Thromb Haemost 1997; 78(01): 024-030
DOI: 10.1055/s-0038-1657495
Gene therapy for hemophilia: hopes and reality for the children of the new century
Schattauer GmbH Stuttgart

Viral Vector-Mediated Gene Therapy for Hemophilia B

Randy C Eisensmith
Institute for Gene Therapy and Molecular Medicine, Mount Sinai School of Medicine, New York, NY, USA
,
Savio L C Woo
Institute for Gene Therapy and Molecular Medicine, Mount Sinai School of Medicine, New York, NY, USA
› Author Affiliations
Further Information

Publication History

Publication Date:
12 July 2018 (online)

 
  • References

  • 1 Roberts HR, Lozier JN. Clinical Aspects and Therapy for Hemophilia B. In Hematology: Basic Principles and Practice. Hoffman R, Bens Jr E, Shattil S, Furie B, Cohen H. eds Churchill Livingston; New York, NY: 1991. pp. 1325-1331
  • 2 Boyd Y, Buckle VJ, Munro EA, Choo KH, Migeon BR, Craig IW. Assignment of the haemophilia B (factor IX) locus to the q26-qter region of the X chromosome. Ann Hum Genet 1984; 48: 145-152
  • 3 Camerino G, Grzeschik KH, Jaye M, De la Salle L, Tolstophev P, Lecocq JP, Heilig R, Mandel JL. Regional localization on the human X chromosome and polymorphism of the coagulation factor IX gene (hemophilia B locus). Proc Natl Acad Sci USA 1984; 81: 498-502
  • 4 Giannelli F, Green PM, High KA, Sommer S, Poon MC, Ludwig M, Schwaab R, Reitsma PH, Gossens M, Yoshioka A, Brownlee GG. Haemophilia B: database of point mutations and short additions and deletions—fourth edition. Nucleic Acids Res 1993; 21: 3075-3087
  • 5 Reiner AP, Davie EW. Introduction to Hemostasis and the Vitamin K-Dependent Coagulation Factors. In: The Metabolic and Molecular Bases of Inherited Disease. Scriver CR, Beaudet AL, Sly WS, Valle D. eds McGraw-Hill, Inc.; New York, NY: 1995. pp 3181-3131 01.
  • 6 Anson DS, Hock RA, Austen D, Smith KJ, Brownlee GG, Verma I, Miller DA. Towards gene therapy for hemophilia B. Mol Biol Med 1987; 4: 11-20
  • 7 St Louis D, Verma IM. An alternative approach to somatic cell gene therapy. Proc Natl Acad Sci USA 1988; 85: 3150-3154
  • 8 Palmer TD, Thompson AR, Miller AD. Production of human factor IX in animals by genetically modified skin fibroblasts: potential therapy for hemophilia B. Blood 1989; 73: 438-445
  • 9 Armentano D, Thompson AR, Darlington G, Woo SLC. 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 1990; 87: 6141-6145
  • 10 Axelrod JH, Read MS, Brinkhous KM, Verma IM. Phenotypic correction of factor IX deficiency in skin fibroblasts of hemophilic dogs. Proc Natl Acad Sci USA 1990; 87: 5173-5177
  • 11 Yao SN, Wilson JM, Nabel EG, Kurachi S, Hachiya HL, Kurachi K. Expression of human factor IX in rat capillary endothelial cells: toward somatic gene therapy for hemophilia B. Proc Natl Acad Sci USA 1991; 88: 8101-8105
  • 12 Dai Y, Roman M, Naviaux RK, Verma IM. Gene therapy via primary myoblasts: long-term expression of factor IX protein following transplantation in vivo. Proc Natl Acad Sci USA 1992; 89: 10892-10895
  • 13 Miyanohara A, Johnson PA, Elam RL, Dai Y, Witztum JL, Verma IM, Friedmann T. Direct gene transfer to the liver with herpes simplex virus type 1 vectors: transient production of physiologically relevant levels of circulating factor IX. New Biol 1992; 4: 238-246
