Expressing transgenes that exceed the packaging capacity of adeno-associated virus capsids

Human Gene Therapy Methods

Volumn 27, Issue 1, 2016, Pages 1-12

  Chamberlain, Kyle ^a   Riyad, Jalish Mahmud ^a   Weber, Thomas ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PARVOVIRUS VECTOR; PROTEIN; CAPSID PROTEIN; VIRUS DNA;

ADENO ASSOCIATED VIRUS; AUTHOR; DNA PACKAGING; GENE CASSETTE; GENE EXPRESSION; HOMOLOGOUS RECOMBINATION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PACKAGING; PARVOVIRIDAE; POLYADENYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; TRANS SPLICING; VIRUS CAPSID; VIRUS GENOME; ANIMAL; DEPENDOPARVOVIRUS; GENE THERAPY; GENE TRANSFER; GENE VECTOR; GENETICS; GENOME SIZE; METABOLISM; TRANSGENE; VIRUS ASSEMBLY;

ANIMALS; CAPSID PROTEINS; DEPENDOVIRUS; DNA, VIRAL; GENE EXPRESSION; GENE TRANSFER TECHNIQUES; GENETIC THERAPY; GENETIC VECTORS; GENOME SIZE; GENOME, VIRAL; HUMANS; TRANSGENES; VIRUS ASSEMBLY;

EID: 84959127834     PISSN: 19466536     EISSN: 19466544     Source Type: Journal    
DOI: 10.1089/hgtb.2015.140     Document Type: Review

References (72)

