Efficient gene transfer into rhesus repopulating hematopoietic stem cells using a simian immunodeficiency virus-based lentiviral vector system

Blood

Volumn 103, Issue 11, 2004, Pages 4062-4069

  Hanawa, Hideki ^b   Hematti, Peiman ^b   Keyvanfar, Keyvan ^b   Metzger, Mark E ^b   Krouse, Allen ^b   Donahue, Robert E ^b   Kepes, Steve ^b   Gray, John ^b   Dunbar, Cynthia E ^b   Persons, Derek A ^b   Nienhuis, Arthur W ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

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

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUTOLOGOUS HEMATOPOIETIC STEM CELL TRANSPLANTATION; BLOOD; CELL BASED GENE THERAPY; CELL CULTURE; CELL POPULATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DNA DETERMINATION; DRUG DELIVERY SYSTEM; FEMALE; GENE TRANSFER; GENETIC CODE; GENETIC TRANSDUCTION; GRANULOCYTE; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; IN VIVO STUDY; MONOCYTE; NONHUMAN; NORMAL HUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RHESUS MONKEY; SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 2542501560     PISSN: 00064971     EISSN: None     Source Type: Journal    
DOI: 10.1182/blood-2004-01-0045     Document Type: Article

References (80)

1. Sorrentino BP, Nienhuis AW. Gene therapy for hematopoietic diseases. In: Stamatoyannopoulos G, Majerus PW, Perlmutter RM, Varmus H, eds. The Molecular Basis of Blood Diseases. 3rd ed. Philadelphia, PA: WB Saunders; 2001:969-1003.
2. Williams DA, Lemischka IR, Nathan DG, Mulligan RC. Introduction of new genetic material into pluripotent haematopoietic stem cells of the mouse. Nature. 1984;310:476-480.
3. Bunting KD, Sangster MY, Ihle JN, Sorrentino BP. Restoration of lymphocyte function in Janus kinase 3-deficient mice by retroviral-mediated gene transfer. Nat Med. 1998;4:58-64.
4. Otsu M, Anderson SM, Bodine DM, Puck O'Shea JJ, Candotti F. Lymphoid development and function in X-linked severe combined immunodeficiency mice after stem cell gene therapy. Mol Ther. 2000;1:145-153.
5. Soudais C, Shiho T, Sharara LI, et al. Stable and functional lymphoid reconstitution of common cytokine receptor gamma chain deficient mice by retroviral-mediated gene transfer, Blood. 2000;95:3071-3077.
6. Strom TS, Turner SJ, Andreansky S, et al. Defects in T-cell-mediated immunity to influenza virus in murine Wiskott-Aldrich syndrome are corrected by oncoretroviral vector-mediated gene transfer into repopulating hematopoietic cells. Blood. 2003;102:3108-3116.
7. Bjorgvinsdottir H, Ding C, Pech N, Gifford MA, Li LL, Dinauer MC. Retroviral mediated gene transfer of gp91 phox into bone marrow cells rescues defect in host defense against Aspergillus fumigatus in murine X-linked chronic granulomatous disease. Blood. 1997;89:41-48.
8. Mardiney M III, Jackson SH, Spratt SK, Li F, Holland SM, Malech HL. Enhanced host defense after gene transfer in the murine p47phox-deficient model of chronic granulomatous disease. Blood, 1997;69:2268-2275.
9. Hacein-Bey-Abina S, Le Deist F, Carlier F, et al. Sustained correction of X-linked severe combined immunodeficiency by ex vivo gene therapy. N Engl J Med. 2002;346:1185-1193.
10. Aiuti A, Slavin S, Aker M, et al. Correction of ADA-SCID by stem cell gene therapy combined with nonmyeloablative conditioning. Science. 2002;296:2410-2413.
11. Orlic D, Girard LJ, Jordan CT, Anderson SM, Cline AP, Bodine DM. The level of mRNA encoding the amphotropic retrovirus receptor in mouse and human hematopoietic stem cells is low and correlates with the efficiency of retroviral transduction. Proc Natl Acad Sci U S A. 1996;93:11097-11102.
12. Kiem H-P, Heyward S, Winkler A, et al. 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. 1997;90:4638-4645.
13. Kelly PF, Vandergriff J, Nathwani A, Nienhuis AW, Vanin EF. Highly efficient gene transfer into cord blood NOD/SCID repopulating cells by oncoretroviral vector particles pseudotyped with the feline endogenous retrovirus (RD114) envelope protein. Blood. 2000;96:1206-1214.
14. Lucas ML, Seidel N, Porada C, et al. Pseudotyping retroviral vectors with RD114 or FeLV-C envelopes improves transduction of human HSC [abstract]. Mol Ther. 2003;7:S115.
