Transposon-based vector systems for gene therapy clinical Trials: Challenges and considerations

Chang Gung Medical Journal

Volumn 34, Issue 6, 2011, Pages 565-579

  Meir, Yaa Jyuhn James ^a   Wu, Sareina Chiung Yuan ^b  

^a CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^b CHANG GUNG UNIVERSITY   (Taiwan)

Author keywords

Gene therapy; Non viral gene delivery; PiggyBac transposon

Indexed keywords

ADENOVIRUS VECTOR; CHITOSAN; DENDRIMER; INTERLEUKIN 12; KRUPPEL LIKE FACTOR 4; LIPOPLEX; LIPOPROTEIN; LIPOSOME; METAL NANOPARTICLE; MYC PROTEIN; NIOSOME; OCTAMER TRANSCRIPTION FACTOR 4; PARVOVIRUS VECTOR; POLYETHYLENEIMINE; POLYLYSINE; POLYMER; QUANTUM DOT; RETROVIRUS VECTOR; SOLID LIPID NANOPARTICLE; TRANSCRIPTION FACTOR SOX2; TRANSMEMBRANE CONDUCTANCE REGULATOR; TRANSPOSASE;

CELL BASED GENE THERAPY; CYSTIC FIBROSIS; CYTOTOXICITY; DNA TRANSPOSITION; ELECTROPORATION; GENE; GENE EXPRESSION; GENE INSERTION; GENE SILENCING; GENE TARGETING; GENOMIC INSTABILITY; GENOTOXICITY; HUMAN; IMMUNOGENICITY; LIPOSOMAL GENE DELIVERY SYSTEM; MICELLE; MICROBUBBLE; MICROCAPSULE; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; NONVIRAL GENE THERAPY; PIGGYBAC GENE; PLURIPOTENT STEM CELL; REVIEW; SLEEPING BEAUTY GENE; STEM CELL TRANSPLANTATION; TOL2 GENE; TRANSGENE; TRANSPOSON; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY;

CLINICAL TRIALS AS TOPIC; DNA TRANSPOSABLE ELEMENTS; GENE THERAPY; GENETIC VECTORS; HUMANS; NERVE TISSUE PROTEINS; TRANSPOSASES;

EID: 84555218212     PISSN: 20720939     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (89)

