Chromatographic purification of recombinant adenoviral and adeno-associated viral vectors: Methods and implications

Gene Therapy

Volumn 12, Issue , 2005, Pages S5-S17

  Burova, E ^a   Ioffe, E ^a  

^a REGENERON PHARMACEUTICALS INC   (United States)

Author keywords

Adeno associated virus; Adenovirus; Chromatography; Purification

Indexed keywords

ADENOVIRUS VECTOR; PARVOVIRUS VECTOR;

AFFINITY CHROMATOGRAPHY; CHROMATOGRAPHY; CONFERENCE PAPER; DENSITY GRADIENT CENTRIFUGATION; GEL PERMEATION CHROMATOGRAPHY; GENE EXPRESSION; GENE TRANSFER; GENETIC TRANSFECTION; HUMAN; IN VIVO STUDY; ION EXCHANGE CHROMATOGRAPHY; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROCESS CONTROL; SEPARATION TECHNIQUE; VIRAL CONTAMINATION; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; VIRUS CHARACTERIZATION; VIRUS PARTICLE; VIRUS PURIFICATION; VIRUS RECOMBINANT; VIRUS RECOMBINATION;

ADENOVIRIDAE; ANIMALS; BIOTECHNOLOGY; CHROMATOGRAPHY; DEPENDOVIRUS; DNA, RECOMBINANT; DNA, VIRAL; GENETIC VECTORS; HUMANS; QUALITY CONTROL; VIROLOGY;

ADENO-ASSOCIATED VIRUS; ADENOVIRIDAE; PARVOVIRUS;

EID: 27544495302     PISSN: 09697128     EISSN: 14765462     Source Type: Journal    
DOI: 10.1038/sj.gt.3302611     Document Type: Article

References (85)

