An efficient antiviral strategy for targeting hepatitis B virus genome using transcription activator-like effector nucleases

Molecular Therapy

Volumn 22, Issue 2, 2014, Pages 303-311

  Chen, Jieliang ^a   Zhang, Wen ^a   Lin, Junyu ^a   Wang, Fan ^a   Wu, Min ^a   Chen, Cuncun ^a   Zheng, Ye ^a   Peng, Xiuhua ^a   Li, Jianhua ^a   Yuan, Zhenghong ^a  

^a FUDAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; CIRCULAR DNA; COVALENTLY CLOSED CIRCULAR DNA; HEPATITIS B CORE ANTIGEN; HEPATITIS B SURFACE ANTIGEN; HEPATITIS B(E) ANTIGEN; NUCLEASE; PREGENOMIC RNA; TRANSCRIPTION ACTIVATOR LIKE EFFECTOR NUCLEASE; UNCLASSIFIED DRUG; VIRUS RNA; ANTIVIRUS AGENT; DEOXYRIBONUCLEASE; PROTEIN BINDING; VIRUS PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY PRODUCTION; ANTIVIRAL ACTIVITY; ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; DNA STRUCTURE; DRUG POTENTIATION; GENE REPRESSION; GENE TARGETING; HEPATITIS B VIRUS; HEPATOMA CELL; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; VIRUS GENOME; VIRUS INACTIVATION; ADMINISTRATION AND DOSAGE; ANIMAL; CELL LINE; DISEASE MODEL; GENE VECTOR; GENETICS; HEPATITIS B, CHRONIC; METABOLISM; PLASMID; VIROLOGY;

DNA VIRUSES; HEPATITIS B VIRUS;

ANIMALS; ANTIVIRAL AGENTS; CELL LINE; DEOXYRIBONUCLEASES; DISEASE MODELS, ANIMAL; DNA, CIRCULAR; GENETIC VECTORS; GENOME, VIRAL; HEPATITIS B VIRUS; HEPATITIS B, CHRONIC; HUMANS; INTERFERON-ALPHA; MICE; PLASMIDS; PROTEIN BINDING; VIRAL PROTEINS;

EID: 84895908706     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2013.212     Document Type: Article

References (49)

