564
Views
10
CrossRef citations to date
0
Altmetric
Review

Gene editing technology as an approach to the treatment of liver diseases

&
Pages 595-608 | Received 28 Dec 2015, Accepted 22 Feb 2016, Published online: 21 Mar 2016

References

  • Ozaki I, Zern MA, Liu S, et al. Ribozyme-mediated specific gene replacement of the alpha1-antitrypsin gene in human hepatoma cells. J Hepatol. 1999;31(1):53–60.
  • Scaglioni P, Melegari M, Takahashi M, et al. Use of dominant negative mutants of the hepadnaviral core protein as antiviral agents. Hepatology. 1996;24(5):1010–1017. doi:10.1002/hep.510240506.
  • Jacobs F, Gordts SC, Muthuramu I, et al. The liver as a target organ for gene therapy: state of the art, challenges, and future perspectives. Pharmaceuticals (Basel). 2012;5(12):1372–1392. doi:10.3390/ph5121372.
  • Urnov FD, Rebar EJ, Holmes MC, et al. Genome editing with engineered zinc finger nucleases. Nat Rev Genet. 2010;11(9):636–646. doi:10.1038/nrg2842.
  • Roth DB, Wilson JH. Relative rates of homologous and nonhomologous recombination in transfected DNA. Proc Natl Acad Sci USA. 1985;82(10):3355–3359.
  • Brugmans L, Kanaar R, Essers J. Analysis of DNA double-strand break repair pathways in mice. Mutat Res. 2007;614(1–2):95–108. doi:10.1016/j.mrfmmm.2006.01.022.
  • Miller DG, Wang P-R, Petek LM, et al. Gene targeting in vivo by adeno-associated virus vectors. Nat Biotechnol. 2006;24(8):1022–1026. doi:10.1038/nbt1231.
  • Paulk NK, Wursthorn K, Wang Z, et al. Adeno-associated virus gene repair corrects a mouse model of hereditary tyrosinemia in vivo. Hepatology. 2010;51(4):1200–1208. doi:10.1002/hep.23481.
  • Yáñez RJ, Porter ACG. Therapeutic gene targeting. Gene Ther. 1998;5(2):149–159. doi:10.1038/sj.gt.3300601.
  • Gamper HB Jr, Cole-Strauss A, Metz R, et al. A plausible mechanism for gene correction by chimeric oligonucleotides. Biochemistry. 2000;39(19):5808–5816.
  • Huen MS, Lu LY, Liu DP, et al. Active transcription promotes single-stranded oligonucleotide mediated gene repair. Biochem Biophys Res Commun. 2007;353(1):33–39. doi:10.1016/j.bbrc.2006.11.146.
  • Lu I-L, Lin C-Y, Lin S-B, et al. Correction/mutation of acid alpha-d-glucosidase gene by modified single-stranded oligonucleotides: in vitro and in vivo studies. Gene Ther. 2003;10(22):1910–1916. doi:10.1038/sj.gt.3302096.
  • Nakamura M, Ando Y, Nagahara S, et al. Targeted conversion of the transthyretin gene in vitro and in vivo. Gene Ther. 2004;11(10):838–846. doi:10.1038/sj.gt.3302228.
  • Kren BT, Wong -PY-P, Steer CJ. Correction of the orntithine transcarbamylase point mutation in neonatal spfash mice using single-stranded oligonucleotides. Mol Ther. 2008;16:s323.
  • Ricciardi AS, McNeer NA, Anandalingam KK, et al. Targeted genome modification via triple helix formation. Methods Mol Biol. 2014;1176:89–106. doi:10.1007/978-1-4939-0992-6_8.
  • Chan PP, Glazer PM. Triplex DNA: fundamentals, advances, and potential applications for gene therapy. J Mol Med (Berl). 1997;75(4):267–282.
  • Majumdar A, Khorlin A, Dyatkina N, et al. Targeted gene knockout mediated by triple helix forming oligonucleotides. Nat Genet. 1998;20(2):212–214. doi:10.1038/2530.
  • Vasquez KM, Wang G, Havre PA, et al. Chromosomal mutations induced by triplex-forming oligonucleotides in mammalian cells. Nucleic Acids Res. 1999;27(4):1176–1181.
  • Cheng K, Ye Z, Guntaka RV, et al. Biodistribution and hepatic uptake of triplex-forming oligonucleotides against type alpha1(I) collagen gene promoter in normal and fibrotic rats. Mol Pharm. 2005;2(3):206–217. doi:10.1021/mp050012x.
  • Ye Z, Houssein HS, Mahato RI. Bioconjugation of oligonucleotides for treating liver fibrosis. Oligonucleotides. 2007;17(4):349–404. doi:10.1089/oli.2007.0097.
  • Yang N, Singh S, Mahato RI. Targeted TFO delivery to hepatic stellate cells. J Control Release. 2011;155(2):323–330. doi:10.1016/j.jconrel.2011.06.037.
