Effects of vector backbone and pseudotype on lentiviral vector-mediated gene transfer: Studies in infant ADA-Deficient mice and rhesus monkeys

Molecular Therapy

Volumn 22, Issue 10, 2014, Pages 1803-1816

  Sarracino, Denise Carbonaro ^a   Tarantal, Alice F ^b   Lee, C Chang I ^b   Martinez, Michele ^b   Jin, Xiangyang ^a   Wang, Xiaoyan ^a   Hardee, Cinnamon L ^a   Geiger, Sabine ^a   Kahl, Christoph A ^c,d   Kohn, Donald B ^a,e  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c CHILDREN S HOSPITAL LOS ANGELES   (United States)

^d OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DEAMINASE; CD34 ANTIGEN; LENTIVIRUS VECTOR; RETROVIRUS VECTOR; VIRUS GLYCOPROTEIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE MARROW; FEMALE; HUMAN IMMUNODEFICIENCY VIRUS 1; INFANT; KNOCKOUT MOUSE; LIVER; LUNG; MOUSE; NEWBORN; NONHUMAN; PSEUDOTYPING; RHESUS MONKEY; SIMIAN IMMUNODEFICIENCY VIRUS; SPLEEN; TISSUE DISTRIBUTION; VESICULOVIRUS; VIRAL GENE DELIVERY SYSTEM; ADMINISTRATION AND DOSAGE; ANIMAL; DEFICIENCY; DISEASE MODEL; GENE EXPRESSION; GENE ORDER; GENE TRANSFER; GENE VECTOR; GENETIC TRANSDUCTION; GENETICS; HUMAN; LENTIVIRINAE; PHARMACOKINETICS; RETROVIRIDAE; SEVERE COMBINED IMMUNODEFICIENCY; TRANSGENE;

GIBBON APE LEUKEMIA VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; MACACA MULATTA; MURINAE; MUS; SIMIAN IMMUNODEFICIENCY VIRUS; VESICULAR STOMATITIS VIRUS;

ADENOSINE DEAMINASE; ANIMALS; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION; GENE ORDER; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; HUMANS; LENTIVIRUS; MACACA MULATTA; MICE; MICE, KNOCKOUT; RETROVIRIDAE; SEVERE COMBINED IMMUNODEFICIENCY; TISSUE DISTRIBUTION; TRANSDUCTION, GENETIC; TRANSGENES;

EID: 84926145124     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2014.88     Document Type: Article

References (56)

