Hepatitis B Virus-Specific miRNAs and Argonaute2 Play a Role in the Viral Life Cycle

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Hayes, C Nelson ^a,b   Akamatsu, Sakura ^a,b   Tsuge, Masataka ^a   Miki, Daiki ^a,b   Akiyama, Rie ^a,b   Abe, Hiromi ^a,b   Ochi, Hidenori ^a,b   Hiraga, Nobuhiko ^a,b   Imamura, Michio ^a,b   Takahashi, Shoichi ^a,b   Aikata, Hiroshi ^a   Kawaoka, Tomokazu ^a,b   Kawakami, Yoshiiku ^a,b   Ohishi, Waka ^a,c   Chayama, Kazuaki ^a,b  

^a HIROSHIMA UNIVERSITY   (Japan)

^b RIKEN   (Japan)

^c RADIATION EFFECTS RESEARCH FOUNDATION   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ARGONAUTE 2 PROTEIN; HEPATITIS B CORE ANTIGEN; HEPATITIS B SURFACE ANTIGEN; MICRORNA; MICRORNA 122; MICRORNA 22; MICRORNA 99A; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; ARGONAUTE PROTEIN; EIF2C2 PROTEIN, HUMAN; PROTEIN BINDING;

ADOLESCENT; ADULT; AGED; ARTICLE; CELL COMPARTMENTALIZATION; CELL NUCLEUS; CELL STRAIN HEPG2; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; FEMALE; GENETIC TRANSFECTION; HEPATITIS B; HEPATITIS B VIRUS; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INTERMETHOD COMPARISON; LIFE CYCLE; LIVER BIOPSY; MAJOR CLINICAL STUDY; MALE; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; SPECIES DIFFERENCE; TISSUE LEVEL; UPREGULATION; VIRUS REPLICATION; BLOOD; CASE CONTROL STUDY; CELL LINE; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; MIDDLE AGED; MOLECULAR GENETICS; PHYSIOLOGY; RNA INTERFERENCE; SIGNAL TRANSDUCTION; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; ARGONAUTE PROTEINS; CASE-CONTROL STUDIES; CELL LINE; FEMALE; GENE EXPRESSION PROFILING; HEPATITIS B; HEPATITIS B CORE ANTIGENS; HEPATITIS B SURFACE ANTIGENS; HEPATITIS B VIRUS; HUMANS; MALE; MICRORNAS; MIDDLE AGED; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; RNA INTERFERENCE; SIGNAL TRANSDUCTION; VIRUS REPLICATION; YOUNG ADULT;

EID: 84867597435     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0047490     Document Type: Article

References (51)

