR-1289 and "Zipcode"-like sequence enrich mRNAs in microvesicles. Mol. Ther. Nucleic Acids 2012, 1, doi: 10. 1038/mtna. 2011. 2.
14. Arroyo, J. D.; Chevillet, J. R.; Kroh, E. M.; Ruf, I. K.; Pritchard, C. C.; Gibson, D. F.; Mitchell, P. S.; Bennett, C. F.; Pogosova-Agadjanyan, E. L.; Stirewalt, D. L.; et al. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc. Natl. Acad. Sci. USA 2011, 108, 5003-5008.
15. Turchinovich, A.; Weiz, L.; Langheinz, A.; Burwinkel, B. Characterization of extracellular circulating microRNA. Nucleic Acids Res. 2011, 39, 7223-7233.
16. Turchinovich, A.; Burwinkel, B. Distinct AGO1 and AGO2 associated miRNA profiles in human cells and blood plasma. RNA Biol. 2012, 9, 1066-1075.
17. Bala, S.; Petrasek, J.; Mundkur, S.; Catalano, D.; Levin, I.; Ward, J.; Alao, H.; Kodys, K.; Szabo, G. Circulating microRNAs in exosomes indicate hepatocyte injury and inflammation in alcoholic, drug-induced, and inflammatory liver diseases. Hepatol. Baltim. Md. 2012, 56, 1946-1957.
18. 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, 423-433.
19. Lässer, C.; Alikhani, V. S.; Ekström, K.; Eldh, M.; Paredes, P. T.; Bossios, A.; Sjöstrand, M.; Gabrielsson, S.; Lötvall, J.; Valadi, H. Human saliva, plasma and breast milk exosomes contain RNA: Uptake by macrophages. J. Transl. Med. 2011, 9, doi: 10. 1186/1479-5876-9-9.
20. Valadi, H.; Ekström, K.; Bossios, A.; Sjöstrand, M.; Lee, J. J.; Lötvall, J. O. Exosome-Mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 2007, 9, 654-659.
21. Deregibus, M. C.; Cantaluppi, V.; Calogero, R.; Iacono, M. L.; Tetta, C.; Biancone, L.; Bruno, S.; Bussolati, B.; Camussi, G. Endothelial progenitor cell-derived microvesicles activate an angiogenic program in endothelial cells by a horizontal transfer of mRNA. Blood 2007, 110, 2440-2448.
22. Waldenström, A.; Gennebäck, N.; Hellman, U.; Ronquist, G. Cardiomyocyte microvesicles contain DNA/RNA and convey biological messages to target cells. PLoS One 2012, 7, e34653.
23. Kogure, T.; Lin, W.-L.; Yan, I. K.; Braconi, C.; Patel, T. Intercellular nanovesicle-mediated microRNA transfer: A mechanism of environmental modulation of hepatocellular cancer cell growth. Hepatology 2011, 54, 1237-1248.
24. Fonsato, V.; Collino, F.; Herrera, M. B.; Cavallari, C.; Deregibus, M. C.; Cisterna, B.; Bruno, S.; Romagnoli, R.; Salizzoni, M.; Tetta, C.; et al. Human liver stem cell-derived microvesicles inhibit hepatoma growth in SCID mice by delivering antitumor MicroRNAs. Stem Cells 2012, 30, 1985-1998.
25. Pan, Q.; Ramakrishnaiah, V.; Henry, S.; Fouraschen, S.; de Ruiter, P. E.; Kwekkeboom, J.; Tilanus, H. W.; Janssen, H. L. A.; van der Laan, L. J. W. Hepatic cell-to-cell transmission of small silencing RNA can extend the therapeutic reach of RNA interference (RNAi). Gut 2012, 61, 1330-1339.
26. Laterza, O. F.; Lim, L.; Garrett-Engele, P. W.; Vlasakova, K.; Muniappa, N.; Tanaka, W. K.; Johnson, J. M.; Sina, J. F.; Fare, T. L.; Sistare, F. D.; et al. Plasma MicroRNAs as sensitive and specific biomarkers of tissue injury. Clin. Chem. 2009, 55, 1977-1983.
27. Etheridge, A.; Lee, I.; Hood, L.; Galas, D.; Wang, K. Extracellular microRNA: A new source of biomarkers. Mutat. Res. 2011, 717, 85-90.