1. Gaspar, HB, Aiuti, A, Porta, F, Candotti, F, Hershfield, MS and Notarangelo, LD (2009). How I treat ADA deficiency. Blood 114: 3524-3532.
2. Aiuti, A, Cattaneo, F, Galimberti, S, Benninghoff, U, Cassani, B, Callegaro, L et al. (2009). Gene therapy for immunodeficiency due to adenosine deaminase deficiency. N Engl J Med 360: 447-458.
3. Candotti, F, Shaw, KL, Muul, L, Carbonaro, D, Sokolic, R, Choi, C et al. (2012). Gene therapy for adenosine deaminase-deficient severe combined immune deficiency: clinical comparison of retroviral vectors and treatment plans. Blood 120: 3635-3646.
4. Gaspar, HB, Cooray, S, Gilmour, KC, Parsley, KL, Zhang, F, Adams, S et al. (2011). Hematopoietic stem cell gene therapy for adenosine deaminase-deficient severe combined immunodeficiency leads to long-term immunological recovery and metabolic correction. Sci Transl Med 3: 97ra80.
5. Blackburn, MR, Datta, SK, Wakamiya, M, Vartabedian, BS and Kellems, RE (1996). Metabolic and immunologic consequences of limited adenosine deaminase expression in mice. J Biol Chem 271: 15203-15210.
6. Carbonaro, DA, Jin, X, Cotoi, D, Mi, T, Yu, XJ, Skelton, DC et al. (2008). Neonatal bone marrow transplantation of ADA-deficient SCID mice results in immunologic reconstitution despite low levels of engraftment and an absence of selective donor T lymphoid expansion. Blood 111: 5745-5754.
7. Mortellaro, A, Hernandez, RJ, Guerrini, MM, Carlucci, F, Tabucchi, A, Ponzoni, M et al. (2006). Ex vivo gene therapy with lentiviral vectors rescues adenosine deaminase (ADA)-deficient mice and corrects their immune and metabolic defects. Blood 108: 2979-2988.
8. Carbonaro, DA, Jin, X, Petersen, D, Wang, X, Dorey, F, Kil, KS et al. (2006). In vivo transduction by intravenous injection of a lentiviral vector expressing human ADA into neonatal ADA gene knockout mice: a novel form of enzyme replacement therapy for ADA deficiency. Mol Ther 13: 1110-1120.
9. Carbonaro, DA, Jin, X, Wang, X, Yu, XJ, Rozengurt, N, Kaufman, ML et al. (2012). Gene therapy/bone marrow transplantation in ADA-deficient mice: roles of enzymereplacement therapy and cytoreduction. Blood 120: 3677-3687.
10. Wolf, D and Goff, SP (2008). Host restriction factors blocking retroviral replication. Annu Rev Genet 42: 143-163.
11. Ayinde, D, Casartelli, N and Schwartz, O (2012). Restricting HIV the SAMHD1 way: through nucleotide starvation. Nat Rev Microbiol 10: 675-680.
12. Nakayama, EE and Shioda, T (2012). TRIM5 and Species Tropism of HIV/SIV. Front Microbiol 3: 13.
13. Kahl, CA, Cannon, PM, Oldenburg, J, Tarantal, AF and Kohn, DB (2008). Tissuespecific restriction of cyclophilin A-independent HIV-1-And SIV-derived lentiviral vectors. Gene Ther 15: 1079-1089.
14. Xu, L, O'Malley, T, Sands, MS, Wang, B, Meyerrose, T, Haskins, ME et al. (2004). In vivo transduction of hematopoietic stem cells after neonatal intravenous injection of an amphotropic retroviral vector in mice. Mol Ther 10: 37-44.
15. Pan, D, Gunther, R, Duan, W, Wendell, S, Kaemmerer, W, Kafri, T et al. (2002). Biodistribution and toxicity studies of VSVG-pseudotyped lentiviral vector after intravenous administration in mice with the observation of in vivo transduction of bone marrow. Mol Ther 6: 19-29.
16. Worsham, DN, Schuesler, T et al. (2006). In vivo gene transfer into adult stem cells in unconditioned mice by in situ delivery of a lentiviral vector. Mol Ther 14: 514-524.
17. Christodoulopoulos, I and Cannon, PM (2001). Sequences in the cytoplasmic tail of the gibbon ape leukemia virus envelope protein that prevent its incorporation into lentivirus vectors. J Virol 75: 4129-4138.
18. Batchelder, CA, Keyser, JL, Lee, CC and Tarantal, AF (2013). Characterization of growth, glomerular number, and tubular proteins in the developing rhesus monkey kidney. Anat Rec (Hoboken) 296: 1747-1757.