1. Adams C, McCarthy HO, Coulter JA, Worthington J, Murphy C, Robson T, Hirst DG. Nitric oxide synthase gene therapy enhances the toxicity of cisplatin in cancer cells. J Gene Med 2009;11:160-8.
2. Conese M, Giola SD, Castellani S. Gene therapy for cystic fibrosis. Expert Opin Ther Pat 2008;18:929-43.
3. Roberts L. Human gene transfer test approved. Science 1989;243:473.
4. Edelstein ML, Abedi MR, Wixon J. Gene therapy clinical trials worldwide to 2007-an update. J Gene Med 2007;9:833-42.
5. Raper SE, Chirmule N, Lee FS, Wivel NA, Bagg A, Gao GP, Wilson JM, Batshaw ML. Fatal systemic inflammatory response syndrome in a ornithine transcarbamylase deficient patient following adenoviral gene transfer. Mol Genet Metab 2003;80:148-58.
6. Cavazzana-Calvo M, Hacein-Bey S, de Saint Basile G, Gross F, Yvon E, Nusbaum P, Selz F, Hue C, Certain S, Casanova JL, Bousso P, Deist FL, Fischer A. Gene therapy of human severe combined immunodeficiency (SCID)-X1 disease. Science 2000;288:669-72.
7. Hacein-Bey-Abina S, Von Kalle C, Schmidt M, Le Deist F, Wulffraat N, McIntyre E, Radford I, Villeval JL, Fraser CC, Cavazzana-Calvo M, Fischer A. A serious adverse event after successful gene therapy for X-linked severe combined immunodeficiency. N Engl J Med 2003;348: 255-6.
8. Hacein-Bey-Abina S, Von Kalle C, Schmidt M, McCormack MP, Wulffraat N, Leboulch Lim A, Osborne CS, Pawliuk R, Morillon E, Sorensen R, Forster A, Fraser P, Cohen JI, de Saint Basile G, Alexander I, Wintergerst U, Frebourg T, Aurias A, Stoppa-Lyonnet D, Romana S, Radford-Weiss I, Gross F, Valensi F, Delabesse E, Macintyre E, Sigaux F, Soulier J, Leiva LE, Wissler M, Prinz C, Rabbitts TH, Le Deist F, Fischer A, Cavazzana-Calvo M. LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1. Science 2003;302:415-9.
9. Gonçalves MA. Adeno-associated virus: from defective virus to effective vector. Virol J 2005;2:43.
10. Kotin RM, Siniscalco M, Samulski RJ, Zhu XD, Hunter L, Laughlin CA, McLaughlin S, Muzyczka N, Rocchi M, Berns KI. Site-specific integration by adeno-associated virus. Proc Natl Acad Sci USA 1990;87:2211-5.
11. Samulski RJ, Zhu X, Xiao X, Brook JD, Housman DE, Epstein N, Hunter LA. Targeted integration of adenoassociated virus (AAV) into human chromosome 19. EMBO J 1991;10:3941-50. erratum 11:1228.
12. Kotin RM, Menninger JC, Ward DC, Berns KI. Mapping and direct visualization of a region-specific viral DNA integration site on chromosome 19q13-qter. Genomics 1991;10:831-4.
13. Bainbridge JWB, Smith AJ, Barker SS, Robbie S, Henderson R, Ophth MRC, Kamaljit Balaggan, Viswanathan A, Holder GE, Stockman A, Tyler N, Petersen-Jones S, Bhattacharya SS, Thrasher AJ, Fitzke FW, Carter BJ, Rubin GS, Moore AT, Ali RR. Effect of gene therapy on visual function in Leber congenital amaurosis. N Engl J Med 2008;358:2231-9.
14. Maguire AM, Simonelli F, Pierce EA, Pugh EN Jr, Mingozzi F, Bennicelli J, Banfi S, Marshall KA, Testa F, Surace EM, Rossi S, Lyubarsky A, Arruda VR, Konkle B, Stone E, Sun J, Jacobs J, Dell'Osso L, Hertle R, Ma JX, Redmond TM, Zhu X, Hauck B, Zelenaia O, Shindler KS, Maguire MG, Wright JF, Volpe NJ, McDonnell JW, Auricchio A, High KA, Bennett J. Safety and efficacy of gene transfer for Leber's congenital amaurosis. N Engl J Med 2008;358:2240-8.
15. Hayes F. Transposon-based strategies for microbial functional genomics and proteomics. Annu Rev Genet 2003;37:3-29.
16. Spradling AC, Rubin GM. Transposition of cloned P elements into Drosophila germ line chromosomes. Science 1982;218:341-7.
17. Bellen HJ, O'Kane CJ, Wilson C, Grossniklaus U, Pearson RK, Gehring WJ. P-element-mediated enhancer detection: A versatile method to study development in Drosophila. Genes Dev 1989;3:1288-300.
18. Thibault ST, Singer MA, Miyazaki WY, Milash B, Dompe NA, Singh CM, Buchholz R, Demsky M, Fawcett R, Francis-Lang HL, Ryner L, Cheung LM, Chong A, Erickson C, Fisher WW, Greer K, Hartouni SR, Howie E, Jakkula L, Joo D, Killpack K, Laufer A, Mazzotta J, Smith RD, Stevens LM, Stuber C, Tan LR, Ventura R, Woo A, Zakrajsek I, Zhao L, Chen F, Swimmer C, Kopczynski C, Duyk G, Winberg ML, Margolis J. A complementary transposon tool kit for Drosophila melanogaster using P and piggyBac. Nat Genet 2004;36: 283-7.