28. Miyamoto, M.; Yanai, M.; Ookubo, S.; Awasaki, N.; Takami, K.; Imai, R. Detection of cell-free, liver-specific mRNAs in peripheral blood from rats with hepatotoxicity: A potential toxicological biomarker for safety evaluation. Toxicol. Sci. 2008, 106, 538-545.
29. Okubo, S.; Miyamoto, M.; Takami, K.; Kanki, M.; Ono, A.; Nakatsu, N.; Yamada, H.; Ohno, Y.; Urushidani, T. Identification of novel liver-specific mRNAs in plasma for biomarkers of drug-induced liver injury and quantitative evaluation in rats treated with various hepatotoxic compounds. Toxicol. Sci. 2013, 132, 21-31.
30. Wang, K.; Zhang, S.; Marzolf, B.; Troisch, P.; Brightman, A.; Hu, Z.; Hood, L. E.; Galas, D. J. Circulating microRNAs, potential biomarkers for drug-induced liver injury. Proc. Natl. Acad. Sci. USA 2009, 106, 4402-4407.
31. Starkey Lewis, P. J.; Dear, J.; Platt, V.; Simpson, K. J.; Craig, D. G. N.; Antoine, D. J.; French, N. S.; Dhaun, N.; Webb, D. J.; Costello, E. M.; et al. Circulating microRNAs as potential markers of human drug-induced liver injury. Hepatology 2011, 54, 1767-1776.
32. Chan, R. W. Y.; Wong, J.; Chan, H. L. Y.; Mok, T. S. K.; Lo, W. Y. W.; Lee, V.; To, K. F.; Lai, P. B. S.; Rainer, T. H.; Lo, Y. M. D.; et al. Aberrant concentrations of liver-derived plasma albumin mRNA in liver pathologies. Clin. Chem. 2010, 56, 82-89.
33. Gui, J.; Tian, Y.; Wen, X.; Zhang, W.; Zhang, P.; Gao, J.; Run, W.; Tian, L.; Jia, X.; Gao, Y. Serum microRNA characterization identifies miR-885-5p as a potential marker for detecting liver pathologies. Clin. Sci. Lond. Engl. 1979 2011, 120, 183-193.
34. Murakami, Y.; Toyoda, H.; Tanahashi, T.; Tanaka, J.; Kumada, T.; Yoshioka, Y.; Kosaka, N.; Ochiya, T.; Taguchi, Y. Comprehensive miRNA expression analysis in peripheral blood can diagnose liver disease. PLoS One 2012, 7, e48366.
35. Li, L.-M.; Hu, Z.-B.; Zhou, Z.-X.; Chen, X.; Liu, F.-Y.; Zhang, J.-F.; Shen, H.-B.; Zhang, C.-Y.; Zen, K. Serum microRNA profiles serve as novel biomarkers for HBV infection and diagnosis of HBV-positive hepatocarcinoma. Cancer Res. 2010, 70, 9798-9807.
36. Cermelli, S.; Ruggieri, A.; Marrero, J. A.; Ioannou, G. N.; Beretta, L. Circulating microRNAs in patients with chronic hepatitis C and non-alcoholic fatty liver disease. PLoS One 2011, 6, e23937.
37. Roderburg, C.; Mollnow, T.; Bongaerts, B.; Elfimova, N.; Vargas Cardenas, D.; Berger, K.; Zimmermann, H.; Koch, A.; Vucur, M.; Luedde, M.; et al. Micro-RNA profiling in human serum reveals compartment-specific roles of miR-571 and miR-652 in liver cirrhosis. PLoS One 2012, 7, e32999.
38. Bihrer, V.; Friedrich-Rust, M.; Kronenberger, B.; Forestier, N.; Haupenthal, J.; Shi, Y.; Peveling-Oberhag, J.; Radeke, H. H.; Sarrazin, C.; Herrmann, E.; et al. Serum miR-122 as a biomarker of necroinflammation in patients with chronic hepatitis C virus infection. Am. J. Gastroenterol. 2011, 106, 1663-1669.
39. Trebicka, J.; Anadol, E.; Elfimova, N.; Strack, I.; Roggendorf, M.; Viazov, S.; Wedemeyer, I.; Drebber, U.; Rockstroh, J.; Sauerbruch, T.; et al. Hepatic and serum levels of miR-122 after chronic HCV induced fibrosis. J. Hepatol. 2012, 58, 234-239.