15. Roe T, Reynolds TC, Yu G, Brown PO. Integration of murine leukemia virus DNA depends on mitosis. EMBO J. 1993;12:2099-2108.
16. Naldini L, Blomer U, Gallay P, et al. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science. 1996;272:263-267.
17. Hennemann B, Conneally E, Pawliuk R, et al. Optimization of retroviral-mediated gene transfer to human NOD/SCID mouse repopulating cord blood cells through a systematic analysis of protocol variables. Exp Hematol. 1999;27:817-825.
18. Kiem HP, Andrews RG, Morris J, et al. Improved gene transfer into baboon marrow repopulating cells using recombinant human fibronectin fragment CH-296 in combination with interleukin-6, stem cell factor, FLT-3 ligand, and megakaryocyte growth and development factor. Blood. 1998;92:1878-1886.
19. + hematopoietic cells. Hum Gene Ther. 1997;8:2193-2206.
20. Takatoku M, Sellers S, Agricola BA, et al. Avoidance of stimulation improves engraftment of cultured and retrovirally transduced hematopoietic cells in primates. J Clin Invest. 2001;108:447-455.
21. Goerner M, Horn PA, Peterson L, et al. Sustained multilineage gene persistence and expression in dogs transplanted with CD34(+) marrow cells transduced by RD114-pseudotyped oncoretrovirus vectors. Blood. 2001;98:2065-2070.
22. Haas DL, Case SS, Crooks GM, Kohn DB. Critical factors influencing stable transduction of human CD34(+) cells with HIV-1-derived lentiviral vectors. Mol Ther. 2000;2:71-80.
23. Korin YD, Zack JA. 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. 1998;72:3161-3168.
24. Sutton RE, Reitsma MA, Uchida N, Bound PO. Transduction of human progenitor hematopoietic stem cells by human immunodeficiency virus type 1 based vectors is cell cycle dependent. J Virol. 1999;73:3649-3660.
25. Miyoshi H, Smith KA, Mosier DE, Verma IM, Torbett BEE. Transduction of human CD34+ cells that mediate long-term engraftment of NOD/SCID mice by HIV vectors. Science. 1999;283:682-686.
26. Guenechea G, Gan OI, Inamitsu T, et al. Transduction of human CD34+ CD38- bone marrow and cord blood-derived SCID-repopulating cells with third-generation lentiviral vectors. Mol Ther. 2000;1:566-573.
27. Hanawa H, Kelly PF, Nathwani AC, et al. Comparison of various envelope proteins for their ability to pseudotype lentiviral vectors and transduce primitive hematopoietic cells from human blood. Mol Ther. 2002;5:242-251.
28. Horn PA, Topp MS, Morris JC, Riddell SR, Kiem HP. Highly efficient gene transfer into baboon marrow repopulating cells using GALV-pseudotype oncoretroviral vectors produced by human packaging cells. Blood. 2002;100:3960-3967.
29. An DS, Wersto RP, Agricola BA, et al. Marking and gene expression by a lentivirus vector in transplanted human and nonhuman primate CD34(+) cells. J Virol. 2000;74:1286-1295.
30. An DS, Kung SK, Bonifacino A, et al. Lentivirus vector-mediated hematopoietic stem cell gene transfer of common gamma-chain cytokine receptor in rhesus macaques. J Virol. 2001;75:3547-3555.
31. Horn PA, Morris JC, Bukovsky AA, et al. Lentivirus-mediated gene transfer into hematopoietic repopulating cells in baboons. Gene Ther. 2002;9:1464-1471.
32. Kung SK, An DS, Bonifacino A, et al. Induction of transgene-specific immunological tolerance in myeloablated nonhuman primates using lentivirally transduced CD34(+) progenitor cells. Mol Ther. 2003;8:981-991.
33. Owens CM, Yang PC, Gottlinger H, Sodroski J. Human and simian immunodeficiency virus capsid proteins are major viral determinants of early, postentry replication blocks in simian cells. J Virol. 2003;77:726-731.
34. Cowan S, Hatziioannou T, Cunningham T, Muesing MA, Gottlinger HG, Beiniasz PD. Cellular inhibitors with Fv1-like activity restrict human and simian immunodeficiency virus tropism. Proc Natl Acad Sci U S A. 2002;99:11914-11919.
35. Stoye JP. An intracellular block to primate lentivirus replication. Proc Natl Acad Sci U S A. 2002;99:11549-11551.
36. Besnier C, Takeuchi Y, Towers G. Restriction of lentivirus in monkeys. Proc Natl Acad Sci U S A. 2002;99:11920-11925.
37. Luciw PA, Shaw KE, Unger RE, et al. Genetic and biological comparisons of pathogenic and nonpathogenic molecular clones of simian immunodeficiency virus (SIVmac). AIDS Res Hum Retroviruses. 1992;8:395-402.
