Production of lentiviral vectors

Molecular Therapy Methods and Clinical Development

Volumn 3, Issue , 2016, Pages 16017-

  Merten, Otto Wilhelm ^a   Hebben, Matthias ^a   Bovolenta, Chiara ^b  

^a GÉNÉTHON   (France)

^b MOLMED S P A   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

LENTIVIRUS VECTOR;

BIOTECHNOLOGICAL PRODUCTION; CELL LINE; DOWNSTREAM PROCESSING; HUMAN; LARGE SCALE PRODUCTION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SUSPENSION CELL CULTURE; VIRUS PURIFICATION; HEK293 CELL LINE; HOLLOW FIBER REACTOR; HUMAN CELL; HUMAN CELL CULTURE; PACKAGING; RARE DISEASE; SAFETY; TRANSIENT TRANSFECTION; VIRAL GENE THERAPY;

EID: 85015227552     PISSN: None     EISSN: 23290501     Source Type: Journal    
DOI: 10.1038/mtm.2016.17     Document Type: Review

References (126)

1. 1 Salmon, F, Grosios, K, Petry, H, Safety profile of recombinant adeno-associated viral vectors: focus on alipogene tiparvovec (Glybera®). Expert Rev Clin Pharmacol 7 (2014), 53–65.
2. 2 Andreadis, ST, Roth, CM, Le Doux, JM, Morgan, JR, Yarmush, ML, Large-scale processing of recombinant retroviruses for gene therapy. Biotechnol Prog 15 (1999), 1–11.
3. 3 Delenda, C, Lentiviral vectors: optimization of packaging, transduction and gene expression. J Gene Med 6:suppl. 1 (2004), S125–S138.
4. 4 Cavazzana-Calvo, M, Hacein-Bey, S, de Saint Basile, G, Gross, F, Yvon, E, Nusbaum, P, et al. Gene therapy of human severe combined immunodeficiency (SCID)-X1 disease. Science 288 (2000), 669–672.
5. 5 Naldini, L, Blömer, U, Gallay, P, Ory, D, Mulligan, R, Gage, FH, et al. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272 (1996), 263–267.
6. 6 Montini, E, Cesana, D, Schmidt, M, Sanvito, F, Bartholomae, CC, Ranzani, M, et al. The genotoxic potential of retroviral vectors is strongly modulated by vector design and integration site selection in a mouse model of HSC gene therapy. J Clin Invest 119 (2009), 964–975.
7. 7 Mukherjee, S, Thrasher, AJ, Gene therapy for PIDs: progress, pitfalls and prospects. Gene 525 (2013), 174–181.
8. 8 Aiuti, A, Biasco, L, Scaramuzza, S, Ferrua, F, Cicalese, MP, Baricordi, C, et al. Lentiviral hematopoietic stem cell gene therapy in patients with Wiskott–Aldrich syndrome. Science, 341, 2013, 1233151.
9. 9 Cartier, N, Hacein-Bey-Abina, S, Bartholomae, CC, Veres, G, Schmidt, M, Kutschera, I, et al. Hematopoietic stem cell gene therapy with a lentiviral vector in X-linked adrenoleukodystrophy. Science 326 (2009), 818–823.
10. 10 Biffi, A, Montini, E, Lorioli, L, Cesani, M, Fumagalli, F, Plati, T, et al. Lentiviral hematopoietic stem cell gene therapy benefits metachromatic leukodystrophy. Science, 341, 2013, 1233158.
11. 11 Cavazzana-Calvo, M, Payen, E, Negre, O, Wang, G, Hehir, K, Fusil, F, et al. Transfusion independence and HMGA2 activation after gene therapy of human β-thalassaemia. Nature 467 (2010), 318–322.
12. 12 Palfi, S, Gurruchaga, JM, Ralph, GS, Lepetit, H, Lavisse, S, Buttery, PC, et al. Long-term safety and tolerability of ProSavin, a lentiviral vector-based gene therapy for Parkinson's disease: a dose escalation, open-label, phase 1/2 trial. Lancet 383 (2014), 1138–1146.
