Nonviral gene delivery with the sleeping beauty transposon system

Human Gene Therapy

Volumn 22, Issue 9, 2011, Pages 1043-1051

  Ivics, Zoltán ^a,b,c   Izsvák, Zsuzsanna ^a,b  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b UNIVERSITY OF DEBRECEN   (Hungary)

^c PAUL EHRLICH INSTITUT   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ASIALOOROSOMUCOID; BLOOD CLOTTING FACTOR 9; ENDOTHELIAL NITRIC OXIDE SYNTHASE; FUMARYLACETOACETASE; GENE PRODUCT; INDOLEAMINE 2,3 DIOXYGENASE; POLYETHYLENEIMINE; SHORT HAIRPIN RNA; TRANSPOSASE; ZINC FINGER PROTEIN;

ANTIANGIOGENIC GENE THERAPY; B CELL LYMPHOMA; DNA TRANSPOSITION; EX VIVO GENE TRANSFER; GENE EXPRESSION; GENE INSERTION; GENE TARGETING; GENE THERAPY; GENE VECTOR; GENETIC MANIPULATION; GLIOBLASTOMA; HEMATOLOGIC DISEASE; HEMATOPOIETIC STEM CELL; HEMOPHILIA B; HUMAN; HYDRODYNAMICS BASED TRANSFECTION; IN VIVO GENE TRANSFER; LUNG GRAFT REJECTION; LUNG TRANSPLANTATION; MESENCHYMAL STEM CELL; MYOBLAST; NEOPLASM; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; PLURIPOTENT STEM CELL; PULMONARY HYPERTENSION; REVIEW; SLEEPING BEAUTY TRANSPOSON SYSTEM; TRANSGENE; TRANSPOSON; TYROSINEMIA;

ANIMALS; DNA TRANSPOSABLE ELEMENTS; GENE EXPRESSION REGULATION; GENE THERAPY; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; HUMANS; STEM CELLS; TRANSGENES;

EID: 80052996913     PISSN: 10430342     EISSN: 15577422     Source Type: Journal    
DOI: 10.1089/hum.2011.143     Document Type: Review

References (88)