  • Singhal G, Akhter MZ, Stern DF, et al. DNA triplex-mediated inhibition of MET leads to cell death and tumor regression in hepatoma. Cancer Gene Ther. 2011;18(7):520–530. doi:10.1038/cgt.2011.21.
  • Bibikova M, Carroll D, Segal DJ, et al. Stimulation of homologous recombination through targeted cleavage by chimeric nucleases. Mol Cell Biol. 2001;21:289–297. doi:10.1128/MCB.21.1.289-297.2001.
  • Porteus MH, Carroll D. Gene targeting using zinc finger nucleases. Nat Biotechnol. 2005;23(8):967–973. doi:10.1038/nbt1125.
  • Hermann M, Maeder ML, Rector K, et al. Evaluation of OPEN zinc finger nucleases for direct gene targeting of the ROSA26 locus in mouse embryos. PLoS ONE. 2012;7(9):e41796. doi:10.1371/journal.pone.0041796.
  • Wilson KA, McEwen AE, Pruett-Miller SM, et al. Expanding the repertoire of target sites for zinc finger nuclease-mediated genome modification. Mol Ther Nucleic Acids. 2013;2(4):e88. doi:10.1038/mtna.2013.13.
  • Camenisch TD, Brilliant MH, Segal DJ. Critical parameters for genome editing using zinc finger nucleases. Mini Rev Med Chem. 2008;8(7):669–676.
  • Moehle EA, Rock JM, Lee YL, et al. Targeted gene addition into a specified location in the human genome using designed zinc finger nucleases. Proc Natl Acad Sci USA. 2007;104(9):3055–3060. doi:10.1073/pnas.0611478104.
  • Minczuk M, Papworth MA, Miller JC, et al. Development of a single-chain, quasi-dimeric zinc-finger nuclease for the selective degradation of mutated human mitochondrial DNA. Nucleic Acids Res. 2008;36(12):3926–3938. doi:10.1093/nar/gkn313.
  • Naldini L. Ex vivo gene transfer and correction for cell-based therapies. Nat Rev Genet. 2011;12(5):301–315. doi:10.1038/nrg2985.
  • Li H, Haurigot V, Doyon Y, et al. In vivo genome editing restores haemostasis in a mouse model of haemophilia. Nature. 2011;475(7355):217–221. doi:10.1038/nature10177.
  • Anguela XM, Sharma R, Doyon Y, et al. Robust ZFN-mediated genome editing in adult hemophilic mice. Blood. 2013;122(19):3283–3287. doi:10.1182/blood-2013-04-497354.
  • Yusa K, Rashid ST, Strick-Marchand H, et al. Targeted gene correction of α1-antitrypsin deficiency in induced pluripotent stem cells. Nature. 2011;478(7369):391–394. doi:10.1038/nature10424.
  • Sharma R, Anguela XM, Doyon Y, et al. In vivo genome editing of the albumin locus as a platform for protein replacement therapy. Blood. 2015;126(15):1777–1784. doi:10.1182/blood-2014-12-615492.
  • Abarrategui-Pontes C, Créneguy A, Thinard R, et al. Codon swapping of zinc finger nucleases confers expression in primary cells and in vivo from a single lentiviral vector. Curr Gene Ther. 2014;14(5):365–376.
  • Boch J, Scholze H, Schornack S, et al. Breaking the code of DNA binding specificity of TAL-type III effectors. Science. 2009;326(5959):1509–1512. doi:10.1126/science.1178811.
  • Hockemeyer D, Wang H, Kiani S, et al. Genetic engineering of human pluripotent cells using TALE nucleases. Nat Biotechnol. 2011;29(8):731–734. doi:10.1038/nbt.1927.
  • Joung JK, Sander JD. TALENs: a widely applicable technology for targeted genome editing. Nat Rev Mol Cell Biol. 2013;14:49–55. doi:10.1038/nrm3486.
  • Miller JC, Tan S, Qiao G, et al. A TALE nuclease architecture for efficient genome editing. Nat Biotechnol. 2011;29(2):143–148. doi:10.1038/nbt.1755.
  • Boch J, Bonas U. Xanthomonas AvrBs3 family-type III effectors: discovery and function. Annu Rev Phytopathol. 2010;48:419–436. doi:10.1146/annurev-phyto-080508-081936.
  • Bollag RJ, Waldman AS, Liskay RM. Homologous recombination in mammalian cells. Annu Rev Genet. 1989;23:199–225. doi:10.1146/annurev.ge.23.120189.001215.
  • Byrne SM, Ortiz L, Mali P, et al. Multi-kilobase homozygous targeted gene replacement in human induced pluripotent stem cells. Nucleic Acids Res. 2015;43(3):e21. doi:10.1093/nar/gku1246.
  • Porro F, Bockor L, De Caneva A, et al. Generation of Ugt1-deficient murine liver cell lines using TALEN technology. PLoS ONE. 2014;9(8):e104816. doi:10.1371/journal.pone.0104816.
  • Sung PS, Murayama A, Kang W, et al. Hepatitis C virus entry is impaired by claudin-1 downregulation in diacylglycerol acyltransferase-1-deficient cells. J Virol. 2014;88(16):9233–9244. doi:10.1128/JVI.01428-14.
