Inhibition of HBV replication in vivo using helper-dependent adenovirus vectors to deliver antiviral RNA interference expression cassettes

Organziation WH. Hepatitis B. Factsheet number 204 (Updated July 2013. Accessed 11 June 2014.) Available from http://www.who.int/mediacentre/factsheets/fs204/en/index.html.

Arbuthnot P. , Kew M. Hepatitis B virus and hepatocellular carcinoma. Int J Exp Pathol 2001; 82: 77–100.

Keeffe E.B. , Dieterich D.T. , Han S.H. A treatment algorithm for the management of chronic hepatitis B virus infection in the United States: an update. Clin Gastroenterol Hepatol 2006; 4: 936–962.

Keeffe E.B. , Dieterich D.T. , Pawlotsky J.M. , Benhamou Y. Chronic hepatitis B: preventing, detecting, and managing viral resistance. Clin Gastroenterol Hepatol 2008; 6: 268–274.

Arbuthnot P. Harnessing RNA interference for the treatment of viral infections. Drug News Perspect 2010; 23: 341–350.

Chen Y. , Cheng G. , Mahato R.I. RNAi for treating hepatitis B viral infection. Pharm Res 2008; 25: 72–86.

Ivacik D. , Ely A. , Arbuthnot P. Countering hepatitis B virus infection using RNAi: how far are we from the clinic? Rev Med Virol 2011; 21: 383–396.

McCaffrey A.P. RNA interference inhibitors of hepatitis B virus. Ann N Y Acad Sci 2009; 1175: 15–23.

Castanotto D. , Rossi J.J. The promises and pitfalls of RNA-interference-based therapeutics. Nature 2009; 457: 426–433.

Brummelkamp T.R. , Bernards R. , Agami R. A system for stable expression of short interfering RNAs in mammalian cells. Science 2002; 296: 550–553.

Lee N.S. , Dohjima T. , Bauer G. Expression of small interfering RNAs targeted against HIV-1 rev transcripts in human cells. Nat Biotechnol 2002; 20: 500–505.

Miyagishi M. , Taira K. U6 promoter driven siRNAs with four uridine 3′ overhangs efficiently suppress targeted gene expression in mammalian cells. Nat Biotechnol 2002; 20: 497–500.

Paul C.P. , Good P.D. , Winer I. , Engelke D.R. Effective expression of small interfering RNA in human cells. Nat Biotechnol 2002; 20: 505–508.

Mowa M.B. , Crowther C. , Arbuthnot P. Therapeutic potential of adenoviral vectors for delivery of expressed RNAi activators. Expert Opin Drug Deliv 2010; 7: 1373–1385.

Schnell M.A. , Zhang Y. , Tazelaar J. Activation of innate immunity in nonhuman primates following intraportal administration of adenoviral vectors. Mol Ther 2001; 3: 708–722.

Taniguchi M. , Seino K. , Nakayama T. The NKT cell system: bridging innate and acquired immunity. Nat Immunol 2003; 4: 1164–1165.

Chen Q. , Wei H. , Sun R. , Zhang J. , Tian Z. Therapeutic RNA silencing of Cys-X3-Cys chemokine ligand 1 gene prevents mice from adenovirus vector-induced acute liver injury. Hepatology 2008; 47: 648–658.

Guidotti L.G. , Chisari F.V. Noncytolytic control of viral infections by the innate and adaptive immune response. Annu Rev Immunol 2001; 19: 65–91.

Carmona S. , Ely A. , Crowther C. Effective inhibition of HBV replication in vivo by anti-HBx short hairpin RNAs. Mol Ther 2006; 13: 411–421.

Crowther C. , Ely A. , Hornby J. Efficient inhibition of hepatitis B virus replication in vivo, using polyethylene glycol-modified adenovirus vectors. Hum Gene Ther 2008; 19: 1325–1331.

Uprichard S.L. , Boyd B. , Althage A. , Chisari F V. Clearance of hepatitis B virus from the liver of transgenic mice by short hairpin RNAs. Proc Natl Acad Sci U S A 2005; 102: 773–778.

Mowa M.B. , Crowther C. , Ely A. , Arbuthnot P. Efficient silencing of hepatitis B virus by helper-dependent adenovirus vector-mediated delivery of antiviral primary micro RNA shuttles. Micro RNA 2012; 1: 19–25.

McCoy R.D. , Davidson B.L. , Roessler B.J. Pulmonary inflammation induced by incomplete or inactivated adenoviral particles. Hum Gene Ther 1995; 6: 1553–1560.

Raper S.E. , Yudkoff M. , Chirmule N. A pilot study of in vivo liver-directed gene transfer with an adenoviral vector in partial ornithine transcarbamylase deficiency. Hum Gene Ther 2002; 13: 163–175.

Yei S. , Mittereder N. , Wert S. , Whitsett J.A. , Wilmott R.W. , Trapnell B.C. In vivo evaluation of the safety of adenovirus-mediated transfer of the human cystic fibrosis transmembrane conductance regulator cDNA to the lung. Hum Gene Ther 1994; 5: 731–744.

Rauschhuber C. , Xu H. , Salazar F.H. , Marion P.L. , Ehrhardt A. Exploring gene-deleted adenoviral vectors for delivery of short hairpin RNAs and reduction of hepatitis B virus infection in mice. J Gene Med 2008; 10: 878–889.