40. Zhang, Y.; Jia, Y.; Zheng, R.; Guo, Y.; Wang, Y.; Guo, H.; Fei, M.; Sun, S. Plasma microRNA-122 as a biomarker for viral-, alcohol-, and chemical-related hepatic diseases. Clin. Chem. 2010, 56, 1830-1838.
41. Zhang, X.; Zhang, Z.; Dai, F.; Shi, B.; Chen, L.; Zhang, X.; Zang, G.; Zhang, J.; Chen, X.; Qian, F.; et al. Comparison of circulating, hepatocyte specific messenger RNA and microRNA as biomarkers for chronic hepatitis B and C. PLoS One 2014, 9, e92112.
42. Zhang, H.; Li, Q.-Y.; Guo, Z.-Z.; Guan, Y.; Du, J.; Lu, Y.-Y.; Hu, Y.-Y.; Liu, P.; Huang, S.; Su, S.-B. Serum levels of microRNAs can specifically predict liver injury of chronic hepatitis B. World J. Gastroenterol. WJG 2012, 18, 5188-5196.
43. Xu, J.; Wu, C.; Che, X.; Wang, L.; Yu, D.; Zhang, T.; Huang, L.; Li, H.; Tan, W.; Wang, C.; et al. Circulating microRNAs, miR-21, miR-122, and miR-223, in patients with hepatocellular carcinoma or chronic hepatitis. Mol. Carcinog. 2011, 50, 136-142.
44. Winther, T. N.; Bang-Berthelsen, C. H.; Heiberg, I. L.; Pociot, F.; Hogh, B. Differential plasma microRNA profiles in HBeAg positive and HBeAg negative children with chronic hepatitis B. PLoS One 2013, 8, e58236.
45. 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, e80384.
46. Cheung, S. T.; Fan, S. T.; Lee, Y. T.; Chow, J. P.; Ng, I. O.; Fong, D. Y.; Lo, C. M. Albumin mRNA in plasma predicts post-transplant recurrence of patients with hepatocellular carcinoma. Transplant 2008, 85, 81-87.
47. Tomimaru, Y.; Eguchi, H.; Nagano, H.; Wada, H.; Kobayashi, S.; Marubashi, S.; Tanemura, M.; Tomokuni, A.; Takemasa, I.; Umeshita, K.; et al. Circulating microRNA-21 as a novel biomarker for hepatocellular carcinoma. J. Hepatol. 2012, 56, 167-175.
48. Qi, P.; Cheng, S.; Wang, H.; Li, N.; Chen, Y.; Gao, C. Serum MicroRNAs as biomarkers for hepatocellular carcinoma in chinese patients with chronic hepatitis B virus infection. PLoS One 2011, 6, e28486.
49. Zhou, J.; Yu, L.; Gao, X.; Hu, J.; Wang, J.; Dai, Z.; Wang, J.-F.; Zhang, Z.; Lu, S.; Huang, X.; et al. Plasma MicroRNA panel to diagnose hepatitis B virus-related hepatocellular carcinoma. J. Clin. Oncol. 2011, 29, 4781-4788.
50. Chan, R. W. Y.; Wong, J.; Lai, P. B. S.; Lo, Y. M. D.; Chiu, R. W. K. The potential clinical utility of serial plasma albumin mRNA monitoring for the post-liver transplantation management. Clin. Biochem. 2013, 46, 1313-1319.
51. Farid, W. R. R.; Pan, Q.; van der Meer, A. J. P.; de Ruiter, P. E.; Ramakrishnaiah, V.; de Jonge, J.; Kwekkeboom, J.; Janssen, H. L. A.; Metselaar, H. J.; Tilanus, H. W.; et al. Hepatocyte-Derived microRNAs as serum biomarkers of hepatic injury and rejection after liver transplantation. Liver Transpl. 2012, 18, 290-297.
52. Pirola, C. J.; Gianotti, T. F.; Castaño, G. O.; Mallardi, P.; Martino, J. S.; Ledesma, M. M. G. L.; Flichman, D.; Mirshahi, F.; Sanyal, A. J.; Sookoian, S. Circulating microRNA signature in non-alcoholic fatty liver disease: From serum non-coding RNAs to liver histology and disease pathogenesis. Gut 2014, doi: 10. 1136/gutjnl-2014-306996.
53. Yamada, H.; Suzuki, K.; Ichino, N.; Ando, Y.; Sawada, A.; Osakabe, K.; Sugimoto, K.; Ohashi, K.; Teradaira, R.; 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.