19. Plasterk RH. The Tc1/mariner transposon family. Curr Top Microbiol Immunol 1996;204:125-43.
20. Osborne BI, Baker B. Movers and shakers: maize transposons as tools for analyzing other plant genomes. Curr Opin Cell Biol 1995;7:406-13.
21. Ivics Z, Hackett PB, Plasterk RH, Izsvák Z. Molecular reconstruction of Sleeping Beauty, a Tc1-like transposon from fish, and its transposition in human cells. Cell 1997;91:501-10.
22. Ivics Z, Meng MA, Mátés L, Boeke JD, Nagy A, Bradley A, Izsvák Z. Transposon mediated genome manipulation in vertebrates. Nat Methods 2009;6:415-22.
23. Koga A, Suzuki M, Inagaki H, Bessho Y, Hori H. Transposable element in fish. Nature 1996;383:30.
24. Kawakami K. Tol2: a versatile gene transfer vector in vertebrates. Genome Biol 2007;8 Suppl 1:S7.
25. Fraser MJ, Brusca JS, Smith GE, Summers MD. Transposon-mediated mutagenesis of a baculovirus. Virology 1985;145:356-61.
26. Ding S, Wu X, Li G, Han M, Zhuang Y, Xu T. Efficient transposition of the piggyBac (PB) transposon in mammalian cells and mice. Cell 2005;122:473-83.
27. Wu SC, Meir JY, Coates CJ, Handler SM, Pelczar P, Kaminsk J. piggyBac is a flexible and highly active transposon as compared to Sleeping Beauty, Tol2 and Mos1 in mammalian cells. Proc Natl Acad Sci USA 2006;103: 15008-13.
28. Miskey C, Izsvák Z, Plasterk RH, Ivics Z. The Frog Prince. a reconstructed transposon from Rana pipiens with high transpositional activity in vertebrate cells. Nucleic Acids Res 2003;31,6873-81.
29. VandenDriessche T, Ivics Z, Izsvák Z, Chuah MK. Emerging potential of transposons for gene therapy and generation of induced pluripotent stem cells. Blood 2009,114:1461-8.
30. Kang Y, Zhang X, Jiang W, Wu C, Chen C, Zheng Y, Gu J, Xu C. Tumor-directed gene therapy in mice using a composite nonviral gene delivery system consisting of the piggyBac transposon and polyethylenimine. BMC Cancer 2009;9:126.
31. Hackett PB, Largaespada DA, Cooper A. Transposon and transposase system for human application. Mol Ther 2010;18:674-83.
32. Nakanishi H, Higuchi Y, Kawakami S, Yamashita F, Hashida M. piggyBac transposon-mediated long-term gene expression in mice. Mol Ther 2010;18:707-14.
33. Mátés L, Chuah MKL, Belay E, Jerchow B, Manoj N, Acosta-Sanchez A, Grzela DP, Schmitt A, Becker K, Matrai J, Ma L, Samara-Kuko E, Gysemans C, Pryputniewicz D, Miskey C, Fletcher B, VandenDriessche T, Ivics Z, Izsvák Z. Molecular evolution of a novel hyperactive Sleeping Beauty transposase enables robust stable gene transfer in vertebrates. Nat Genet 2009;41: 753-61.
34. Cadiñanos J, Bradley A. Generation of an inducible and optimized piggyBac transposon system. Nucleic Acids Res 2007;35:e87.
35. Yusa K, Liqin Zhou L, Li MA, Bradley A, Craig NL. A hyperactive piggyBac transposase for mammalian applications. Proc Natl Acad Sci USA 2011;108:1531-6.
36. Zayed H, Izsvák Z, Khare D, Heinemann U, Ivics Z. The DNA-bending protein HMGB1 is a cellular cofactor of Sleeping Beauty transposition. Nucleic Acids Res 2003;31:2313-22.
37. Izsvák Z, Stüwe EE, Fiedler D, Katzer A, Jeggo PA, Ivics Z. Healing the wounds inflicted by sleeping beauty transposition by double-strand break repair in mammalian somatic cells. Mol Cell 2004;13:279-90.
38. Walisko O, Izsvák Z, Szaboó Szabó K, Kaufman CD, Herold S, Ivics Z. Sleeping Beauty transposase modulates cell-cycle progression through interaction with Miz-1. Proc Natl Acad Sci USA 2006;103:4062-7.
39. Garrison BS, Yant SR, Mikkelsen JG, Kay MA. Postintegrative gene silencing within the Sleeping Beauty transposition system. Mol Cell Biol 2007;27:8824-33.
40. Huang X, Guo H, Tammana S, Jung YC, Mellgren E, Bassi P, Cao Q, Tu ZJ, Kim YC, Ekker SC, Wu X, Wang SM, Zhou X. Gene transfer efficiency and genome-wide integration profiling of Sleeping Beauty, Tol2, and piggyBac transposns in human primary T cells. Mol Ther 2010;18:1803-13.
