Establishment and validation of new complementing cells for production of E1-deleted adenovirus vectors in serum-free suspension culture

Journal of Virological Methods

Volumn 208, Issue , 2014, Pages 177-188

  Gilbert, Rénald ^a,b   Guilbault, Claire ^a   Gagnon, David ^a   Bernier, Alice ^a   Bourget, Lucie ^a   Elahi, Seyyed Mehdy ^a   Kamen, Amine ^a,c   Massie, Bernard ^a,d  

^a NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c MCGILL UNIVERSITY   (Canada)

^d UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Adenovirus vectors; Cell line; Replication competent adenovirus; Serum free medium; Suspension culture

Indexed keywords

ADENOVIRUS VECTOR; CULTURE MEDIUM;

ADENOVIRUS; ARTICLE; CELL CLONING; CELL ENGINEERING; CONTROLLED STUDY; CYTOTOXICITY; E1A GENE; E1B GENE; GENE DELETION; GENE SILENCING; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; LUNG CARCINOMA; REPLICATION COMPETENT ADENOVIRUS; SUSPENSION CELL CULTURE; TRANSGENE; VIRUS GENE; BIOTECHNOLOGY; CELL LINE; CULTURE MEDIUM; EPITHELIUM CELL; GENE VECTOR; GENETICS; GROWTH, DEVELOPMENT AND AGING; HELPER CELL; HUMAN ADENOVIRUS C; PHARMACEUTICS; PHYSIOLOGY; PROCEDURES; VIRUS CULTURE; VIRUS LOAD;

ADENOVIRUSES, HUMAN; BIOTECHNOLOGY; CELL LINE; CULTURE MEDIA, SERUM-FREE; EPITHELIAL CELLS; GENETIC VECTORS; HUMANS; T-LYMPHOCYTES, HELPER-INDUCER; TECHNOLOGY, PHARMACEUTICAL; VIRAL LOAD; VIRUS CULTIVATION;

EID: 84909951511     PISSN: 01660934     EISSN: 18790984     Source Type: Journal    
DOI: 10.1016/j.jviromet.2014.08.013     Document Type: Article

References (48)

