Molecular evidence of lentiviral vector-mediated gene transfer into human self-renewing, multi-potent, long-term NOD/SCID repopulating hematopoietic cells

Molecular Therapy

Volumn 6, Issue 5, 2002, Pages 615-626

  Ailles, Laurie ^a   Schmidt, Manfred ^b   Santoni De Sio, Francesca Romana ^a   Glimm, Hanno ^b   Cavalieri, Simona ^a   Bruno, Stefania ^a   Piacibello, Wanda ^a   Von Kalle, Christof ^b   Naldini, Luigi ^a  

^a UNIVERSITY OF TURIN   (Italy)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Bone marrow transplantation; Clonal analysis; Gene transfer; Hematopoietic stem cells; Lentiviral vectors; NOD SCID mouse repopulation assay

Indexed keywords

CYTOKINE; DNA; LENTIVIRUS VECTOR; CD34 ANTIGEN; GREEN FLUORESCENT PROTEIN; PHOTOPROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; CELL DIFFERENTIATION; CELL LINEAGE; CELL SELECTION; CELL STIMULATION; CELL TRANSPORT; CLINICAL PROTOCOL; CLONE; COMBINED IMMUNODEFICIENCY; CONTROLLED STUDY; DNA MODIFICATION; GENE EXPRESSION; GENE THERAPY; GENE TRANSFER; GENETIC SUSCEPTIBILITY; GENETIC TRANSDUCTION; HEMATOPOIETIC CELL; HEMATOPOIETIC STEM CELL TRANSPLANTATION; IMMUNOSUPPRESSIVE TREATMENT; IN VIVO STUDY; INCUBATION TIME; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; POPULATION DYNAMICS; RECIPIENT; SCID MOUSE; TRANSGENE; UMBILICAL CORD BLOOD; ANIMAL; BIOSYNTHESIS; BONE MARROW TRANSPLANTATION; CELL CYCLE; CELL LINE; CELL SEPARATION; CYTOLOGY; FLOW CYTOMETRY; GENE VECTOR; GENETICS; HELA CELL; HEMATOPOIETIC STEM CELL; HUMAN; LENTIVIRINAE; METABOLISM; MOUSE MUTANT;

ANIMALIA; LENTIVIRUS;

ANIMALS; ANTIGENS, CD34; BONE MARROW TRANSPLANTATION; CELL CYCLE; CELL DIFFERENTIATION; CELL LINE; CELL LINEAGE; CELL SEPARATION; CYTOKINES; FLOW CYTOMETRY; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; HELA CELLS; HEMATOPOIETIC STEM CELLS; HUMANS; LENTIVIRUS; LUMINESCENT PROTEINS; MICE; MICE, SCID; POLYMERASE CHAIN REACTION; TRANSGENES;

EID: 0036852308     PISSN: 15250016     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1525-0016(02)90720-3     Document Type: Article

References (57)