1. Buning H. Gene therapy enters the pharma market: The short story of a long journey. EMBO Mol Med 2013; 5: 1-3
2. Hoggan MD, Blacklow NR, Rowe WP. Studies of small DNA viruses found in various adenovirus preparations: Physical, biological, and immunological characteristics. Proc Natl Acad Sci U S A 1966; 55: 1467-1474
3. Nault JC, Datta S, Imbeaud S, et al. Recurrent AAV2-related insertional mutagenesis in human hepatocellular carcinomas. Nat Genet 2015; 47: 1187-1193
4. Atchison RW, Casto BC, Hammon WM. Adenovirus-Associated defective virus particles. Science 1965; 149: 754
5. Samulski RJ, Muzyczka N. AAV-mediated gene therapy for research and therapeutic purposes. Ann Rev Virol 2014; 1: 427-451
6. Berns KI, Adler S. Separation of two types of adeno-Associated virus particles containing complementary polynucleotide chains. J Virol 1972; 9: 394-396
7. Hoggan MD. Adenovirus associated viruses. Prog Med Virol 1970; 12: 211-239
8. Rose JA, Berns KI, Hoggan MD, et al. Evidence for a single-stranded adenovirus-Associated virus genome: Formation of a DNA density hybrid on release of viral DNA. Proc Natl Acad Sci U S A 1969; 64: 863-869
9. Kotin RM, Siniscalco M, Samulski RJ, et al. Sitespecific integration by adeno-Associated virus. Proc Natl Acad Sci U S A 1990; 87: 2211-2215
10. Linden RM, Ward P, Giraud C, et al. Site-specific integration by adeno-Associated virus. Proc Natl Acad Sci U S A 1996; 93: 11288-11294
11. Samulski RJ, Zhu X, Xiao X, et al. Targeted integration of adeno-Associated virus (AAV) into human chromosome 19. EMBO J 1991; 10: 3941-3950
12. Tratschin JD, Miller IL, Carter BJ. Genetic analysis of adeno-Associated virus: Properties of deletion mutants constructed in vitro and evidence for an adeno-Associated virus replication function. J Virol 1984; 51: 611-619
13. Clark KR, Sferra TJ, Johnson PR. Recombinant adeno-Associated viral vectors mediate long-Term transgene expression in muscle. Hum Gene Ther 1997; 8: 659-669
14. Duan D, Sharma P, Yang J, et al. Circular intermediates of recombinant adeno-Associated virus have defined structural characteristics responsible for long-Term episomal persistence in muscle tissue. J Virol 1998; 72: 8568-8577
15. Nakai H, Storm TA, Kay MA. Recruitment of single-stranded recombinant adeno-Associated virus vector genomes and intermolecular recombination are responsible for stable transduction of liver in vivo. J Virol 2000; 74: 9451-9463
16. Schnepp BC, Jensen RL, Chen CL, et al. Characterization of adeno-Associated virus genomes isolated from human tissues. J Virol 2005; 79: 14793-14803
17. Nonnenmacher M, Weber T. Intracellular transport of recombinant adeno-Associated virus vectors. Gene Ther 2012; 19: 649-658
18. de la Maza LM, Carter BJ. Molecular structure of adeno-Associated virus variant DNA. J Biol Chem 1980; 255: 3194-3203
19. Srivastava A, Lusby EW, Berns KI. Nucleotide sequence and organization of the adenoassociated virus 2 genome. J Virol 1983; 45: 555-564
20. Gerry HW, Kelly TJ Jr., Berns KI. Arrangement of nucleotide sequences in adeno-Associated virus DNA. J Mol Biol 1973; 79: 207-225
21. Shao H, Lv Y, Ye J, et al. Isolation of a goose parvovirus from swan and its molecular characteristics. Acta Virol 2014; 58: 194-198
22. Wong FC, Spearman JG, Smolenski MA, et al. Equine parvovirus: Initial isolation and partial characterization. Can J Comp Med 1985; 49: 50-54
23. Diffoot N, Chen KC, Bates RC, et al. The complete nucleotide sequence of parvovirus LuIII and localization of a unique sequence possibly responsible for its encapsidation pattern. Virology 1993; 192: 339-345
24. Siegl G. Physicochemical characteristics of the DNA of parvovirus Lu 3. Arch Gesamte Virusforsch 1973; 43: 334-344
25. Hermonat PL, Quirk JG, Bishop BM, et al. The packaging capacity of adeno-Associated virus (AAV) and the potential for wild-Type-plus AAV gene therapy vectors. FEBS Lett 1997; 407: 78-84
26. Dong JY, Fan PD, Frizzell RA. Quantitative analysis of the packaging capacity of recombinant adenoassociated virus. Hum Gene Ther 1996; 7: 2101-2112
