High-level β-globin expression and preferred intragenic integration after lentiviral transduction of human cord blood stem cells

Journal of Clinical Investigation

Volumn 114, Issue 7, 2004, Pages 953-962

  Imren, Suzan ^a   Fabry, Mary E ^b   Westerman, Karen A ^c   Pawliuk, Robert ^c   Tang, Patrick ^a   Rosten, Patricia M ^a   Nagel, Ronald L ^b   Leboulch, Philippe ^c   Eaves, Connie J ^a,d   Humphries, R Keith ^a,d  

^a BRITISH COLUMBIA CANCER AGENCY   (Canada)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BETA A T87Q GLOBIN; BETA GLOBIN; GENE PRODUCT; LENTIVIRUS VECTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BONE MARROW CELL; CELL REGENERATION; CELL TRANSPLANTATION; CONTROLLED STUDY; ERYTHROID CELL; EXPERIMENTAL MODEL; GENE INDUCTION; GENOMICS; GLOBIN GENE; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; SCID MOUSE; TRANSGENE;

ANIMALS; CELL LINEAGE; CELL TRANSPLANTATION; CELLS, CULTURED; CHROMOSOMES, HUMAN; FETAL BLOOD; GENE THERAPY; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; GLOBINS; HEMATOPOIETIC STEM CELLS; HUMANS; LENTIVIRUS; MICE; MICE, INBRED NOD; MICE, SCID; TRANSDUCTION, GENETIC; TRANSGENES;

EID: 9644291600     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI200421838     Document Type: Article

References (73)