  • Sun N, Zhao H. Transcription activator-like effector nucleases (TALENs): a highly efficient and versatile tool for genome editing. Biotechnol Bioeng. 2013;110(7):1811–1821. doi:10.1002/bit.24890.
  • Horvath P, Barrangou R. CRISPR/Cas, the immune system of bacteria and archaea. Science. 2010;327(5962):167–170. doi:10.1126/science.1179555.
  • Wiedenheft B, Sternberg SH, Doudna JA. RNA-guided genetic silencing systems in bacteria and archaea. Nature. 2012;482(7385):331–338. doi:10.1038/nature10886.
  • Barrangou R, Fremaux C, Deveau H, et al. CRISPR provides acquired resistance against viruses in prokaryotes. Science. 2007;315(5819):1709–1712. doi:10.1126/science.1138140.
  • Garneau JE, Dupuis MÈ, Villion M, et al. The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature. 2010;468(7320):67–71. doi:10.1038/nature09523.
  • Bhaya D, Davison M, Barrangou R. CRISPR-Cas systems in bacteria and archaea: versatile small RNAs for adaptive defense and regulation. Ann Rev Genet. 2011;45:273–297. doi:10.1146/annurev-genet-110410-132430.
  • Deltcheva E, Chylinski K, Sharma CM, et al. CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature. 2011;471(7340):602–607. doi:10.1038/nature09886.
  • Charpentier E, Doudna JA. Biotechnology: rewriting a genome. Nature. 2013;495(7439):50–51. doi:10.1038/495050a.
  • Jinek M, Chylinski K, Fonfara I, et al. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science. 2012;337(6096):816–821. doi:10.1126/science.1225829.
  • Sternberg SH, Redding S, Jinek M, et al. DNA interrogation by the CRISPR RNA-guided endonuclease Cas9. Nature. 2014;507(7490):62–67. doi:10.1038/nature13011.
  • Cho SW, Kim S, Kim JM, et al. Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease. Nat Biotechnol. 2013;31(3):230–232. doi:10.1038/nbt.2507.
  • Cong L, Ran FA, Cox D, et al. Multiplex genome engineering using CRISPR/Cas systems. Science. 2013;339(6121):819–823. doi:10.1126/science.1231143.
  • Mali P, Yang L, Esvelt KM, et al. RNA-guided human genome engineering via Cas9. Science. 2013;339(6121):823–826. doi:10.1126/science.1232033.
  • Yin H, Xue W, Chen S, et al. Genome editing with Cas9 in adult mice corrects a disease mutation and phenotype. Nat Biotechnol. 2014;32(6):551–553. doi:10.1038/nbt.2884.
  • Xue W, Chen S, Yin H, et al. CRISPR-mediated direct mutation of cancer genes in the mouse liver. Nature. 2014;514(7522):380–384. doi:10.1038/nature13589.
  • Platt RJ, Chen S, Zhou Y, et al. CRISPR-Cas9 knockin mice for genome editing and cancer modeling. Cell. 2014;159(2):440–455. doi:10.1016/j.cell.2014.09.014.
  • Fu Y, Foden JA, Khayter C, et al. High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat Biotechnol. 2013;31(9):822–826. doi:10.1038/nbt.2623.
  • Pattanayak V, Lin S, Guilinger JP, et al. High-throughput profiling of off-target DNA cleavage reveals RNA-programmed Cas9 nuclease specificity. Nat Biotechnol. 2013;31(9):839–843. doi:10.1038/nbt.2673.
  • Mali P, Esvelt KM, Church GM. Cas9 as a versatile tool for engineering biology. Nat Methods. 2013;10(10):957–963. doi:10.1038/nmeth.2649.
  • Ran FA, Hsu PD, Lin C-Y, et al. Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell. 2013;154(6):1380–1389. doi:10.1016/j.cell.2013.08.021.
  • Tan EP, Li Y, Velasco-Herrera MD, et al. Off-target assessment of CRISPR-cas9 guiding RNAs in human iPS and mouse ES cells. Genesis. 2015;53(2):225–236. doi:10.1002/dvg.22835.
  • Wang D, Mou H, Li S, et al. Adenovirus-mediated somatic genome editing of Pten by CRISPR/Cas9 in mouse liver in spite of Cas9-specific immune responses. Hum Gene Ther. 2015;26(7):432–442. doi:10.1089/hum.2015.087.
  • Zetsche B, Gootenberg JS, Abudayyeh OO, et al. Cpf1 Is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell. 2015;163(3):759–771. doi:10.1016/j.cell.2015.09.038.
  • Nakade S, Tsubota T, Sakane Y, et al. Microhomology-mediated end-joining-dependent integration of donor DNA in cells and animals using TALENs and CRISPR/Cas9. Nat Commun. 2014;5:5560. doi:10.1038/ncomms6560.