54. 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, e105192.
55. Ward, J.; Kanchagar, C.; Veksler-Lublinsky, I.; Lee, R. C.; McGill, M. R.; Jaeschke, H.; Curry, S. C.; Ambros, V. R. Circulating microRNA profiles in human patients with acetaminophen hepatotoxicity or ischemic hepatitis. Proc. Natl. Acad. Sci. USA 2014, 111, 12169-12174.
56. Chen, Y.; Shen, A.; Rider, P. J.; Yu, Y.; Wu, K.; Mu, Y.; Hao, Q.; Liu, Y.; Gong, H.; Zhu, Y.; 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, 4511-4521.
57. Novellino, L.; Rossi, R. L.; Bonino, F.; Cavallone, D.; Abrignani, S.; Pagani, M.; Brunetto, M. R. Circulating hepatitis B surface antigen particles carry hepatocellular microRNAs. PLoS One 2012, 7, e31952.
58. Carpentier, A.; Conti, F.; Carrière, M.; Aoudjehane, L.; Miroux, C.; Moralès, O.; Calmus, Y.; Groux, H.; Auriault, C.; Pancré, V.; et al. Analysis of gene transcription in sera during chronic hepatitis C infection. J. Med. Virol. 2009, 81, 473-480.
59. Randall, G.; Panis, M.; Cooper, J. D.; Tellinghuisen, T. L.; Sukhodolets, K. E.; Pfeffer, S.; Landthaler, M.; Landgraf, P.; Kan, S.; Lindenbach, B. D.; et al. Cellular cofactors affecting hepatitis C virus infection and replication. Proc. Natl. Acad. Sci. USA 2007, 104, 12884-12889.
60. Jangra, R. K.; Yi, M.; Lemon, S. M. Regulation of hepatitis C virus translation and infectious virus production by the MicroRNA miR-122. J. Virol. 2010, 84, 6615-6625.
61. Jopling, C. L.; Yi, M.; Lancaster, A. M.; Lemon, S. M.; Sarnow, P. Modulation of hepatitis C virus RNA abundance by a liver-specific MicroRNA. Science 2005, 309, 1577-1581.
62. Roberts, A. P. E.; Lewis, A. P.; Jopling, C. L. miR-122 activates hepatitis C virus translation by a specialized mechanism requiring particular RNA components. Nucleic Acids Res. 2011, doi: 10. 1093/nar/gkr426.
63. Sarasin-Filipowicz, M.; Krol, J.; Markiewicz, I.; Heim, M. H.; Filipowicz, W. Decreased levels of microRNA miR-122 in individuals with hepatitis C responding poorly to interferon therapy. Nat. Med. 2009, 15, 31-33.
64. Köberle, V.; Pleli, T.; Schmithals, C.; Augusto Alonso, E.; Haupenthal, J.; Bönig, H.; Peveling-Oberhag, J.; Biondi, R. M.; Zeuzem, S.; Kronenberger, B.; et al. Differential stability of cell-free circulating microRNAs: Implications for their utilization as biomarkers. PLoS One 2013, 8, e75184.
65. Callegari, E.; Gramantieri, L.; Domenicali, M.; D'Abundo, L.; Sabbioni, S.; Negrini, M. MicroRNAs in liver cancer: A model for investigating pathogenesis and novel therapeutic approaches. Cell Death Differ. 2014, doi: 10. 1038/cdd. 2014. 136.
66. Meng, F.; Henson, R.; Wehbe-Janek, H.; Ghoshal, K.; Jacob, S. T.; Patel, T. MicroRNA-21 regulates expression of the PTEN tumor suppressor gene in human hepatocellular cancer. Gastroenterology 2007, 133, 647-658.
67. Wong, Q. W.-L.; Lung, R. W.-M.; Law, P. T.-Y.; Lai, P. B.-S.; Chan, K. Y.-Y.; To, K.; Wong, N. MicroRNA-223 is commonly repressed in hepatocellular carcinoma and potentiates expression of Stathmin1. Gastroenterology 2008, 135, 257-269.
68. Tsai, W.-C.; Hsu, P. W.-C.; Lai, T.-C.; Chau, G.-Y.; Lin, C.-W.; Chen, C.-M.; Lin, C.-D.; Liao, Y.-L.; Wang, J.-L.; Chau, Y.-P.; et al. MicroRNA-122, a tumor suppressor microRNA that regulates intrahepatic metastasis of hepatocellular carcinoma. Hepatology 2009, 49, 1571-1582.