38. Dunbar CE, Cottler-Fox M, O'Shaughnessy JA, et al. Retrovirally marked CD34-enriched peripheral blood and bone marrow cells contribute to long-term engraftment after autologous transplantation. Blood. 1995;85:3048-3057.
39. Donahue RE, Kirby MR, Metzger ME, Agricola BA, Sellers SE, Cullis HM. Peripheral blood CD34+ cells differ from bone marrow CD34+ cells in Thy-1 expression and cell cycle status in nonhuman primates mobilized or not mobilized with granulocyte colony-stimulating factor and/or stem cell factor. Blood. 1996;87:1644-1653.
40. Persons DA, Allay JA, Riberdy JM, et al. Use of the green fluorescent protein as a marker to identify and track genetically modified hematopoietic cells. Nat Med. 1998;4:1201-1205.
41. Schmidt M, Zickler P, Hoffmann G, et al. Polyclonal long-term repopulating stem cell clones in a primate model. Blood. 2002;100:2737-2743.
42. Price MA, Case SS, Carbonaro DA, et al. Expression from second-generation feline immunodeficiency virus vectors is impaired in human hematopoietic cells. Mol Ther. 2002;6:645-652.
43. Ruggieri A, Negre D, Cosset FL. SIV vectors. Methods Mol Biol. 2003;229:233-249.
44. Negre D, Duisit G, Mangeot PE, Moullier P, Darlix JL, Cosset FL. Lentiviral vectors derived from simian immunodeficiency virus. Curr Top Microbiol Immunol. 2002;261:53-74.
45. Mangeot PE, Duperrier K, Negre D, et al. High levels of transduction of human dendritic cells with optimized SIV vectors. Mol Ther. 2002;5:283-290.
46. Pandya S, Boris-Lawrie K, Leung NJ, Akkina R, Planelles V. Development of an Rev-independent, minimal simian immunodeficiency virus-derived vector system. Hum Gen Ther. 2001;12:847-857.
47. Sandrin V, Boson B, Salmon P, et al. Lentiviral vectors pseudotyped with a modified RD114 envelope glycoprotein show increased stability in sera and augmented transduction of primary lymphocytes and CD34+ cells derived from human and nonhuman primates. Blood. 2002;100:823-832.
48. Kootstra NA, Munk C, Tonnu N, Landau NR, Verma IM. Abrogation of postentry restriction of HIV-1-based lentiviral vector transduction in simian cells. Proc Natl Acad Sci U S A. 2003;100:1298-1303.
49. Morris JC, Conerly M, Thomasson B, Storek J, Riddell SR, Kiem HP. Induction of cytotoxic T-lymphocyte responses to enhanced green and yellow fluorescent proteins after myeloablative conditioning. Blood. 2004;103:492-499.
50. Donahue RE, Wersto RP, Allay JA, et al; High levels of lymphoid expression of enhanced green fluorescent protein in nonhuman primates transplanted with cytokine-mobilized peripheral blood CD34+ cells. Blood. 2000;95:445-452.
51. Kluge KA, Bonifacino AC, Sellers S, Agricola BA, Donahue RE, Dunbar CE. Retroviral transduction and engraftment ability of primate hematopoietic progenitor and stem cells transduced under serum-free versus serum-containing conditions. Mol Ther. 2002;5:316-322.
52. Hu J, Kelly P, Bonifacino A, et al. Direct comparison of RD114-pseudotyped versus amphotropic-pseudotyped retroviral vectors for transduction of rhesus macaque long-term repopulating cells. Mol Ther. 2003;8:611-617.
53. Hematti P, Sellers SE, Agricola BA, Metzger ME, Donahue RE, Dunbar CE. Retroviral transduction efficiency of G-CSF+SCF-mobilized peripheral blood CD34+ cells is superior to G-CSF or G-CSF+Flt3-L-mobilized cells in nonhuman primates. Blood. 2003;101:2199-2205.
54. Horn PA, Thomasson BM, Wood BL, Andrews RG, Morris JC, Kiem HP. Distinct hematopoietic stem/progenitor cell populations are responsible for repopulating NOD/SCID mice versus nonhuman primates. Blood. 2003;102:4329-4335.
55. Kurre P, Morris J, Thomasson B, Kohn DB, Kiem HP. Scaffold attachment region-containing retrovirus vectors improve long-term proviral expression after transplantation of GFP-modified CD34+ baboon repopulating cells. Blood. 2003;102:3117-3119.
56. Reya T, Duncan AW, Ailles L, et al. The role for Wnt signaling in self-renewal of haematopoietic stem cells. Nature. 2003;423:409-414.
57. Amsellem S, Pflumio F, Bardinet D, et al. Ex vivo expansion of human hematopoietic stem cells by direct delivery of the HOXB4 homeoprotein. Nat Med. 2003;9:1423-1427.
