microRNA-122 Abundance in Hepatocellular Carcinoma and Non-Tumor Liver Tissue from Japanese Patients with Persistent HCV versus HBV Infection

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Spaniel, Carolyn ^a,b   Honda, Masao ^c   Selitsky, Sara R ^a   Yamane, Daisuke ^a   Shimakami, Tetsuro ^c   Kaneko, Shuichi ^c   Lanford, Robert E ^d   Lemon, Stanley M ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b University of Texas Medical Branch School of Medicine   (United States)

^c KANAZAWA UNIVERSITY GRADUATE SCHOOL OF MEDICAL SCIENCE   (Japan)

^d SOUTHWEST FOUNDATION FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON; INTERLEUKIN 28; MICRORNA 122; PEGINTERFERON ALPHA; RIBAVIRIN;

ADULT; AGED; ANIMAL TISSUE; ARTICLE; CANCER TISSUE; CHIMPANZEE; CLINICAL ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; CORRELATION ANALYSIS; DISEASE ASSOCIATION; FEMALE; GENE; GENOTYPE; HEPATITIS B; HEPATITIS B VIRUS; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; HUMAN TISSUE; IL28B GENE; IMMUNE RESPONSE; JAPANESE; LIVER CARCINOGENESIS; LIVER CELL CARCINOMA; LIVER PARENCHYMA; LIVER RESECTION; MALE; NONHUMAN; PREDICTION; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SINGLE NUCLEOTIDE POLYMORPHISM; TREATMENT RESPONSE; VIRUS REPLICATION;

AGED; ANIMALS; ASIAN CONTINENTAL ANCESTRY GROUP; CARCINOMA, HEPATOCELLULAR; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HEPATITIS B; HEPATITIS C; HUMANS; INTERFERONS; LIVER; LIVER NEOPLASMS; MALE; MICRORNAS; MIDDLE AGED; PAN TROGLODYTES;

EID: 84885155219     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0076867     Document Type: Article

References (65)

1. Ferlay JSH, Bray F, Forman D, Mathers C, Parkin DM, (2010). ancer Incidence Mortal Worldwide IARC CancerBase No. 10.
2. Wang XGJ, Thorgeirsson S, editors (2011) Molecular Genetics of Liver Neoplasia. New York: Springer Verlag Science. pp. pp. 51-73.
3. Lok AS, Everhart JE, Wright EC, Di Bisceglie AM, Kim HY, et al. (2011) Maintenance peginterferon therapy and other factors associated with hepatocellular carcinoma in patients with advanced hepatitis C. Gastroenterology 140: 840-849. doi:10.1053/j.gastro.2010.11.050. PubMed: 21129375.
4. White D, El-Serag H, (2011) Epidemiology of Hepatocellular Carcinoma. In: Wang X, [(surname)], Thorgeirsson S, eds. Molecular Genetics of Liver Neoplasia. New York, NY: Springer Verlag Science. pp. pp. 51-73.
5. Kiyosawa K, Umemura T, Ichijo T, Matsumoto A, Yoshizawa K, et al. (2004) Hepatocellular carcinoma: recent trends in Japan. Gastroenterology 127: S17-S26. doi:10.1053/j.gastro.2004.03.068. PubMed: 15508082.
6. McGivern DR, Lemon SM, (2011) Virus-specific mechanisms of carcinogenesis in hepatitis C virus associated liver cancer. Oncogene 30: 1969-1983. doi:10.1038/onc.2010.594. PubMed: 21258404.
7. Tsai WL, Chung RT, (2010) Viral hepatocarcinogenesis. Oncogene 29: 2309-2324. doi:10.1038/onc.2010.36. PubMed: 20228847.
8. Nakamoto Y, Guidotti LG, Kuhlen CV, Fowler P, Chisari FV, (1998) Immune pathogenesis of hepatocellular carcinoma. J Exp Med 188: 341-350. doi:10.1084/jem.188.2.341. PubMed: 9670046.
9. Lerat H, Honda M, Beard MR, Loesch K, Sun J, et al. (2002) Steatosis and liver cancer in transgenic mice expressing the structural and nonstructural proteins of hepatitis C virus. Gastroenterology 122: 352-365. doi:10.1053/gast.2002.31001. PubMed: 11832450.