  • 14 Roman M, Axelrod JH, Dai Y, Naviaux RK, Friedmann T, Verma I. Circulating human or canine factor IX from retrovirally transduced primary myoblasts and established myoblast cell lines grafted into murine skeletal muscle. Som Cell Mol Genet 1992; 18: 247-258
  • 15 Yao SN, Kurachi K. Expression of human factor IX in mice after injection of genetically modified fibroblasts. Proc Natl Acad Sci USA 1992; 89: 3357-3361
  • 16 Gerrard AJ, Hudson DL, Brownlee GG, Watt FM. Towards gene therapy for haemophilia B using primary human keratinocytes. Nat Genet 1993; 3: 180-183
  • 17 Cristiano RJ, Smith LC, Kay MA, Brinkley BR, Woo SLC. Hepatic gene therapy: efficient gene delivery and expression in primary hepatocytes utilizing a conjugated adenovirus-DNA complex. Proc Natl Acad Sci USA 1993; 90: 11548-11552
  • 18 Kay MA, Rothenberg S, Landen C, Bellinger D, Leland F, Toman C, Finegold M, Thompson AR, Read MS, Brinkhous KM, Woo SLC. In vivo gene therapy of hemophilia B: sustained partial correction in factor IX deficient dogs. Science 1993; 262: 117-119
  • 19 Matsushita T, Emi N, Takahashi I, Takamatsu J, Saito H. Construction and its expression of a new retroviral vector containing a human blood coagulation factor IX cDNA. Thrombosis Res 1993; 69: 387-393
  • 20 Smith TAG, Mahaffey MG, Kayda DB, Saunder JM, Yei S, Trapnell BC, McClelland A, Kaleko M. Adenovirus mediated expression of therapeutic plasma levels of human factor IX in mice. Nature Genet 1993; 5: 397-402
  • 21 Kay MA, Landen CN, Rothenberg SR, Taylor lA, Leland F, Wiehle S, Fang B, Bellinger D, Finegold M, Thompson AR, Read M, Brinkhous KM, Woo SLC. In vivo hepatic gene therapy: complete albeit transient correction of factor IX deficiency in hemophilia B dogs. Proc Natl Acad Sci USA 1994; 91: 2353-2357
  • 22 Lozier JN, Brinkhous KM. Gene therapy and the hemophilias. JAMA 1994; 271: 47-51
  • 23 Lozier JN, Thompson AR, Hu PC, Read M, Brinkhous KM, High KA, Curiel DT. Efficient transfection of primary cells in a canine hemophilia B model using adenovirus-DNA complexes. Hum Gene Ther 1994; 5: 313-322
  • 24 Yao SN, Smith KJ, Kurachi K. Primary myoblast-mediated gene transfer: persistent expression of human factor IX in mice. Gene Ther 1994; 1: 099-107
  • 25 Baru M, Axelrod JH, Nur I. Liposome-encapsulated DNA-mediated gene transfer and synthesis of human factor IX in mice. Gene 1995; 161: 143-150
  • 26 Dai Y, Schwarz EM, Gu D, Zhang WW, Sarvetnick N, Verma IM. 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 1995; 92: 1401-1405
  • 27 Fang B, Eisensmith RC, Wang H, Kay MA, Cross RE, Landen CN, Gordon G, Bellinger DA, Read MS, Hu PC, Brinkhous KM, Woo SLC. Gene therapy for hemophilia B: host immunosuppression prolongs the therapeutic effect of adenovi rus-mediated factor IX expression. Hum Gene Ther 1995; 6: 1039-1044
  • 28 Fang B, Wang H, Gordon G, Bellinger DA, Read MS, Brinkhous KM, Woo SLC, Eisensmith RC. Lack of persistence of El-recombinant adenoviral vectors containing a temperature-sensitive E2A mutation in immunocompetent mice and dogs. Gene Ther 1995; 3: 217-222
  • 29 Hao QL, Malik P, Salazar R, Tang H, Gordon EM, Kohn DB. Expression of biologically active human factor IX in human hematopoietic cells after retroviral vector-mediated gene transduction. Hum Gene Ther 1995; 6: 873-880
