A rapid protocol for construction and production of high-capacity adenoviral vectors

Nature Protocols

Volumn 4, Issue 4, 2009, Pages 547-564

  Jager, Lorenz ^a   Hausl, Martin A ^a   Rauschhuber, Christina ^a   Wolf, Nicola M ^a   Kay, Mark A ^b   Erhardt, Anja ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; CESIUM CHLORIDE; GENOMIC DNA;

ARTICLE; CELL CULTURE; CELL DENSITY; CELL GROWTH; CELL SUSPENSION; CELL VIABILITY; CLONING VECTOR; CULTURE TECHNIQUE; DNA ISOLATION; DNA SEQUENCE; GENE AMPLIFICATION; GENE CONSTRUCT; GENE EXPRESSION; GENETIC PROCEDURES; HUMAN; HUMAN CELL; PRIORITY JOURNAL; TRANSGENE; VIRAL GENE DELIVERY SYSTEM; VIRUS CAPSID; VIRUS TITRATION;

ADENOVIRIDAE; CELL LINE; CLONING, MOLECULAR; DIALYSIS; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; GENOME, VIRAL; TRANSGENES; VIRUS CULTIVATION;

ANIMALIA; MIRIDAE;

EID: 64749089254     PISSN: 17542189     EISSN: 17502799     Source Type: Journal    
DOI: 10.1038/nprot.2009.4     Document Type: Article

References (68)