19. Wang, B, O'Malley, TM, Xu, L, Vite, C, Wang, P, O'Donnell, PA et al. (2006). Expression in blood cells may contribute to biochemical and pathological improvements after neonatal intravenous gene therapy for mucopolysaccharidosis VII in dogs. Mol Genet Metab 87: 8-21.
20. Worsham, DN, Schuesler, T, von Kalle, C and Pan, D (2006). In vivo gene transfer into adult stem cells in unconditioned mice by in situ delivery of a lentiviral vector. Mol Ther 14: 514-524.
21. Evans, ME, Kumkhaek, C, Hsieh, MM, Donahue, RE, Tisdale, JF and Uchida, N (2014). TRIM5 variations influence transduction efficiency with lentiviral vectors in both human and rhesus CD34(+) cells in vitro and in vivo. Mol Ther 22: 348-358.
22. Blackburn, MR, Volmer, JB, Thrasher, JL, Zhong, H, Crosby, JR, Lee, JJ et al. (2000). Metabolic consequences of adenosine deaminase deficiency in mice are associated with defects in alveogenesis, pulmonary inflammation, and airway obstruction. J Exp Med 192: 159-170.
23. Booth, C, Algar, VE, Xu-Bayford, J, Fairbanks, L, Owens, C and Gaspar, HB (2012). Non-infectious lung disease in patients with adenosine deaminase deficient severe combined immunodeficiency. J Clin Immunol 32: 449-453.
24. Grunebaum, E, Cutz, E and Roifman, CM (2012). Pulmonary alveolar proteinosis in patients with adenosine deaminase deficiency. J Allergy Clin Immunol 129: 1588-1593.
25. Croyle, MA, Callahan, SM, Auricchio, A, Schumer, G, Linse, KD, Wilson, JM et al. (2004). PEGylation of a vesicular stomatitis virus G pseudotyped lentivirus vector prevents inactivation in serum. J Virol 78: 912-921.
26. Agudo, J, Ruzo, A, Kitur, K, Sachidanandam, R, Blander, JM and Brown, BD (2012). A TLR and non-TLR mediated innate response to lentiviruses restricts hepatocyte entry and can be ameliorated by pharmacological blockade. Mol Ther 20: 2257-2267.
27. Zhang, F, Frost, AR, Blundell, MP, Bales, O, Antoniou, MN and Thrasher, AJ (2010). A ubiquitous chromatin opening element (UCOE) confers resistance to DNA methylation-mediated silencing of lentiviral vectors. Mol Ther 18: 1640-1649.
28. Titman, P, Pink, E, Skucek, E, O'Hanlon, K, Cole, TJ, Gaspar, J et al. (2008). Cognitive and behavioral abnormalities in children after hematopoietic stem cell transplantation for severe congenital immunodeficiencies. Blood 112: 3907-3913.
29. Mankowski, JL, Spelman, JP, Ressetar, HG, Strandberg, JD, Laterra, J, Carter, DL et al. (1994). Neurovirulent simian immunodeficiency virus replicates productively in endothelial cells of the central nervous system in vivo and in vitro. J Virol 68: 8202-8208.
30. Moses, AV, Stenglein, SG, Strussenberg, JG, Wehrly, K, Chesebro, B and Nelson, JA (1996). Sequences regulating tropism of human immunodeficiency virus type 1 for brain capillary endothelial cells map to a unique region on the viral genome. J Virol 70: 3401-3406.
31. Cuddihy, AR, Suterwala, BT, Ge, S, Kohn, LA, Jang, J, Andrade, J et al. (2012). Rapid thymic reconstitution following bone marrow transplantation in neonatal mice is VEGF-dependent. Biol Blood Marrow Transplant 18: 683-689.
32. Park, F, Ohashi, K, Chiu, W, Naldini, L and Kay, MA (2000). Efficient lentiviral transduction of liver requires cell cycling in vivo. Nat Genet 24: 49-52.
33. Cavazzana-Calvo, M, Payen, E, Negre, O, Wang, G, Hehir, K, Fusil, F et al. (2010). Transfusion independence and HMGA2 activation after gene therapy of human ?-thalassaemia. Nature 467: 318-322.
34. Themis, M, Waddington, SN, Schmidt, M, von Kalle, C, Wang, Y, Al-Allaf, F et al. (2005). Oncogenesis following delivery of a nonprimate lentiviral gene therapy vector to fetal and neonatal mice. Mol Ther 12: 763-771.
35. Nowrouzi, A, Cheung, WT, Li, T, Zhang, X, Arens, A, Paruzynski, A et al. (2013). The fetal mouse is a sensitive genotoxicity model that exposes lentiviral-Associated mutagenesis resulting in liver oncogenesis. Mol Ther 21: 324-337.
36. Ranzani, M, Cesana, D, Bartholomae, CC, Sanvito, F, Pala, M, Benedicenti, F et al. (2013). Lentiviral vector-based insertional mutagenesis identifies genes associated with liver cancer. Nat Methods 10: 155-161.