27. Brocchieri L, Karlin S. Protein length in eukaryotic and prokaryotic proteomes. Nucleic Acids Res 2005; 33: 3390-3400
28. Palfi A, Chadderton N, McKee AG, et al. Efficacy of codelivery of dual AAV2/5 vectors in the murine retina and hippocampus. Hum Gene Ther 2012; 23: 847-858
29. Allocca M, Doria M, Petrillo M, et al. Serotypedependent packaging of large genes in adenoassociated viral vectors results in effective gene delivery in mice. J Clin Invest 2008; 118: 1955-1964
30. Lai Y, Yue Y, Duan D. Evidence for the failure of adeno-Associated virus serotype 5 to package a viral genome or = 8.2 kb. Mol Ther 2010; 18: 75-79
31. Dong B, Nakai H, Xiao W. Characterization of genome integrity for oversized recombinant AAV vector. Mol Ther 2010; 18: 87-92
32. Wu ZJ, Yang HY, Colosi P. Effect of genome size on AAV vector packaging. Mol Ther 2010; 18: 80-86
33. Hirsch ML, Agbandje-McKenna M, Samulski RJ. Little vector, big gene transduction: Fragmented genome reassembly of adeno-Associated virus. Mol Ther 2010; 18: 6-8
34. Hirsch ML, Li C, Bellon I, et al. Oversized AAV transductifon is mediated via a DNA-PKcsindependent, Rad51C-dependent repair pathway. Mol Ther 2013; 21: 2205-2216
35. Ostedgaard LS, Rokhlina T, Karp PH, et al. A shortened adeno-Associated virus expression cassette for CFTR gene transfer to cystic fibrosis airway epithelia. Proc Natl Acad Sci U S A 2005; 102: 2952-2957
36. McFarland TJ, Zhang Y, Atchaneeyaskul LO, et al. Evaluation of a novel short polyadenylation signal as an alternative to the SV40 polyadenylation signal. Plasmid 2006; 56: 62-67
37. Kaufman RJ, Wasley LC, Dorner AJ. Synthesis, processing, and secretion of recombinant human factor-VIII expressed in mammalian-cells. J Biol Chem 1988; 263: 6352-6362
38. Burton M, Nakai H, Colosi P, et al. Coexpression of factor VIII heavy and light chain adeno-Associated viral vectors produces biologically active protein. Proc Natl Acad Sci U S A 1999; 96: 12725-12730
39. Hu C, Lipshutz GS. AAV-based neonatal gene therapy for hemophilia A: Long-Term correction and avoidance of immune responses in mice. Gene Ther 2012; 19: 1166-1176
40. Bostick B, Shin JH, Yue Y, et al. AAVmicrodystrophin therapy improves cardiac performance in aged female mdx mice. Mol Ther 2011; 19: 1826-1832
41. Gregorevic P, Blankinship MJ, Allen JM, et al. Systemic microdystrophin gene delivery improves skeletal muscle structure and function in old dystrophic mdx mice. Mol Ther 2008; 16: 657-664
42. Odom GL, Gregorevic P, Allen JM, et al. Gene therapy of mdx mice with large truncated dystrophins generated by recombination using rAAV6. Mol Ther 2011; 19: 36-45
43. Halbert CL, Allen JM, Miller AD. Efficient mouse airway transduction following recombination between AAV vectors carrying parts of a larger gene. Nat Biotechnol 2002; 20: 697-701
44. Sondergaard PC, Griffin DA, Pozsgai ER, et al. AAV.Dysferlin overlap vectors restore function in dysferlinopathy animal models. Ann Clin Transl Neurol 2015; 2: 256-270
45. Pryadkina M, Lostal W, Bourg N, et al. A comparison of AAV strategies distinguishes overlapping vectors for efficient systemic delivery of the 6.2 kb Dysferlin coding sequence. Mol Ther Methods Clin Dev 2015; 2: 15009
46. Trapani I, Colella P, Sommella A, et al. Effective delivery of large genes to the retina by dual AAV vectors. EMBO Mol Med 2014; 6: 194-211
47. Dyka FM, Boye SL, Chiodo VA, et al. Dual adenoassociated virus vectors result in efficient in vitro and in vivo expression of an oversized gene, MYO7A. Hum Gene Ther Methods 2014; 25: 166-177
48. Lopes VS, Boye SE, Louie CM, et al. Retinal gene therapy with a large MYO7A cDNA using adenoassociated virus. Gene Ther 2013; 20: 824-833
49. Yan Z, Zak R, Zhang Y, et al. Inverted terminal repeat sequences are important for intermolecular recombination and circularization of adenoassociated virus genomes. J Virol 2005; 79: 364-379