58. Ailles LE, Naldini L. HIV-1-derived lentiviral vectors. Curr Top Microbiol Immunol. 2002;261:31-52.
59. May C, Rivella S, Gallegari J, et al. Therapeutic haemoglobin synthesis in beta-thalassemic mice expressing lentivirus-encoded human beta-globin. Nature. 2000;406:82-86.
60. Rivella S, May C, Chadburn A, Riviere I, Sadelain M. A novel murine model of Cooley anemia and its rescue by lentiviral-mediated human beta-globin gene transfer. Blood. 2003;101:2932-2339.
61. Pawliuk R, Westerman KA, Fabry ME, et al. Correction of sickle cell disease in transgenic mouse models by gene therapy. Science. 2001;294:2368-2371.
62. Levasseur DN, Ryan TM, Pawlik KM, Townes TM. Correction of a mouse model of sickle cell disease: lentiviral/antisickling beta-globin gene transduction of unmobilized, purified hematopoietic stem cells. Blood. 2003;102:4312-4319.
63. Imren S, Payen E, Westerman KA, et al. Permanent and panerythroid correction of murine beta thalassemia by multiple lentiviral integration in hematopoietic stem cells. Proc Natl Acad Sci U S A. 2002;99:14380-14385.
64. Persons DA, Hargrove PW, Allay ER, Hanawa H, Nienhuis AW. 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. 2003;101:2175-2183.
65. Hanawa H, Hargrove PW, Kepes T, Nienhuis AW, Persons DA. Extended beta-globin locus control region enhancer elements promote consistent therapeutic expression of a gamma-globin lentiviral vector in murine beta-thalassemia in the context of reduced vector copy number [abstract]. Mol Ther. 2003;7:S157.
66. Sorrentino BP. Gene therapy to protect haematopoietic cells from cytotoxic cancer drugs. Nat Rev Cancer. 2002;2:431-441.
67. Persons DA, Nienhuis AW. In vivo selection to improve gene therapy of hematopoietic disorders. Curr Opin Mol Ther. 2002;4:491-498.
68. Sawai N, Zhou S, Vanin EF, Houghton P, Brent TP, Sorrentino BP. Protection and in vivo selection of hematopoietic stem cells using temozolomide, O6-benzylguanine and an alkyltransferase-expressing retroviral vector. Mol Ther. 2001;3:78-87.
69. Jansen M, Sorg UR, Ragg S, et al. Hematoprotection and enrichment of transduced cells in vivo after gene transfer of MGMT (P140K) into hematopoietic stem cells. Cancer Gene Ther. 2002;9:737-746.
70. Bowman JE, Reese JS, Lingas KT, Gerson SL. Myeloablation is not required to select and maintain expression of the drug-resistance gene, mutant MGMT, in primary and secondary recipients. Mol Ther. 2003;8:42-50.
71. Persons DA, Allay ER, Sawai N, et al. Successful treatment of murine beta-thaiassemia using in vivo selection of genetically modified, drug-resistant hematopoietic stem cells. Blood. 2003;102:506-513.
72. Neff T, Hom PA, Peterson LJ, et al. Methylguanine methyltransferase-mediated in vivo selection and chemoprotection of allogeneic stem cells in a large-animal model. J Clin Invest. 2003;112:1581-1588.
73. Schroder AR, Shinn P, Chen H, Berry C, Ecker JR, Bushman F. HIV-1 integration in the human genome favors active genes and local hotspots. Cell. 2002;110:521-529.
74. Wu X, Li Y, Crise B, Burgess SM. Transcription start regions in the human genome are favored targets for MLV integration. Science. 2003;300:1749-1751.
75. Woods NB, Muessig A, Schmidt M, et al. Lentiviral vector transduction of NOD/SCID repopulating cells results in multiple vector integrations per transduced cell: risk of insertional mutagenesis. Blood. 2003;101:1284-1289.
76. Hacein-Bey-Abina S, Von Kalle C, Schmidt M, et al. LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1. Science. 2003;302:415-419.
77. Kohn DB, Sadelain M, Glorioso JC. Occurrence of leukaemia following gene therapy of X-linked SCID. Nat Rev Cancer. 2003;3:477-488.
78. Williams DA, Baum C. Medicine Gene therapy-new challenges ahead. Science. 2003;302:400-401.
79. Baum C, Dullmann J, Li Z, et al. Side effects of retroviral gene transfer into hematopoietic stem cells. Blood. 2003;101:2099-2114.
80. Calmels B, Kim HJ, Adler R, et al. Retriviral vector integration into the genome of rhesus macaque long-term repopulating cells appears to be non-random, and recurrent integration loci include MDS1 and HIPK2 [abstract]. Blood. 2003;102:199a.