  • Sakuma T, Takenaga M, Kawabe Y, et al. Homologous recombination-independent large gene cassette knock-in in CHO cells using TALEN and MMEJ-directed donor plasmids. Int J Mol Sci. 2015;16(10):23849–23866. doi:10.3390/ijms161023849.
  • Hisano Y, Sakuma T, Nakade S, et al. Precise in-frame integration of exogenous DNA mediated by CRISPR/Cas9 system in zebrafish. Sci Rep. 2015;5:8841. doi:10.1038/srep08841.
  • Xu L, Mei M, Ma X, et al. High expression reduces an antibody response after neonatal gene therapy with B domain-deleted human factor VIII in mice. J Thromb Haemost. 2007;5(9):1805–1812. doi:10.1111/j.1538-7836.2007.02629.x.
  • Mátrai J, Cantore A, Bartholomae CC, et al. Hepatocyte-targeted expression by integrase-defective lentiviral vectors induces antigen-specific tolerance in mice with low genotoxic risk. Hepatology. 2011;53(5):1696–1707. doi:10.1002/hep.24230.
  • Kennedy EM, Bassit LC, Mueller H, et al. Suppression of hepatitis B virus DNA accumulation in chronically infected cells using a bacterial CRISPR/Cas RNA-guided DNA endonuclease. Virology. 2015;476:196–205. doi:10.1016/j.virol.2014.12.001.
  • Liu X, Hao R, Chen S, et al. Inhibition of hepatitis B virus by the CRISPR/Cas9 system via targeting the conserved regions of the viral genome. J Gen Virol. 2015;96(8):2252–2261. doi:10.1099/vir.0.000159.
  • Schmitt F, Pastore N, Abarrategui-Pontes C, et al. Correction of hyperbilirubinemia in Gunn rats by surgical delivery of low doses of helper-dependent adenoviral vectors. Human Gene Ther Meth. 2014;25(3):181–186. doi:10.1089/hgtb.2013.236.
  • Marrone J, Lehmann GL, Soria LR, et al. Adenoviral transfer of human aquaporin-1 gene to rat liver improves bile flow in estrogen-induced cholestasis. Gene Ther. 2014;21(12):1058–1064. doi:10.1038/gt.2014.78.
  • Oka K, Mullins CE, Kushwaha RS, et al. Gene therapy for rhesus monkeys heterozygous for LDL receptor deficiency by balloon catheter hepatic delivery of helper-dependent adenoviral vector. Gene Ther. 2015;22(1):87–95. doi:10.1038/gt.2014.85.
  • Montenegro-Miranda PS, Pañeda A, ten Bloemendaal L, et al. Adeno-associated viral vector serotype 5 poorly transduces liver in rat models. PLoS ONE. 2013;8(12):e82597. doi:10.1371/journal.pone.0082597.
  • Greig JA, Peng H, Ohlstein J, et al. Intramuscular Injection of AAV8 in mice and macaques is associated with substantial hepatic targeting and transgene expression. PLoS ONE. 2014;9(11):e112268. doi:10.1371/journal.pone.0112268.
  • Murillo O, Luqui DM, Gazquez C, et al. Long-term metabolic correction of Wilson’s disease in a murine model by gene therapy. J Hepatol. 2016;64(2):419–426. doi:10.1016/j.jhep.2015.09.014.
  • Yant SR, Meuse L, Chiu W, et al. Somatic integration and long-term transgene expression in normal and haemophilic mice using a DNA transposon system. Nat Genet. 2000;25(1):35–41. doi:10.1038/75568.
  • Kren BT, Unger GM, Sjeklocha L, et al. Nanocapsule-delivered Sleeping Beauty mediates therapeutic Factor VIII expression in liver sinusoidal endothelial cells of hemophilia A mice. J Clin Invest. 2009;119(7):2086–2099. doi:10.1172/JCI34332.
  • Ohlfest JR, Frandsen JL, Fritz S, et al. Phenotypic correction and long-term expression of factor VIII in hemophilic mice by immunotolerization and nonviral gene transfer using the Sleeping Beauty transposon system. Biotechnol J. 2005;105(7):2691–2698.
  • Mikkelsen JG, Yant SR, Meuse L, et al. Helper-Independent Sleeping Beauty transposon-transposase vectors for efficient nonviral gene delivery and persistent gene expression in vivo. Mol Ther. 2003;8(4):654–665.
  • Aronovich EL, Bell JB, Belur LR, et al. Prolonged expression of a lysosomal enzyme in mouse liver after Sleeping Beauty transposon-mediated gene delivery: implications for non-viral gene therapy of mucopolysaccharidoses. J Gene Med. 2007;9(5):403–415. doi:10.1002/jgm.1028.
  • Wilber A, Wangensteen KJ, Chen Y, et al. Messenger RNA as a source of transposase for Sleeping Beauty transposon-mediated correction of hereditary tyrosinemia type I. Mol Ther. 2007;15(7):1280–1287. doi:10.1038/sj.mt.6300160.
  • Di Matteo M, Samara-Kuko E, Ward NJ, et al. Hyperactive piggyBac transposons for sustained and robust liver-targeted gene therapy. Mol Ther. 2014;22(9):1614–1624. doi:10.1038/mt.2014.131.