13. 13 Levine, BL, Performance-enhancing drugs: design and production of redirected chimeric antigen receptor (CAR) T cells. Cancer Gene Ther 22 (2015), 79–84.
14. 14 Poeschla, E, Gilbert, J, Li, X, Huang, S, Ho, A, Wong-Staal, F, Identification of a human immunodeficiency virus type 2 (HIV-2) encapsidation determinant and transduction of nondividing human cells by HIV-2-based lentivirus vectors. J Virol 72 (1998), 6527–6536.
15. 15 Kim, SS, Kothari, N, You, XJ, Robinson, WE Jr, Schnell, T, Uberla, K, et al. Generation of replication-defective helper-free vectors based on simian immunodeficiency virus. Virology 282 (2001), 154–167.
16. 16 Curran, MA, Kaiser, SM, Achacoso, PL, Nolan, GP, Efficient transduction of nondividing cells by optimized feline immunodeficiency virus vectors. Mol Ther 1 (2000), 31–38.
17. 17 Berkowitz, RD, Ilves, H, Plavec, I, Veres, G, Gene transfer systems derived from Visna virus: analysis of virus production and infectivity. Virology 279 (2001), 116–129.
18. 18 Mselli-Lakhal, L, Guiguen, F, Greenland, T, Mornex, JF, Chebloune, Y, Gene transfer system derived from the caprine arthritis-encephalitis lentivirus. J Virol Methods 136 (2006), 177–184.
19. 19 Mitrophanous, K, Yoon, S, Rohll, J, Patil, D, Wilkes, F, Kim, V, et al. Stable gene transfer to the nervous system using a non-primate lentiviral vector. Gene Ther 6 (1999), 1808–1818.
20. 20 Ramezani, A, Hawley, RG, Overview of the HIV-1 lentiviral vector system. Curr Protoc Mol Biol, 2002 (Chapter 16: Unit 16.21).
21. 21 Dull, T, Zufferey, R, Kelly, M, Mandel, RJ, Nguyen, M, Trono, D, et al. A third-generation lentivirus vector with a conditional packaging system. J Virol 72 (1998), 8463–8471.
22. 22 Kim, VN, Mitrophanous, K, Kingsman, SM, Kingsman, AJ, Minimal requirement for a lentivirus vector based on human immunodeficiency virus type 1. J Virol 72 (1998), 811–816.
23. 23 Miyoshi, H, Blömer, U, Takahashi, M, Gage, FH, Verma, IM, Development of a self-inactivating lentivirus vector. J Virol 72 (1998), 8150–8157.
24. 24 Zufferey, R, Dull, T, Mandel, RJ, Bukovsky, A, Quiroz, D, Naldini, L, et al. Self-inactivating lentivirus vector for safe and efficient in vivo gene delivery. J Virol 72 (1998), 9873–9880.
25. 25 Schambach, A, Swaney, WP, van der Loo, JC, Design and production of retro- and lentiviral vectors for gene expression in hematopoietic cells. Methods Mol Biol 506 (2009), 191–205.
26. 26 Throm, RE, Ouma, AA, Zhou, S, Chandrasekaran, A, Lockey, T, Greene, M, et al. Efficient construction of producer cell lines for a SIN lentiviral vector for SCID-X1 gene therapy by concatemeric array transfection. Blood 113 (2009), 5104–5110.
27. 27 Frecha, C, Szécsi, J, Cosset, FL, Verhoeyen, E, Strategies for targeting lentiviral vectors. Curr Gene Ther 8 (2008), 449–460.
28. 28 Swanstrom, R, Wills, JW, Synthesis, assembly, and processing of viral proteins. Coffin, J, Hughes, SH, Varmus, H, (eds.) Retroviruses, 1997, Cold Spring Harbor Laboratory Press, Cold Spring Harbor/NY, 263–334.
29. 29 Kotsopoulou, E, Kim, VN, Kingsman, AJ, Kingsman, SM, Mitrophanous, KA, A Rev-independent human immunodeficiency virus type 1 (HIV-1)-based vector that exploits a codon-optimized HIV-1 gag-pol gene. J Virol 74 (2000), 4839–4852.