1. http://www.wiley.co.uk/genetherapy/clinical/. A Journal of Gene Medicine website.
2. Green M et al. Adenovirus DNA I. Molecular weight and conformation. PNAS USA 1967; 57: 1302-1309.
3. Lonberg-Holm K, Crowell RL, Philipson L. Unrelated animal viruses share receptors. Nature 1976; 259: 679-681.
4. St George JA. Gene therapy progress and prospects: adenoviral vectors. Gene Therapy 2003; 10: 1135-1141.
5. Volpers C, Kochanek S. Adenoviral vectors for gene transfer and therapy. J Gene Med 2004; 6 (Suppl 1): S164-S171.
6. Danthinne X, Imperiale MJ. Production of first generation adenovirus vectors: a review. Gene Therapy 2000; 7: 1707-1714.
7. Berns KI. Parvovirus replication. Microbiol Rev 1990; 54: 316-329.
8. Siegl G et al. Characteristics and taxonomy of Parvoviridae. Intervirology 1985; 23: 61-73.
9. Flotte TR. Gene therapy progress and prospects: recombinant adeno-associated virus (rAAV) vectors. Gene Therapy 2004; 11: 805-810.
10. Monahan PE, Samulski RJ. AAV vectors: is clinical success on the horizon? Gene Therapy 2000; 7: 24-30.
11. Jooss K, Yang Y, Fisher KJ, Wilson JM. Transduction of dendritic cells by DNA viral vectors directs the immune response to transgene products in muscle fibers. J Virol 1998; 72: 4212-4223.
12. Grimm D, Kleinschmidt JA. Progress in adeno-associated virus type 2 vector production: promises and prospects for clinical use. Hum Gene Ther 1999; 10: 2445-2450.
13. Hermonat PL, Muzyczka N. Use of adeno-associated virus as a mammalian DNA cloning vector: transduction of neomycin resistance into mammalian tissue culture cells. Proc Natl Acad Sci USA 1984; 81: 6466-6470.
14. Tratschin JD, Miller IL, Smith MG, Carter BJ. Adeno-associated virus vector for high-frequency integration, expression, and rescue of genes in mammalian cells. Mol Cell Biol 1985; 5: 3251-3260.
15. McLaughlin SK, Collis P, Hermonat PL, Muzyczka N. Adeno- associated virus general transduction vectors: analysis of proviral structures. J Virol 1988; 62: 1963-1973.
16. Xiao X, Li J, Samulski RJ. Production of high-titer recombinant adeno-associated virus vectors in the absence of helper adenovirus. J Virol 1998; 72: 2224-2232.
17. Blanche F et al. An improved anion-exchange HPLC method for the detection and purification of adenoviral particles. Gene Therapy 2000; 7: 1055-1062.
18. Huyghe BG et al. Purification of a type 5 recombinant adenovirus encoding human p53 by column chromatography. Hum Gene Ther 1995; 6: 1403-1416.
19. Green AP et al. A new scalable method for the purification of recombinant adenovirus vectors. Hum Gene Ther 2002; 13: 1921-1934.
20. Clark KR, Liu X, McGrath JP, Johnson PR. Highly purified recombinant adeno-associated virus vectors are biologically active and free of detectable helper and wild-type viruses. Hum Gene Ther 1999; 10: 1031-1039.
21. Auricchio A et al. Isolation of highly infectious and pure adeno- associated virus type 2 vectors with a single-step gravity-flow column. Hum Gene Ther 2001; 12: 71-76.
22. Graham FL, Smiley J, Russell WC, Nairn R. Characteristics of a human cell line transformed by DNA from human adenovirus type 5. J Gen Virol 1977; 36: 59-74.
23. Fallaux FJ et al. New helper cells and matched early region 1-deleted adenovirus vectors prevent generation of replication- competent adenoviruses. Hum Gene Ther 1998; 9: 1909-1917.
24. Schiedner G, Hertel S, Kochanek S. Efficient transformation of primary human amniocytes by E1 functions of Ad5: generation of new cell lines for adenoviral vector production. Hum Gene Ther 2000; 11: 2105-2116.
25. Gao GP, Engdahl RK, Wilson JM. A cell line for high-yield production of E1-deleted adenovirus vectors without the emergence of replication-competent virus. Hum Gene Ther 2000; 11: 213-219.
26. Kochanek S, Schiedner G, Volpers C. High-capacity 'gutless' adenoviral vectors. Curr Opin Mol Ther 2001; 3: 454-463.
27. Kochanek S et al. A new adenoviral vector: replacement of all viral coding sequences with 28 kb of DNA independently expressing both full-length dystrophin and beta-galactosidase. Proc Natl Acad Sci USA 1996; 93: 5731-5736.
28. Parks RJ et al. A helper-dependent adenovirus vector system: removal of helper virus by Cre-mediated excision of the viral packaging signal. Proc Natl Acad Sci USA 1996; 93: 13565-13570.
29. Umana P et al. Efficient FLPe recombinase enables scalable production of helper-dependent adenoviral vectors with negligible helper-virus contamination. Nat Biotechnol 2001; 19: 582-585.
30. Samulski RJ, Chang LS, Shenk T. A recombinant plasmid from which an infectious adeno-associated virus genome can be excised in vitro and its use to study viral replication. J Virol 1987; 61: 3096-3101.