1. Olivieri, N.F. 1999. The beta-thalassemias. N. Engl. J. Med. 341:99-109.
2. Walters, M.C., et al. 1996. Barriers to bone marrow transplantation for sickle cell anemia. Biol. Blood Marrow Transplant. 2:100-104.
3. Tuan, D., and London, I.M. 1984. Mapping of DNase I-hypersensitive sites in the upstream DNA of human embryonic epsilon-globin gene in K562 leukemia cells. Proc. Natl. Acad. Sci. U. S. A. 81:2718-2722.
4. Tuan, D., Solomon, W., Li, Q., and London, I.M. 1985. The "beta-like-globin" gene domain in human erythroid cells. Proc. Natl. Acad. Sci. U. S. A. 82:6384-6388.
5. Wright, S., Rosenthal, A., Flavell, R., and Grosveld, F. 1984. DNA sequences required for regulated expression of beta-globin genes in murine erythroleukemia cells. Cell. 38:265-273.
6. Forrester, W.C., Takegawa, S., Papayannopoulou, T., Stamatoyannopoulos, G., and Groudine, M. 1987. Evidence for a locus activation region: the formation of developmentally stable hypersensitive sites in globin-expressing hybrids. Nucleic Acids Res. 15:10159-10177.
7. Grosveld, F., et al. 1987. The regulation of expression of human beta-globin genes. Prog. Clin. Biol. Res. 251:133-144.
8. Blom van Assendelft, G., Hanscombe, O., Grosveld, F., and Greaves, D.R. 1989. The beta-globin dominant control region activates homologous and heterologous promoters in a tissue-specific manner. Cell. 56:969-977.
9. Talbot, D., et al. 1989. A dominant control region from the human beta-globin locus conferring integration site-independent gene expression. Nature. 338:352-355.
10. Fraser, P., Hurst, J., Collis, P., and Grosveld, F. 1990. DNaseI hypersensitive sires 1, 2 and 3 of the human beta-globin dominant control region direct position-independent expression. Nucleic Acids Res. 18:3503-3508.
11. Leboulch, P., et al. 1994. Mutagenesis of retroviral vectors transducing human beta-globin gene and beta-globin locus control region derivatives results in stable transmission of an active transcriptional structure. EMBO J. 13:3065-3076.
12. Sadelain, M., Wang, C.H., Antoniou, M., Grosveld, F., and Mulligan, R.C. 1995. Generation of a high-titer retroviral vector capable of expressing high levels of the human beta-globin gene. Proc. Natl. Acad. Sci. U. S. A. 92:6728-6732.
13. Raftopoulos, H., Ward, M., Leboulch, P., and Bank, A. 1997. Long-term transfer and expression of the human beta-globin gene in a mouse transplanr model. Blood. 90:3414-3422.
14. Kalberer, C.P., et al. 2000. Preselecrion of retrovirally transduced bone marrow avoids subsequent stem cell gene silencing and age-dependent extincrion of expression of human beta-globin in engrafted mice. Proc. Natl. Acad. Sci. U. S. A. 97:5411-5415.
15. Nicolini, F.E., et al. 2002. Expression of a human beta-globin transgene in erythroid cells derived from recrovirally transduced transplantable human fetal liver and cord blood cells. Blood. 100:1257-1264.
16. Oh, I.H., et al. 2004. Expression of an anti-sickling beta-globin in human erythroblasts derived from retrovirally transduced primitive normal and sickle cell disease hematopoietic cells. Exp. Hematol. 32:461-469.
17. Dzierzak, E.A., Papayannopoulou, T., and Mulligan, R.C. 1988. Lineage-specific expression of a human beta-globin gene in murine bone marrow transplant recipients reconstituted with retrovirus-transduced stem cells. Nature. 331:35-41.
18. Bender, M.A., Gelinas, R.E., and Miller, A.D. 1989. A majority of mice show long-term expression of a human beta-globin gene after recrovirus transfer into hematopoietic stem cells. Mol. Cell. Biol. 9:1426-1434.
19. Plavec, I., Papayannopoulou, T., Maury, C., and Meyer, F. 1993. A human beta-globin gene fused to the human beta-globin locus control region is expressed at high levels in erythroid cells of mice engrafted with retrovirus-transduced hemacopoieric stem cells. Blood, 81:1384-1392.
20. Rivella, S., and Sadelain, M. 1998. Genetic treatment of severe hemoglobinopathies: the combat against transgene variegation and transgene silencing. Semin. Hematol. 35:112-125.
21. Rebel, V.I., et al. 1999, One-day ex vivo culture allows effective gene transfer into human non-obese diabetic/severe combined immune-deficient repopulating cells using high-titer vesicular stomatitis virus G protein pseudotyped retrovirus. Blood. 93:2217-2224.
22. Hennemann, B., et al. 2000. Efficient retrovirus-mediated gene transfer to transplantable human bone marrow cells in the absence of fibronectin. Blood. 96:2432-2439.