30. 30 Wagner, R, Graf, M, Bieler, K, Wolf, H, Grunwald, T, Foley, P, et al. Rev-independent expression of synthetic gag-pol genes of human immunodeficiency virus type 1 and simian immunodeficiency virus: implications for the safety of lentiviral vectors. Hum Gene Ther 11 (2000), 2403–2413.
31. 31 Sastry, L, Xu, Y, Johnson, T, Desai, K, Rissing, D, Marsh, J, et al. Certification assays for HIV-1-based vectors: frequent passage of gag sequences without evidence of replication-competent viruses. Mol Ther 8 (2003), 830–839.
32. 32 Tareen, SU, Nicolai, CJ, Campbell, DJ, Flynn, PA, Slough, MM, Vin, CD, et al. A Rev-independent gag/pol eliminates detectable psi-gag recombination in lentiviral vectors. Biores Open Access 2 (2013), 421–430.
33. 33 Fernandes, J, Jayaraman, B, Frankel, A, The HIV-1 Rev response element: an RNA scaffold that directs the cooperative assembly of a homo-oligomeric ribonucleoprotein complex. RNA Biol 9 (2012), 6–11.
34. 34 Zolotukhin, AS, Valentin, A, Pavlakis, GN, Felber, BK, Continuous propagation of RRE(−) and Rev(−)RRE(−) human immunodeficiency virus type 1 molecular clones containing a cis-acting element of simian retrovirus type 1 in human peripheral blood lymphocytes. J Virol 68 (1994), 7944–7952.
35. 35 Gasmi, M, Glynn, J, Jin, MJ, Jolly, DJ, Yee, JK, Chen, ST, Requirements for efficient production and transduction of human immunodeficiency virus type 1-based vectors. J Virol 73 (1999), 1828–1834.
36. 36 Nappi, F, Schneider, R, Zolotukhin, A, Smulevitch, S, Michalowski, D, Bear, J, et al. Identification of a novel posttranscriptional regulatory element by using a rev- and RRE-mutated human immunodeficiency virus type 1 DNA proviral clone as a molecular trap. J Virol 75 (2001), 4558–4569.
37. 37 Rohll, JB, Mitrophanous, KA, Martin-Rendon, E, Ellard, FM, Radcliffe, PA, Mazarakis, ND, et al. Design, production, safety, evaluation, and clinical applications of nonprimate lentiviral vectors. Methods Enzymol 346 (2002), 466–500.
38. 38 Levine, BL, Humeau, LM, Boyer, J, MacGregor, RR, Rebello, T, Lu, X, et al. Gene transfer in humans using a conditionally replicating lentiviral vector. Proc Natl Acad Sci USA 103 (2006), 17372–17377.
39. 39 Lu, X, Humeau, L, Slepushkin, V, Binder, G, Yu, Q, Slepushkina, T, et al. Safe two-plasmid production for the first clinical lentivirus vector that achieves >99% transduction in primary cells using a one-step protocol. J Gene Med 6 (2004), 963–973.
40. 40 Schonely, K, Afable, C, Slepushkin, V, Lu, X, Andre, K, Boehmer, J, et al. QC release testing of an HIV-1 based lentiviral vector lot and transduced cellular product. Bioproc J 2 (2003), 39–47.
41. 41 Gama-Norton, L, Botezatu, L, Herrmann, S, Schweizer, M, Alves, PM, Hauser, H, et al. Lentivirus production is influenced by SV40 large T-antigen and chromosomal integration of the vector in HEK293 cells. Hum Gene Ther 22 (2011), 1269–1279.
42. 42 Merten, OW, Charrier, S, Laroudie, N, Fauchille, S, Dugué, C, Jenny, C, et al. Large-scale manufacture and characterization of a lentiviral vector produced for clinical ex vivo gene therapy application. Hum Gene Ther 22 (2011), 343–356.
43. 43 Ausubel, LJ, Hall, C, Sharma, A, Shakeley, R, Lopez, P, Quezada, V, et al. Production of CGMP-grade lentiviral vectors. Bioprocess Int 10 (2012), 32–43.