10. McGivern DR, Lemon SM, (2009) Tumor suppressors, chromosomal instability, and hepatitis C virus-associated liver cancer. Annu Rev Pathol 4: 399-415. doi:10.1146/annurev.pathol.4.110807.092202. PubMed: 18928409.
11. Wilson RC, Doudna JA, (2013) Molecular mechanisms of RNA interference. Annu Rev Biophys 42: 217-239. doi:10.1146/annurev-biophys-083012-130404. PubMed: 23654304.
12. Djuranovic S, Nahvi A, Green R, (2011) A parsimonious model for gene regulation by miRNAs. Science 331: 550-553. doi:10.1126/science.1191138. PubMed: 21292970.
13. Meijer HA, Kong YW, Lu WT, Wilczynska A, Spriggs RV, et al. (2013) Translational repression and eIF4A2 activity are critical for microRNA-mediated gene regulation. Science 340: 82-85. doi:10.1126/science.1231197. PubMed: 23559250.
14. Chang J, Nicolas E, Marks D, Sander C, Lerro A, et al. (2004) miR-122, a mammalian liver-specific microRNA, is processed from hcr mRNA and may downregulate the high affinity cationic amino acid transporter CAT-1. RNA Biol 1: 106-113. doi:10.4161/rna.1.2.1066. PubMed: 17179747.
15. Lanford RE, Hildebrandt-Eriksen ES, Petri A, Persson R, Lindow M, et al. (2010) Therapeutic silencing of microRNA-122 in primates with chronic hepatitis C virus infection. Science 327: 198-201. doi:10.1126/science.1178178. PubMed: 19965718.
16. Bai S, Nasser MW, Wang B, Hsu SH, Datta J, et al. (2009) MicroRNA-122 inhibits tumorigenic properties of hepatocellular carcinoma cells and sensitizes these cells to sorafenib. J Biol Chem 284: 32015-32027. doi:10.1074/jbc.M109.016774. PubMed: 19726678.
17. Lewis AP, Jopling CL, (2010) Regulation and biological function of the liver-specific miR-122. Biochem Soc Trans 38: 1553-1557. doi:10.1042/BST0381553. PubMed: 21118125.
18. Jopling CL, Yi M, Lancaster AM, Lemon SM, Sarnow P, (2005) Modulation of hepatitis C virus RNA abundance by a liver-specific MicroRNA. Science 309: 1577-1581. doi:10.1126/science.1113329. PubMed: 16141076.
19. Shimakami T, Yamane D, Jangra RK, Kempf BJ, Spaniel C, et al. (2012) Stabilization of hepatitis C virus RNA by an Ago2-miR-122 complex. Proc Natl Acad Sci U S A 109: 941-946. doi:10.1073/pnas.1112263109. PubMed: 22215596.
20. Li Y, Masaki T, Yamane D, McGivern DR, Lemon SM, (2013) Competing and noncompeting activities of miR-122 and the 5' exonuclease Xrn1 in regulation of hepatitis C virus replication. Proc Natl Acad Sci U S A 110: 1881-1886. doi:10.1073/pnas.1213515110. PubMed: 23248316.
21. Kutay H, Bai S, Datta J, Motiwala T, Pogribny I, et al. (2006) Downregulation of miR-122 in the rodent and human hepatocellular carcinomas. J Cell Biochem 99: 671-678. doi:10.1002/jcb.20982. PubMed: 16924677.
22. Gramantieri L, Ferracin M, Fornari F, Veronese A, Sabbioni S, et al. (2007) Cyclin G1 is a target of miR-122a, a microRNA frequently down-regulated in human hepatocellular carcinoma. Cancer Res 67: 6092-6099. doi:10.1158/0008-5472.CAN-06-4607. PubMed: 17616664.
23. Hou J, Lin L, Zhou W, Wang Z, Ding G, et al. (2011) Identification of miRNomes in human liver and hepatocellular carcinoma reveals miR-199a/b-3p as therapeutic target for hepatocellular carcinoma. Cancer Cell 19: 232-243. doi:10.1016/j.ccr.2011.01.001. PubMed: 21316602.