31. Samulski RJ, Chang LS, Shenk T. Helper-free stocks of recombinant adeno-associated viruses: normal integration does not require viral gene expression. J Virol 1989; 63: 3822-3828.
32. Grimm D, Kern A, Rittner K, Kleinschmidt JA. Novel tools for production and purification of recombinant adenoassociated virus vectors. Hum Gene Ther 1998; 9: 2745-2760.
33. Salvetti A et al. Factors influencing recombinant adeno-asso- ciated virus production. Hum Gene Ther 1998; 9: 695-706.
34. Chadeuf G et al. Efficient recombinant adeno-associated virus production by a stable rep-cap HeLa cell line correlates with adenovirus-induced amplification of the integrated rep-cap genome. J Gene Med 2000; 2: 260-268.
35. Mathews LC, Gray JT, Gallagher MR, Snyder RO. Recombinant adeno-associated viral vector production using stable packaging and producer cell lines. Methods Enzymol 2002; 346: 393-413.
36. Gao G et al. Purification of recombinant adeno-associated virus vectors by column chromatography and its performance in vivo. Hum Gene Ther 2000; 11: 2079-2091.
37. Saudan P, Vlach J, Beard P. Inhibition of S-phase progression by adeno-associated virus Rep78 protein is mediated by hypophos- phorylated pRb. EMBO J 2000; 19: 4351-4361.
38. Schmidt M, Afione S, Kotin RM. Adeno-associated virus type 2 Rep78 induces apoptosis through caspase activation independently of p53. J Virol 2000; 74: 9441-9450.
39. Clark KR, Voulgaropoulou F, Fraley DM, Johnson PR. Cell lines for the production of recombinant adeno-associated virus. Hum Gene Ther 1995; 6: 1329-1341.
40. Gao GP et al. High-titer adeno-associated viral vectors from a Rep/Cap cell line and hybrid shuttle virus. Hum Gene Ther 1998; 9: 2353-2362.
41. Qiao C et al. A novel gene expression control system and its use in stable, high-titer 293 cell-based adeno-associated virus packaging cell lines. J Virol 2002; 76: 13015-13027.
42. Johnston KM et al. HSV/AAV hybrid amplicon vectors extend transgene expression in human glioma cells. Hum Gene Ther 1997; 8: 359-370.
43. Urabe M, Ding C, Kotin RM. Insect cells as a factory to produce adeno-associated virus type 2 vectors. Hum Gene Ther 2002; 13: 1935-1943.
44. Smith RH, Ding C, Kotin RM. Serum-free production and column purification of adeno-associated virus type 5. J Virol Methods 2003; 114: 115-124.
45. Kamen A, Henry O. Development and optimization of an adenovirus production process. J Gene Med 2004; 6 (Suppl 1): S184-S192.
46. Drittanti L et al. Optimised helper virus-free production of high- quality adeno-associated virus vectors. J Gene Med 2001; 3: 59-71.
47. O'Riordan CR, Lachapelle AL, Vincent KA, Wadsworth SC. Scaleable chromatographic purification process for recombinant adeno-associated virus (rAAV). J Gene Med 2000; 2: 444-454.
48. Anderson R et al. A method for the preparation of highly purified adeno-associated virus using affinity column chromatography, protease digestion and solvent extraction. J Virol Methods 2000; 85: 23-34.
49. Potter M et al. Streamlined large-scale production of recombinant adeno-associated virus (rAAV) vectors. Methods Enzymol 2002; 346: 413-430.
50. Zolotukhin S et al. Recombinant adeno-associated virus purification using novel methods improves infectious titer and yield. Gene Therapy 1999; 6: 973-985.
51. Green M, Pina M. Biochemical studies on adenovirus multiplication. VI. Properties of highly purified tumorigenic human adenoviruses and their DNA's. Proc Natl Acad Sci USA 1964; 51: 1251-1259.
52. Zolotukhin S et al. Production and purification of serotype 1, 2, and 5 recombinant adeno-associated viral vectors. Methods 2002; 28: 158-167.
53. Stewart PL, Burnett RM. Adenovirus structure by X-ray crystallography and electron microscopy. Curr Top Microbiol Immunol 1995; 199 (Part 1): 25-38.
54. Brument N et al. A versatile and scalable two-step ion-exchange chromatography process for the purification of recombinant adeno-associated virus serotypes-2 and -5. Mol Ther 2002; 6: 678-686.
55. Kaludov N, Handelman B, Chiorini JA. Scalable purification of adeno-associated virus type 2, 4, or 5 using ion-exchange chromatography. Hum Gene Ther 2002; 13: 1235-1243.
56. Tamayose K, Hirai Y, Shimada T. A new strategy for large-scale preparation of high-titer recombinant adeno-associated virus vectors by using packaging cell lines and sulfonated cellulose column chromatography. Hum Gene Ther 1996; 7: 507-513.
57. Summerford C, Samulski RJ. Membrane-associated heparan sulfate proteoglycan is a receptor for adeno-associated virus type 2 virions. J Virol 1998; 72: 1438-1445.