41. Izsvák Z, Ivics Z, Plasterk RH. Sleeping Beauty, a wide host-range transposon vector for genetic transformation in vertebrates. J Mol Biol 2000;302:93-102.
42. Balciunas D, Wangensteen KJ, Wilber A, Bell J, Geurts A, Sivasubbu S, Wang X, Hackett PB, Largaespada DA, McIvor RS, Ekker SC. Harnessing a high cargo-capacity transposon for genetic applications in vertebrates. PLoS Genet 2006;2:e169.
43. Suster ML, Sumiyama K, Kawakami K. Transposonmediated BAC transgenesis in zebrafish and mice. BMC Genomics 2009;10:477.
44. Wilson MH, Coates CJ, George AL. PiggyBac transposonmediated gene transfer in human cells. Mol Ther 2007;5:139-45.
45. Meir YJ, Weirauch MT, Chung P, Yu RK, Wu SC. Genome-wide target profiling of piggyBac and Tol2 in HEK 293: pros and cons for gene discovery and gene therapy. BMC Biotechnol 2011;11:28.
46. Grabundzija I, Irgang M, Mátés L, Belay E, Matrai J, Gogol-Döring A, Kawakami K, Chen W, Ruiz P, Chuah MK, VandenDriessche T, Ivics Z. Comparative analysis of transposable element vector systems in human cells. Mol Ther 2010;18:1200-9.
47. Galvan DL, Nakazawa Y, Kaja A, Kettlun C, Cooper LJ, Rooney CM, Wilson MH. Genome-wide mapping of PiggyBac transposon integrations in primary human T cells. J Immunother 2009;32:837-44.
48. Huang X, Guo H, Tammana S, Jung YC, Mellgren E, Bassi P, Cao Q, Tu ZJ, Kim YC, Ekker SC, Wu X, Wang SM, Zhou X. Gene transfer efficiency and genome-wide integration profiling of Sleeping Beauty, Tol2, and piggyBac transposons in human primary T Cells. Mol Ther 2010;6:1-11.
49. Yant SR, Wu X, Huang Y, Garrison B, Burgess SM, Kay MA. High-resolution genome-wide mapping of transposon integration in mammals. Mol Cell Biol 2005;25:2085-94.
50. Hong BK, Calmels B, Hanawa H, Gray J, Donahue RE, Persons DA, Nienhuis AW, Hematti P, Dunbar CE. Retroviral insertion site analysis in rhesus macaques transplanted with CD34_ hematopoietic stem cells transduced with a simian immunodeficiency virus-based lentiviral vector. Mol Ther 2004;9:S269.
51. Kang Y, Scheetz TE, Moressi CJ, Tran, DT, Xia L, Davidson BL, Casavant TL, McCray PB. In vitro and in vivo analysis of feline immunodeficiency virus-based lentiviral vector integration. Mol Ther 2004;9:S2.
52. Mitchell S, Beitzel BF, Schroder AR, Shinn P, Chen H, Berry CC, Ecker JR, Bushman FD. Retroviral DNA integration: ASLV, HIV, and MLV show distinct target site preferences. PLoS Biol 2004;2:E234.
53. Nakai H, Montini E, Fuess S, Storm TA, Grompe M, Kay MA. AAV serotype 2 vectors preferentially integrate into active genes in mice. Nat Genet 2003;34:297-302.
54. Wu X, Li Y, Crise B, Burgess SM. Transcription start region in the human genome are favored targets for MLV integration. Science 2003;300:1749-51.
55. Ruginis T, Taglia L, Matusiak D, Lee BS, Benya RV. Consequence of gastrin-releasing peptide receptor activation in a human colon cancer cell line: a proteomic approach. J Proteome Res 2006;5:1460-8.
56. Ozawa T, Itoyama T, Sadamori N, Yamada Y, Hata T, Tomonaga M, Isobe M. Rapid isolation of viral integration site reveals frequent integration of HTLV-1 into expressed loci. J Hum Genet 2004;49:154-65.
57. Reddy-Alla S, Schmitt B, Birkenfeld J, Eulenburg V, Dutertre S, Böhringer C, Götz M, Betz H, Papadopoulos T. PH-Domain-driven targeting of collybistin but not Cdc42 activation is required for synaptic gephyrin clustering. Eur J Neurosci 2010;31:1173-84.
58. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006;126:663-76.
59. Sommer CA, Sommer AG, Longmire TA, Christodoulou C, Thomas DD, Gostissa M, Alt FW, Murphy GJ, Kotton DN, Mostoslavsky G. Excision of reprogramming transgenes improves the differentiation potential of iPS cells generated with a single excisable vector. Stem Cells. 2010;28:64-74.
60. Lowry WE, Plath K. The many ways to make an iPS cell. Nat Biotechnol 2008;26:1246-8.
61. Woltjen K, Michael IP, Mohseni P, Desai R, Mileikovsky M, Hämäläinen R, Cowling R, Wang W, Liu P, Gertsenstein M, Kaji K, Sung HK, Nagy A. piggyBac transposition reprograms fibroblasts to induced pluripotent stem cells. Nature 2009;458:766-70.