1. Kamel-Reid, S., and Dick, J. E. (1988). Engraftment of immune-deficient mice with human hematopoietic stem cells. Science 242: 1706-1709.
2. Cashman, J., Bockhold, K., Hogge, D. E., Eaves, A. C., and Eaves, C. J. (1997). Sustained proliferation, multi-lineage differentiation and maintenance of primitive human haemopoietic cells in NOD/SCID mice transplanted with human cord blood. Br. J. Haematol. 98: 1026-1036.
3. Dunbar, C. E., et al. (1995). Retrovirally marked CD34-enriched peripheral blood and bone marrow cells contribute to long-term engraftment after autologous transplantation. Blood 85: 3048-3057.
4. Brenner, M. (1996). Gene marking. Hum. Gene Ther. 7: 1927-1936.
5. Kiem, H. P., et al. (1997). Gene transfer into marrow repopulating cells: comparison between amphotropic and gibbon ape leukemia virus pseudotyped retroviral vectors in a competitive repopulation assay in baboons. Blood 90: 4638-4645.
6. van Hennik, P. B., et al. (1998). Highly efficient transduction of the green fluorescent protein gene in human umbilical cord blood stem cells capable of cobbleston formation in long-term cultures and multilineage engraftment of immunodeficient mice. Blood 92: 4013-4022.
7. Kelly, P. F., Vandergriff, J., Nathwani, A., Nienhuis, A. W., and Vanin, E. F. (2000). Highly efficient gene transfer into cord blood nonobese diabetic/severe combined immunodeficiency repopulating cells by oncoretroviral vector particles pseudotyped with the feline endogenous retrovirus (RD114) envelope protein. Blood 96: 1206-1214.
8. Larochelle, A., et al. (1996). Identification of primitive human hematopoietic cells capable of repopulating NOD/SCID mouse bone marrow: implications for gene therapy. Nat. Med. 2: 1329-1337.
9. Conneally, E., Eaves, C. J., and Humphries, R. K. (1998). Efficient retroviral-mediated gene transfer to human cord blood stem cells with in vivo repopulating potential. Blood 91: 3487-3493.
10. Marandin, A., et al. (1998). Retrovirus-mediated gene transfer into human CD34+38low primitive cells capable of reconstituting long-term cultures in vitro and nonobese diabetic-severe combined immunodeficiency mice in vivo. Hum. Gene Ther. 9: 1497-1511.
11. Schilz, A. J., et al. (1998). High efficiency gene transfer to human hematopoietic SCID-repopulating cells under serum-free conditions. Blood 92: 3163-3171.
12. Barquinero, J., et al. (2000). Efficient transduction of human hematopoietic repopulating cells generating stable engraftment of transgene-expressing cells in NOD/SCID mice. Blood 95: 3085-3093.
13. Guenechea, G., Gan, O. I., Dorrell, C., and Dick, J. E. (2001). Distinct classes of human stem cells that differ in proliferative and self-renewal potential. Nat. Immunol. 2: 75-82.
14. Williams, D. A. (1993). Ex vivo expansion of hematopoietic stem and progenitor cells-robbing Peter to pay Paul? Blood 81: 3169-3172.
15. Bhatia, M., et al. (1997). Quantitative analysis reveals expansion of human hematopoietic repopulating cells after short-term ex vivo culture. J. Exp. Med. 186: 619-624.
16. Gothot, A., van der Loo, J. C., Clapp, D. W., and Srour, E. F. (1998). Cell cycle-related changes in repopulating capacity of human mobilized peripheral blood CD34(+) cells in non-obese diabetic/severe combined immune-deficient mice. Blood 92: 2641-2649.
17. Cavazzana-Calvo, M, et al. (2000). Gene therapy of human severe combined immunodeficiency (SCID)-X1 disease. Science 288: 669-672.
18. Aiuti, A., et al. (2000). Correction of ADA-SCID by stem cell gene therapy combined with nonmyeloablative conditioning. Science 296: 2410-2413.
19. Naldini, L., et al. (1996). In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272: 263-267.
20. Akkina, R. k., et al. (1996). High-efficiency gene transfer into CD34+ cells with a human immunodeficiency virus type 1-based retroviral vector pseudotyped with vesicular stomatitis virus envelope glycoprotein G. J. Virol. 70: 2581-2585.
21. Reiser, J. et al. (1996). Transduction of nondividing cells using pseudotyped defective high-titer HIV type 1 particles. Proc. Natl. Acad. Sci. USA 93: 15266-15271.
22. Uchida, N., et al. (1998). HIV, but not murine leukemia virus, vectors mediate high efficiency gene transfer into freshly isolated G0/G1 human hematopoietic stem cells. Proc. Natl. Acad. Sci. USA 95: 11939-11944.
23. Case, S. S., et al. (1999). Stable transduction of quiescent CD34(+)CD38(-) human hematopoietic cells by HIV-1-based lentiviral vectors. Proc. Natl. Acad. Sci. USA 96: 2988-2993.
24. Zennou, V., et al. (2000). HIV-1 genome nuclear import is mediated by a central DNA flap. Cell 101: 173-185.
25. Follenzi, A., Ailles, L. E., Bakovic, S., Geuna, M., and Naldini, L. (2000). Gene transfer by lentiviral vectors is limited by nuclear translocation and rescued by HIV-1 pol sequences. Nat. Genet. 25: 217-222.
26. Miyoshi, H., Smith, K. A., Mosier, D. E., Verma, I. M., and Torbett, B. E. (1999). Transduction of human CD34+ cells that mediate long-term engraftment of NOD/SCID mice by HIV vectors. Science 283: 682-686.
27. Guenechea, G., et al. (2000). Transduction of human CD34+CD38- bone marrow and cord blood-derived SCID-repopulating cells with third-generation lentiviral vectors. Mol. Ther. 1: 566-573.
28. Woods, N. B., et al. (2000). Lentiviral gene transfer into primary and secondary NOD/SCID repopulating cells. Blood 96: 3725-3733.