1. Acsadi G., Jani A., Massie B., Simoneau M., Holland P., Blaschuk K., Karpati G. A differential efficiency of adenovirus-mediated in vivo gene transfer into skeletal muscle cells of different maturity. Hum. Mol. Genet. 1994, 3:579-584.
2. Berdichevsky M., Gentile M.P., Hughes B., Meis P., Peltier J., Blumentals I., Aunins J., Altaras N.E. Establishment of higher passage PER.C6 cells for adenovirus manufacture. Biotechnol. Prog. 2008, 24:158-165.
3. Boulanger P.A., Blair G.E. Expression and interactions of human adenovirus oncoproteins. Biochem. J. 1991, 275:281-299.
4. Bourbeau D., Lau C.J., Jaime J., Koty Z., Zehntner S.P., Lavoie G., Mes-Masson A.M., Nalbantoglu J., Massie B. Improvement of antitumor activity by gene amplification with a replicating but nondisseminating adenovirus. Cancer Res. 2007, 67:3387-3395.
5. Bourbeau D., Lavoie G., Nalbantoglu J., Massie B. Suicide gene therapy with an adenovirus expressing the fusion gene CD::UPRT in human glioblastomas: different sensitivities correlate with p53 status. J. Gene Med. 2004, 6:1320-1332.
6. Bruder J.T., Appiah A., Kirkman W.M., Chen P., Tian J., Reddy D., Brough D.E., Lizonova A., Kovesdi I. Improved production of adenovirus vectors expressing apoptotic transgenes. Hum. Gene Ther. 2000, 11:139-149.
7. Choi Y.J., Morel L., Bourque D., Mullick A., Massie B., Miguez C.B. Bestowing inducibility on the cloned methanol dehydrogenase promoter (PmxaF) of Methylobacterium extorquens by applying regulatory elements of Pseudomonas putida F1. Appl. Environ. Microbiol. 2006, 72:7723-7729.
8. Cote J., Bourget L., Garnier A., Kamen A. Study of adenovirus production in serum-free 293SF suspension culture by GFP-expression monitoring. Biotechnol. Prog. 1997, 13:709-714.
9. Cote J., Garnier A., Massie B., Kamen A. Serum-free production of recombinant proteins and adenoviral vectors by 293SF-3F6 cells. Biotechnol. Bioeng. 1998, 59:567-575.
10. Crystal R.G. Adenovirus: the first effective in vivo gene delivery vector. Hum. Gene Ther. 2014, 25:3-11.
11. de Gruijl T.D., van de Ven R. Chapter six - adenovirus-based immunotherapy of cancer: promises to keep. Adv. Cancer Res. 2012, 115:147-220.
12. Fallaux F.J., Bout A., van der Velde I., van den Wollenberg D.J., Hehir K.M., Keegan J., Auger C., Cramer S.J., van Ormondt H., van der Eb A.J., Valerio D., Hoeben R.C. New helper cells and matched early region 1-deleted adenovirus vectors prevent generation of replication-competent adenoviruses. Hum. Gene Ther. 1998, 9:1909-1917.
13. Farson D., Tao L., Ko D., Li Q., Brignetti D., Segawa K., Mittelstaedt D., Harding T., Yu D.C., Li Y. Development of novel E1-complementary cells for adenoviral production free of replication-competent adenovirus. Mol. Ther. 2006, 14:305-311.
14. Gall J.G., Lizonova A., EttyReddy D., McVey D., Zuber M., Kovesdi I., Aughtman B., King C.R., Brough D.E. Rescue and production of vaccine and therapeutic adenovirus vectors expressing inhibitory transgenes. Mol. Biotechnol. 2007, 35:263-273.
15. Gao G.P., Engdahl R.K., Wilson J.M. 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.
16. Gervais C., Paquette D., Burns-Tardis A., Martin L., Massie B. Development of high output expression vectors for antibody production in mammalian cells. Animal Cell Technology: Basic & Applied Aspects 1998, 349-354. Kluwer Academic Publishers, Netherlands. K. Nagai, M. Wachi (Eds.).
17. Graham F.L., Smiley J., Russell W.C., Nairn R. Characteristics of a human cell line transformed by DNA from human adenovirus type 5. J. Gen. Virol. 1977, 36:59-74.
18. Graham F.L., van der Eb A.J. A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology 1973, 52:456-467.
19. Gu J., Zhang L., Huang X., Lin T., Yin M., Xu K., Ji L., Roth J.A., Fang B. A novel single tetracycline-regulative adenoviral vector for tumor-specific Bax gene expression and cell killing in vitro and in vivo. Oncogene 2002, 21:4757-4764.
20. Gunning P., Leavitt J., Muscat G., Ng S.Y., Kedes L. A human beta-actin expression vector system directs high-level accumulation of antisense transcripts. Proc. Natl. Acad. Sci. U. S. A 1987, 84:4831-4835.
21. Harlow E., Franza B.R., Schley C. Monoclonal antibodies specific for adenovirus early region 1A proteins: extensive heterogeneity in early region 1A products. J. Virol. 1985, 55:533-546.
22. 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.
23. Hehir K.M., Armentano D., Cardoza L.M., Choquette T.L., Berthelette P.B., White G.A., Couture L.A., Everton M.B., Keegan J., Martin J.M., Pratt D.A., Smith M.P., Smith A.E., Wadsworth S.C. Molecular characterization of replication-competent variants of adenovirus vectors and genome modifications to prevent their occurrence. J. Virol. 1996, 70:8459-8467.
24. Howe J.A., Pelka P., Antelman D., Wilson C., Cornell D., Hancock W., Ramachandra M., Avanzini J., Horn M., Wills K., Sutjipto S., Ralston R. Matching complementing functions of transformed cells with stable expression of selected viral genes for production of E1-deleted adenovirus vectors. Virology 2006, 345:220-230.