1. Luo, J. et al. A protocol for rapid generation of recombinant adenoviruses using the AdEasy system. Nat. Protoc. 2, 1236-1247 (2007).
2. Yang, Y., Ertl, H.C. & Wilson, J.M. MHC class I-restricted cytotoxic T lymphocytes to viral antigens destroy hepatocytes in mice infected with E1-deleted recombinant adenoviruses. Immunity 1, 433-442 (1994).
3. Hardy, S., Kitamura, M., Harris-Stansil, T., Dai, Y. & Phipps, M.L. Construction of adenovirus vectors through Cre-lox recombination. J. Virol. 71, 1842-1849 (1997).
4. Hartigan-O'Connor, D., Amalfitano, A. & Chamberlain, J.S. Improved production of gutted adenovirus in cells expressing adenovirus preterminal protein and DNA polymerase. J. Virol. 73, 7835-7841 (1999).
5. Fisher, K.J., Choi, H., Burda, J., Chen, S.J. & Wilson, J.M. Recombinant adenovirus deleted of all viral genes for gene therapy of cystic fibrosis. Virology 217, 11-22 (1996).
6. Parks, R.J. 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 93, 13565-13570 (1996).
7. Zhang, Y. & Bergelson, J.M. Adenovirus receptors. J. Virol. 79 12125-12131 (2005).
8. Benihoud, K., Yeh, P. & Perricaudet, M. Adenovirus vectors for gene delivery. Curr. Opin. Biotechnol. 10, 440-447 (1999).
9. Kozarsky, K.F. & Wilson, J.M. Gene therapy: Adenovirus vectors. Curr. Opin. Genet. Dev. 3, 499-503 (1993).
10. Wickham, T.J., Roelvink, P.W., Brough, D.E. & Kovesdi, I. Adenovirus targeted to heparan-containing receptors increases its gene delivery efficiency to multiple cell types. Nat. Biotechnol. 14, 1570-1573 (1996).
11. Kawano, R. et al. Transduction of full-length dystrophin to multiple skeletal muscles improves motor performance and life span in utrophin/dystrophin double knockout mice. Mol. Ther. 16, 825-831 (2008).
12. Deol, J.R. et al. Successful compensation for dystrophin deficiency by a helper-dependent adenovirus expressing full-length utrophin. Mol. Ther. 15, 1767-1774 (2007).
13. Gilbert, R. et al. Prolonged dystrophin expression and functional correction of mdx mouse muscle following gene transfer with a helper-dependent (gutted) adenovirus-encoding murine dystrophin. Hum. Mol. Genet. 12, 1287-1299 (2003).
14. Brown, B.D. et al. Helper-dependent adenoviral vectors mediate therapeutic factor VIII expression for several months with minimal accompanying toxicity in a canine model of severe hemophilia A. Blood 103, 804-810 (2004).
15. McCormack, W.M. Jr. et al. Helper-dependent adenoviral gene therapy mediates longterm correction of the clotting defect in the canine hemophilia A model. J. Thromb. Haemost. 4, 1218-1225 (2006).
16. Cerullo, V. et al. Correction of murine hemophilia A and immunological differences of factor VIII variants delivered by helper-dependent adenoviral vectors. Mol. Ther. 15, 2080-2087 (2007).
17. Koeberl, D.D. et al. Efficacy of helper-dependent adenovirus vector-mediated gene therapy in murine glycogen storage disease type Ia. Mol. Ther. 15, 1253-1258 (2007).
18. Oka, K. et al. Sustained phenotypic correction in a mouse model of hypoalphalipoproteinemia with a helper-dependent adenovirus vector. Gene. Ther. 14, 191-202 (2007).
19. Toietta, G. et al. Lifelong elimination of hyperbilirubinemia in the Gunn rat with a single injection of helper-dependent adenoviral vector. Proc. Natl. Acad. Sci. USA 102, 3930-3935 (2005).
20. Mian, A. et al. Long-term correction of ornithine transcarbamylase deficiency by WPREmediated overexpression using a helper-dependent adenovirus. Mol. Ther. 10, 492-499 (2004).
21. Nomura, S. et al. Low-density lipoprotein receptor gene therapy using helper-dependent adenovirus produces long-term protection against atherosclerosis in a mouse model of familial hypercholesterolemia. Gene. Ther. 11, 1540-1548 (2004).
22. Brunetti-Pierri, N. et al. Sustained phenotypic correction of canine hemophilia B after systemic administration of helper-dependent adenoviral vector. Hum. Gene. Ther. 16, 811-820 (2005).
23. Ehrhardt, A. et al. A gene-deleted adenoviral vector results in phenotypic correction of canine hemophilia B without liver toxicity or thrombocytopenia. Blood 102, 2403-2411 (2003).
24. Ehrhardt, A. & Kay, M.A. A new adenoviral helper-dependent vector results in long-term therapeutic levels of human coagulation factor IX at low doses in vivo. Blood 99, 3923-3930 (2002).
25. Lamartina, S. et al. Helper-dependent adenovirus for the gene therapy of proliferative retinopathies: Stable gene transfer, regulated gene expression and therapeutic efficacy. J. Gene. Med. 9, 862-874 (2007).
26. Butti, E. et al. IL4 gene delivery to the CNS recruits regulatory T cells and induces clinical recovery in mouse models of multiple sclerosis. Gene. Ther. 15, 504-515 (2008).
27. Brunetti-Pierri, N. et al. Pseudo-hydrodynamic delivery of helper-dependent adenoviral vectors into non-human primates for liver-directed gene therapy. Mol. Ther. 15, 732-740 (2007).
28. Jager, L. & Ehrhardt, A. Emerging adenoviral vectors for stable correction of genetic disorders. Curr. Gene. Ther. 7, 272-283 (2007).
29. Soifer, H. et al. A novel, helper-dependent, adenovirus-retrovirus hybrid vector: Stable transduction by a two-stage mechanism. Mol. Ther. 5, 599-608 (2002).
30. Picard-Maureau, M. et al. Foamy virus-adenovirus hybrid vectors. Gene. Ther. 11, 722-728 (2004).
31. Yant, S.R. et al. Transposition from a gutless adeno-transposon vector stabilizes transgene expression in vivo. Nat. Biotechnol. 20, 999-1005 (2002).
32. Ehrhardt, A. et al. Somatic integration from an adenoviral hybrid vector into a hot spot in mouse liver results in persistent transgene expression levels in vivo. Mol. Ther. 15, 146-156 (2007).
33. Lieber, A., Steinwaerder, D.S., Carlson, C.A. & Kay, M.A. Integrating adenovirus-adenoassociated virus hybrid vectors devoid of all viral genes. J. Virol. 73, 9314-9324 (1999).
34. Recchia, A., Perani, L., Sartori, D., Olgiati, C. & Mavilio, F. Site-specific integration of functional transgenes into the human genome by adeno/AAV hybrid vectors. Mol. Ther. 10, 660-670 (2004).
