Gene therapy for hemophilia: Hopes and hurdles

Critical Reviews in Oncology/Hematology

Volumn 28, Issue 3, 1998, Pages 153-171

  Chuah, Marinee K L ^a   Collen, Desire ^a   Vandendriessche, Thierry ^a  

^a Cardiac Unit   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD CLOTTING FACTOR 8; VIRUS VECTOR;

ADENOVIRUS; ANIMAL CELL; ANIMAL MODEL; GENE THERAPY; GENETIC TRANSFECTION; HEMOPHILIA; HEMOPHILIA A; HEMOPHILIA B; MOLONEY LEUKEMIA ONCOVIRUS; MOUSE; NONHUMAN; RETROVIRUS; REVIEW;

ANIMALS; FACTOR IX; FACTOR VIII; GENE THERAPY; GENETIC VECTORS; HEMOPHILIA A; HUMANS;

EID: 0032169125     PISSN: 10408428     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1040-8428(98)00022-5     Document Type: Review

References (124)

1. Lozier JN, Brinkhous KM Gene therapy and the hemophilias (see comments). J Am Med Assoc. 271:1994;47-51.
2. Morgan RA, Anderson WF Human gene therapy. Annu Rev Biochem. 62:1993;191-217.
3. Hoeben RC Gene therapy for the haemophilias: current status. Biologicals. 23:1995;27-29.
4. Eisensmith RC, Woo SL Viral vector-mediated gene therapy for hemophilia B. Thromb Haemost. 78:1997;24-30.
5. Connelly S, Kaleko M Gene therapy for hemophilia A. Thromb Haemost. 78:1997;31-36.
6. Kurachi K, Yao SN, Furukawa M et al. Deficiencies in factors IX and VIII: what is now known. Hosp Pract Off Ed. 27:1992;41-51.
7. Fallaux FJ, Hoeben RC Gene therapy for the hemophilias. Curr Opin Hematol. 3:1996;385-389.
8. Thompson AR Status of gene transfer for hemophilia A and B. Thromb Haemost. 66:1991;119-122.
9. Thompson AR Progress towards gene therapy for the hemophilias. Thromb Haemost. 74:1995;45-51.
10. Peerlinck K, Arnout J, Di Giambattista M et al. Factor VIII inhibitors in previously treated haemophilia A patients with a double virus-inactivated plasma derived factor VIII concentrate. Thromb Haemost. 77:1997;80-86.
11. St. Louis D, Verma IM An alternative approach to somatic cell gene therapy. Proc Natl Acad Sci USA. 85:1988;3150-3154.
12. Axelrod JH, Read MS, Brinkhous KM et al. Phenotypic correction of factor IX deficiency in skin fibroblasts of hemophilic dogs. Proc Natl Acad Sci USA. 87:1990;5173-5177.
13. Hoeben RC, van der Jagt RC, Schoute F et al. Expression of functional factor VIII in primary human skin fibroblasts after retrovirus-mediated gene transfer. J Biol Chem. 265:1990;7318-7323.
14. Israel DI, Kaufman RJ Retroviral-mediated transfer and amplification of a functional human factor VIII gene. Blood. 75:1990;1074-1080.
15. Scharfmann R, Axelrod JH, Verma IM Long-term in vivo expression of retrovirus-mediated gene transfer in mouse fibroblast implants. Proc Natl Acad Sci USA. 88:1991;4626-4630.
16. Lynch CM, Israel DI, Kaufman RJ et al. Sequences in the coding region of clotting factor VIII act as dominant inhibitors of RNA accumulation and protein production. Hum Gene Ther. 4:1993;259-272.
17. Chuah MK, Vandendriessche T, Morgan RA Development and analysis of retroviral vectors expressing human factor VIII as a potential gene therapy for hemophilia A. Hum Gene Ther. 6:1995;1363-1377.
18. Dwarki VJ, Belloni P, Nijjar T et al. Gene therapy for hemophilia A: production of therapeutic levels of human factor VIII in vivo in mice. Proc Natl Acad Sci USA. 92:1995;1023-1027.
19. Dai YF, Qiu XF, Xue JL et al. High efficient transfer and expression of human clotting factor IX cDNA in cultured human primary skin fibroblasts from hemophilia B patient by retroviral vectors. Sci China B. 35:1992;183-193.