1. Lok, AS and McMahon, BJ (2007). Chronic hepatitis B. Hepatology 45: 507-539.
2. Lee, JY and Locarnini, S (2004). Hepatitis B virus: pathogenesis, viral intermediates, and viral replication. Clin Liver Dis 8: 301-320.
3. Levrero, M, Pollicino, T, Petersen, J, Belloni, L, Raimondo, G and Dandri, M (2009). Control of cccDNA function in hepatitis B virus infection. J Hepatol 51: 581-592.
4. Schiffer, JT, Aubert, M, Weber, ND, Mintzer, E, Stone, D and Jerome, KR (2012). Targeted DNA mutagenesis for the cure of chronic viral infections. J Virol 86: 8920-8936.
5. Zhu, Y, Yamamoto, T, Cullen, J, Saputelli, J, Aldrich, CE, Miller, DS et al. (2001). Kinetics of hepadnavirus loss from the liver during inhibition of viral DNA synthesis. J Virol 75: 311-322.
6. Belloni, L, Pollicino, T, De Nicola, F, Guerrieri, F, Raffa, G, Fanciulli, M et al. (2009). Nuclear HBx binds the HBV minichromosome and modifies the epigenetic regulation of cccDNA function. Proc Natl Acad Sci USA 106: 19975-19979.
7. Moscou, MJ and Bogdanove, AJ (2009). A simple cipher governs DNA recognition by TAL effectors. Science 326: 1501.
8. Miller, JC, Tan, S, Qiao, G, Barlow, KA, Wang, J, Xia, DF et al. (2011). A TALE nuclease architecture for efficient genome editing. Nat Biotechnol 29: 143-148.
9. Bedell, VM, Wang, Y, Campbell, JM, Poshusta, TL, Starker, CG, Krug, RG 2nd et al. (2012). In vivo genome editing using a high-efficiency TALEN system. Nature 491: 114-118.
10. Cade, L, Reyon, D, Hwang, WY, Tsai, SQ, Patel, S, Khayter, C et al. (2012). Highly efficient generation of heritable zebrafish gene mutations using homo- and heterodimeric TALENs. Nucleic Acids Res 40: 8001-8010.
11. Mussolino, C, Morbitzer, R, Lütge, F, Dannemann, N, Lahaye, T and Cathomen, T (2011). A novel TALE nuclease scaffold enables high genome editing activity in combination with low toxicity. Nucleic Acids Res 39: 9283-9293.
12. Bowyer, SM and Sim, JG (2000). Relationships within and between genotypes of hepatitis B virus at points across the genome: footprints of recombination in certain isolates. J Gen Virol 81(Pt 2): 379-392.
13. Zhou, T, Guo, H, Guo, JT, Cuconati, A, Mehta, A and Block, TM (2006). Hepatitis B virus e antigen production is dependent upon covalently closed circular (ccc) DNA in HepAD38 cell cultures and may serve as a cccDNA surrogate in antiviral screening assays. Antiviral Res 72: 116-124.
14. Waugh, DS and Sauer, RT (1993). Single amino acid substitutions uncouple the DNA binding and strand scission activities of Fok I endonuclease. Proc Natl Acad Sci USA 90: 9596-9600.
15. Zoulim, F (2012). Are novel combination therapies needed for chronic hepatitis B? Antiviral Res 96: 256-259.
16. Chen, J, Wu, M, Zhang, X, Zhang, W, Zhang, Z, Chen, L et al. (2013). Hepatitis B virus polymerase impairs interferon-a-induced STA T activation through inhibition of importin-a5 and protein kinase C-d. Hepatology 57: 470-482.
17. Doong, SL, Tsai, CH, Schinazi, RF, Liotta, DC and Cheng, YC (1991). Inhibition of the replication of hepatitis B virus in vitro by 2′,3′-dideoxy-3′-thiacytidine and related analogues. Proc Natl Acad Sci USA 88: 8495-8499.
18. Belloni, L, Allweiss, L, Guerrieri, F, Pediconi, N, Volz, T, Pollicino, T et al. (2012). IFN-a inhibits HBV transcription and replication in cell culture and in humanized mice by targeting the epigenetic regulation of the nuclear cccDNA minichromosome. J Clin Invest 122: 529-537.
19. Delmas, J, Schorr, O, Jamard, C, Gibbs, C, Trépo, C, Hantz, O et al. (2002). Inhibitory effect of adefovir on viral DNA synthesis and covalently closed circular DNA formation in duck hepatitis B virus-infected hepatocytes in vivo and in vitro. Antimicrob Agents Chemother 46: 425-433.
20. Shi, L, Li, S, Shen, F, Li, H, Qian, S, Lee, DH et al. (2012). Characterization of nucleosome positioning in hepadnaviral covalently closed circular DNA minichromosomes. J Virol 86: 10059-10069.
21. Wu, J, Meng, Z, Jiang, M, Pei, R, Trippler, M, Broering, R et al. (2009). Hepatitis B virus suppresses toll-like receptor-mediated innate immune responses in murine parenchymal and nonparenchymal liver cells. Hepatology 49: 1132-1140.
22. Wang, S, Chen, Z, Hu, C, Qian, F, Cheng, Y, Wu, M et al. (2013). Hepatitis B virus surface antigen selectively inhibits TLR2 ligand-induced IL-12 production in monocytes/macrophages by interfering with JNK activation. J Immunol 190: 5142-5151.
23. Revill, P and Yuan, Z (2013). New insights into how HBV manipulates the innate immune response to establish acute and persistent infection. Antivir Ther (Lond) 18: 1-15.
24. Yu, S, Chen, J, Wu, M, Chen, H, Kato, N and Yuan, Z (2010). Hepatitis B virus polymerase inhibits RIG-I- and Toll-like receptor 3-mediated beta interferon induction in human hepatocytes through interference with interferon regulatory factor 3 activation and dampening of the interaction between TBK1/IKKepsilon and DDX3. J Gen Virol 91(Pt 8): 2080-2090.