35. Kreppel, F. & Kochanek, S. Long-term transgene expression in proliferating cells mediated by episomally maintained high-capacity adenovirus vectors. J. Virol. 78, 9-22 (2004).
36. Dorigo, O. et al. Development of a novel helper-dependent adenovirus-Epstein-Barr virus hybrid system for the stable transformation of mammalian cells. J Virol 78, 6556-6566 (2004).
37. Suzuki, K. et al. Highly efficient transient gene expression and gene targeting in primate embryonic stem cells with helper-dependent adenoviral vectors. Proc. Natl. Acad. Sci. USA 105, 13781-13786 (2008).
38. Ohbayashi, F. et al. Correction of chromosomal mutation and random integration in embryonic stem cells with helper-dependent adenoviral vectors. Proc. Natl. Acad. Sci. USA 102, 13628-13633 (2005).
39. Cregan, S.P. et al. Helper-dependent adenovirus vectors: Their use as a gene delivery system to neurons. Gene. Ther. 7, 1200-1209 (2000).
40. Wang, H., Cao, H., Wohlfahrt, M., Kiem, H.P. & Lieber, A. Tightly regulated gene expression in human hematopoietic stem cells after transduction with helperdependent Ad5/35 vectors. Exp. Hematol. 36, 823-831 (2008).
41. Balamotis, M.A., Huang, K. & Mitani, K. Efficient delivery and stable gene expression in a hematopoietic cell line using a chimeric serotype 35 fiber pseudotyped helperdependent adenoviral vector. Virology 324, 229-237 (2004).
42. Cerullo, V. et al. Toll-like receptor 9 triggers an innate immune response to helper-dependent adenoviral vectors. Mol. Ther. 15 378-385 (2007).
43. Zhu, J., Huang, X. & Yang, Y. Innate immune response to adenoviral vectors is mediated by both Toll-like receptor-dependent and -independent pathways. J. Virol. 81, 3170-3180 (2007).
44. Koehler, D.R. et al. Aerosol delivery of an enhanced helper-dependent adenovirus formulation to rabbit lung using an intratracheal catheter. J. Gene. Med. 7, 1409-1420 (2005).
45. Croyle, M.A., Yu, Q.C. & Wilson, J.M. Development of a rapid method for the PEGylation of adenoviruses with enhanced transduction and improved stability under harsh storage conditions. Hum. Gene. Ther. 11 1713-1722 (2000).
46. Ruzsics, Z. et al. Transposon-assisted cloning and traceless mutagenesis of adenoviruses: Development of a novel vector based on species D. J. Virol. 80, 8100-8113 (2006).
47. Umana, P. et al. Efficient FLPe recombinase enables scalable production of helperdependent adenoviral vectors with negligible helper-virus contamination. Nat. Biotechnol. 19, 582-585 (2001).
48. Ng, P., Beauchamp, C., Evelegh, C., Parks, R. & Graham, F.L. Development of a FLP/frt system for generating helper-dependent adenoviral vectors. Mol. Ther. 3, 809-815 (2001).
49. Meneses-Acosta, A. et al. Development of a suspension serum-free helper-dependent adenovirus production system and assessment of co-infection conditions. J. Virol. Methods 148, 106-114 (2008).
50. Zhou, H. et al. A Cre-expressing cell line and an E1/E2a double-deleted virus for preparation of helper-dependent adenovirus vector. Mol. Ther. 3, 613-622 (2001).
51. Barjot, C., Hartigan-O'Connor, D., Salvatori, G., Scott, J.M. & Chamberlain, J.S. Gutted adenoviral vector growth using E1/E2b/ E3-deleted helper viruses. J. Gene. Med. 4, 480-489 (2002).
52. Ng, P., Parks, R.J. & Graham, F.L. Preparation of helper-dependent adenoviral vectors. Methods Mol. Med. 69, 371-388 (2002).
53. Sandig, V. et al. Optimization of the helper-dependent adenovirus system for production and potency in vivo. Proc. Natl. Acad. Sci. USA 97, 1002-1007 (2000).
54. Rauschhuber, C., Xu, H., Salazar, F.H., Marion, P.L. & Ehrhardt, A. Exploring genedeleted adenoviral vectors for delivery of short hairpin RNAs and reduction of hepatitis B virus infection in mice. J. Gene. Med. 10, 878-889 (2008).
55. Palmer, D. & Ng, P. Improved system for helper-dependent adenoviral vector production. Mol. Ther. 8, 846-852 (2003).
56. Hillgenberg, M., Schnieders, F., Loser, P. & Strauss, M. System for efficient helperdependent minimal adenovirus construction and rescue. Hum. Gene. Ther. 12, 643-657 (2001).
57. Shi, C.X., Graham, F.L. & Hitt, M.M. A convenient plasmid system for construction of helper-dependent adenoviral vectors and its application for analysis of the breastcancer-specific mammaglobin promoter. J. Gene. Med. 8, 442-451 (2006).
58. Toietta, G. et al. Generation of helper-dependent adenoviral vectors by homologous recombination. Mol. Ther. 5, 204-210 (2002).
59. Mizuguchi, H. & Kay, M.A. Efficient construction of a recombinant adenovirus vector by an improved in vitro ligation method. Hum. Gene. Ther. 9, 2577-2583 (1998).
60. Parks, R.J. & Graham, F.L. A helper-dependent system for adenovirus vector production helps define a lower limit for efficient DNA packaging. J. Virol. 71, 3293-3298 (1997).
61. Bett, A.J., Prevec, L. & Graham, F.L. Packaging capacity and stability of human adenovirus type 5 vectors. J. Virol. 67, 5911-5921 (1993).
62. Sambrook, J. & Russell, D.W. Molecular Cloning: A Laboratory Manual (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, 2001).
63. Offringa, R., Kwappenberg, K., Rabelink, M., Rea, D. & Hoeben, R. Adenoviral transduction of dendritic cells. Methods Mol. Med. 109, 83-96 (2005).
64. Ugai, H. et al. Stability of a recombinant adenoviral vector: optimization of conditions for storage, transport and delivery. Jpn. J. Cancer. Res. 93, 598-603 (2002).
65. Nyberg-Hoffman, C. & Aguilar-Cordova, E. Instability of adenoviral vectors during transport and its implication for clinical studies. Nat. Med. 5, 955-957 (1999).
66. Puntel, M. et al. Quantification of high-capacity helper-dependent adenoviral vector genomes in vitro and in vivo, using quantitative TaqMan real-time polymerase chain reaction. Hum. Gene. Ther. 17, 531-544 (2006).
67. Palmer, D.J. & Ng, P. Physical and infectious titers of helper-dependent adenoviral vectors: A method of direct comparison to the adenovirus reference material. Mol. Ther. 10, 792-798 (2004).
68. Haase, S.B. & Calos, M.P. Replication control of autonomously replicating human sequences. Nucleic Acids. Res. 19, 5053-5058 (1991).