1. Fields BN, Knipe DM, Howley PM (2007) Fields virology. Philadelphia: Wolters Kluwer Health/Lippincott Williams & Wilkins.
2. McMahon BJ, (2009) The natural history of chronic hepatitis B virus infection. Hepatology 49: S45-55.
3. Brechot C, Kremsdorf D, Soussan P, Pineau P, Dejean A, et al. (2010) Hepatitis B virus (HBV)-related hepatocellular carcinoma (HCC): molecular mechanisms and novel paradigms. Pathologie-biologie 58: 278-287.
4. Ji F, Yang B, Peng X, Ding H, You H, et al. (2011) Circulating microRNAs in hepatitis B virus-infected patients. Journal of viral hepatitis 18: e242-251.
5. Novellino L, Rossi RL, Bonino F, Cavallone D, Abrignani S, et al. (2012) Circulating Hepatitis B Surface Antigen Particles Carry Hepatocellular microRNAs. PloS one 7: e31952.
6. Qi P, Cheng SQ, Wang H, Li N, Chen YF, et al. (2011) Serum MicroRNAs as Biomarkers for Hepatocellular Carcinoma in Chinese Patients with Chronic Hepatitis B Virus Infection. PloS one 6: e28486.
7. Ura S, Honda M, Yamashita T, Ueda T, Takatori H, et al. (2009) Differential microRNA expression between hepatitis B and hepatitis C leading disease progression to hepatocellular carcinoma. Hepatology 49: 1098-1112.
8. Zhang GL, Li YX, Zheng SQ, Liu M, Li X, et al. (2010) Suppression of hepatitis B virus replication by microRNA-199a-3p and microRNA-210. Antiviral research 88: 169-175.
9. Chen Y, Cheng G, Mahato RI, (2008) RNAi for treating hepatitis B viral infection. Pharmaceutical research 25: 72-86.
10. Xi Y, Nakajima G, Gavin E, Morris CG, Kudo K, et al. (2007) Systematic analysis of microRNA expression of RNA extracted from fresh frozen and formalin-fixed paraffin-embedded samples. RNA 13: 1668-1674.
11. Turchinovich A, Weiz L, Langheinz A, Burwinkel B, (2011) Characterization of extracellular circulating microRNA. Nucleic acids research 39: 7223-7233.
12. Liu AM, Zhang C, Burchard J, Fan ST, Wong KF, et al. (2011) Global regulation on microRNA in hepatitis B virus-associated hepatocellular carcinoma. Omics: a journal of integrative biology 15: 187-191.
13. Bala S, Marcos M, Szabo G, (2009) Emerging role of microRNAs in liver diseases. World journal of gastroenterology: WJG 15: 5633-5640.
14. Desmet VJ, Gerber M, Hoofnagle JH, Manns M, Scheuer PJ, (1994) Classification of chronic hepatitis: diagnosis, grading and staging. Hepatology 19: 1513-1520.
15. Tsuge M, Hiraga N, Takaishi H, Noguchi C, Oga H, et al. (2005) Infection of human hepatocyte chimeric mouse with genetically engineered hepatitis B virus. Hepatology 42: 1046-1054.
16. Weibrecht I, Leuchowius KJ, Clausson CM, Conze T, Jarvius M, et al. (2010) Proximity ligation assays: a recent addition to the proteomics toolbox. Expert review of proteomics 7: 401-409.
17. Cullen BR, (2011) Viruses and microRNAs: RISCy interactions with serious consequences. Genes & development 25: 1881-1894.
18. Wang Y, Kato N, Jazag A, Dharel N, Otsuka M, et al. (2006) Hepatitis C virus core protein is a potent inhibitor of RNA silencing-based antiviral response. Gastroenterology 130: 883-892.
19. Ren M, Qin D, Li K, Qu J, Wang L, et al. (2012) Correlation between hepatitis B virus protein and microRNA processor Drosha in cells expressing HBV. Antiviral research.
20. Wang S, Qiu L, Yan X, Jin W, Wang Y, et al. (2011) Loss of MiR-122 expression in patients with hepatitis B enhances hepatitis B virus replication through cyclin G1 modulated P53 activity. Hepatology 55: 730-741.
21. Hu J, Xu Y, Hao J, Wang S, Li C, et al. (2012) MiR-122 in hepatic function and liver diseases. Protein & cell 3: 364-371.
22. 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 biology 1: 106-113.
23. Narbus CM, Israelow B, Sourisseau M, Michta ML, Hopcraft SE, et al. (2011) HepG2 cells expressing microRNA miR-122 support the entire hepatitis C virus life cycle. Journal of virology 85: 12087-12092.
24. 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. Proceedings of the National Academy of Sciences of the United States of America 109: 941-946.
25. Wilson JA, Zhang C, Huys A, Richardson CD, (2011) Human Ago2 is required for efficient microRNA 122 regulation of hepatitis C virus RNA accumulation and translation. Journal of virology 85: 2342-2350.
26. 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.
27. 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. The FASEB journal: official publication of the Federation of American Societies for Experimental Biology 25: 4511-4521.
28. 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. Biochemical and biophysical research communications 398: 771-777.