  • 30 Poon MC, Aledort LM, Anderle K, Kunschak M, Morfini M. Comparison of the recovery and half-life of a high-purity factor IX concentrate with those of a factor IX complex concentrate. Factor IX Study Group. Transfusion 1995; 35: 319-323
  • 31 Evans JP, Brinkhous KM, Brayer GD, Reisner HM, High KA. Canine hemophilia B resulting from a point mutation with unusual consequences. Proc Natl Acad Sci USA 1989; 86: 10095-10099
  • 32 Choo KH, Gould KG, Rees DJ, Brownlee GG. Molecular cloning of the gene for human anti-haemophilic factor IX. Nature 1982; 299: 178-180
  • 33 Kurachi K, Davie EW. Isolation and characterization of a cDN A coding for human factor IX. Proc Natl Acad Sci USA 1982; 79: 6461-6464
  • 34 Evans JP, Watzke HH, Ware JL, Stafford DW, High KA. Molecular cloning of a cDNA encoding canine factor IX. Blood 1989; 74: 207-212
  • 35 Katsumi A, Emi N, Abe A, Hasegawa Y, Ito M, Saito H. Humoral and cellular immunity to an encoded protein induced by direct DNA injection. Hum Gene Ther 1994; 5: 1335-1339
  • 36 Brinkhous KM, Davis PD, Graham JB, Dodds WJ. Expression and linkage of genes for X-linked hemophilias A and B in the dog. Blood 1973; 41: 577-585
  • 37 Kay MA, Li Q, Liu TJ, Leland F, Toman C, Finegold M, Woo SLC. Hepatic gene therapy: persistent expression of human alpha-1-antitrypsin in mice after direct gene delivery in vivo. Human Gene Ther 1992; 3: 641-647
  • 38 Lieber A, Peeters MJ, Gown A, Perkins J, Kay MA. A modified urokinase plasminogen activator induces liver regeneration without bleeding. Hum Gene Ther 1995; 6: 1029-1037
  • 39 Bowles N, Eisensmith RC, Mohuiddin R, Pyron M, Woo SLC. A simple and efficient method for the concentration and purification of recombinant retrovirus for increased transduction in vivo. Hum Gene Ther 1996; 7: 1735-1742
  • 40 Bosch A, McCray PB, Chang SMW, Ulich TR, Simonet WS, Jolly DJ, Davidson BL. Proliferation induced by keratinocyte growth factor enhances in vivo retroviral-medi-ated gene transfer to mouse hepatocytes. J Clin Invest 1996; 98: 2683-2687
  • 41 Weinberg JB, Matthews TJ, Cullen BR, Malim MH. Productive human immunodeficiency virus type 1 (HIV-1) infection of nonproliferating human monocytes. J Exp Med 1991; 174: 1477-1482
  • 42 Lewis P, Hensel M, Emerman M. Human immunodeficiency virus infection of cells arrested in the cell cycle. EMBO J 1992; 11: 3053-3058
  • 43 Naldini L, Blömer U, Gallay P, Ory D, Mulligan R, Gage FH, Verma IM, Trono D. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 1996; 272: 263-267
  • 44 Naldini L, Blömer U, Gage FH, Trono D, Verma IM. 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 Science 1996; 93: 11382-11388
  • 45 Corbeau P, Kraus G, Wong-Stall F. Efficient gene transfer by a human immunodeficiency virus type 1 (HTV-l)-derived vector utilizing a stable HIV packaging cell line. Proc Natl Acad Sci USA 1996; 93: 14070-14075
  • 46 Brinkhous KM, Langdell RD, Penick GD, Graham JB, Wagner RH. Newer approaches to study hemophilia and hemophiloid states. J Amer Med Assoc 1954; 154: 481-486
  • 47 Stratford-Perricaudet LD, Levrero M, Chasse JF, Peiricaudet M, Briand P. Evaluation of the transfer and expression in mice of an enzyme-encoding gene using a human adenovirus vector. Human Gene Ther 1990; 1: 241-256
  • 48 Li Q, Kay MA, Finegold M, Stratford-Perricaudet LD, Woo SLC. Assessment of recombinant adenoviral vectors for hepatic gene therapy. Hum Gene Ther 1993; 4: 403-409