24. Varnholt H, Drebber U, Schulze F, Wedemeyer I, Schirmacher P, et al. (2008) MicroRNA gene expression profile of hepatitis C virus-associated hepatocellular carcinoma. Hepatology 47: 1223-1232. PubMed: 18307259.
25. Coulouarn C, Factor VM, Andersen JB, Durkin ME, Thorgeirsson SS, (2009) Loss of miR-122 expression in liver cancer correlates with suppression of the hepatic phenotype and gain of metastatic properties. Oncogene 28: 3526-3536. doi:10.1038/onc.2009.211. PubMed: 19617899.
26. Bedossa P, Poynard T, (1996) An algorithm for the grading of activity in chronic hepatitis C. The METAVIR Cooperative Study Group. Hepatology 24: 289-293. doi:10.1002/hep.510240201. PubMed: 8690394.
27. Desmet VJ, Gerber M, Hoofnagle JH, Manns M, Scheuer PJ, (1994) Classification of Chronic Hepatitis: Diagnosis, Grading and Staging. Hepatology 19: 1513-1520. doi:10.1002/hep.1840190629. PubMed: 8188183.
28. Honda M, Sakai A, Yamashita T, Nakamoto Y, Mizukoshi E, et al. (2010) Hepatic ISG expression is associated with genetic variation in interleukin 28B and the outcome of IFN therapy for chronic hepatitis C. Gastroenterology 139: 499-509. doi:10.1053/j.gastro.2010.04.049. PubMed: 20434452.
29. Schroeder A, Mueller O, Stocker S, Salowsky R, Leiber M, et al. (2006) The RIN: an RNA integrity number for assigning integrity values to RNA measurements. BMC Mol Biol 7: 3. doi:10.1186/1471-2199-7-3. PubMed: 16448564.
30. Lanford RE, Guerra B, Lee H, Averett DR, Pfeiffer B, et al. (2003) Antiviral effect and virus-host interactions in response to alpha interferon, gamma interferon, poly(i)-poly(c), tumor necrosis factor alpha, and ribavirin in hepatitis C virus subgenomic replicons. J Virol 77: 1092-1104. doi:10.1128/JVI.77.2.1092-1104.2003. PubMed: 12502825.
31. Nagaoki Y, Hyogo H, Aikata H, Tanaka M, Naeshiro N, et al. (2012) Recent trend of clinical features in patients with hepatocellular carcinoma. Hepatol Res 42: 368-375. doi:10.1111/j.1872-034X.2011.00929.x. PubMed: 22151896.
32. Wang Y, Lu Y, Toh ST, Sung WK, Tan P, et al. (2010) Lethal-7 is down-regulated by the hepatitis B virus x protein and targets signal transducer and activator of transcription 3. J Hepatol 53: 57-66. doi:10.1016/j.jhep.2009.12.043. PubMed: 20447714.
33. Hatziapostolou M, Polytarchou C, Aggelidou E, Drakaki A, Poultsides GA, et al. (2011) An HNF4alpha-miRNA inflammatory feedback circuit regulates hepatocellular oncogenesis. Cell 147: 1233-1247. doi:10.1016/j.cell.2011.10.043. PubMed: 22153071.
34. Trebicka J, Anadol E, Elfimova N, Strack I, Roggendorf M, et al. (2013) Hepatic and serum levels of miR-122 after chronic HCV-induced fibrosis. J Hepatol 58: 234-239. doi:10.1016/S0168-8278(13)60572-3. PubMed: 23085648.
35. Morita K, Taketomi A, Shirabe K, Umeda K, Kayashima H, et al. (2011) Clinical significance and potential of hepatic microRNA-122 expression in hepatitis C. Liver Int 31: 474-484. doi:10.1111/j.1478-3231.2010.02433.x. PubMed: 21199296.
36. Sarasin-Filipowicz M, Krol J, Markiewicz I, Heim MH, Filipowicz W, (2009) Decreased levels of microRNA miR-122 in individuals with hepatitis C responding poorly to interferon therapy. Nat Med 15: 31-33. doi:10.1038/nm.1902. PubMed: 19122656.