23. Dorrell, C., Gan, O.I., Pereira, D.S., Hawley, R.G., and Dick, J.E. 2000. Expansion of human cord blood CD34(+)CD38(-) cells in ex vivo culture during retroviral transduction without a corresponding increase in SCID repopulating cell (SRC) frequency: dissociation of SRC phenotype and function. Blood. 95:102-110.
24. Uchida, N., et al. 1998. HIV, but nor murine leukernia virus, vectors mediate high efficiency gene transfer into freshly isolated G0/G1 human hematopoietic stem cells. Proc. Natl. Acad. Sci. U. S. A. 95:11939-11944.
25. + cells that mediate long-term engraftment of NOD/SCID mice by HIV vectors. Science. 283:682-686.
26. 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. U. S. A. 96:2988-2993.
27. 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.
28. - bone marrow and cord blood-derived SCID-repopulating cells with third-generation lentiviral vectors. Mol. Ther. 1:566-573.
29. Woods, N.B., et al. 2000. Lentiviral gene transfer into primary and secondary NOD/SCID repopulating cells. Blood. 96:3725-3733.
30. + NOD/SCID-repopulating cells. Blood. 99:709-712.
31. Ailles, L., et al. 2002. Molecular evidence of lentiviral vector-mediated gene transfer into human self-renewing, multi-potent, long-term NOD/SCID repopulating hematopoietic cells. Mol. Ther. 6:615-626.
32. Mazutier, F., Gan, O.I., McKenzie, J.L., Doedens, M., and Dick, J.E. 2004. Lenrivector-mediated clonal Tracking reveals intrinsic heterogeneity in the human hemacopoietic stem cell compartment and culture-induced stem cell impairment. Blood. 103:545-552.
33. Naldini, L., and Verma, I.M. 2000. Lentiviral vectors. Adv. Virus Res. 55:599-609.
34. 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.
35. Pfeifer, A., and Verma, I.M. 2001. Gene therapy: promises and problems. Annu. Rev. Genomics Hum. Genet. 2:177-211.
36. May, C., et al. 2000. Therapeutic haemoglobin synthesis in beta-thalassaemic mice expressing lentivirus-encoded human beta-globin. Nature. 406:82-86.
37. Pawliuk, R., et al. 2001. Correction of sickle cell disease in transgenic mouse models by gene therapy. Science. 294:2368-2371.
38. Imren, S., et al. 2002. Permanent and panerythroid correction of murine beta thalassemia by multiple lentiviral integration in hematopoietic stem cells. Proc. Natl. Acad. Sci. U. S. A. 99:14380-14385.
39. May, C., Rivella, S., Chadburn, A., and Sadelain, M. 2002. Successful treatment of murine beta-thalassemia intermedia by transfer of the human beta-globin gene. Blood. 99:1902-1908.
40. Persons, D.A., Hargrove, P.W., Allay, E.R., Hanawa, H., and Nienhuis, A.W. 2003. The degree of phenotypic correction of murine beta -thalassemia intermedia following lentiviral-mediated transfer of a human gamma-globin gene is influenced by chromosomal position effects and vector copy number. Blood. 101:2175-2183.
41. Levasseur, D.N., Ryan, T.M., Pawlik, K.M., and Townes, T.M. 2003. Correction of a mouse model of sickle cell disease: lentiviral/antisickling beta-globin gene transduction of unmobilized, purified hematopoietic stem cells. Blood. 102:4312-4319.
42. Holyoake, T.L., Nicolini, F.E., and Eaves, C.J. 1999. Functional differences between transplantable human hematopoietic stem cells from fetal liver, cord blood, and adult marrow. Exp. Hematol. 27:1418-1427.
43. Glimm, H., et al. 2001. Previously undetected human hematopoietic cell populations with short-term repopulating activity selectively engraft NOD/SCID-beta2 microglobulin-null mice. J. Clin. Invest. 107:199-206.
44. Hacein-Bey-Abina, S., et al. 2003. LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1. Science. 302:415-419.
45. Wang, J.C., Doedens, M., and Dick, J.E. 1997. Primitive human hematopoietic cells are enriched in cord blood compared with adult bone marrow or mobilized peripheral blood as measured by the quantitative in vivo SCID-repopulating cell assay. Blood. 89:3919-3924.
46. Conneally, E., Cashman, J., Petzer, A., and Eaves, C. 1997. Expansion in vitro of transplan table human cord blood stem cells demonstrated using a quantitative assay of their lympho-myeloid repopulating activity in nonobese diabetic-scid/scid mice. Proc. Natl. Acad. Sci. U. S. A. 94:9836-9841.
47. Ailles, L.E., and Naldini, L. 2002. HIV-1-derived lentiviral vectors. Curr. Top. Microbiol. Immunol. 261:31-52.
48. Amsellem, S., Raver, E., Fichelson, S., Pflumio, F., and Dubart-Kupperschmitt, A. 2002. Maximal lentivirus-mediated gene transfer and susrained transgene expression in human hematopoietic primitive cells and their progeny. Mol. Ther. 6:673-677.