20. Page SM, Brownlee GG An ex vivo keratinocyte model for gene therapy of hemophilia B. J Invest Dermatol. 109:1997;139-145.
21. Fenjves ES, Yao SN, Kurachi K et al. Loss of expression of a retrovirus-transduced gene in human keratinocytes. J Invest Dermatol. 106:1996;576-578.
22. Yao SN, Wilson JM, Nabel EG et al. Expression of human factor IX in rat capillary endothelial cells: toward somatic gene therapy for hemophilia B. Proc Natl Acad Sci USA. 88:1991;8101-8105.
23. Hortelano G, Al Hendy A, Ofosu FA et al. Delivery of human factor IX in mice by encapsulated recombinant myoblasts: a novel approach towards allogeneic gene therapy of hemophilia B. Blood. 87:1996;5095-5103.
24. Yao SN, Kurachi K Expression of human factor IX in mice after injection of genetically modified myoblasts. Proc Natl Acad Sci USA. 89:1992;3357-3361.
25. Yao SN, Smith KJ, Kurachi K Primary myoblast-mediated gene transfer: persistent expression of human factor IX in mice. Gene Ther. 1:1994;99-107.
26. Dai Y, Roman M, Naviaux RK et al. Gene therapy via primary myoblasts: long-term expression of factor IX protein following transplantation in vivo. Proc Natl Acad Sci USA. 89:1992;10892-10895.
27. Baru M, Sha'anani J, Nur I Retroviral-mediated in vivo gene transfer into muscle cells and synthesis of human factor IX in mice. Intervirology. 38:1995;356-360.
28. Hao QL, Malik P, Salazar R et al. Expression of biologically active human factor IX in human hematopoietic cells after retroviral vector-mediated gene transduction. Hum Gene Ther. 6:1995;873-880.
29. Hoeben RC, Einerhand MP, Briet E et al. Toward gene therapy in haemophilia A: retrovirus-mediated transfer of a factor VIII gene into murine haematopoietic progenitor cells. Thromb Haemost. 67:1992;341-345.
30. Hurwitz DR, Kirchgesser M, Merrill W et al. Systemic delivery of human growth hormone or human factor IX in dogs by reintroduced genetically modified autologous bone marrow stromal cells. Hum Gene Ther. 8:1997;137-156.
31. Wang L, Zoppe M, Hackeng TM et al. A factor IX-deficient mouse model for hemophilia B gene therapy. Proc Natl Acad Sci USA. 94:1997;11563-11566.
32. Lin HF, Maeda N, Smithies O et al. A coagulation factor IX-deficient mouse model for human hemophilia B. Blood. 90:1997;3962-3966.
33. Bi L, Lawler AM, Antonorakis SE et al. Targeted disruption of the mouse factor VIII gene produces a model of haemophilia A [letter]. Nat Genet. 10:1995;119-121.
34. Giles AR, Tinlin S, Hoogendoorn H et al. Development of factor VIII:C antibodies in dogs with hemophilia A (factor VIII:C deficiency). Blood. 63:1984;451-456.
35. Evans JP, Brinkhous KM, Brayer GD et al. Canine hemophilia B resulting from a point mutation with unusual consequences. Proc Natl Acad Sci USA. 86:1989;10095-10099.
36. Zatloukal K, Cotten M, Berger M et al. In vivo production of human factor VII in mice after intrasplenic implantation of primary fibroblasts transfected by receptor-mediated, adenovirus-augmented gene delivery. Proc Natl Acad Sci USA. 91:1994;5148-5152.
37. Lozier JN, Thompson AR, Hu PC et al. Efficient transfection of primary cells in a canine hemophilia B model using adenovirus-polylysine-DNA complexes. Hum Gene Ther. 5:1994;313-322.
38. Gitschier J, Wood WI, Goralka TM et al. Characterization of the human factor VIII gene. Nature. 312:1984;326-330.
39. Wood WI, Capon DJ, Simonsen CC et al. Expression of active human factor VIII from recombinant DNA clones. Nature. 312:1984;330-337.
40. Toole JJ, Knopf JL, Wozney JM et al. Molecular cloning of a cDNA encoding human antihaemophilic factor. Nature. 312:1984;342-347.