1. Aronovich, E.L., Bell, J.B., Belur, L.R., et al. (2007). Prolonged expression of a lysosomal enzyme in mouse liver after Sleeping Beauty transposon-mediated gene delivery: implications for non-viral gene therapy of mucopolysaccharidoses. J. Gene Med. 9, 403-415. (Pubitemid 46796586)
2. Aronovich, E.L., Bell, J.B., Khan, S.A., et al. (2009). Systemic correction of storage disease in MPS I NOD/SCID mice using the Sleeping Beauty transposon system. Mol. Ther. 17, 1136-1144.
3. Baum, C., Von Kalle, C., Staal, F.J., et al. (2004). Chance or necessity? Insertional mutagenesis in gene therapy and its consequences. Mol. Ther. 9, 5-13. (Pubitemid 38208322)
4. Belay, E., Matrai, J., Acosta-Sanchez, A., et al. (2010). Novel hyperactive transposons for genetic modification of induced pluripotent and adult stem cells: A nonviral paradigm for coaxed differentiation. Stem Cells 28, 1760-1771.
5. Bell, J.B., Podetz-Pedersen, K.M., Aronovich, E.L., et al. (2007). Preferential delivery of the Sleeping Beauty transposon system to livers of mice by hydrodynamic injection. Nat. Protoc. 2, 3153-3165.
6. Belur, L.R., Frandsen, J.L., Dupuy, A.J., et al. (2003). Gene insertion and long-term expression in lung mediated by the Sleeping Beauty transposon system. Mol. Ther. 8, 501-507. (Pubitemid 37161472)
7. Belur, L.R., Podetz-Pedersen, K., Frandsen, J., and McIvor, R.S. (2007). Lung-directed gene therapy in mice using the nonviral Sleeping Beauty transposon system. Nat. Protoc. 2, 3146-3152.
8. Bonini, C., Grez, M., Traversari, C., et al. (2003). Safety of ret-roviral gene marking with a truncated NGF receptor. Nat. Med. 9, 367-369. (Pubitemid 36460048)
9. Bowers, W.J., Mastrangelo, M.A., Howard, D.F., et al. (2006). Neuronal precursor-restricted transduction via in utero CNS gene delivery of a novel bipartite HSV amplicon/transposase hybrid vector. Mol. Ther. 13, 580-588. (Pubitemid 43257626)
10. Bushman, F.D. (2003). Targeting survival: integration site selection by retroviruses and LTR-retrotransposons. Cell 115, 135-138. (Pubitemid 37329577)
11. Chen, Z.J., Kren, B.T., Wong, P.Y., et al. (2005). Sleeping Beauty-mediated down-regulation of huntingtin expression by RNA interference. Biochem. Biophys. Res. Commun. 329, 646-652. (Pubitemid 40311792)
12. de Silva, S., Mastrangelo, M.A., Lotta, L.T., Jr., et al. (2010). Herpes simplex virus/Sleeping Beauty vector-based embryonic gene transfer using the HSB5 mutant: Loss of apparent transposition hyperactivity in vivo. Hum. Gene Ther. 21, 1603-1613.
13. Ellis, J. (2005). Silencing and variegation of gammaretrovirus and lentivirus vectors. Hum. Gene Ther. 16, 1241-1246. (Pubitemid 41611651)
14. Essner, J.J., McIvor, R.S., and Hackett, P.B. (2005). Awakening gene therapy with Sleeping Beauty transposons. Curr. Opin. Pharmacol. 5, 513-519. (Pubitemid 41258570)
15. Fernando, S., and Fletcher, B.S. (2006). Sleeping Beauty transposon-mediated nonviral gene therapy. BioDrugs 20, 219-229. (Pubitemid 44050430)
16. Galla, M., Schambach, A., Falk, C.S., et al. (2011). Avoiding cy-totoxicity of transposases by dose-controlled mRNA delivery. Nucleic Acids Res. 39, 7147-7160.
17. Garrison, B.S., Yant, S.R., Mikkelsen, J.G., and Kay, M.A. (2007). Postintegrative gene silencing within the Sleeping Beauty transposition system. Mol. Cell. Biol. 27, 8824-8833.
18. Geurts, A.M., Hackett, C.S., Bell, J.B., et al. (2006). Structure-based prediction of insertion-site preferences of transposons into chromosomes. Nucleic Acids Res. 34, 2803-2811. (Pubitemid 43985641)
19. Grabundzija, I., Irgang, M., Mates, L., et al. (2010). Comparative analysis of transposable element vector systems in human cells. Mol. Ther. 18, 1200-1209.
20. Hacein-Bey-Abina, S., Von Kalle, C., Schmidt, M., et al. (2003). LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1. Science 302, 415-419. (Pubitemid 37296260)
21. Hacein-Bey-Abina, S., Garrigue, A., Wang, G.P., et al. (2008). Insertional oncogenesis in 4 patients after retrovirus-mediated gene therapy of SCID-X1. J. Clin. Invest. 118, 3132-3142.