Marion P.L. , Salazar F.H. , Liittschwager K. A transgenic mouse lineage useful for testing antivirals targeting hepatitis B virus. In Schinazi R.F. , Sommadossi J-P , Rich C.M. (Editors). Frontiers in viral hepatitis. Amsterdam: Elsevier Science 2003; pp. 197–202.

He T.C. , Zhou S. , da Costa L.T. , Yu J. , Kinzler K.W. , Vogelstein B. A simplified system for generating recombinant adenoviruses. Proc Natl Acad Sci U S A 1998; 95: 2509–2514.

Palmer D. , Ng P. Improved system for helper-dependent adenoviral vector production. Mol Ther 2003; 8: 846–852.

Mok H. , Palmer D.J. , Ng P. , Barry M.A. Evaluation of polyethylene glycol modification of first-generation and helper-dependent adenoviral vectors to reduce innate immune responses. Mol Ther 2005; 11: 66–79.

Weinberg M.S. , Ely A. , Barichievy S. Specific inhibition of HBV replication in vitro and in vivo with expressed long hairpin RNA. Mol Ther 2007; 15: 534–541.

Jiang H. , Wang Z. , Serra D. , Frank M.M. , Amalfitano A. Recombinant adenovirus vectors activate the alternative complement pathway, leading to the binding of human complement protein C3 independent of anti-ad antibodies. Mol Ther 2004; 10: 1140–1142.

He L. , Hakimi J. , Salha D. , Miron I. , Dunn P. , Radvanyi L. A sensitive flow cytometry-based cytotoxic T-lymphocyte assay through detection of cleaved caspase 3 in target cells. J Immunol Methods 2005; 304: 43–59.

Ely A. , Naidoo T. , Mufamadi S. , Crowther C. , Arbuthnot P. Expressed anti-HBV primary microRNA shuttles inhibit viral replication efficiently in vitro and in vivo. Mol Ther 2008; 16: 1105–1112.

Jooss K. , Yang Y. , Fisher K.J. , Wilson J.M. Transduction of dendritic cells by DNA viral vectors directs the immune response to transgene products in muscle fibers. J Virol 1998; 72: 4212–4223.

Brunetti-Pierri N. , Clarke C. , Mane V. Phenotypic correction of ornithine transcarbamylase deficiency using low dose helper-dependent adenoviral vectors. J Gene Med 2008; 10: 890–896.

Brunetti-Pierri N. , Stapleton G.E. , Law M. Efficient, long-term hepatic gene transfer using clinically relevant HDAd doses by balloon occlusion catheter delivery in nonhuman primates. Mol Ther 2009; 17: 327–333.

Zaiss A.K. , Machado H.B. , Herschman H.R. The influence of innate and pre-existing immunity on adenovirus therapy. J Cell Biochem 2009; 108: 778–790.

Cotter M.J. , Muruve D.A. The induction of inflammation by adenovirus vectors used for gene therapy. Front Biosci 2005; 10: 1098–1105.

Liu Q. , Zaiss A.K. , Colarusso P. The role of capsid-endothelial interactions in the innate immune response to adenovirus vectors. Hum Gene Ther 2003; 14: 627–643.

McCaffrey A.P. , Fawcett P. , Nakai H. The host response to adenovirus, helper-dependent adenovirus, and adeno-associated virus in mouse liver. Mol Ther 2008; 16: 931–941.

Muruve D.A. The innate immune response to adenovirus vectors. Hum Gene Ther 2004; 15: 1157–1166.

Muruve D.A. , Cotter M.J. , Zaiss A.K. Helper-dependent adenovirus vectors elicit intact innate but attenuated adaptive host immune responses in vivo. J Virol 2004; 78: 5966–5972.

Arbuthnot P. , Longshaw V. , Naidoo T. , Weinberg M.S. Opportunities for treating chronic hepatitis B and C virus infection using RNA interference. J Viral Hepat 2007; 14: 447–459.

Brunetti-Pierri N. , Ng P. Helper-dependent adenoviral vectors for liver-directed gene therapy. Hum Mol Genet 2011; 20: R7–R13.

Brunetti-Pierri N. , Ng T. , Iannitti D.A. Improved hepatic transduction, reduced systemic vector dissemination, and long-term transgene expression by delivering helper-dependent adenoviral vectors into the surgically isolated liver of nonhuman primates. Hum Gene Ther 2006; 17: 391–404.

Grimm D. , Streetz K.L. , Jopling C.L. Fatality in mice due to oversaturation of cellular microRNA/short hairpin RNA pathways. Nature 2006; 441: 537–541.

Danielsson A. , Elgue G. , Nilsson B.M. An ex vivo loop system models the toxicity and efficacy of PEGylated and unmodified adenovirus serotype 5 in whole human blood. Gene Ther 2010; 17: 752–762.

Schiffer J.T. , Aubert M. , Weber N.D. , Mintzer E. , Stone D. , Jerome K.R. Targeted DNA mutagenesis for the cure of chronic viral infections. J Virol 2012; 86: 8920–8936.

Moolla N. , Kew M. , Arbuthnot P. Regulatory elements of hepatitis B virus transcription. J Viral Hepat 2002; 9: 323–331.