25. Chang, J, Block, TM and Guo, JT (2012). The innate immune response to hepatitis B virus infection: implications for pathogenesis and therapy. Antiviral Res 96: 405-413.
26. Bonvin, M, Achermann, F, Greeve, I, Stroka, D, Keogh, A, Inderbitzin, D et al. (2006). Interferon-inducible expression of APOBEC3 editing enzymes in human hepatocytes and inhibition of hepatitis B virus replication. Hepatology 43: 1364-1374.
27. Li, J, Liu, K, Liu, Y, Xu, Y, Zhang, F, Yang, H et al. (2013) Exosomes mediate the cell-to-cell transmission of IFN-a-induced antiviral activity. Nat Immunol 14(8): 793-803.
28. Gordien, E, Rosmorduc, O, Peltekian, C, Garreau, F, Bréchot, C and Kremsdorf, D (2001). Inhibition of hepatitis B virus replication by the interferon-inducible MxA protein. J Virol 75: 2684-2691.
29. Li, J, Lin, S, Chen, Q, Peng, L, Zhai, J, Liu, Y et al. (2010). Inhibition of hepatitis B virus replication by MyD88 involves accelerated degradation of pregenomic RNA and nuclear retention of pre-S/S RNAs. J Virol 84: 6387-6399.
30. Randall, RE and Goodbourn, S (2008). Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J Gen Virol 89(Pt 1): 1-47.
31. Fernández, M, Quiroga, JA and Carreño, V (2003). Hepatitis B virus downregulates the human interferon-inducible MxA promoter through direct interaction of precore/core proteins. J Gen Virol 84(Pt 8): 2073-2082.
32. Rosmorduc, O, Sirma, H, Soussan, P, Gordien, E, Lebon, P, Horisberger, M et al. (1999). Inhibition of interferon-inducible MxA protein expression by hepatitis B virus capsid protein. J Gen Virol 80 (Pt 5): 1253-1262.
33. Houghton, JA, Morton, CL, Adkins, DA and Rahman, A (1993). Locus of the interaction among 5-fluorouracil, leucovorin, and interferon-alpha 2a in colon carcinoma cells. Cancer Res 53: 4243-4250.
34. Sung, JJ, Wong, ML, Bowden, S, Liew, CT, Hui, AY, Wong, VW et al. (2005). Intrahepatic hepatitis B virus covalently closed circular DNA can be a predictor of sustained response to therapy. Gastroenterology 128: 1890-1897.
35. Uprichard, SL, Boyd, B, Althage, A and Chisari, FV (2005). Clearance of hepatitis B virus from the liver of transgenic mice by short hairpin RNAs. Proc Natl Acad Sci USA 102: 773-778.
36. Meng, Z, Xu, Y, Wu, J, Tian, Y, Kemper, T, Bleekmann, B et al. (2008). Inhibition of hepatitis B virus gene expression and replication by endoribonuclease-prepared siRNA. J Virol Methods 150: 27-33.
37. Xia, C, Chen, YC, Gong, H, Zeng, W, Vu, GP, Trang, P et al. (2013). Inhibition of hepatitis B virus gene expression and replication by ribonuclease P. Mol Ther 21: 995-1003.
38. McMahon, MA, Rahdar, M and Porteus, M (2012). Gene editing: not just for translation anymore. Nat Methods 9: 28-31.
39. Cong, L, Ran, FA, Cox, D, Lin, S, Barretto, R, Habib, N et al. (2013). Multiplex genome engineering using CRISPR/Cas systems. Science 339: 819-823.
40. Zimmerman, KA, Fischer, KP, Joyce, MA and Tyrrell, DL (2008). Zinc finger proteins designed to specifically target duck hepatitis B virus covalently closed circular DNA inhibit viral transcription in tissue culture. J Virol 82: 8013-8021.
41. Cradick, TJ, Keck, K, Bradshaw, S, Jamieson, AC and McCaffrey, AP (2010). Zinc-finger nucleases as a novel therapeutic strategy for targeting hepatitis B virus DNAs. Mol Ther 18: 947-954.
42. Crispe, IN, Giannandrea, M, Klein, I, John, B, Sampson, B and Wuensch, S (2006). Cellular and molecular mechanisms of liver tolerance. Immunol Rev 213: 101-118.
43. Cuestas, ML, Mathet, VL, Oubiña, JR and Sosnik, A (2010). Drug delivery systems and liver targeting for the improved pharmacotherapy of the hepatitis B virus (HBV) infection. Pharm Res 27: 1184-1202.
44. Wooddell, CI, Rozema, DB, Hossbach, M, John, M, Hamilton, HL, Chu, Q et al. (2013). Hepatocyte-targeted RNAi therapeutics for the treatment of chronic hepatitis B virus infection. Mol Ther 21: 973-985.
45. Chen, CC, Sun, CP, Ma, HI, Fang, CC, Wu, PY, Xiao, X et al. (2009). Comparative study of anti-hepatitis B virus RNA interference by double-stranded adeno-associated virus serotypes 7, 8, and 9. Mol Ther 17: 352-359.
46. Li, Q, Kay, MA, Finegold, M, Stratford-Perricaudet, LD and Woo, SL (1993). Assessment of recombinant adenoviral vectors for hepatic gene therapy. Hum Gene Ther 4: 403-409.
47. Schiffer, JT, Swan, DA, Stone, D and Jerome, KR (2013). Predictors of hepatitis B cure using gene therapy to deliver DNA cleavage enzymes: a mathematical modeling approach. PLoS Comput Biol 9: e1003131.
48. Wang, YX, Wen, YM and Nassal, M (2012). Carbonyl J acid derivatives block protein priming of hepadnaviral P protein and DNA-dependent DNA synthesis activity of hepadnaviral nucleocapsids. J Virol 86: 10079-10092.
49. Xu, L, Zhao, P, Mariano, A and Han, R (2013). Targeted Myostatin Gene Editing in Multiple Mammalian Species Directed by a Single Pair of TALE Nucleases. Mol Ther Nucleic Acids 2: e112.