  • Cepko CL, Roberts BE, Mulligan RC. Construction and applications of a highly transmissible murine retrovirus shuttle vector. Cell. 1984;37(3):1053–1062.
  • Cooper DN. Murine retroviral vectors and human gene therapy. Science. 1985;228(4700):650–653.
  • Gordon K, Ruddle FH. Gene transfer into mouse embryos. Dev Biol (N Y 1985). 1985;4:1–36.
  • Ledley FD, Woo SL. Molecular basis of alpha 1-antitrypsin deficiency and its potential therapy by gene transfer. J Inherit Metab Dis. 1986;9(Suppl 1):85–91.
  • Miller AD. Development of applications of retroviral vectors. In: Coffin JM, Hughes SH, Vermus HE, editors. Retroviruses. Cold Spring Harbor, NY: Cold Spring Harbor Press; 1997. p. 437–473.
  • Fassati A, Goff SP. Characterization of intracellular reverse transcription complexes of Moloney murine leukemia virus. J Virol. 1999;73(11):8919–8925.
  • Elis E, Ehrlich M, Prizan-Ravid A, et al. p12 tethers the murine leukemia virus pre-integration complex to mitotic chromosomes. PLoS Pathog. 2012;8(12):e1003103. doi:10.1371/journal.ppat.1003103.
  • Young GR, Stoye JP, Kassiotis G. Are human endogenous retroviruses pathogenic? An approach to testing the hypothesis. Bioessays. 2013;35(9):794–803. doi:10.1002/bies.201300049.
  • High KH, Nathwani A, Spencer T, et al. Current status of haemophilia gene therapy. Haemophilia. 2014;20(Suppl 4):43–49. doi:10.1111/hae.12411.
  • Prevec L, Schneider M, Rosenthal KL, et al. Use of human adenovirus-based vectors for antigen expression in animals. J Gen Virol. 1989;70(Pt 2):429–434. doi:10.1099/0022-1317-70-2-429.
  • Jaffe HA, Danel C, Longenecker G, et al. Adenovirus-mediated in vivo gene transfer and expression in normal rat liver. Nat Genet. 1992;1(5):372–378. doi:10.1038/ng0892-372.
  • Yang Y, Li Q, Ertl HCJ, et al. Cellular and humoral immune responses to viral antigens create barriers to lung-directed gene therapy with recombinant adenoviruses. J Virol. 1995;69(4):2004–2015.
  • Morral N, O’Neal W, Rice K, et al. Administration of helper-dependent adenoviral vectors and sequential delivery of different vector serotype for long-term liver-directed gene transfer in baboons. Proc Natl Acad Sci USA. 1999;96(22):12816–12821.
  • Ghosh SS, Takahashi M, Thummala NR, et al. Liver-directed gene therapy: promises, problems and prospects at the turn of the century. J Hepatol. 2000;32(1 Suppl):238–252.
  • Cheng R, Peng J, Yan Y, et al. Efficient gene editing in adult mouse livers via adenoviral delivery of CRISPR/Cas9. FEBS Lett. 2014;588(21):3954–3958. doi:10.1016/j.febslet.2014.09.008.
  • Atchinson RW, Casto BC, Hammon WM. Adenovirus-associated defective virus particles. Science. 1965;149(3685):754–756.
  • Daya S, Berns KI. Gene therapy using adeno-associated virus vectors. Clin Microbiol Rev. 2008;21(4):583–593. doi:10.1128/CMR.00008-08.
  • Walz C, Schlehofer JR, Flentje M, et al. Adeno-associated virus sensitizes HeLa cell tumors to gamma rays. J Virol. 1992;66(9):5651–5657.
  • Yakinoglu AO, Heilbronn R, Burkle A, et al. DNA amplification of adeno-associated virus as a response to cellular genotoxic stress. J Virol. 1988;48(11):3123–3129.
  • Yakobson B, Hrynko TA, Peak MJ, et al. Replication of adeno-associated virus in cells irradiated with UV light at 254 nm. J Virol. 1989;63(3):1023–1030.
  • Nakai H, Yant SR, Storm TA, et al. Extrachromosomal recombinant adeno-associated virus vector genomes are primarily responsible for stable liver transduction in vivo. J Virol. 2001;75(15):6969–6976. doi:10.1128/JVI.75.15.6969-6976.2001.
  • Gaudet D, Méthot J, Déry S, et al. Efficacy and long-term safety of alipogene tiparvovec (AAV1-LPLS447X) gene therapy for lipoprotein lipase deficiency: an open-label trial. Gene Ther. 2013;20(4):361–369. doi:10.1038/gt.2012.43.
  • van Dijk R, Beuers U, Bosma PJ. Gene replacement therapy for genetic hepatocellular jaundice. Clin Rev Allergy Immunol. 2015;48:243–253. doi:10.1007/s12016-014-8454-7.
  • Nault JC, Datta S, Imbeaud S, et al. Recurrent AAV2-related insertional mutagenesis in human hepatocellular carcinomas. Nat Genet. 2015;47(10):1187–1193. doi:10.1038/ng.3389.