41. Toole JJ, Pittman DD, Orr EC et al. A large region (approximately equal to 95 kDa) of human factor VIII is dispensable for in vitro procoagulant activity. Proc Natl Acad Sci USA. 83:1986;5939-5942.
42. Berntorp E Second generation, B-domain deleted recombinant factor VIII. Thromb Haemost. 78:1997;256-260.
43. Hoeben RC, Fallaux FJ, Cramer SJ et al. Expression of the blood-clotting factor-VIII cDNA is repressed by a transcriptional silencer located in its coding region. Blood. 85:1995;2447-2454.
44. Fallaux FJ, Hoeben RC, Cramer SJ et al. The human clotting factor VIII cDNA contains an autonomously replicating sequence consensus- and matrix attachment region-like sequence that binds a nuclear factor, represses heterologous gene expression, and mediates the transcriptional effects of sodium butyrate. Mol Cell Biol. 16:1996;4264-4272.
45. Koeberl DD, Halbert CL, Krumm A et al. Sequences within the coding regions of clotting factor VIII and CFTR block transcriptional elongation. Hum Gene Ther. 6:1995;469-479.
46. Pittman DD, Kaufman RJ Structure-function relationships of factor VIII elucidated through recombinant DNA technology. Thromb Haemost. 61:1989;161-165.
47. Dorner AJ, Kaufman RJ The levels of endoplasmic reticulum proteins and ATP affect folding and secretion of selective proteins. Biologicals. 22:1994;103-112.
48. Kaufman RJ, Wasley LC, Dorner AJ Synthesis, processing, and secretion of recombinant human factor VIII expressed in mammalian cells. J Biol Chem. 263:1988;6352-6362.
49. Kaufman RJ Expression and structure-function properties of recombinant factor VIII. Transfus Med Rev. 6:1992;235-246.
50. Miller AD Retroviral vectors. Curr Top Microbiol Immunol. 158:1992;1-24.
51. Miller AD, Miller DG, Garcia JV et al. Use of retroviral vectors for gene transfer and expression. Methods Enzymol. 217:1993;581-599.
52. Cornetta K, Morgan RA, Anderson WF Safety issues related to retroviral-mediated gene transfer in humans. Hum Gene Ther. 2:1991;5-14.
53. Anderson WF, McGarrity GJ, Moen RC Report to the NIH Recombinant DNA Advisory Committee on murine replication-competent retrovirus (RCR) assays (February 17, 1993). Hum Gene Ther. 4:1993;311-321.
54. Donahue RE, Kessler SW, Bodine D et al. Helper virus induced T cell lymphoma in nonhuman primates after retroviral mediated gene transfer. J Exp Med. 176:1992;1125-1135.
55. Hamer DH, Leder P Splicing and the formation of stable RNA. Cell. 18:1979;1299-1302.
56. Palmiter RD, Sandgren EP, Avarbock MR et al. Heterologous introns can enhance expression of transgenes in mice. Proc Natl Acad Sci USA. 88:1991;478-482.
57. Krall W, Kohn DB Expression levels by retroviral vectors based upon the N2 and the MFG backbones (letter). Gene Ther. 3:1996;365.
58. Hoeben RC, Fallaux FJ, Van Tilburg NH et al. Toward gene therapy for hemophilia A: long-term persistence of factor VIII-secreting fibroblasts after transplantation into immunodeficient mice. Hum Gene Ther. 4:1993;179-186.
59. Drize NJ, Surin VL, Gan OI et al. Gene therapy model for stromal precursor cells of hematopoietic microenvironment. Leukemia. 6:1992;1749-1755.
60. Prockop DJ Marrow stromal cells as stem cells for nonhematopoietic tissues. Science. 276:1997;71-74.
61. Li KJ, Dilber MS, Abedi MR et al. Retroviral-mediated gene transfer into human bone marrow stromal cells: studies of efficiency and in vivo survival in SCID mice. Eur J Haematol. 55:1995;302-306.
62. Nolta JA, Hanley MB, Kohn DB Sustained human hematopoiesis in immunodeficient mice by cotransplantation of marrow stroma expressing human interleukin-3: analysis of gene transduction of long-lived progenitors. Blood. 83:1994;3041-3051.