44. 44 Smith, SL, Shioda, T, Advantages of COS-1 monkey kidney epithelial cells as packaging host for small-volume production of high-quality recombinant lentiviruses. J Virol Methods 157 (2009), 47–54.
45. 45 Marino, MP, Luce, MJ, Reiser, J, Small- to large-scale production of lentivirus vectors. Methods Mol Biol 229 (2003), 43–55.
46. 46 Graham, FL, van der Eb, AJ, A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology 52 (1973), 456–467.
47. 47 Boussif, O, Lezoualc'h, F, Zanta, MA, Mergny, MD, Scherman, D, Demeneix, B, et al. A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: polyethylenimine. Proc Natl Acad Sci USA 92 (1995), 7297–7301.
48. 48 Kuroda, H, Kutner, RH, Bazan, NG, Reiser, J, Simplified lentivirus vector production in protein-free media using polyethylenimine-mediated transfection. J Virol Methods 157 (2009), 113–121.
49. 49 Pham, PL, Kamen, A, Durocher, Y, Large-scale transfection of mammalian cells for the fast production of recombinant protein. Mol Biotechnol 34 (2006), 225–237.
50. 50 Kutner, RH, Zhang, XY, Reiser, J, Production, concentration and titration of pseudotyped HIV-1-based lentiviral vectors. Nat Protoc 4 (2009), 495–505.
51. 51 Patel, M, Wilcox, DA, Giddings, AM, McKay, TR, Olsen, JC, Modification of HEk 293 cell integrin expression profile allows convenient large-scale roller bottle production of lentiviral vectors. Mol Ther, 9, 2004, S33.
52. 52 Slepushkin, V, Chang, N, Cohen, R, Gan, Y, Jiang, B, Deausen, E, et al. Large-scale purification of a lentiviral vector by size exclusion chromatography or Mustang Q ion exchange chromatography. Bioproc J 2 (2003), 89–95.
53. 53 Karolewski, BA, Watson, DJ, Parente, MK, Wolfe, JH, Comparison of transfection conditions for a lentivirus vector produced in large volumes. Hum Gene Ther 14 (2003), 1287–1296.
54. 54 Negré, O, Denaro, M, Gillet-Legrand, B, Fusil, F, Hehir, K, Dorazio, R, et al. Long-term correction of murine beta-thalassemia following busulfan conditioning and transplant of bone marrow transduced with clinical-grade lentiviral vector (LentiGlobin™). Mol Ther, 16, 2008, S85.
55. 55 Dupont, F, Large Scale Manufacturing of a Lentiviral Vector (ProSavin®) for Phase I/II Clinical Trial, 2008 Presented at the CONSERT Labcourse, Evry/F, 29 June–1 July 2008.
56. 56 Greene, MR, Lockey, T, Mehta, PK, Kim, YS, Eldridge, PW, Gray, JT, et al. Transduction of human CD34+ repopulating cells with a self-inactivating lentiviral vector for SCID-X1 produced at clinical scale by a stable cell line. Hum Gene Ther Methods 23 (2012), 297–308.
57. 57 Chang, LJ, Zaiss, AK, Lentiviral vectors. Preparation and use. Methods Mol Med 69 (2002), 303–318.
58. 58 Follenzi, A, Naldini, L, HIV-based vectors. Preparation and use. Methods Mol Med 69 (2002), 259–274.
59. 59 Reiser, J, Production and concentration of pseudotyped HIV-1-based gene transfer vectors. Gene Ther 7 (2000), 910–913.
60. 60 Ballas, C, Johnson, TT, Cornetta, K, Harvest Timing and Media Composition Effects on Lentiviral Vector Production, 2005 Presented at the 8th Annual Meeting of the ASGT, 1 June–5 June 2005, St. Louis, MO.
61. 61 Couture, LA, Vector Production in Support of Early Clinical Trials, 2008 Presented at the ASGT Meeting, 28 May–1 June 2008, Boston, MA.
62. 62 Sheu, J, Beltzer, J, Fury, B, Wilczek, K, Tobin, S, Falconer, D, et al. Large-scale production of lentiviral vector in a closed system hollow fiber bioreactor. Mol Ther Methods Clin Dev, 2, 2015, 15020.