  • 49 Fang B, Eisensmith RC, Li XHC, Finegold MJ, Shedlovsky A, Dove W, Woo SLC. Gene therapy for phenylketonuria: phenotypic correction in a genetically deficient mouse model by adenovirus-mediated hepatic gene transfer. Gene Therapy 1994; 1: 247-254
  • 50 Kay MA, Graham F, Leland F, Woo SLC. Therapeutic serum concentrations of human alpha-1-antitrypsin after adenoviral-mediated gene transfer into mouse hepatocytes. Hepatology 1995; 21: 815-819
  • 51 Barr D, Tubb T, Ferguson D, Scaria A, Lieber A, Wilson C, Perkins J, Kay MA. Strain-related variations in adenovirally mediated transgene expression from mouse hepatocytes in vivo: comparisons between immunocompetent and immunodeficient inbred strains. Gene Ther 1995; 2: 151-155
  • 52 Li J, Fang B, Eisensmith RC, Li XHC, Nasonkin I, Lin-Li RC, Mims M, Hughes A, Montgomery C, Roberts J, Parker T, Levine D, Woo SLC. In vivo gene therapy for hyper-lipidemia: phenotypic correction in Watanabe rabbits by hepatic delivery of the LDL receptor gene. J Clin Invest 1995; 95: 768-773
  • 53 Yang Y, Ertl HCJ, Wilson JM. MHC class I-restricted cytotoxic T lymphocytes to viral antigens destroy hepatocytes in mice infected with El-deleted recombinant adenoviruses. Immunity 1994; 1: 433-442
  • 54 Yang Y, Nunes FA, Berencsi K, Furth EE, Gönczöl E, Wilson JM. Cellular immunity to viral antigens limits El-deleted adenoviruses for gene therapy. Proc Natl Acad Sci USA 1994; 91: 4407-4411
  • 55 Yang Y, Nunes FA, Berencsi K, Gönczöl E, Englehardt JF, Wilson JM. Inactivation of E2a in recombinant adenoviruses improves the prospect for gene therapy in cystic fibrosis. Nature Genet 1994; 7: 362-369
  • 56 Englehardt JF, Litzky L, Wilson JM. Prolonged transgene expression in Cotton rat lung with recombinant adenoviruses defective in E2a. Human Gene Ther 1994; 5: 1217-1229
  • 57 Englehardt JF, Ye X, Doranz B, Wilson JM. Ablation of E2A in recombinant adenoviruses improves transgene persistence and decreases inflammatory response in mouse liver. Proc Natl Acad Sci USA 1994; 91: 6196-6200
  • 58 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. Nature Med 1995; 1: 890-893
  • 59 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 1996; 3: 412-420
  • 60 Kolls JK, Lei D, Odom G, Nelson S, Summer WR, Gerber MA, Shellito JE. Use of CD4 lymphocyte depletion to prolong transgene expression of El-deleted adenoviral vectors. Human Gene Ther 1996; 7: 489-497
  • 61 Kay MA, Holterman AX, Meuse L, Gown A, Ochs H, Linsley P, Wilson C. Long-term hepatic adenovirus-mediated gene expression in mice following CTLA4Ig administration. Nat Genet 1995; 11: 191-197
  • 62 Kuzmin AI, Finegold MJ, Eisensmith RC. Liposome-mediated macrophage depletion increases the safety, efficacy and persistence of adenovirus-mediated gene transfer in vivo. Gene Ther. 1997. in press
  • 63 Hersh J, Crystal RG, Bewing B. Modulation of gene expression after replication-deficient, recombinant adenovirus-mediated gene transfer by the product of a second adenovirus vector. Gene Therapy 1995; 2: 124-131
  • 64 Lochmuller H, Petrof BJ, Pari G, Larochelle N, Dodelet V, Wang Q, Allen C, Prescott S, Massie B, Nalbantoglu J, Karpati G. Transient immunosuppression by FK506 permits a sustained high-level dystrophin expression after adenovirus-mediated dystrophin minigene transfer to skeletal muscles of adult dystrophic (mdx) mice. Gene Ther 1996; 3: 706-716