63. Kay MA, Rothenberg S, Landen CN et al. In vivo gene therapy of hemophilia B: sustained partial correction in factor IX-deficient dogs (see comments). Science. 262:1993;117-119.
64. Rettinger SD, Kennedy SC, Wu X et al. Liver-directed gene therapy: quantitative evaluation of promoter elements by using in vivo retroviral transduction. Proc Natl Acad Sci USA. 91:1994;1460-1464.
65. Ory DS, Neugeboren BA, Mulligan RC A stable human-derived packaging cell line for production of high titer retrovirus/vesicular stomatitis virus G pseudotypes. Proc Natl Acad Sci USA. 93:1996;11400-11406.
66. Takeuchi Y, Porter CD, Strahan KM et al. Sensitization of cells and retroviruses to human serum by α-1,3-galactosyltransferase. Nature. 379:1996;85-88.
67. Cosset FL, Takeuchi Y, Battini JL et al. High-titer packaging cells producing recombinant retroviruses resistant to human serum. J Virol. 69:1995;7430-7436.
68. Lieber A, Peeters MJ, Gown A et al. A modified urokinase plasminogen activator induces liver regeneration without bleeding. Hum Gene Ther. 6:1995;1029-1037.
69. Bosch A, McCray PB Jr, Chang SM et al. Proliferation induced by keratinocyte growth factor enhances in vivo retroviral-mediated gene transfer to mouse hepatocytes. J Clin Invest. 98:1996;2683-2687.
70. Miyanohara A, Yee JK, Bouic K et al. Efficient in vivo transduction of the neonatal mouse liver with pseudotyped retroviral vectors. Gene Ther. 2:1995;138-142.
71. Naldini L, Blomer U, Gage FH et al. Efficient transfer, integration, and sustained long-term expression of the transgene in adult rat brains injected with a lentiviral vector. Proc Natl Acad Sci USA. 93:1996;11382-11388.
72. Naldini L, Blomer U, Gallay P et al. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector (see comments). Science. 272:1996;263-267.
73. Blomer U, Naldini L, Kafri T et al. Highly efficient and sustained gene transfer in adult neurons with a lentivirus vector. J Virol. 71:1997;6641-6649.
74. Zufferey R, Nagy D, Mandel RJ et al. Multiply attenuated lentiviral vector achieves efficient gene delivery in vivo. Nat Biotechnol. 15:1997;871-875.
75. Berkner KL Development of adenovirus vectors for the expression of heterologous genes. Biotechniques. 6:1988;616-629.
76. Connelly S, Smith TA, Dhir G et al. In vivo gene delivery and expression of physiological levels of functional human factor VIII in mice. Hum Gene Ther. 6:1995;185-193.
77. Connelly S, Gardner JM, McClelland A et al. High-level tissue-specific expression of functional human factor VIII in mice. Hum Gene Ther. 7:1996;183-195.
78. Connelly S, Gardner JM, Lyons RM et al. Sustained expression of therapeutic levels of human factor VIII in mice. Blood. 87:1996;4671-4677.
79. Connelly S, Mount J, Mauser A et al. Complete short-term correction of canine hemophilia A by in vivo gene therapy. Blood. 88:1996;3846-3853.
80. Smith TA, Mehaffey MG, Kayda DB et al. Adenovirus mediated expression of therapeutic plasma levels of human factor IX in mice. Nat Genet. 5:1993;397-402.
81. Tinlin S, Webster S, Giles AR The development of homologous (canine/anti-canine) antibodies in dogs with haemophilia A (factor VIII deficiency): a 10-year longitudinal study. Thromb Haemost. 69:1993;21-24.
82. Yang Y, Ertl HC, Wilson JM MHC class I-restricted cytotoxic T lymphocytes to viral antigens destroy hepatocytes in mice infected with E1-deleted recombinant adenoviruses. Immunity. 1:1994;433-442.
83. Yang Y, Nunes FA, Berencsi K et al. Cellular immunity to viral antigens limits E1-deleted adenoviruses for gene therapy. Proc Natl Acad Sci USA. 91:1994;4407-4411.
84. Yeh P, Dedieu JF, Orsini C et al. Efficient dual transcomplementation of adenovirus E1 and E4 regions from a 293-derived cell line expressing a minimal E4 functional unit. J Virol. 70:1996;559-565.