  • Berns KI, Byrne BJ, Flotte TR, et al. Adeno-associated virus type 2 and hepatocellular carcinoma?. Human Gene Ther. 2015;26(12):779–781. doi:10.1089/hum.2015.29014.kib.
  • Büning H, Schmidt M. Adeno-associated vector toxicity-to be or not to be?. Mol Ther. 2015;23(11):1673–1675. doi:10.1038/mt.2015.182.
  • Ling C, Wang Y, Zhang Y, et al. Selective in vivo targeting of human liver tumors by optimized AAV3 vectors in a murine xenograft model. Human Gene Ther. 2014;25(12):1023–1034. doi:10.1089/hum.2014.099.
  • Lisowski L, Dane AP, Chu K, et al. Selection and evaluation of clinically relevant AAV variants in a xenograft liver model. Nature. 2014;506(7488):382–386. doi:10.1038/nature12875.
  • Nathwani A, Tuddenham EG, Rangarajan S, et al. Adenovirus-associated virus vector-mediated gene transfer in hemophilia B. N Engl J Med. 2011;365(25):2357–2365. doi:10.1056/NEJMoa1108046.
  • Xu Z, Ye J, Zhang A, et al. Gene therapy for hemophilia B with liver-specific element mediated by Rep-RBE site-specific integration system. J Cardiovasc Pharmacol. 2015;65(2):153–159. doi:10.1097/FJC.0000000000000172.
  • Senís E, Fatouros C, Große S, et al. CRISPR/Cas9-mediated genome engineering: an adeno-associated viral (AAV) vector toolbox. Biotechnol J. 2014;9(11):1402–1412. doi:10.1002/biot.201400046.
  • Ran FA, Cong L, Yan WX, et al. In vivo genome editing using Staphylococcus aureus Cas9. Nature. 2015;520(7546):186–191. doi:10.1038/nature14299.
  • Hareendran S, Balakrishnan B, Sen D, et al. Adeno-associated virus (AAV) vectors in gene therapy: immune challenges and strategies to circumvent them. Rev Med Virol. 2013;23(6):399–413. doi:10.1002/rmv.1762.
  • Sowd GA, Fanning E. A wolf in sheep’s clothing: SV40 co-opts host genome maintenance proteins to replicate viral DNA. PLoS Pathog. 2012;8(11):e1002994. doi:10.1371/journal.ppat.1002994.
  • Strayer DS. SV40-based gene therapy vectors: turning an adversary into a friend. Curr Opin Mol Ther. 2000;2(5):570–578.
  • Arad U, Zeira E, El-Latif MA, et al. Liver-targeted gene therapy by SV40-based vectors using the hydrodynamic injection method. Human Gene Ther. 2005;16(3):361–371. doi:10.1089/hum.2005.16.361.
  • Strayer D, Branco F, Zern MA, et al. Durability of transgene expression and vector integration: recombinant SV40-derived gene therapy vectors. Mol Ther. 2002;6(2):227–237.
  • Ivics Z, Hackett PB, Plasterk RH, et al. Molecular reconstruction of Sleeping Beauty, a Tc1-like transposon from fish, and its transposition in human cells. Cell. 1997;91(4):501–510.
  • Aronovich EL, McIvor RS, Hackett PB. The Sleeping Beauty transposon system: a non-viral vector for gene therapy. Hum Mol Genet. 2011;20(R1):R14–R20. doi:10.1093/hmg/ddr140.
  • Mátés L, Chuah MK, Belay E, et al. Molecular evolution of a novel hyperactive Sleeping Beauty transposase enables robust stable gene transfer in vertebrates. Nat Genet. 2009;41(6):753–761. doi:10.1038/ng.343.
  • Vigdal TJ, Kaufman CD, Izsvák Z, et al. Common physical properties of DNA affecting target site selection of Sleeping Beauty and other Tc1/mariner transposable elements. J Mol Biol. 2002;323(3):441–452.
  • Yant SR, Wu X, Huang Y, et al. High-resolution genome-wide mapping of transposon integration in mammals. Mol Cell Biol. 2005;25(6):2085–2094. doi:10.1128/MCB.25.6.2085-2094.2005.
  • Williams DA. Sleeping Beauty vector system moves toward human trials in the United States. Mol Ther. 2008;16(9):1515–1516. doi:10.1038/mt.2008.169.
  • Cary LC, Goebel M, Corsaro BG, et al. Transposon mutagenesis of baculoviruses: analysis of Trichoplusia ni transposon IFP2 insertions within the FP-locus of nuclear polyhedrosis viruses. Virology. 1989;172(1):156–169.
  • Ding S, Wu X, Li G, et al. Efficient transposition of the piggyBac (PB) transposon in mammalian cells and mice. Cell. 2005;122(3):473–483. doi:10.1016/j.cell.2005.07.013.
  • Wilson MH, Coates CJ, George AL Jr. PiggyBac transposon-mediated gene transfer in human cells. Mol Ther. 2007;15(1):139–145. doi:10.1038/sj.mt.6300028.