22. Hackett, P.B., Ekker, S.C., Largaespada, D.A., and McIvor, R.S. (2005). Sleeping Beauty transposon-mediated gene therapy for prolonged expression. Adv. Genet. 54, 189-232. (Pubitemid 43591151)
23. Hackett, P.B., Largaespada, D.A., and Cooper, L.J. (2010). A transposon and transposase system for human application. Mol. Ther. 18, 674-683.
24. Hagedorn, C., Wong, S.P., Harbottle, R., and Lipps, H.J. (2011). Scaffold/matrix attached region-based nonviral episomal vectors. Hum. Gene Ther. 22, 915-923.
25. Hartman, Z.C., Appledorn, D.M., and Amalfitano, A. (2008). Adenovirus vector induced innate immune responses: impact upon efficacy and toxicity in gene therapy and vaccine applications. Virus Res. 132, 1-14. (Pubitemid 351232078)
26. Hausl, M.A., Zhang, W., Muther, N., et al. (2010). Hyperactive Sleeping Beauty transposase enables persistent phenotypic correction in mice and a canine model for hemophilia B. Mol. Ther. 18, 1896-1906.
27. He, C.X., Shi, D., Wu, W.J., et al. (2004). Insulin expression in livers of diabetic mice mediated by hydrodynamics-based administration. World J. Gastroenterol. 10, 567-572. (Pubitemid 38325316)
28. + hematopoietic cells using the Sleeping Beauty transposon. Exp. Hematol. 34, 1333-1343. (Pubitemid 44374844)
29. + lymphoid malignancies. Mol. Ther. 16, 580-589. (Pubitemid 351314999)
30. Huang, X., Wilber, A., McIvor, R.S., and Zhou, X. (2009). DNA transposons for modification of human primary T lymphocytes. Methods Mol. Biol. 506, 115-126.
31. Ivics, Z., and Izsvak, Z. (2006). Transposons for gene therapy! Curr. Gene Ther. 6, 593-607.
32. Ivics, Z., Hackett, P.B., Plasterk, R.H., and Izsvak, Z. (1997). Molecular reconstruction of Sleeping Beauty, a Tc1-like trans-poson from fish, and its transposition in human cells. Cell 91, 501-510. (Pubitemid 27508239)
33. Ivics, Z., Katzer, A., Stuwe, E.E., et al. (2007). Targeted Sleeping Beauty transposition in human cells. Mol. Ther. 15, 1137-1144. (Pubitemid 46813616)
34. Ivics, Z., Li, M.A., Mates, L., et al. (2009). Transposon-mediated genome manipulation in vertebrates. Nat. Methods 6, 415-422.
35. Izsvák, Z., and Ivics, Z. (2004). Sleeping Beauty transposition: Biology and applications for molecular therapy. Mol. Ther. 9, 147-156. (Pubitemid 38256540)
36. Izsvák, Z., Khare, D., Behlke, J., et al. (2002). Involvement of a bifunctional, paired-like DNA-binding domain and a transpositional enhancer in Sleeping Beauty transposition. J. Biol. Chem. 277, 34581-34588.
37. Izsvák, Z., Chuah, M.K., VandenDriessche, T., and Ivics, Z. (2009). Efficient stable gene transfer into human cells by the Sleeping Beauty transposon vectors. Methods 49, 287-297.
38. Izsvák, Z., Hackett, P.B., Cooper, L.J., and Ivics, Z. (2010). Translating Sleeping Beauty transposition into cellular therapies: Victories and challenges. Bioessays 32, 756-767.
39. Jahner, D., Stuhlmann, H., Stewart, C.L., et al. (1982). De novo methylation and expression of retroviral genomes during mouse embryogenesis. Nature 298, 623-628. (Pubitemid 12099716)
40. Jin, Z., Maiti, S., Huls, H., et al. (2011). The hyperactive Sleeping Beauty transposase SB100X improves the genetic modification of T cells to express a chimeric antigen receptor. Gene Ther. [Epub ahead of print]
41. Kaufman, C.D., Izsvak, Z., Katzer, A., and Ivics, Z. (2005). Frog Prince transposon-based RNAi vectors mediate efficient gene knockdown in human cells. J. RNAi Gene Silenc. 1, 97-104.
42. Kren, B.T., Unger, G.M., Sjeklocha, L., et al. (2009). Nanocapsule-delivered Sleeping Beauty mediates therapeutic factor VIII expression in liver sinusoidal endothelial cells of hemophilia A mice. J. Clin. Invest. 119, 2086-2099.
43. Liu, F., Song, Y., and Liu, D. (1999). Hydrodynamics-based transfection in animals by systemic administration of plasmid DNA. Gene Ther. 6, 1258-1266. (Pubitemid 29359019)
44. Liu, G., Geurts, A.M., Yae, K., et al. (2005). Target-site preferences of Sleeping Beauty transposons. J. Mol. Biol. 346, 161-173. (Pubitemid 40128313)