29. Waidmann O, Bihrer V, Pleli T, Farnik H, Berger A, et al. (2012) Serum microRNA-122 levels in different groups of patients with chronic hepatitis B virus infection. Journal of viral hepatitis 19: e58-65.
30. Heermann KH, Goldmann U, Schwartz W, Seyffarth T, Baumgarten H, et al. (1984) Large surface proteins of hepatitis B virus containing the pre-s sequence. Journal of virology 52: 396-402.
31. Patient R, Hourioux C, Sizaret PY, Trassard S, Sureau C, et al. (2007) Hepatitis B virus subviral envelope particle morphogenesis and intracellular trafficking. Journal of virology 81: 3842-3851.
32. Bouttier M, Saumet A, Peter M, Courgnaud V, Schmidt U, et al. (2012) Retroviral GAG proteins recruit AGO2 on viral RNAs without affecting RNA accumulation and translation. Nucleic acids research 40: 775-786.
33. Eulalio A, Behm-Ansmant I, Schweizer D, Izaurralde E, (2007) P-body formation is a consequence, not the cause, of RNA-mediated gene silencing. Molecular and cellular biology 27: 3970-3981.
34. Lian SL, Li S, Abadal GX, Pauley BA, Fritzler MJ, et al. (2009) The C-terminal half of human Ago2 binds to multiple GW-rich regions of GW182 and requires GW182 to mediate silencing. RNA 15: 804-813.
35. Giner A, Lakatos L, Garcia-Chapa M, Lopez-Moya JJ, Burgyan J, (2010) Viral protein inhibits RISC activity by argonaute binding through conserved WG/GW motifs. PLoS pathogens 6: e1000996.
36. Johnston M, Geoffroy MC, Sobala A, Hay R, Hutvagner G, (2010) HSP90 protein stabilizes unloaded argonaute complexes and microscopic P-bodies in human cells. Molecular biology of the cell 21: 1462-1469.
37. Pare JM, Tahbaz N, Lopez-Orozco J, LaPointe P, Lasko P, et al. (2009) Hsp90 regulates the function of argonaute 2 and its recruitment to stress granules and P-bodies. Molecular biology of the cell 20: 3273-3284.
38. Lan YT, Li J, Liao W, Ou J, (1999) Roles of the three major phosphorylation sites of hepatitis B virus core protein in viral replication. Virology 259: 342-348.
39. Rudel S, Wang Y, Lenobel R, Korner R, Hsiao HH, et al. (2011) Phosphorylation of human Argonaute proteins affects small RNA binding. Nucleic acids research 39: 2330-2343.
40. Zeng Y, Sankala H, Zhang X, Graves PR, (2008) Phosphorylation of Argonaute 2 at serine-387 facilitates its localization to processing bodies. The Biochemical journal 413: 429-436.
41. Sir D, Tian Y, Chen WL, Ann DK, Yen TS, et al. (2010) The early autophagic pathway is activated by hepatitis B virus and required for viral DNA replication. Proceedings of the National Academy of Sciences of the United States of America 107: 4383-4388.
42. Li J, Liu Y, Wang Z, Liu K, Wang Y, et al. (2011) Subversion of cellular autophagy machinery by hepatitis B virus for viral envelopment. Journal of virology 85: 6319-6333.
43. Sir D, Ann DK, Ou JH (2010) Autophagy by hepatitis B virus and for hepatitis B virus. Autophagy 6.
44. Potenza N, Papa U, Mosca N, Zerbini F, Nobile V, et al. (2011) Human microRNA hsa-miR-125a-5p interferes with expression of hepatitis B virus surface antigen. Nucleic acids research 39: 5157-5163.
45. Zhang X, Zhang E, Ma Z, Pei R, Jiang M, et al. (2011) Modulation of hepatitis B virus replication and hepatocyte differentiation by MicroRNA-1. Hepatology 53: 1476-1485.
46. Hu W, Wang X, Ding X, Li Y, Zhang X, et al. (2012) MicroRNA-141 Represses HBV Replication by Targeting PPARA. PloS one 7: e34165.
47. Li D, Liu X, Lin L, Hou J, Li N, et al. (2011) MicroRNA-99a inhibits hepatocellular carcinoma growth and correlates with prognosis of patients with hepatocellular carcinoma. The Journal of biological chemistry 286: 36677-36685.
48. Turcatel G, Rubin N, El-Hashash A, Warburton D, (2012) MIR-99a and MIR-99b modulate TGF-beta induced epithelial to mesenchymal plasticity in normal murine mammary gland cells. PloS one 7: e31032.
49. Murata M, Matsuzaki K, Yoshida K, Sekimoto G, Tahashi Y, et al. (2009) Hepatitis B virus X protein shifts human hepatic transforming growth factor (TGF)-beta signaling from tumor suppression to oncogenesis in early chronic hepatitis B. Hepatology. 49: 1203-1217.
50. Xu D, Takeshita F, Hino Y, Fukunaga S, Kudo Y, et al. (2011) miR-22 represses cancer progression by inducing cellular senescence. The Journal of cell biology 193: 409-424.
51. Jiang R, Deng L, Zhao L, Li X, Zhang F, et al. (2011) miR-22 promotes HBV-related hepatocellular carcinoma development in males. Clinical cancer research: an official journal of the American Association for Cancer Research 17: 5593-5603.