37. Tanaka Y, Nishida N, Sugiyama M, Kurosaki M, Matsuura K, et al. (2009) Genome-wide association of IL28B with response to pegylated interferon-alpha and ribavirin therapy for chronic hepatitis C. Nat Genet 41: 1105-1109. doi:10.1038/ng.449. PubMed: 19749757.
38. Yoshizawa H, (2002) Hepatocellular carcinoma associated with hepatitis C virus infection in Japan: projection to other countries in the foreseeable future. Oncology 62 (Suppl 1):: 8-17. doi:10.1159/000048270. PubMed: 11868791.
39. Sarasin-Filipowicz M, Oakeley EJ, Duong FH, Christen V, Terracciano L, et al. (2008) Interferon signaling and treatment outcome in chronic hepatitis C. Proc Natl Acad Sci U S A 105: 7034-7039. doi:10.1073/pnas.0707882105. PubMed: 18467494.
40. Urban TJ, Thompson AJ, Bradrick SS, Fellay J, Schuppan D, et al. (2010) IL28B genotype is associated with differential expression of intrahepatic interferon-stimulated genes in patients with chronic hepatitis C. Hepatology 52: 1888-1896. doi:10.1002/hep.23912. PubMed: 20931559.
41. Abe H, Hayes CN, Ochi H, Maekawa T, Tsuge M, et al. (2011) IL28 variation affects expression of interferon stimulated genes and peg-interferon and ribavirin therapy. J Hepatol 54: 1094-1101. doi:10.1002/hep.24499. PubMed: 21145800.
42. Elyakim E, Sitbon E, Faerman A, Tabak S, Montia E, et al. (2010) hsa-miR-191 is a candidate oncogene target for hepatocellular carcinoma therapy. Cancer Res 70: 8077-8087. doi:10.1158/0008-5472.CAN-10-1313. PubMed: 20924108.
43. Jangra RK, Yi M, Lemon SM, (2010) miR-122 regulation of hepatitis C virus translation and infectious virus production. J Virol 84: 6615-6625. doi:10.1128/JVI.00417-10. PubMed: 20427538.
44. Fornari F, Gramantieri L, Giovannini C, Veronese A, Ferracin M, et al. (2009) MiR-122/cyclin G1 interaction modulates p53 activity and affects doxorubicin sensitivity of human hepatocarcinoma cells. Cancer Res 69: 5761-5767. doi:10.1158/0008-5472.CAN-08-4797. PubMed: 19584283.
45. Tsai WC, Hsu SD, Hsu CS, Lai TC, Chen SJ, et al. (2012) MicroRNA-122 plays a critical role in liver homeostasis and hepatocarcinogenesis. J Clin Invest 122: 2884-2897. doi:10.1172/JCI63455. PubMed: 22820290.
46. Hsu SH, Wang B, Kota J, Yu J, Costinean S, et al. (2012) Essential metabolic, anti-inflammatory, and anti-tumorigenic functions of miR-122 in liver. J Clin Invest 122: 2871-2883. doi:10.1172/JCI63539. PubMed: 22820288.
47. Burns DM, D'Ambrogio A, Nottrott S, Richter JD, (2011) CPEB and two poly(A) polymerases control miR-122 stability and p53 mRNA translation. Nature 473: 105-108. doi:10.1038/nature09908. PubMed: 21478871.
48. Lardizábal MN, Nocito AL, Daniele SM, Ornella LA, Palatnik JF, et al. (2012) Reference genes for real-time PCR quantification of microRNAs and messenger RNAs in rat models of hepatotoxicity. PLOS ONE 7: e36323. doi:10.1371/journal.pone.0036323. PubMed: 22563491.
49. Norman KL, Sarnow P, (2010) Modulation of hepatitis C virus RNA abundance and the isoprenoid biosynthesis pathway by microRNA miR-122 involves distinct mechanisms. J Virol 84: 666-670. doi:10.1128/JVI.01156-09. PubMed: 19846523.
50. Li Y, Masaki T, Lemon SM, (2013) miR-122 and the Hepatitis C RNA genome: More than just stability. RNA Biol 10: 919-24. PubMed: 23770926.
51. Janssen HL, Reesink HW, Lawitz EJ, Zeuzem S, Rodriguez-Torres M, et al. (2013) Treatment of HCV Infection by Targeting MicroRNA. N Engl J Med, 368: 1685-94. PubMed: 23534542.