85. Armentano D, Sookdeo CC, Hehir KM et al. Characterization of an adenovirus gene transfer vector containing an E4 deletion. Hum Gene Ther. 6:1995;1343-1353.
86. Wang Q, Jia XC, Finer MH A packaging cell line for propagation of recombinant adenovirus vectors containing two lethal gene-region deletions. Gene Ther. 2:1995;775-783.
87. Gao GP, Yang Y, Wilson JM Biology of adenovirus vectors with E1 and E4 deletions for liver-directed gene therapy. J Virol. 70:1996;8934-8943.
88. Mitani K, Graham FL, Caskey CT et al. Rescue, propagation, and partial purification of a helper virus-dependent adenovirus vector. Proc Natl Acad Sci USA. 92:1995;3854-3858.
89. Clemens PR, Kochanek S, Sunada Y et al. In vivo muscle gene transfer of full-length dystrophin with an adenoviral vector that lacks all viral genes. Gene Ther. 3:1996;965-972.
90. Kochanek S, Clemens PR, Mitani K et al. A new adenoviral vector: Replacement of all viral coding sequences with 28 kb of DNA independently expressing both full-length dystrophin and β-galactosidase. Proc Natl Acad Sci USA. 93:1996;5731-5736.
91. Chen HH, Mack LM, Kelly R et al. Persistence in muscle of an adenoviral vector that lacks all viral genes. Proc Natl Acad Sci USA. 94:1997;1645-1650.
92. Parks RJ, Chen L, Anton M et al. A helper-dependent adenovirus vector system: removal of helper virus by Cre-mediated excision of the viral packaging signal. Proc Natl Acad Sci USA. 93:1996;13565-13570.
93. Parks RJ, Graham FL A helper-dependent system for adenovirus vector production helps define a lower limit for efficient DNA packaging. J Virol. 71:1997;3293-3298.
94. Lieber A, He CY, Kirillova I et al. Recombinant adenoviruses with large deletions generated by Cre-mediated excision exhibit different biological properties compared with first-generation vectors in vitro and in vivo. J Virol. 70:1996;8944-8960.
95. Smith TA, White BD, Gardner JM et al. Transient immunosuppression permits successful repetitive intravenous administration of an adenovirus vector. Gene Ther. 3:1996;496-502.
96. Yang Y, Greenough K, Wilson JM Transient immune blockade prevents formation of neutralizing antibody to recombinant adenovirus and allows repeated gene transfer to mouse liver. Gene Ther. 3:1996;412-420.
97. Yang Y, Trinchieri G, Wilson JM Recombinant IL-12 prevents formation of blocking IgA antibodies to recombinant adenovirus and allows repeated gene therapy to mouse lung [see comments]. Nat Med. 1:1995;890-893.
98. Kotin RM Prospects for the use of adeno-associated virus as a vector for human gene therapy. Hum Gene Ther. 5:1994;793-801.
99. Xiao X, Li J, Samulski RJ Efficient long-term gene transfer into muscle tissue of immunocompetent mice by adeno-associated virus vector. J Virol. 70:1996;8098-8108.
100. Kaplitt MG, Leone P, Samulski RJ et al. Long-term gene expression and phenotypic correction using adeno-associated virus vectors in the mammalian brain. Nat Genet. 8:1994;148-154.
101. Snyder RO, Miao CH, Patijn GA et al. Persistent and therapeutic concentrations of human factor IX in mice after hepatic gene transfer of recombinant AAV vectors. Nat Genet. 16:1997;270-276.
102. Cristiano RJ, Smith LC, Kay MA et al. Hepatic gene therapy: efficient gene delivery and expression in primary hepatocytes utilizing a conjugated adenovirus-DNA complex. Proc Natl Acad Sci USA. 90:1993;11548-11552.
103. Kurachi K, Furukawa M, Yao SN et al. Biology of factor IX. Hematol Oncol Clin North Am. 6:1992;991-997.
104. Liles D, Landen CN, Monroe DM et al. Extravascular administration of factor IX: potential for replacement therapy of canine and human hemophilia B. Thromb Haemost. 77:1997;944-948.