29. Sirven, A., et al. (2000). The human immunodeficiency virus type-1 central DNA flap is a crucial determinant for lentiviral vector nuclear import and gene transduction of human hematopoietic stem cells. Blood 96: 4103-4110.
30. Ramezani, A., Hawley, T. S., and Hawley, R. G. (2000). Lentiviral vectors for enhanced gene expression in human hematopoietic cells. Mol. Ther. 2: 458-469.
31. Gatlin, J., Padgett, A., Melkus, M. W., Kelly, P. F., and Garcia, J. V. (2001). Long-term engraftment of nonobese diabetic/severe combined immunodeficiency virus type 1 vector. Hum. Gene Ther. 12: 1079-1089.
32. Sutton, R. E., Reitsma, M. J., Uchida, N., and Brown, P. O. (1999). Transduction of human progenitor hematopoietic stem cells by human immunodeficiency virus type 1-based vectors is cell cycle dependent. J. Virol. 73: 3649-3660.
33. Korin, Y. D., and Zack, J. A. (1998). Progression to the G1b phase of the cell cycle is required for completion of human immunodeficiency virus type 1 reverse transcription in T cells. J. Virol. 72: 3161-3168.
34. Korin, Y. D., and Zack, J. A. (1999). Nonproductive human immunodeficiency virus type 1 infection in nucleoside-treated G0 lymphocytes. J. Virol. 73: 6526-6532.
35. Piacibello, W., et al. (1999). Engraftment in nonobese diabetic severe combined immunodeficient mice of human CD34(+) cord blood cells after ex vivo expansion: evidence for the amplification and self-renewal of repopulating stem cells. Blood 93: 3736-3749.
36. Haas, D. L., Case, S. S., Crooks, G. M., and Kohn, D. B. (2000). Critical factors influencing stable tranduction of human CD34(+) cells with HIV-1 derived lentiviral vectors. Mol. Ther. 2: 71-80.
37. Szilvassy, S. J., Humphries, R. K., Lansdorp, p. M., Eaves, A. C., and Eaves, C.J. (1990). Quantitative assay for totipotent reconstituting hematopoietic stem cells by a competitive repopulation strategy. Proc. Natl. Acad. Sci. USA 87: 8736-8740.
38. Schmidt, M., et al. (2001). Detection and direct genomic sequencing of multiple rare unknown flanking DNA in highly complex samples. Hum. Gene Ther. 12: 743-749.
39. Schmidt, M., et al. (2002). Polyclonal long-term repopulating stem cell clones in a primate model. Blood 100: 2737-2743.
40. Scherr, M., et al. (2002). Lentiviral gene transfer into peripheral blood-derived CD34+ NOD/SCID-repopulating cells. Blood 99: 709-712.
41. Vigna, E., and Naldini, L. (2000). Lentiviral vectors: excellent tools for experimental gene transfer and promising candidates for gene therapy. J. Gene Med. 2: 308-316.
42. Follenzi, A., Sabatino, G., Lombardo, A., Boccaccio, C., and Naldini, L. (2002). Efficient gene delivery and targeted expression to hepatocytes in vivo by improved lentiviral vectors. Hum. Gene Ther. 13; 243-260.
43. Pfiefer, A., et al. (2001). Transduction of liver cells by lentiviral vectors: analysis in living animals by fluorescence imaging. Mol. Ther. 3: 319-322.
44. Kinoshita, S., Chen, B.K., Kaneshima, H., and Nolan, G.P. (1998). Host control of HIV-1 parasitism in T cells by the nuclear factor of activated T cells. Cell 95: 595-604.
45. Kootstra, N.A., Zwart, B.M., and Schuitemaker, H. (2000). Diminished human immunodeficiency virus type 1 reverse transcription and nuclear transport in primary macrophages arrested in early G(1) phase of the cell cycle. J. Virol. 74: 1712-1717.
46. Wu, Y., and Marsh, J.W. (2000). Selective transcription and modulation of resting T cell activity by preintegrated HIV DNA. Science 293: 1503-1506.
47. Zhang, Z., et al. (1999). Sexual transmission and propagation of SIV and HIV in resting and activated CD4+ T cells. Science 286: 1353-1357.
48. Unutmaz, D., KewalRamani, V.N. Marmon, S., and Littman, D.R. (1999). Cytokine signals are sufficient for HIV-1 infection of resting human T lymphocytes. J. Exp. Med. 189: 1735-1746.
49. Wilpshaar, J., et al. (2000). Similar repopulating capacity of mitotically active and resting umbilical cord blood CD34(+) cells in NOD/SCID mice. Blood 96: 2100-2107.
50. Glimm, H., Oh, I.H., and Eaves, C.J. (2000). Human hematopoietic stem cells stimulated to proliferate in vitro lose engraftment potential during their S/G(2)M transit and do not reenter G(0). Blood 96: 4185-4193.
51. Nolta, J.A., Dao, M.A., Wells, S., Smogorzewska, E.M., and Kohn, D.B. (1996). Transduction of pluripotent human hematopoietic stem cells demonstrated by clonal analysis after engraftment in immune-deficient mice. Proc. Natl. Acad. Sci. USA 93: 2414-2419.
52. Lois, C., Hong, E.J., Pease, S., Brown, E.J., and Baltimore, D. (2002). Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors. Science 295: 868-872.
53. Pfeifer, A., Ikawa, M., Dayn, Y., and Verma, I.M. (2002). Transgenesis by lentiviral vectors: lack of gene silencing in mammalian embryonic stem cells and preimplantation embryos. Proc. Natl. Acad. Sci. USA 99: 2140-2145.
54. May, C., et al. (2000). Therapeutic haemoglobin synthesis in β-thalassaemic mice expressing lentivirus-encoded human β-globin. Nature 406: 82-86.
55. Pawliuk, R., et al. (20001). Correction of sickle cell disease in transgenic mouse models by gene therapy. Science 294: 2368-2371.
56. Dull, T., et al. (1998). A third-generation lentivirus vector with a conditional packaging system. J. Virol. 72: 8463-9471.
57. Shultz, L.D., et al. (1995). Multiple defects in innate and adaptive immunologic function in NOD/LtSz-scid mice. J. Immunol. 154: 180-191.