25. Imler J.L., Chartier C., Dreyer D., Dieterle A., Sainte-Marie M., Faure T., Pavirani A., Mehtali M. Novel complementation cell lines derived from human lung carcinoma A549 cells support the growth of E1-deleted adenovirus vectors. Gene Ther. 1996, 3:75-84.
26. Kagawa S., Pearson S.A., Ji L., Xu K., McDonnell T.J., Swisher S.G., Roth J.A., Fang B. A binary adenoviral vector system for expressing high levels of the proapoptotic gene bax. Gene Ther. 2000, 7:75-79.
27. Khare R., Chen C.Y., Weaver E.A., Barry M.A. Advances and future challenges in adenoviral vector pharmacology and targeting. Curr. Gene Ther. 2011, 11:241-258.
28. Kim J.S., Lee S.H., Cho Y.S., Park K., Kim Y.H., Lee J.H. Development of a packaging cell line for propagation of replication-deficient adenovirus vector. Exp. Mol. Med. 2001, 33:145-149.
29. Kovesdi I., Hedley S.J. Adenoviral producer cells. Viruses 2010, 2:1681-1703.
30. Lochmuller H., Jani A., Huard J., Prescott S., Simoneau M., Massie B., Karpati G., Acsadi G. Emergence of early region 1-containing replication-competent adenovirus in stocks of replication-defective adenovirus recombinants (delta E1+delta E3) during multiple passages in 293 cells. Hum. Gene Ther. 1994, 5:1485-1491.
31. Louis N., Evelegh C., Graham F.L. Cloning and sequencing of the cellular-viral junctions from the human adenovirus type 5 transformed 293 cell line. Virology 1997, 233:423-429.
32. Massie, B. Adenovirus E1 complementing cell line. Patent [US005891690A]. 4-6-1999.
33. Massie B., Couture F., Lamoureux L., Mosser D.D., Guilbault C., Jolicoeur P., Belanger F., Langelier Y. Inducible overexpression of a toxic protein by an adenovirus vector with a tetracycline-regulatable expression cassette. J. Virol. 1998, 72:2289-2296.
34. Matthews D.A., Cummings D., Evelegh C., Graham F.L., Prevec L. Development and use of a 293 cell line expressing lac repressor for the rescue of recombinant adenoviruses expressing high levels of rabies virus glycoprotein. J. Gen. Virol. 1999, 80:345-353.
35. Mullick A., Xu Y., Warren R., Koutroumanis M., Guilbault C., Broussau S., Malenfant F., Bourget L., Lamoureux L., Lo R., Caron A.W., Pilotte A., Massie B. The cumate gene-switch: a system for regulated expression in mammalian cells. BMC Biotechnol. 2006, 6:43.
36. Murakami P., Havenga M., Fawaz F., Vogels R., Marzio G., Pungor E., Files J., Do L., Goudsmit J., McCaman M. Common structure of rare replication-deficient E1-positive particles in adenoviral vector batches. J. Virol. 2004, 78:6200-6208.
37. Murakami P., Pungor E., Files J., Do L., van R.R., Vogels R., Bout A., McCaman M. A single short stretch of homology between adenoviral vector and packaging cell line can give rise to cytopathic effect-inducing, helper-dependent E1-positive particles. Hum. Gene Ther. 2002, 13:909-920.
38. Robert M.A., Zeng Y., Raymond B., Desfosse L., Mairey E., Tremblay J.P., Massie B., Gilbert R. Efficacy and site-specificity of adenoviral vector integration mediated by the phage phiC31 integrase. Hum. Gene Ther. Methods 2012, 23:393-407.
39. Rollier C.S., Reyes-Sandoval A., Cottingham M.G., Ewer K., Hill A.V. Viral vectors as vaccine platforms: deployment in sight. Curr. Opin. Immunol. 2011, 23:377-382.
40. Shen C.F., Kamen A. Hyperosmotic pressure on HEK 293 cells during the growth phase, but not the production phase, improves adenovirus production. J. Biotechnol. 2012, 157:228-236.
41. Shen C.F., Voyer R., Tom R., Kamen A. Reassessing culture media and critical metabolites that affect adenovirus production. Biotechnol. Prog. 2010, 26:200-207.
42. Transfiguracion J., Bernier A., Arcan N., Chahal P., Kamen A. Validation of high-performance liquid chromatographic assay for the quantification of adenovirus type 5 particles. J. Chromatogr. B 2001, 761:187-194.
43. Umana P., Gerdes C.A., Stone D., Davis J.R., Ward D., Castro M.G., Lowenstein P.R. Efficient FLPe recombinase enables scalable production of helper- dependent adenoviral vectors with negligible helper-virus contamination. Nat. Biotechnol. 2001, 19:582-585.
44. Xie L., Pilbrough W., Metallo C., Zhong T., Pikus L., Leung J., Aunins J.G., Zhou W. Serum-free suspension cultivation of PER.C6(R) cells and recombinant adenovirus production under different pH conditions. Biotechnol. Bioeng. 2002, 80:569-579.
45. Xu Q., Arevalo M.T., Pichichero M.E., Zeng M. A new complementing cell line for replication-incompetent E1-deleted adenovirus propagation. Cytotechnology 2006, 51:133-140.
46. Zhang X., Greenberg B.H., Cowling R.T. Improving the titer of recombinant adenovirus by suppressing problematic transgene transcription during packaging. Biotechniques 2008, 44:85-89.
47. Zhao C., Crews C.J., Derdeyn C.A., Blackwell J.L. Lac-regulated system for generating adenovirus 5 vaccine vectors expressing cytolytic human immunodeficiency virus 1 genes. J. Virol. Methods 2009, 160:101-110.
48. Zhu J., Grace M., Casale J., Chang A.T., Musco M.L., Bordens R., Greenberg R., Schaefer E., Indelicato S.R. Characterization of replication-competent adenovirus isolates from large-scale production of a recombinant adenoviral vector. Hum. Gene Ther. 1999, 10:113-121.