  • 65 Armentano D, Sookdeo CC, Hehir KM, Gregory RJ, St GeorgeJA, Prince GA, Wadsworth SC, Smith AE. Characterization of an adenovirus gene transfer vector containing an E4 deletion. Human Gene Ther 1995; 6: 1343-1353
  • 66 Krougliak V, Graham FL. Development of cell lines capable of complementing El,E4 and protein IX defective adenovirus type 5 mutants. Human Gene Ther 1995; 6: 1575-1586
  • 67 Lee MG, Haddada H, Perricaudet M. Reducing the immune response against adenoviral vectors. J Cell Biochem 1995; suppl 21A 359
  • 68 Wang Q, Jia XC, Finer MH. A packaging cell line for propagation of recombinant adenovirus vectors containing two lethal gene-region deletions. Gene Ther 1995; 2: 775-783
  • 69 Gao GP, Yang Y, Wilson JM. Biology of adenovirus vectors with El and E4 deletions for liver-directed gene therapy. J Virol 1996; 70: 8934-8943
  • 70 Gorziglia MI, Kadan MJ, Yei S, Lim J, Lee GM, Luthra R, Trapnell BC. Elimination of both El and E2 from adenovirus vectors further improves prospects for in vivo human gene therapy. J Virol 1996; 70: 4173-4178
  • 71 Yeh P, Dedieu JF, Orsini C, Vigne E, Denefle P, Perricaudet M. Efficient dual transcomplementation of adenovirus El and E4 regions from a 293-derived cell line expressing a minimal E4 functional unit. J Virol 1996; 70: 559-565
  • 72 Zhou H, O’Neal W, Morral N, Beaud AL. et al Development of a complementing cell line and a system for construction of adenovirus vectors with El and E2a deleted. J Virol 1996; 70: 7030-7038
  • 73 Mitani K, Graham FL, Caskey CT, Kochanek S. Rescue, propagation, and partial purification of a helper virus-dependent adenovirus vector. Proc Natl Acad Sci USA 1995; 92: 3854-3858
  • 74 Fisher KJ, Choi H, Burda J, Chen S-J, Wilson JM. Recombinant adenovirus deleted of all viral genes for gene therapy of cystic fibrosis. Virol 1996; 217: 11-22
  • 75 Kochanek S, Clemens PR, Mitani K, Chen HH, Chan S, Caskey CT. A new adenoviral vector: replacement of all viral coding sequences with 28 kb of DNA independently expressing both full-length dystrophin and beta-galactosidase. Proc Natl Acad Sci USA 1996; 93: 5731-5736
  • 76 Lieber A, He CY, Kirillova I, Kay MA. 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 1996; 70: 8944-8960
  • 77 Kaplitt MG, Leone P, Samulski RJ, Xiao X, Pfaff DW, O’Malley KL, During MJ. Long-term expression and phenotypic correction using adeno-associated virus vectors in the mammalian brain. Nat Genet 1994; 8: 148-154
  • 78 Xiao X, Li J, Samulski RJ. Efficient long-term gene transfer into muscle tissue of immunocompetent mice by adeno-associated virus vector. J Virol 1996; 70: 8098-8108
  • 79 Ferrari FK, Samulski T, Shenk T, Samulski RJ. Second-strand synthesis is a rate-limiting step for efficient transduction by recombinant adeno-associated virus vectors. J Virol 1996; 70: 3227-3234
  • 80 Fisher KJ, Gao GP, Weitzman MD, DeMatteo R, Burda JF, Wilson JM. Transduction with recombinant adeno-associated virus for gene therapy is limited by leading-strand synthesis. J Virol 1996; 70: 520-532
  • 81 Alexander IE, Russell DW, Miller AD. DNA-damaging agents greatly increase the transduction of nondividing cells by adeno-associated virus vectors. J Virol 1994; 68: 8282-8287