63. 63 Marceau, N, Gasmi, M, Scalable lentiviral vector production system compatible with industrial pharmaceutical applications, 2013 WO 2013076309 A1.
64. 64 Witting, SR, Li, LH, Jasti, A, Allen, C, Cornetta, K, Brady, J, et al. Efficient large volume lentiviral vector production using flow electroporation. Hum Gene Ther 23 (2012), 243–249.
65. 65 Ansorge, S, Lanthier, S, Transfiguracion, J, Durocher, Y, Henry, O, Kamen, A, Development of a scalable process for high-yield lentiviral vector production by transient transfection of HEK293 suspension cultures. J Gene Med 11 (2009), 868–876.
66. 66 Durocher, Y, Perret, S, Kamen, A, High-level and high-throughput recombinant protein production by transient transfection of suspension-growing human 293-EBNA1 cells. Nucleic Acids Res, 30, 2002, E9.
67. 67 Tom, R, Bisson, L, Durocher, Y, Transfection of HEK293-EBNA1 cells in suspension with linear PEI for production of recombinant proteins. CSH Protoc, 2008, 2008, 4977.
68. 68 Jaalouk, DE, Crosato, M, Brodt, P, Galipeau, J, Inhibition of histone deacetylation in 293GPG packaging cell line improves the production of self-inactivating MLV-derived retroviral vectors. Virol J, 3, 2006, 27.
69. 69 Sena-Esteves, M, Tebbets, JC, Steffens, S, Crombleholme, T, Flake, AW, Optimized large-scale production of high titer lentivirus vector pseudotypes. J Virol Methods 122 (2004), 131–139.
70. 70 Gossen, M, Bujard, H, Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc Natl Acad Sci USA 89 (1992), 5547–5551.
71. 71 Yu, H, Rabson, AB, Kaul, M, Ron, Y, Dougherty, JP, Inducible human immunodeficiency virus type 1 packaging cell lines. J Virol 70 (1996), 4530–4537.
72. 72 Kaul, M, Yu, H, Ron, Y, Dougherty, JP, Regulated lentiviral packaging cell line devoid of most viral cis-acting sequences. Virology 249 (1998), 167–174.
73. 73 Xu, K, Ma, H, McCown, TJ, Verma, IM, Kafri, T, Generation of a stable cell line producing high-titer self-inactivating lentiviral vectors. Mol Ther 3 (2001), 97–104.
74. 74 Cockrell, AS, Ma, H, Fu, K, McCown, TJ, Kafri, T, A trans-lentiviral packaging cell line for high-titer conditional self-inactivating HIV-1 vectors. Mol Ther 14 (2006), 276–284.
75. 75 Ni, Y, Sun, S, Oparaocha, I, Humeau, L, Davis, B, Cohen, R, et al. Generation of a packaging cell line for prolonged large-scale production of high-titer HIV-1-based lentiviral vector. J Gene Med 7 (2005), 818–834.
76. 76 Ikeda, Y, Takeuchi, Y, Martin, F, Cosset, FL, Mitrophanous, K, Collins, M, Continuous high-titer HIV-1 vector production. Nat Biotechnol 21 (2003), 569–572.
77. 77 Wielgosz, MM, Kim, YS, Carney, GG, Zhan, J, Reddivari, M, Coop, T, et al. Generation of a lentiviral vector producer cell clone for human Wiskott–Aldrich syndrome gene therapy. Mol Ther Methods Clin Dev, 2, 2015, 14063.
78. 78 Bonner, M, Ma, Z, Zhou, S, Ren, A, Chandrasekaran, A, Gray, JT, et al. Development of a Second Generation Stable Lentiviral Packaging Cell Line In Support Of Clinical Gene Therapy Protocols. http://wwwabstracts2viewcom/asgct/indexphp, 2015 In: 18th ASGCT Annual Meeting, New Orleans.
79. 80 Stewart, HJ, Leroux-Carlucci, MA, Sion, CJ, Mitrophanous, KA, Radcliffe, PA, Development of inducible EIAV-based lentiviral vector packaging and producer cell lines. Gene Ther 16 (2009), 805–814.