49. Zielske, S.P., and Gerson, S.L. 2003. Cytokines, including stem cell factor alone, enhance lentiviral transduction in nondividing human LTCIC and NOD/SCID repopularing cells. Mol. Ther. 7:325-333.
50. Woods, N.B., Ooka, A., and Karlsson, S. 2002. Development of gene therapy for hematopoietic stem cells using lentiviral vectors. Leukemia. 16:563-569.
51. Scherr, M., and Eder, M. 2002. Gene transfer into hematopoietic stem cells using lentiviral vectors. Curr. Gene Ther. 2:45-55.
52. Zielske, S.P., Reese, J.S., Lingas, K.T., Donze, J.R., and Gerson, S.L. 2003. In vivo selection of MGMT(P140K) lentivirus-transduced human NOD/SCID repopulating cells without pretransplant irradiation conditioning. J. Clin. Invest. 112:1561-1570. doi:10.1172/JCI200317922.
53. Piacibello, W., et al. 2002. Lentiviral gene transfer and ex vivo expansion of human primitive stem cells capable of primary, secondary, and tertiary multilineage repopulation in NOD/SCID mice. Nonobese diabetic/severe combined immunodeficient. Blood. 100:4391-4400.
54. Takatoku, M., et al. 2001. Avoidance of stimulation improves engraftment of cultured and retrovirally transduced hematopoietic cells in primares. J. Clin. Invest. 108:447-455. doi:10.1172/JCI200112593.
55. van der Loo, J.C., et al. 1998. Nonobese diabetic/ severe combined immunodeficiency (NOD/SCID) mouse as a model system to study the engraftment and mobilization of human peripheral blood stem cells. Blood. 92:2556-2570.
56. Hennemann, B., et al. 1999. Optimization of retroviral-mediated gene transfer to human NOD/SCID mouse repopulating cord blood cells through a systematic analysis of protocol variables. Exp. Hematol. 27:817-825.
57. Cashman, J.D., Clark-Lewis, I., Eaves, A.C., and Eaves, C.J. 1999. Differentiation stage-specific regulation of primitive human hematopoietic progenitor cycling by exogenous and endogenous inhibitors in an in vivo model. Blood. 94:3722-3729.
58. 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.
59. Oh, I.H., Lau, A., and Eaves, C.J. 2000. During ontogeny primitive (CD34(+)CD38(-)) hematopoietic cells show altered expression of a subset of genes associated with early cycokine and differentiation responses of their adult counterparts. Blood. 96:4160-4168.
60. Kuramoto, K., et al. 2004. The impact of chronic low-dose busulfan on clonal dynamics in nonhuman primates. Blood. 104:1273-1280.
61. Persons, D.A., et al. 2001. Functional requirements for phenotypic correction of murine beta-thalassemia: implications for human gene therapy. Blood. 97:3275-3282.
62. Lander, E. S., et al. 2001. Initial sequencing and analysis of the human genome. Nature. 409:860-921.
63. Venter, J.C., et al. 2001. The sequence of the human genome. Science. 291:1304-1351.
64. Schroder, A.R., et al. 2002. HIV-1 integration in the human genome favors active genes and local hotspots. Cell. 110:521-529.
65. Wu, X., Li, Y., Crise, B., and Burgess, S.M. 2003. Transcription start regions in the human genome are favored targets for MLV integration. Science. 300:1749-1751.
66. Westerman, K.A., Morales, T., Pawliuk, R., Cohen, E., and LeBoulch, P. 2003. A high titer, "supersplit" packaging system in combination with self-inactivating vector for the prevention of replication competent lentivirus (RCL) contamination [abstract]. Mol. Ther. 7:6A.
67. Pawliuk, R., Kay, P., Lansdorp, P., and Humphries, R.K. 1994. Selection of retrovirally transduced hematopoietic cells using CD24 as a marker of gene transfer. Blood. 84:2868-2877.
68. Sutherland, H.J., Eaves, C.J., Eaves, A.C., Dragowska, W., and Lansdorp, P.M. 1989. Characterization and partial purification of human marrow cells capable of initiating long-term hematopoiesis in vitro. Blood. 74:1563-1570.
69. Meyerrose, T.E., Herrbrich, P., Hess, D.A., and Nolta, J.A. 2003. Immune-deficient mouse models for analysis of human seem cells. Biotechniques. 35:1262-1272.
70. Verlinden, S.F., van Es, H.H., and van Bekkum, D.W. 1998. Serial bone marrow sampling for long-term follow up of human hematopoiesis in NOD/SCID mice. Exp. Hematol. 26:627-630.
71. Eaves, C., et al. 1997. Hematopoietic stem cells: inferences from in vivo assays. Stem Cells. 15(Suppl. 1):1-5.
72. Fabry, M.E., et al. 1995. A second generation transgenic mouse model expressing both hemoglobin S (HbS) and HbS-Antilles results in increased phenotypic severity. Blood. 86:2419-2428.
73. Riley, J., et al. 1990. A novel, rapid method for the isolation of terminal sequences from yeast artificial chromosome (YAC) clones. Nucleic Acids Res. 18:2887-2890.