50. Duan D, Yan Z, Yue Y, et al. Structural analysis of adeno-Associated virus transduction circular intermediates. Virology 1999; 261: 8-14
51. Straus SE, Sebring ED, Rose JA. Concatemers of alternating plus and minus strands are intermediates in adenovirus-Associated virus DNA synthesis. Proc Natl Acad Sci U S A 1976; 73: 742-746
52. Duan D, Yue Y, Yan Z, et al. A new dual-vector approach to enhance recombinant adenoassociated virus-mediated gene expression through intermolecular cis activation. Nat Med 2000; 6: 595-598
53. Yan Z, Zhang Y, Duan D, et al. Trans-splicing vectors expand the utility of adeno-Associated virus for gene therapy. Proc Natl Acad Sci U S A 2000; 97: 6716-6721
54. Chao H, Sun L, Bruce A, et al. Expression of human factor VIII by splicing between dimerized AAV vectors. Mol Ther 2002; 5: 716-722
55. Duan D, Yue Y, Engelhardt JF. Expanding AAV packaging capacity with trans-splicing or overlapping vectors: A quantitative comparison. Mol Ther 2001; 4: 383-391
56. Reich SJ, Auricchio A, Hildinger M, et al. Efficient trans-splicing in the retina expands the utility of adeno-Associated virus as a vector for gene therapy. Hum Gene Ther 2003; 14: 37-44
57. Sun L, Li J, Xiao X. Overcoming adeno-Associated virus vector size limitation through viral DNA heterodimerization. Nat Med 2000; 6: 599-602
58. Choi VW, McCarty DM, Samulski RJ. Host cell DNA repair pathways in adeno-Associated viral genome processing. J Virol 2006; 80: 10346-10356
59. Yan Z, Lei-Butters DC, Zhang Y, et al. Hybrid adeno-Associated virus bearing nonhomologous inverted terminal repeats enhances dual-vector reconstruction of minigenes in vivo. Hum Gene Ther 2007; 18: 81-87
60. Trapani I, Toriello E, de Simone S, et al. Improved dual AAV vectors with reduced expression of truncated proteins are safe and effective in the retina of a mouse model of Stargardt disease. Hum Mol Genet 2015; 24: 6811-6825
61. Lai Y, Yue Y, Liu M, et al. Efficient in vivo gene expression by trans-splicing adeno-Associated viral vectors. Nat Biotechnol 2005; 23: 1435-1439
62. Lai Y, Yue Y, Liu M, et al. Synthetic intron improves transduction efficiency of trans-splicing adeno-Associated viral vectors. Hum Gene Ther 2006; 17: 1036-1042
63. Lostal W, Bartoli M, Bourg N, et al. Efficient recovery of dysferlin deficiency by dual adenoassociated vector-mediated gene transfer. Hum Mol Genet 2010; 19: 1897-1907
64. Ho M, Post CM, Donahue LR, et al. Disruption of muscle membrane and phenotype divergence in two novel mouse models of dysferlin deficiency. Hum Mol Genet 2004; 13: 1999-2010
65. Ghosh A, Yue Y, Lai Y, et al. A hybrid vector system expands adeno-Associated viral vector packaging capacity in a transgene-independent manner. Mol Ther 2008; 16: 124-130
66. Ghosh A, Yue Y, Duan D. Viral serotype and the transgene sequence influence overlapping adenoassociated viral (AAV) vector-mediated gene transfer in skeletal muscle. J Gene Med 2006; 8: 298-305
67. Ghosh A, Yue Y, Duan D. Efficient transgene reconstitution with hybrid dual AAV vectors carrying the minimized bridging sequences. Hum Gene Ther 2011; 22: 77-83
68. Zhang Y, Duan D. Novel mini-dystrophin gene dual adeno-Associated virus vectors restore neuronal nitric oxide synthase expression at the sarcolemma. Hum Gene Ther 2012; 23: 98-103
69. Lai Y, Thomas GD, Yue Y, et al. Dystrophins carrying spectrin-like repeats 16 and 17 anchor nNOS to the sarcolemma and enhance exercise performance in a mouse model of muscular dystrophy. J Clin Invest 2009; 119: 624-635
70. Koo T, Popplewell L, Athanasopoulos T, et al. Triple trans-splicing adeno-Associated virus vectors capable of transferring the coding sequence for full-length dystrophin protein into dystrophic mice. Hum Gene Ther 2014; 25: 98-108
71. Yang Y, Walsh CE. Spliceosome-mediated RNA trans-splicing. Mol Ther 2005; 12: 1006-1012
72. Aranko AS, Volkmann G. Protein trans-splicing as a protein ligation tool to study protein structure and function. Biomol Concepts 2011; 2: 183-198