80. 81 Stewart, HJ, Fong-Wong, L, Strickland, I, Chipchase, D, Kelleher, M, Stevenson, L, et al. A stable producer cell line for the manufacture of a lentiviral vector for gene therapy of Parkinson's disease. Hum Gene Ther 22 (2011), 357–369.
81. 82 Broussau, S, Jabbour, N, Lachapelle, G, Durocher, Y, Tom, R, Transfiguracion, J, et al. Inducible packaging cells for large-scale production of lentiviral vectors in serum-free suspension culture. Mol Ther 16 (2008), 500–507.
82. 83 Pacchia, AL, Adelson, ME, Kaul, M, Ron, Y, Dougherty, JP, An inducible packaging cell system for safe, efficient lentiviral vector production in the absence of HIV-1 accessory proteins. Virology 282 (2001), 77–86.
83. 84 Sparacio, S, Pfeiffer, T, Schaal, H, Bosch, V, Generation of a flexible cell line with regulatable, high-level expression of HIV Gag/Pol particles capable of packaging HIV-derived vectors. Mol Ther 3 (2001), 602–612.
84. 85 Sanber, KS, Knight, SB, Stephen, SL, Bailey, R, Escors, D, Minshull, J, et al. Construction of stable packaging cell lines for clinical lentiviral vector production. Sci Rep, 5, 2015, 9021.
85. 86 Coroadinha, AS, Schucht, R, Gama-Norton, L, Wirth, D, Hauser, H, Carrondo, MJ, The use of recombinase mediated cassette exchange in retroviral vector producer cell lines: predictability and efficiency by transgene exchange. J Biotechnol 124 (2006), 457–468.
86. 87 Schucht, R, Coroadinha, AS, Zanta-Boussif, MA, Verhoeyen, E, Carrondo, MJ, Hauser, H, et al. A new generation of retroviral producer cells: predictable and stable virus production by Flp-mediated site-specific integration of retroviral vectors. Mol Ther 14 (2006), 285–292.
87. 88 Carrondo, M, Panet, A, Wirth, D, Coroadinha, AS, Cruz, P, Falk, H, et al. Integrated strategy for the production of therapeutic retroviral vectors. Hum Gene Ther 22 (2011), 370–379.
88. 89 Stornaiuolo, A, Piovani, BM, Bossi, S, Zucchelli, E, Corna, S, Salvatori, F, et al. RD2-MolPack-Chim3, a packaging cell line for stable production of lentiviral vectors for anti-HIV gene therapy. Hum Gene Ther Methods 24 (2013), 228–240.
89. 90 Hanawa, H, Persons, DA, Nienhuis, AW, Mobilization and mechanism of transcription of integrated self-inactivating lentiviral vectors. J Virol 79 (2005), 8410–8421.
90. 91 Xu, W, Russ, JL, Eiden, MV, Evaluation of residual promoter activity in γ-retroviral self-inactivating (SIN) vectors. Mol Ther 20 (2012), 84–90.
91. 92 Marin, V, Stornaiuolo, A, Piovan, C, Corna, S, Bossi, S, Pema, M, et al. RD-MolPack technology for the constitutive production of self-inactivating lentiviral vectors pseudo-typed with the non-toxic RD114-TR envelope. Mol Ther Methods Clin Dev, 2016 (in press).
92. 93 Porcellini, S, Alberici, L, Gubinelli, F, Lupo, R, Olgiati, C, Rizzardi, GP, et al. The F12-Vif derivative Chim3 inhibits HIV-1 replication in CD4+ T lymphocytes and CD34+-derived macrophages by blocking HIV-1 DNA integration. Blood 113 (2009), 3443–3452.
93. 94 Porcellini, S, Gubinelli, F, Alberici, L, Piovani, BM, Rizzardi, GP, Bovolenta, C, Chim3 confers survival advantage to CD4+ T cells upon HIV-1 infection by preventing HIV-1 DNA integration and HIV-1-induced G2 cell-cycle delay. Blood 115 (2010), 4021–4029.