105. Anson DS, Hock RA, Austen D et al. Towards gene therapy for hemophilia B. Mol Biol Med. 4:1987;11-20.
106. Hoeben RC, Migchielsen AA, van der Jagt RC et al. Inactivation of the Moloney murine leukemia virus long terminal repeat in murine fibroblast cell lines is associated with methylation and dependent on its chromosomal position. J Virol. 65:1991;904-912.
107. Zhou JM, Qiu XF, Lu DR et al. Long-term expression of human factor IX cDNA in rabbits. Sci China B. 36:1993;1333-1341.
108. Lu DR, Zhou JM, Zheng B et al. Stage I clinical trial of gene therapy for hemophilia B. Sci China B. 36:1993;1342-1351.
109. Qiu X, Lu D, Zhou J et al. Implantation of autologous skin fibroblast genetically modified to secrete clotting factor IX partially corrects the hemorrhagic tendencies in two hemophilia B patients. Chin Med J Engl. 109:1996;832-839.
110. Roman M, Axelrod JH, Dai Y et al. Circulating human or canine factor IX from retrovirally transduced primary myoblasts and established myoblast cell lines grafted into murine skeletal muscle. Somat Cell Mol Genet. 18:1992;247-258.
111. Armentano D, Thompson AR, Darlington G et al. Expression of human factor IX in rabbit hepatocytes by retrovirus-mediated gene transfer: potential for gene therapy of hemophilia B. Proc Natl Acad Sci USA. 87:1990;6141-6145.
112. Gerrard AJ, Hudson DL, Brownlee GG et al. Towards gene therapy for haemophilia B using primary human keratinocytes. Nat Genet. 3:1993;180-183.
113. Gerrard AJ, Austen DE, Brownlee GG Recombinant factor IX secreted by transduced human keratinocytes is biologically active. Br J Haematol. 95:1996;561-563.
114. Liu HW, Ofosu FA, Chang PL Expression of human factor IX by microencapsulated recombinant fibroblasts. Hum Gene Ther. 4:1993;291-301.
115. Brauker JH, Carr Brendel VE, Martinson LA et al. Neovascularization of synthetic membranes directed by membrane microarchitecture. J Biomed Mater Res. 29:1995;1517-1524.
116. Carr Brendel VE, Geller RL, Thomas TJ et al. Transplantation of cells in an immunoisolation device for gene therapy. Methods Mol Biol. 63:1997;373-387.
117. Nelson DM, Metzger ME, Donahue RE et al. In vivo retrovirus-mediated gene transfer into multiple hematopoietic lineages in rabbits without preconditioning. Hum Gene Ther. 8:1997;747-754.
118. Kay MA, Landen CN, Rothenberg SR et al. In vivo hepatic gene therapy: complete albeit transient correction of factor IX deficiency in hemophilia B dogs. Proc Natl Acad Sci USA. 91:1994;2353-2357.
119. Dai Y, Schwarz EM, Gu D et al. Cellular and humoral immune responses to adenoviral vectors containing factor IX gene: tolerization of factor IX and vector antigens allows for long-term expression. Proc Natl Acad Sci USA. 92:1995;1401-1405.
120. Fang B, Eisensmith RC, Wang H et al. Gene therapy for hemophilia B: host immunosuppression prolongs the therapeutic effect of adenovirus-mediated factor IX expression. Hum Gene Ther. 6:1995;1039-1044.
121. Fang B, Wang H, Gordon G et al. Lack of persistence of E1-recombinant adenoviral vectors containing a temperature-sensitive E2A mutation in immunocompetent mice and hemophilia B dogs. Gene Ther. 3:1996;217-222.
122. Lozier JN, Yankaskas JR, Ramsey WJ et al. Gut epithelial cells as targets for gene therapy of hemophilia. Hum Gene Ther. 8:1997;1481-1490.
123. Koeberl DD, Alexander IE, Halbert CL et al. Persistent expression of human clotting factor IX from mouse liver after intravenous injection of adeno-associated virus vectors. Proc Natl Acad Sci USA. 94:1997;1426-1431.
124. Herzog RW, Hagstrom JN, Kung SH et al. Stable gene transfer and expression of human blood coagulation factor IX after intramuscular injection of recombinant adeno-associated virus. Proc Natl Acad Sci USA. 94:1997;5804-5809.