69. Yang, Z.; Miao, R.; Li, G.; Wu, Y.; Robson, S. C.; Yang, X.; Zhao, Y.; Zhao, H.; Zhong, Y. Identification of recurrence related microRNAs in hepatocellular carcinoma after surgical resection. Int. J. Mol. Sci. 2013, 14, 1105-1118.
70. Jia, H.-Y.; Wang, Y.-X.; Yan, W.-T.; Li, H.-Y.; Tian, Y.-Z.; Wang, S.-M.; Zhao, H.-L. MicroRNA-125b functions as a tumor suppressor in hepatocellular carcinoma cells. Int. J. Mol. Sci. 2012, 13, 8762-8774.
71. Muller, C.; Petermann, D.; Pfeffel, F.; Oesterreicher, C.; Fugger, R. Lack of specificity of albumin-mRNA-positive cells as a marker of circulating hepatoma cells. Hepatology 1997, 25, 896-899.
72. Tiniakos, D. G.; Vos, M. B.; Brunt, E. M. Nonalcoholic fatty liver disease: Pathology and pathogenesis. Annu. Rev. Pathol. Mech. Dis. 2010, 5, 145-171.
73. Cheung, O.; Puri, P.; Eicken, C.; Contos, M. J.; Mirshahi, F.; Maher, J. W.; Kellum, J. M.; Min, H.; Luketic, V. A.; Sanyal, A. J. Nonalcoholic steatohepatitis is associated with altered hepatic MicroRNA expression. Hepatology 2008, 48, 1810-1820.
74. Singaravelu, R.; Chen, R.; Lyn, R. K.; Jones, D. M.; O'Hara, S.; Rouleau, Y.; Cheng, J.; Srinivasan, P.; Nasheri, N.; Russell, R. S.; et al. Hepatitis C virus induced up-regulation of microRNA-27: A novel mechanism for hepatic steatosis. Hepatology 2014, 59, 98-108.
75. Selzner, N.; Levy, G. Measurements of serial plasma levels of albumin mRNA for management of patients post transplant: Does it add value? Clin. Biochem. 2013, 46, 1311-1312.
76. 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, e45652.
77. Köberle, V.; Kronenberger, B.; Pleli, T.; Trojan, J.; Imelmann, E.; Peveling-Oberhag, J.; Welker, M.-W.; Elhendawy, M.; Zeuzem, S.; Piiper, A.; et al. Serum microRNA-1 and microRNA-122 are prognostic markers in patients with hepatocellular carcinoma. Eur. J. Cancer 2013, 49, 3442-3449.
78. Kirschner, M. B.; Kao, S. C.; Edelman, J. J.; Armstrong, N. J.; Vallely, M. P.; van Zandwijk, N.; Reid, G. Haemolysis during sample preparation alters microRNA content of plasma. PLoS One 2011, 6, e24145.
79. McDonald, J. S.; Milosevic, D.; Reddi, H. V.; Grebe, S. K.; Algeciras-Schimnich, A. Analysis of circulating microRNA: Preanalytical and analytical challenges. Clin. Chem. 2011, 57, 833-840.
80. Pritchard, C. C.; Kroh, E.; Wood, B.; Arroyo, J. D.; Dougherty, K. J.; Miyaji, M. M.; Tait, J. F.; Tewari, M. Blood cell origin of circulating microRNAs: A cautionary note for cancer biomarker studies. Cancer Prev. Res. 2012, 5, 492-497.
81. Blondal, T.; Jensby Nielsen, S.; Baker, A.; Andreasen, D.; Mouritzen, P.; Wrang Teilum, M.; Dahlsveen, I. K. Assessing sample and miRNA profile quality in serum and plasma or other biofluids. Methods 2013, 59, 164-169.
82. Mitchell, P. S.; Parkin, R. K.; Kroh, E. M.; Fritz, B. R.; Wyman, S. K.; Pogosova-Agadjanyan, E. L.; Peterson, A.; Noteboom, J.; O'Briant, K. C.; Allen, A.; et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc. Natl. Acad. Sci. USA 2008, 105, 10513-10518.
83. Wang, K.; Yuan, Y.; Cho, J.-H.; McClarty, S.; Baxter, D.; Galas, D. J. Comparing the MicroRNA Spectrum between Serum and Plasma. PLoS One 2012, 7, e41561.