37. Rittelmeyer, I, Rothe, M, Brugman, MH, Iken, M, Schambach, A, Manns, MP et al. (2013). Hepatic lentiviral gene transfer is associated with clonal selection, but not with tumor formation in serially transplanted rodents. Hepatology 58: 397-408.
38. Tarantal, AF and Skarlatos, SI (2012). Center for fetal monkey gene transfer for heart, lung, and blood diseases: an NHLBI resource for the gene therapy community. Hum Gene Ther 23: 1130-1135.
39. Hanazono, Y, Brown, KE, Handa, A, Metzger, ME, Heim, D, Kurtzman, GJ et al. (1999). In vivo marking of rhesus monkey lymphocytes by adenoassociated viral vectors: direct comparison with retroviral vectors. Blood 94: 2263-2270.
40. Kahl, CA, Tarantal, AF, Lee, CI, Jimenez, DF, Choi, C, Pepper, K et al. (2006). Effects of busulfan dose escalation on engraftment of infant rhesus monkey hematopoietic stem cells after gene marking by a lentiviral vector. Exp Hematol 34: 369-381.
41. Podsakoff, GM, Engel, BC, Carbonaro, DA, Choi, C, Smogorzewska, EM, Bauer, G et al. (2005). Selective survival of peripheral blood lymphocytes in children with HIV-1 following delivery of an anti-HIV gene to bone marrow CD34(+) cells. Mol Ther 12: 77-86.
42. Hanawa, H, Hematti, P, Keyvanfar, K, Metzger, ME, Krouse, A, Donahue, RE et al. (2004). Efficient gene transfer into rhesus repopulating hematopoietic stem cells using a simian immunodeficiency virus-based lentiviral vector system. Blood 103: 4062-4069.
43. Haas, DL, Case, SS, Crooks, GM and Kohn, DB (2000). Critical factors influencing stable transduction of human CD34(+) cells with HIV-1-derived lentiviral vectors. Mol Ther 2: 71-80.
44. Cooper, AR, Patel, S, Senadheera, S, Plath, K, Kohn, DB and Hollis, RP (2011). Highly efficient large-scale lentiviral vector concentration by tandem tangential flow filtration. J Virol Methods 177: 1-9.
45. Soneoka, Y, Cannon, PM, Ramsdale, EE, Griffiths, JC, Romano, G, Kingsman, SM et al. (1995). A transient three-plasmid expression system for the production of high titer retroviral vectors. Nucleic Acids Res 23: 628-633.
46. Blackburn, MR, Datta, SK and Kellems, RE (1998). Adenosine deaminase-deficient mice generated using a two-stage genetic engineering strategy exhibit a combined immunodeficiency. J Biol Chem 273: 5093-5100.
47. Tarantal, A (2005). Ultrasound imaging in rhesus and long-tailed macaques: Reproductive and research applications. In: Wolfe-Coote S (ed.). The Laboratory Primate. Elsevier Academic Press: Amsterdam; Boston. 317-351.
48. Tarantal, AF, McDonald, RJ, Jimenez, DF, Lee, CC, O'Shea, CE, Leapley, AC et al. (2005). Intrapulmonary and intramyocardial gene transfer in rhesus monkeys (Macaca mulatta): safety and efficiency of HIV-1-derived lentiviral vectors for fetal gene delivery. Mol Ther 12: 87-98.
49. Lee, CC, Jimenez, DF, Kohn, DB and Tarantal, AF (2005). Fetal gene transfer using lentiviral vectors and the potential for germ cell transduction in rhesus monkeys (Macaca mulatta). Hum Gene Ther 16: 417-425.
50. Kaplan, EL and Meier, P (1958). Nonparametric-estimation from incomplete observations. J Am Statis Assoc 53: 457-481.
51. Mantel, N (1966). Evaluation of survival data and two new rank order statistics arising in its consideration. Cancer Chemother Rep 50: 163-170.
52. Tukey, JW (1957). Variances of variance-components .2. The unbalanced single classification. Ann Math Statis 28: 43-56.
53. Fitzmaurice, G, Davidian, M, Verbeke, G and Molenberghs, G (2008). Longitudinal Data Analysis. Chapman and Hall/CRC: Boca Raton, FL.
54. Gabrielsson, JL and Weiner, DL (1999). Methodology for pharmacokinetic/pharmacodynamic data analysis. Pharm Sci Technol Today 2: 244-252.
55. Jaki, T and Wolfsegger, MJ (2011). Estimation of pharmacokinetic parameters with the R package PK. Pharm Stat 10: 284-288.
56. SAS Institute (2012). SAS/STAT user's guide, Version 9.3. 9.3 ed. SAS Institute: Cary, NC.