52. McGivern DR, Lemon SM, (2011) Virus-specific mechanisms of carcinogenesis in hepatitis C virus associated liver cancer. Oncogene 30: 1969-1983. doi:10.1038/onc.2010.594. PubMed: 21258404.
53. Chen Y, Shen A, Rider PJ, Yu Y, Wu K, et al. (2011) 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 25: 4511-4521. doi:10.1096/fj.11-187781. PubMed: 21903935.
54. Wang S, Qiu L, Yan X, Jin W, Wang Y, et al. (2012) Loss of microRNA 122 expression in patients with hepatitis B enhances hepatitis B virus replication through cyclin G(1)-modulated P53 activity. Hepatology 55: 730-741. doi:10.1002/hep.24809. PubMed: 22105316.
55. Liu WH, Yeh SH, Chen PJ, (2011) Role of microRNAs in hepatitis B virus replication and pathogenesis. Biochim Biophys Acta 1809: 678-685. doi:10.1016/j.bbagrm.2011.04.008. PubMed: 21565290.
56. Qiu L, Fan H, Jin W, Zhao B, Wang Y, et al. (2010) miR-122-induced down-regulation of HO-1 negatively affects miR-122-mediated suppression of HBV. Biochem Biophys Res Commun 398: 771-777. doi:10.1016/j.bbrc.2010.07.021. PubMed: 20633528.
57. Liang Y, Shilagard T, Xiao SY, Snyder N, Lau D, et al. (2009) Visualizing hepatitis C virus infections in human liver by two-photon microscopy. Gastroenterology 137: 1448-1458. doi:10.1053/j.gastro.2009.07.050. PubMed: 19632233.
58. Jung CJ, Iyengar S, Blahnik KR, Ajuha TP, Jiang JX, et al. (2011) Epigenetic modulation of miR-122 facilitates human embryonic stem cell self-renewal and hepatocellular carcinoma proliferation. PLOS ONE 6: e27740. doi:10.1371/journal.pone.0027740. PubMed: 22140464.
59. Arai E, Ushijima S, Gotoh M, Ojima H, Kosuge T, et al. (2009) Genome-wide DNA methylation profiles in liver tissue at the precancerous stage and in hepatocellular carcinoma. Int J Cancer 125: 2854-2862. doi:10.1002/ijc.24708. PubMed: 19569176.
60. Jung JK, Park SH, Jang KL, (2010) Hepatitis B virus X protein overcomes the growth-inhibitory potential of retinoic acid by downregulating retinoic acid receptor-beta2 expression via DNA methylation. J Gen Virol 91: 493-500. doi:10.1099/vir.0.015149-0. PubMed: 19828754.
61. Hsia CC, Thorgeirsson SS, Tabor E, (1994) Expression of hepatitis B surface and core antigens and transforming growth factor-alpha in "oval cells" of the liver in patients with hepatocellular carcinoma. J Med Virol 43: 216-221. doi:10.1002/jmv.1890430304. PubMed: 7523580.
62. Pedersen IM, Cheng G, Wieland S, Volinia S, Croce CM, et al. (2007) Interferon modulation of cellular microRNAs as an antiviral mechanism. Nature 449: 919-922. doi:10.1038/nature06205. PubMed: 17943132.
63. Wieland S, Thimme R, Purcell RH, Chisari FV, (2004) Genomic analysis of the host response to hepatitis B virus infection. Proc Natl Acad Sci U S A 101: 6669-6674. doi:10.1073/pnas.0401771101. PubMed: 15100412.
64. Bigger CB, Guerra B, Brasky KM, Hubbard G, Beard MR, et al. (2004) Intrahepatic gene expression during chronic hepatitis C virus infection in chimpanzees. J Virol 78: 13779-13792. doi:10.1128/JVI.78.24.13779-13792.2004. PubMed: 15564486.
65. Lanford RE, Guerra B, Bigger CB, Lee H, Chavez D, et al. (2007) Lack of response to exogenous interferon-alpha in the liver of chimpanzees chronically infected with hepatitis C virus. Hepatology 46: 999-1008. doi:10.1002/hep.21776. PubMed: 17668868.