  • Lee C-Y, Li J-F, Liou J-S, et al. A gene delivery system for human cells mediated by both a cell-penetrating peptide and a piggyBac transposase. Biomaterials. 2011;32(26):6264–6276. doi:10.1016/j.biomaterials.2011.05.012.
  • Doherty JE, Huye LE, Yusa K, et al. Hyperactive piggyBac gene transfer in human cells and in vivo. Human Gene Ther. 2012;23(3):311–320. doi:10.1089/hum.2011.138.
  • Burnight ER, Staber JM, Korsakov P, et al. A hyperactive transposase promotes persistent gene transfer of a piggyBac DNA transposon. Mol Ther Nucleic Acids. 2012;1:e50. doi:10.1038/mtna.2012.12.
  • Jin L, Zeng X, Liu M, et al. Current progress in gene delivery technology based on chemical methods and nano-carriers. Theranostics. 2014;4(3):240–255. doi:10.7150/thno.6914.
  • Yin H, Kanasty RL, Eltoukhy AA, et al. Non-viral vectors for gene-based therapy. Nat Rev Genet. 2014;15(8):541–555. doi:10.1038/nrg3763.
  • Ibraheem D, Elaissari A, Fessi H. Gene therapy and DNA delivery systems. Int J Pharm. 2014;459(1–2):70–83. doi:10.1016/j.ijpharm.2013.11.041.
  • Rehman Z, Hoekstra D, Zuhorn IS. Mechanism of polyplex- and lipoplex-mediated delivery of nucleic acids: real-time visualization of transient membrane destabilization without endosomal lysis. ACS Nano. 2013;7(5):3767–3777. doi:10.1021/nn3049494.
  • Nakamura S, Maehara T, Watanabe S, et al. Improvement of hydrodynamics-based gene transfer of nonviral DNA targeted to murine hepatocytes. Biomed Res Int. 2013;2013:1–9. doi:10.1155/2013/928790.
  • Dong Y, Love KT, Dorkin JR, et al. Lipopeptide nanoparticles for potent and selective siRNA delivery in rodents and nonhuman primates. Proc Natl Acad Sci USA. 2014;111(11):3955–3960. doi:10.1073/pnas.1322937111.
  • Li S-D, Huang L. Targeted delivery of siRNA by nonviral vectors: lessons learned from recent advances. Curr Opin Investig Drugs. 2008;9(12):1317–1323.
  • Sakashita M, Mochizuki S, Sakurai K. Hepatocyte-targeting gene delivery using a lipoplex composed of galactose-modified aromatic lipid synthesized with click chemistry. Bioorg Med Chem. 2014;22(19):5212–5219. doi:10.1016/j.bmc.2014.08.012.
  • Prakash TP, Graham MJ, Yu J, et al. Targeted delivery of antisense oligonucleotides to hepatocytes using triantennary N-acetyl galactosamine improves potency 10-fold in mice. Nucleic Acid Ther. 2014;42(13):8796–8807. doi:10.1093/nar/gku531.
  • Liu F, Song Y, Liu D. Hydrodynamics-based transfection in animals by systemic administration of plasmid DNA. Gene Ther. 1999;6(7):1258–1266. doi:10.1038/sj.gt.3300947.
  • Zhang G, Budker V, Wolff JA. High levels of foreign gene expression in hepatocytes after tail vein injections of naked plasmid DNA. Human Gene Ther. 1999;10(10):1735–1737. doi:10.1089/10430349950017734.
  • Hackett PB, Ekker SC, Largaespada DA, et al. Sleeping Beauty transposon-mediated gene therapy for prolonged expression. Adv Genet. 2005;54:189–232. doi:10.1016/S0065-2660(05)54009-4.
  • Herrero MJ, Sabater L, Guenechea G, et al. DNA delivery to ‘ex vivo’ human liver segments. Gene Ther. 2012;19(5):504–512. doi:10.1038/gt.2011.144.
  • Kamimura K, Kanefuji T, Yokoo T, et al. Safety assessment of liver-targeted hydrodynamic gene delivery in dogs. PLoS ONE. 2014;9(9):e107203. doi:10.1371/journal.pone.0107203.
  • Sendra L, Carreño O, Miguel A, et al. Low RNA translation activity limits the efficacy of hydrodynamic gene transfer to pig liver in vivo. J Gene Med. 2014;16(7–8):179–192. doi:10.1002/jgm.2777.
  • Kamimura K, Suda T, Zhang G, et al. Parameters affecting image-guided, hydrodynamic gene delivery to swine liver. Mol Ther Nucleic Acids. 2013;2:e128. doi:10.1038/mtna.2013.52.
  • Yoshino H, Hashizume K, Kobayashi E. Naked plasmid DNA transfer to the porcine liver using rapid injection with large volume. Gene Ther. 2006;13(24):1696–1702. doi:10.1038/sj.gt.3302833.