45. Liu, H., Liu, L., Fletcher, B.S., and Visner, G.A. (2006). Sleeping Beauty-based gene therapy with indoleamine 2,3-dioxygenase inhibits lung allograft fibrosis. FASEB J. 20, 2384-2386.
46. Liu, L., Sanz, S., Heggestad, A.D., et al. (2004). Endothelial targeting of the Sleeping Beauty transposon within lung. Mol. Ther. 10, 97-105. (Pubitemid 38885655)
47. Liu, L., Liu, H., Visner, G., and Fletcher, B.S. (2006a). Sleeping Beauty-mediated eNOS gene therapy attenuates monocrota-line-induced pulmonary hypertension in rats. FASEB J. 20, 2594-2596.
48. Liu, L., Mah, C., and Fletcher, B.S. (2006b). Sustained FVIII expression and phenotypic correction of hemophilia A in neonatal mice using an endothelial-targeted Sleeping Beauty transposon. Mol. Ther. 13, 1006-1015.
49. Mates, L., Chuah, M.K., Belay, E., et al. (2009). Molecular evolution of a novel hyperactive Sleeping Beauty transposase enables robust stable gene transfer in vertebrates. Nat. Genet. 41, 753-761.
50. Modlich, U., Navarro, S., Zychlinski, D., et al. (2009). Insertional transformation of hematopoietic cells by self-inactivating lentiviral and gammaretroviral vectors. Mol. Ther. 17, 1919-1928.
51. Moldt, B., Yant, S.R., Andersen, P.R., et al. (2007). Cis-acting gene regulatory activities in the terminal regions of Sleeping Beauty DNA transposon-based vectors. Hum. Gene Ther. 18, 1193-1204. (Pubitemid 350261968)
52. Moldt, B., Miskey, C., Staunstrup, N.H., et al. (2011). Comparative genomic integration profiling of Sleeping Beauty transpo-sons mobilized with high efficacy from integrase-defective lentiviral vectors in primary human cells. Mol. Ther. 19, 1499-1510.
53. Montini, E., Held, P.K., Noll, M., et al. (2002). In vivo correction of murine tyrosinemia type I by DNA-mediated transposition. Mol. Ther. 6, 759-769. (Pubitemid 36054309)
54. Ohlfest, J.R., Demorest, Z.L., Motooka, Y., et al. (2005a). Combinatorial antiangiogenic gene therapy by nonviral gene transfer using the Sleeping Beauty transposon causes tumor regression and improves survival in mice bearing intracranial human glioblastoma. Mol. Ther. 12, 778-788. (Pubitemid 41614473)
55. Ohlfest, J.R., Frandsen, J.L., Fritz, S., et al. (2005b). Phenotypic correction and long-term expression of factor VIII in hemo-philic mice by immunotolerization and nonviral gene transfer using the Sleeping Beauty transposon system. Blood 105, 2691-2698. (Pubitemid 40446258)
56. Orban, T.I., Apati, A., Nemeth, A., et al. (2009). Applying a "double-feature" promoter to identify cardiomyocytes differentiated from human embryonic stem cells following transposon-based gene delivery. Stem Cells 27, 1077-1087.
57. Ortiz-Urda, S., Thyagarajan, B., Keene, D.R., et al. (2002). Stable nonviral genetic correction of inherited human skin disease. Nat. Med. 8, 1166-1170. (Pubitemid 35175973)
58. Peng, P.D., Cohen, C.J., Yang, S., et al. (2009). Efficient nonviral Sleeping Beauty transposon-based TCR gene transfer to peripheral blood lymphocytes confers antigen-specific antitumor reactivity. Gene Ther. 16, 1042-1049.
59. Schambach, A., Mueller, D., Galla, M., et al. (2006). Overcoming promoter competition in packaging cells improves production of self-inactivating retroviral vectors. Gene Ther. 13, 1524-1533. (Pubitemid 44567149)
60. Schambach, A., Galla, M., Maetzig, T., et al. (2007). Improving transcriptional termination of self-inactivating gamma-retroviral and lentiviral vectors. Mol. Ther. 15, 1167-1173. (Pubitemid 46813620)
61. Schroder, A.R., Shinn, P., Chen, H., et al. (2002). HIV-1 integration in the human genome favors active genes and local hot-spots. Cell 110, 521-529. (Pubitemid 35232295)
62. Singh, H., Manuri, P.R., Olivares, S., et al. (2008). Redirecting specificity of T-cell populations for CD19 using the Sleeping Beauty system. Cancer Res. 68, 2961-2971. (Pubitemid 351556297)
63. Staunstrup, N.H., Moldt, B., Mates, L., et al. (2009). Hybrid lentivirus-transposon vectors with a random integration profile in human cells. Mol. Ther. 17, 1205-1214.
64. Suda, T., Suda, K., and Liu, D. (2008). Computer-assisted hy-drodynamic gene delivery. Mol. Ther. 16, 1098-1104.