94. 95 Di Nunzio, F, Piovani, B, Cosset, FL, Mavilio, F, Stornaiuolo, A, Transduction of human hematopoietic stem cells by lentiviral vectors pseudotyped with the RD114-TR chimeric envelope glycoprotein. Hum Gene Ther 18 (2007), 811–820.
95. 96 Kim, YS, Wielgosz, MM, Hargrove, P, Kepes, S, Gray, J, Persons, DA, et al. Transduction of human primitive repopulating hematopoietic cells with lentiviral vectors pseudotyped with various envelope proteins. Mol Ther 18 (2010), 1310–1317.
96. 97 Trobridge, GD, Wu, RA, Hansen, M, Ironside, C, Watts, KL, Olsen, P, et al. Cocal-pseudotyped lentiviral vectors resist inactivation by human serum and efficiently transduce primate hematopoietic repopulating cells. Mol Ther 18 (2010), 725–733.
97. 98 Chisti, Y, Strategies in downstream processing. Subramanian, G, (eds.) Bioseparation and Bioprocessing: A Handbook, 2nd edn, vol. 1, 2007, Wiley-VCH, New York, 29–62.
98. 99 Tiscornia, G, Singer, O, Verma, IM, Production and purification of lentiviral vectors. Nat Protoc 1 (2006), 241–245.
99. 100 Scherr, M, Battmer, K, Eder, M, Schüle, S, Hohenberg, H, Ganser, A, et al. Efficient gene transfer into the CNS by lentiviral vectors purified by anion exchange chromatography. Gene Ther 9 (2002), 1708–1714.
100. 101 Baekelandt, V, Eggermont, K, Michiels, M, Nuttin, B, Debyser, Z, Optimized lentiviral vector production and purification procedure prevents immune response after transduction of mouse brain. Gene Ther 10 (2003), 1933–1940.
101. 102 Yamada, K, McCarty, DM, Madden, VJ, Walsh, CE, Lentivirus vector purification using anion exchange HPLC leads to improved gene transfer. Biotechniques 34 (2003), 1074–1078, 1080.
102. 103 Segura, MM, Kamen, A, Garnier, A, Downstream processing of oncoretroviral and lentiviral gene therapy vectors. Biotechnol Adv 24 (2006), 321–337.
103. 104 Rodrigues, T, Carrondo, MJ, Alves, PM, Cruz, PE, Purification of retroviral vectors for clinical application: biological implications and technological challenges. J Biotechnol 127 (2007), 520–541.
104. 105 Bellintani, F, Piacenza, L, Sciarretta, R, Martelli, L, Massa, S, Vallanti, G, et al. Large scale process for the production and purification of lentiviral vectors for clinical applications. Hum Gene Ther, 19, 2008, 1089.
105. 106 Segura, MM, Garnier, A, Durocher, Y, Coelho, H, Kamen, A, Production of lentiviral vectors by large-scale transient transfection of suspension cultures and affinity chromatography purification. Biotechnol Bioeng 98 (2007), 789–799.
106. 107 Koldej, R, Cmielewski, P, Stocker, A, Parsons, DW, Anson, DS, Optimisation of a multipartite human immunodeficiency virus based vector system; control of virus infectivity and large-scale production. J Gene Med 7 (2005), 1390–1399.
107. 108 Geraerts, M, Michiels, M, Baekelandt, V, Debyser, Z, Gijsbers, R, Upscaling of lentiviral vector production by tangential flow filtration. J Gene Med 7 (2005), 1299–1310.
108. 109 Boudeffa, D, Fenard, D, Mormin, M, Galy, A, Merten, O-W, Development of innovative scalable protocols for the purification of lentiviral vectors pseudotyped with GaLV-TR or mutated measles virus glycoproteins, 2015 Presented at the 18th Annual Meeting of the ASGCT, 13 May–16 May 2015, New Orleans, LA/USA.
109. 110 Segura, MM, Garnier, A, Kamen, A, Purification and characterization of retrovirus vector particles by rate zonal ultracentrifugation. J Virol Methods 133 (2006), 82–91.
110. 111 Charrier, S, Laroudie, N, Viornery, A, Seye, K, Bucher-Laurent, S, Audit, M, et al. Reproducible transduction of CD34+ cells with a highly-purified lentiviral vector developed for Wiskott–Aldrich Syndrome gene therapy. Mol Ther, 16, 2008, S167.