  • Delgado D, del Pozo-Rodríguez A, Angeles Solinís M, et al. New gene delivery system based on oligochitosan and solid lipid nanoparticles: ‘in vitro’ and ‘in vivo’ evaluation. Eur J Pharm Sci. 2013;50(3–4):484–491. doi:10.1016/j.ejps.2013.08.013.
  • Ding B, Li T, Zhang J, et al. Advances in liver-directed gene therapy for hepatocellular carcinoma by nonviral delivery systems. Curr Gene Ther. 2012;12(2):92–102.
  • Barzel A, Paulk NK, Shi Y, et al. Promoterless gene targeting without nucleases ameliorates haemophilia B in mice. Nature. 2015;517:360–364. doi:10.1038/nature13864.
  • Monahan PE, Sun J, Gui T, et al. Employing a gain-of-function factor IX variant R338L to advance the efficacy and safety of Hemophilia B human gene therapy: preclinical evaluation supporting an ongoing adeno-associated virus clinical trial. Human Gene Ther. 2015;26:69–81. doi:10.1089/hum.2014.106.
  • Chuah MK, Petrus I, De Bleser P, et al. Liver-specific transcriptional modules identified by genome-wide in silico analysis enable efficient gene therapy in mice and non-human primates. Mol Ther. 2014;22(9):1605–1613. doi:10.1038/mt.2014.114.
  • Sherman A, Schlachterman A, Cooper M, et al. Portal vein delivery of viral vectors for gene therapy for hemophilia. Methods Mol Biol. 2014;1114:413–426. doi:10.1007/978-1-62703-761-7_27.
  • Loring HS, Flotte TR. Current status of gene therapy for α-1 antitrypsin deficiency. Expert Opin Biol Ther. 2014;3:1–8.
  • Chiuchiolo MJ, Kaminsky SM, Sondhi D, et al. Intrapleural administration of an AAVrh.10 vector coding for human α1-antitrypsin for the treatment of α1-antitrypsin deficiency. Human Gene Ther Clin Dev. 2013;24(4):161–173. doi:10.1089/humc.2013.168.
  • Eggenschwiler R, Loya K, Wu G, et al. Sustained knockdown of a disease-causing gene in patient-specific induced pluripotent stem cells using lentiviral vector-based gene therapy. Stem Cells Trans Med. 2013;2(9):641–654. doi:10.5966/sctm.2013-0017.
  • Quiviger M, Arfi A, Mansard D, et al. High and prolonged sulfamidase secretion by the liver of MPS-IIIA mice following hydrodynamic tail vein delivery of antibiotic-free pFAR4 plasmid vector. Gene Ther. 2014;21:1001–1007. doi:10.1038/gt.2014.75.
  • Aronovich EL, Hackett PB. Lysosomal storage disease: gene therapy on both sides of the blood-brain barrier. Mol Genet Metab. 2015;114:83–93. doi:10.1016/j.ymgme.2014.09.011.
  • Pañeda A, Lopez-Franco E, Kaeppel C, et al. Safety and liver transduction efficacy of rAAV5-cohPBGD in nonhuman primates: a potential therapy for acute intermittent porphyria. Human Gene Ther. 2013;24(12):1007–1017. doi:10.1089/hum.2013.166.
  • Lagor WR, Johnston JC, Lock M, et al. Adeno-associated viruses as liver-directed gene delivery vehicles: focus on lipoprotein metabolism. Methods Mol Biol. 2013;1027:273–307. doi:10.1007/978-1-60327-369-5_13.
  • Chen S-J, Sanmiguel J, Lock M, et al. Biodistribution of AAV8 vectors expressing human low-density lipoprotein receptor in a mouse model of homozygous familial hypercholesterolemia. Human Gene Ther Clin Dev. 2013;24(4):154–160. doi:10.1089/humc.2013.082.
  • van Dijk R, Montenegro-Miranda PS, Riviere C, et al. Polyinosinic acid blocks adeno-associated virus macrophage endocytosis in vitro and enhances adeno-associated virus liver-directed gene therapy in vivo. Human Gene Ther. 2013;24(9):807–813. doi:10.1089/hum.2013.086.
  • Chandler RJ, Tarasenko TN, Cusmano-Ozog K, et al. Liver-directed adeno-associated virus serotype 8 gene transfer rescues a lethal murine model of citrullinemia type 1. Gene Ther. 2013;20(12):1188–1191. doi:10.1038/gt.2013.53.
  • Wilson JM. Lessons learned from the gene therapy trial for ornithine transcarbamylase deficiency. Mol Genet Metab. 2009;96(4):151–157. doi:10.1016/j.ymgme.2008.12.016.
  • Hacein-Bey-Abina S, Garrigue A, Wang GP, et al. Insertional oncogenesis in 4 patients after retrovirus-mediated gene therapy of SCID-X1. J Clin Invest. 2008;118(9):3132–3142. doi:10.1172/JCI35700.
  • Ran FA, Hsu PD, Wright J, et al. Genome engineering using the CRISPR-Cas9 system. Nat Protoc. 2013;8(11):2281–2308. doi:10.1038/nprot.2013.143.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.