65. + hematopoi-etic stem/progenitor cells, using the Sleeping Beauty transpo-son system. Hum. Gene Ther. 20, 1607-1626.
66. Tamhane, M., and Akkina, R. (2008). Stable gene transfer of CCR5 and CXCR4 siRNAs by Sleeping Beauty transposon system to confer HIV-1 resistance. AIDS Res. Ther. 5, 16.
67. Thrasher, A.J., Gaspar, H.B., Baum, C., et al. (2006). Gene therapy: X-SCID transgene leukaemogenicity. Nature 443, E5-E6; discussion E6-E7. (Pubitemid 44435140)
68. VandenDriessche, T., Ivics, Z., Izsvak, Z., and Chuah, M.K. (2009). Emerging potential of transposons for gene therapy and generation of induced pluripotent stem cells. Blood 114, 1461-1468.
69. Vigdal, T.J., Kaufman, C.D., Izsvak, Z., et al. (2002). Common physical properties of DNA affecting target site selection of Sleeping Beauty and other Tc1/mariner transposable elements. J. Mol. Biol. 323, 441-452. (Pubitemid 35283672)
70. Vink, C.A., Gaspar, H.B., Gabriel, R., et al. (2009). Sleeping Beauty transposition from nonintegrating lentivirus. Mol. Ther. 17, 1197-1204.
71. Voigt, K., Izsvak, Z., and Ivics, Z. (2008). Targeted gene insertion for molecular medicine. J. Mol. Med. 86, 1205-1219.
72. Walisko, O., Schorn, A., Rolfs, F., et al. (2008). Transcriptional activities of the Sleeping Beauty transposon and shielding its genetic cargo with insulators. Mol. Ther. 16, 359-369. (Pubitemid 351168045)
73. Wang, X., Sarkar, D.P., Mani, P., et al. (2009). Long-term reduction of jaundice in Gunn rats by nonviral liver-targeted delivery of Sleeping Beauty transposon. Hepatology 50, 815-824.
74. Wilber, A., Frandsen, J.L., Geurts, J.L., et al. (2006). RNA as a source of transposase for Sleeping Beauty-mediated gene insertion and expression in somatic cells and tissues. Mol. Ther. 13, 625-630. (Pubitemid 43257631)
75. Wilber, A., Linehan, J.L., Tian, X., et al. (2007). Efficient and stable transgene expression in human embryonic stem cells using transposon-mediated gene transfer. Stem Cells 25, 2919-2927. (Pubitemid 350127877)
76. Williams, D.A. (2008). Sleeping Beauty vector system moves toward human trials in the United States. Mol. Ther. 16, 1515-1516.
77. Wolf, D., and Goff, S.P. (2009). Embryonic stem cells use ZFP809 to silence retroviral DNAs. Nature 458, 1201-1204.
78. Wu, A., Oh, S., Ericson, K., et al. (2007). Transposon-based in-terferon c gene transfer overcomes limitations of episomal plasmid for immunogene therapy of glioblastoma. Cancer Gene Ther. 14, 550-560. (Pubitemid 46788330)
79. 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. (Pubitemid 36712571)
80. + hema-topoietic stem and progenitor cells by a hyperactive Sleeping Beauty transposon system. Blood 114, 1319-1330.
81. Yamanaka, S. (2009). A fresh look at iPS cells. Cell 137, 13-17.
82. Yant, S.R., Meuse, L., Chiu, W., et al. (2000). Somatic integration and long-term transgene expression in normal and haemo-philic mice using a DNA transposon system. Nat. Genet. 25, 35-41. (Pubitemid 30257033)
83. Yant, S.R., Ehrhardt, A., Mikkelsen, J.G., et al. (2002). Transposition from a gutless adeno-transposon vector stabilizes transgene expression in vivo. Nat. Biotechnol. 20, 999-1005.
84. Yant, S.R., Wu, X., Huang, Y., et al. (2005). High-resolution genome-wide mapping of transposon integration in mammals. Mol. Cell. Biol. 25, 2085-2094. (Pubitemid 40354609)
85. Yant, S.R., Huang, Y., Akache, B., and Kay, M.A. (2007). Site-directed transposon integration in human cells. Nucleic Acids Res. 35, e50.
86. Zayed, H., Izsvak, Z., Walisko, O., and Ivics, Z. (2004). Development of hyperactive Sleeping Beauty transposon vectors by mutational analysis. Mol. Ther. 9, 292-304. (Pubitemid 38256555)
87. Zhang, G., Budker, V., and Wolff, J.A. (1999). High levels of foreign gene expression in hepatocytes after tail vein injections of naked plasmid DNA. Hum. Gene Ther. 10, 1735-1737. (Pubitemid 29328217)
88. Zhu, J., Kren, B.T., Park, C.W., et al. (2007). Erythroid-specific expression of b-globin by the Sleeping Beauty transposon for sickle cell disease. Biochemistry 46, 6844-6858. (Pubitemid 46906414)