111. 112 Merten, O-W, Retro- and lentiviral production platforms. Hum Gene Ther, 19, 2008, 1067.
112. 113 Truran, R, Buckley, R, Radcliffe, P, Miskin, J, Mitrophanous, K, Virus purification, 2009 WO 2009153563 A1.
113. 114 Escarpe, P, Zayek, N, Chin, P, Borellini, F, Zufferey, R, Veres, G, et al. Development of a sensitive assay for detection of replication-competent recombinant lentivirus in large-scale HIV-based vector preparations. Mol Ther 8 (2003), 332–341.
114. 115 Miskin, J, Chipchase, D, Rohll, J, Beard, G, Wardell, T, Angell, D, et al. A replication competent lentivirus (RCL) assay for equine infectious anaemia virus (EIAV)-based lentiviral vectors. Gene Ther 13 (2006), 196–205.
115. 116 Amirache, F, Lévy, C, Costa, C, Mangeot, PE, Torbett, BE, Wang, CX, et al. Mystery solved: VSV-G-LVs do not allow efficient gene transfer into unstimulated T cells, B cells, and HSCs because they lack the LDL receptor. Blood 123 (2014), 1422–1424.
116. 117 Brown, BD, Venneri, MA, Zingale, A, Sergi Sergi, L, Naldini, L, Endogenous microRNA regulation suppresses transgene expression in hematopoietic lineages and enables stable gene transfer. Nat Med 12 (2006), 585–591.
117. 118 Cantore, A, Ranzani, M, Bartholomae, CC, Volpin, M, Valle, PD, Sanvito, F, et al. Liver-directed lentiviral gene therapy in a dog model of hemophilia B. Sci Transl Med, 7, 2015, 277ra28.
118. 119 Ikeda, Y, Collins, MK, Radcliffe, PA, Mitrophanous, KA, Takeuchi, Y, Gene transduction efficiency in cells of different species by HIV and EIAV vectors. Gene Ther 9 (2002), 932–938.
119. 120 Girard-Gagnepain, A, Amirache, F, Costa, C, Lévy, C, Frecha, C, Fusil, F, et al. Baboon envelope pseudotyped LVs outperform VSV-G-LVs for gene transfer into early-cytokine-stimulated and resting HSCs. Blood 124 (2014), 1221–1231.
120. 121 Brendel, C, Goebel, B, Daniela, A, Brugman, M, Kneissl, S, Schwäble, J, et al. CD133-targeted gene transfer into long-term repopulating hematopoietic stem cells. Mol Ther 23 (2015), 63–70.
121. 122 Lévy, C, Amirache, F, Costa, C, Frecha, C, Muller, CP, Kweder, H, et al. Lentiviral vectors displaying modified measles virus gp overcome pre-existing immunity in in vivo-like transduction of human T and B cells. Mol Ther 20 (2012), 1699–1712.
122. 123 Hebben, M, Pre-industrial Manufacturing of Lentiviral Vectors by Transient Transfection in Single Use Systems, 2015 Presented at the Spring Meeting of ISBiotech, 9 March–11 March 2015, Washington/DC.
123. 124 Kafri, T, van Praag, H, Ouyang, L, Gage, FH, Verma, IM, A packaging cell line for lentivirus vectors. J Virol 73 (1999), 576–584.
124. 125 Klages, N, Zufferey, R, Trono, D, A stable system for the high-titer production of multiply attenuated lentiviral vectors. Mol Ther 2 (2000), 170–176.
125. 126 Farson, D, Witt, R, McGuinness, R, Dull, T, Kelly, M, Song, J, et al. A new-generation stable inducible packaging cell line for lentiviral vectors. Hum Gene Ther 12 (2001), 981–997.
126. 79 Hu, P, Li, Y, Sands, MS, McCown, T, Kafri, T, Generation of a stable packaging cell line producing high-titer PPT-deleted integration-deficient lentiviral vectors. Mol Ther Methods Clin Dev, 2, 2015, 15025.