84. Kim, D.-J.; Linnstaedt, S.; Palma, J.; Park, J. C.; Ntrivalas, E.; Kwak-Kim, J. Y. H.; Gilman-Sachs, A.; Beaman, K.; Hastings, M. L.; Martin, J. N.; et al. Plasma components affect accuracy of circulating cancer-related microRNA quantitation. J. Mol. Diagn. JMD 2012, 14, 71-80.
85. Wong, S. C. C.; Ma, B. B. Y.; Lai, P. B. S.; Ng, S. S. M.; Lee, J. F. Y.; Hui, E. P.; Lam, M. Y. Y.; Chan, C. M. L.; Chan, A. T. C. The effect of centrifugation on circulating mRNA quantitation opens up a new scenario in expression profiling from patients with metastatic colorectal cancer. Clin. Biochem. 2007, 40, 1277-1284.
86. Schageman, J.; Zeringer, E.; Li, M.; Barta, T.; Lea, K.; Gu, J.; Magdaleno, S.; Setterquist, R.; Vlassov, A. V. The complete exosome workflow solution: From isolation to characterization of RNA cargo. BioMed. Res. Int. 2013, 2013, doi: 10. 1155/2013/253957.
87. Holford, N. C.; Sandhu, H. S.; Thakkar, H.; Butt, A. N.; Swaminathan, R. Stability of β-Actin mRNA in Plasma. Ann. N. Y. Acad. Sci. 2008, 1137, 108-111.
88. Page, K.; Guttery, D. S.; Zahra, N.; Primrose, L.; Elshaw, S. R.; Pringle, J. H.; Blighe, K.; Marchese, S. D.; Hills, A.; Woodley, L.; et al. Influence of plasma processing on recovery and analysis of circulating nucleic acids. PLoS One 2013, 8, e77963.
89. Sourvinou, I. S.; Markou, A.; Lianidou, E. S. Quantification of circulating miRNAs in plasma: Effect of preanalytical and analytical parameters on their isolation and stability. J. Mol. Diagn. 2013, 15, 827-834.
90. Chen, X.; Ba, Y.; Ma, L.; Cai, X.; Yin, Y.; Wang, K.; Guo, J.; Zhang, Y.; Chen, J.; Guo, X.; et al. Characterization of microRNAs in serum: A novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res. 2008, 18, 997-1006.
91. Jensen, S. G.; Lamy, P.; Rasmussen, M. H.; Ostenfeld, M. S.; Dyrskjøt, L.; Orntoft, T. F.; Andersen, C. L. Evaluation of two commercial global miRNA expression profiling platforms for detection of less abundant miRNAs. BMC Genomics 2011, 12, doi: 10. 1186/1471-2164-12-435.
92. Zhu, H.-T.; Dong, Q.-Z.; Wang, G.; Zhou, H.-J.; Ren, N.; Jia, H.-L.; Ye, Q.-H.; Qin, L.-X. Identification of suitable reference genes for qRT-PCR analysis of circulating microRNAs in hepatitis B virus-infected patients. Mol. Biotechnol. 2011, 50, 49-56.
93. Schwarzenbach, H.; Hoon, D. S. B.; Pantel, K. Cell-Free nucleic acids as biomarkers in cancer patients. Nat. Rev. Cancer 2011, 11, 426-437.
94. Duttagupta, R.; Jiang, R.; Gollub, J.; Getts, R. C.; Jones, K. W. Impact of cellular miRNAs on circulating miRNA biomarker signatures. PLoS One 2011, 6, e20769.
95. Kirschner, M. B.; van Zandwijk, N.; Reid, G. Cell-Free microRNAs: Potential biomarkers in need of standardized reporting. Front. Genet. 2013, 4, doi: 10. 3389/fgene. 2013. 00056.
96. Bustin, S. A.; Benes, V.; Garson, J.; Hellemans, J.; Huggett, J.; Kubista, M.; Mueller, R.; Nolan, T.; Pfaffl, M. W.; Shipley, G.; et al. The need for transparency and good practices in the qPCR literature. Nat. Methods 2013, 10, 1063-1067.
97. Bustin, S. A.; Benes, V.; Garson, J. A.; Hellemans, J.; Huggett, J.; Kubista, M.; Mueller, R.; Nolan, T.; Pfaffl, M. W.; Shipley, G. L.; et al. The MIQE guidelines: Minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 2009, 55, 611-622.