58. Schnepp B, Clark KR. Highly purified recombinant adeno- associated virus vectors. Preparation and quantitation. Methods Mol Med 2002; 69: 427-443.
59. Rabinowitz JE et al. Cross-packaging of a single adeno- associated virus (AAV) type 2 vector genome into multiple AAV serotypes enables transduction with broad specificity. J Virol 2002; 76: 791-801.
60. Kaludov N et al. Adeno-associated virus serotype 4 (AAV4) and AAV5 both require sialic acid binding for hemagglutination and efficient transduction but differ in sialic acid linkage specificity. J Virol 2001; 75: 6884-6893.
61. Walters RW et al. Binding of adeno-associated virus type 5 to 2, 3-linked sialic acid is required for gene transfer. J Biol Chem 2001; 276: 20610-20616.
62. Auricchio A, O'Connor E, Hildinger M, Wilson JM. A single-step affinity column for purification of serotype-5 based adeno- associated viral vectors. Mol Ther 2001; 4: 372-374.
63. Di Pasquale G et al. Identification of PDGFR as a receptor for AAV-5 transduction. Nat Med 2003; 9: 1306-1312.
64. Andreadis ST et al. Large-scale processing of recombinant retroviruses for gene therapy. Biotechnol Prog 1999; 15: 1-11.
65. Crooks AJ, Lee JM, Dowsett AB, Stephenson JR. Purification and analysis of infectious virions and native non-structural antigens from cells infected with tick-borne encephalitis virus. J Chroma- togr 1990; 502: 59-68.
66. Shabram PW et al. Analytical anion-exchange HPLC of recombinant type-5 adenoviral particles. Hum Gene Ther 1997; 8: 453-465.
67. Klyushnichenko V, Bernier A, Kamen A, Harmsen E. Improved high-performance liquid chromatographic method in the analysis of adenovirus particles. J Chromatogr B 2001; 755: 27-36.
68. Transfiguracion J et al. Validation of a high-performance liquid chromatographic assay for the quantification of adenovirus type particles. J Chromatogr B 2001; 761: 187-194.
69. Vellekamp G et al. Empty capsids in column-purified recombinant adenovirus preparations. Hum Gene Ther 2001; 12: 1923-1936.
70. Debelak D et al. Cation-exchange high-performance liquid chromatography of recombinant adeno-associated virus type 2. J Chromatogr B 2000; 740: 195-202.
71. Mittereder N, March KL, Trapnell BC. Evaluation of the concentration and bioactivity of adenovirus vectors for gene therapy. J Virol 1996; 70: 7498-7509.
72. Lehmberg E et al. Reversed-phase high-performance liquid chromatographic assay for the adenovirus type 5 proteome. J Chromatogr B 1999; 732: 411-423.
73. Schnell MA et al. Activation of innate immunity in nonhuman primates following intraportal administration of adenoviral vectors. Mol Ther 2001; 3: 708-722.
74. Wickham TJ, Roelvink PW, Brough DE, Kovesdi I. Adenovirus targeted to heparan-containing receptors increases its gene delivery efficiency to multiple cell types. Nat Biotechnol 1996; 14: 1570-1573.
75. Douglas JT et al. A system for the propagation of adenoviral vectors with genetically modified receptor specificities. Nat Biotechnol 1999; 17: 470-475.
76. Parrott MB et al. Metabolically biotinylated adenovirus for cell targeting, ligand screening, and vector purification. Mol Ther 2003; 8: 688-700.
77. Sandig V et al. Optimization of the helper-dependent adenovirus system for production and potency in vivo. Proc Natl Acad Sci USA 2000; 97: 1002-1007.
78. Palmer D, Ng P. Improved system for helper-dependent adenoviral vector production. Mol Ther 2003; 8: 846-852.
79. Miao CH et al. Nonrandom transduction of recombinant adeno-asso- ciated virus vectors in mouse hepatocytes in vivo: cell cycling does not influence hepatocyte transduction. J Virol 2000; 74: 3793-3803.
80. Grimm D. Research advances in virology. In: Samal SK, Liebler- Tenorio E, Delsert C, Paton D (eds). Adeno-Associated Virus (AAV) S17 Serotypes as Vectors for Human Gene Therapy. Puthen Chalai, Global Research Network: India, 2000, pp 91-114.
81. Gao GP et al. Novel adeno-associated viruses from rhesus monkeys as vectors for human gene therapy. Proc Natl Acad Sci USA 2002; 99: 11854-11859.
82. Chao H et al. Several log increase in therapeutic transgene delivery by distinct adeno-associated viral serotype vectors. Mol Ther 2000; 2: 619-623.
83. Hildinger M et al. Hybrid vectors based on adeno-associated virus serotypes 2 and 5 for muscle-directed gene transfer. J Virol 2001; 75: 6199-6203.
84. Buning H et al. Receptor targeting of adeno-associated virus vectors. Gene Therapy 2003; 10: 1142-1151.
85. Wu P et al. Mutational analysis of the adeno-associated virus type 2 (AAV2) capsid gene and construction of AAV2 vectors with altered tropism. J Virol 2000; 74: 8635-8647.