62. Yusa K, Rad R, Takeda J, Bradley A. Generation of transgene-free induced pluripotent mouse stem cells by the piggyBac transposon. Nat Methods 2009;6:363-9.
63. Yant SR, Yong H, Akache B, Kay MA. Site-directed transposon integration in human cells. Nucleic Acids Res 2007;35:e50.
64. Torchilin VP. Nanoparticulates as DrugCarriers, London: Imperial College Press, 2006:1-6.
65. Brigham KL, Meyrick B, Christman B, Magnuson M, King G, Berry LC Jr. In vivo transfection of murine lungs with a functioning prokaryotic gene using a liposome vehicle. Am J Med Sci 1989;298:278-81.
66. Alton EWF, Middleton PG, Caplen NJ, Smith SN, Steel DM, Munkonge FM, Jeffery PK, Geddes DM, Hart SL, Williamson R, Fasold KI, Miller AD, Dickinson P, Stevenson BJ, McLachlan G, Dorin JR, Porteous DJ. Non-invasive liposome mediated gene delivery can correct the ion transport defect in cystic fibrosis mutant mice. Nat Genet 1993;5:135-42.
67. Alton EWFW, Geddes DM, Gill DR, Higgins CF, Hyde SC, Innes JA, Porteous DJ. Towards gene therapy for cystic fibrosis: a clinical progress report. Gene Ther 1998;5:291-2.
68. Davies JC, Duncan M Geddes DM, Alton EWFW. Prospects for gene therapy for cystic fibrosis. Mol Med Today 1998;4:292-9.
69. Xing X, Zhang S, Chang JY, Tucker SD, Chen H, Huang L, Hung MC. Safety study and characterization of E1Aliposome complex gene delivery protocol in an ovarian cancer model. Gene Ther 1998;5:1538-44.
70. Stopeck AT, Hersh EM, Akporiaye ET, Harris DT, Grogan T, Unger E, Warneke J, Schluter SF, Stahl S. Phase I study of direct gene transfer of an allogeneic histocompatibility antigen, HLA-B7, in patients with metastatic melanoma. J Clin Oncol 1997;15:341-9.
71. Templeton NS, Lasic DD, Frederik PM, Strey HH, Roberts DD, Pavlakis GN. Improved DNA-liposome complexes for increased systemic delivery and gene expression. Nat Biotechnol 1997;15:647-52.
72. Yang JP, Huang L. Overcoming the inhibitory effects of serum on lipofection by increasing the charge ratio of cationic liposome and DNA. Gene Ther 1997;4:950-60.
73. Eliyahu H, Barenholz Y, Domb AJ. Polymers for DNA delivery. Molecules 2005;10:34-64.
74. Luten J, Nostrum CF, DeSmedt SC, Hennink WE. Biodegradable polymers as non-viral carriers for plasmid DNA delivery. J Controlled Release 2008;126:97-110.
75. Lucas ML, Heller R. IL-12 gene therapy using an electrically mediated nonviral approach reduces metastatic growth of melanoma. DNA Cell Biol 2003;22:755-63.
76. Wells DJ. Gene therapy progress and prospects. Electroporation and other physical methods. Gene Therapy 2004;11:1363-9.
77. André F, Mir LM. DNA electrotransfer: its principles and an updated review of its therapeutic applications. Gene Ther 2004;1:S33-42.
78. Ayuni EL, Gazdhar A, Giraud MN, Kadner A, Gugger M, Cecchini M, Caus T, Carrel TP, Schmid RA, Tevaearai HT. In vivo electroporation mediated gene delivery to the beating heart. PLoS One 2010;5:e14467.
79. Mayer S, Grayburn PA. Myocardial contrast agents: recent advances and future directions. Prog Cardiovasc Dis 2001;44:33e44.
80. Unger EC, Hersh E, Vannan M, Matsunaga TO, McCreery T. Local drug and gene delivery through microbubbles. Prog Cardiovasc Dis 2001;44:45e54.
81. Porter TR, Iversen PL, Li S, Xie F. Interaction of diagnostic ultrasound with synthetic oligonucleotide-labeled perfluorocarbon-exposed sonicated dextrose albumin microbubbles. J Ultrasound Med 1996;15:577-84.
82. Shohet RV, Chen S, Zhou YT, Wang Z, Meidell RS, Unger RH, Grayburn PA Echocardiographic destruction of albumin microbubbles directs gene delivery to the myocardium. Circulation 2000;101:2554-6.
83. Bekeredjian R, Chen S, Frenkel PA, Grayburn PA, Shohet RV. Ultrasound-targeted microbubble destruction can repeatedly direct highly specific plasmid expression to the heart. Circulation 2003;108:1022-6.
84. Carson AR, McTiernan CF, Lavery L, Hodnick A, Grata M, Leng X, Wang J, Chen X, Modzelewski RA, Villanueva FS. Gene therapy of carcinoma using ultrasound targeted microbubble destruction. Ultrasound Med Biol 2011;37:393-402.
85. Hammerschmidt DE. Development of a gutless vector. J Lab Clin Med 1999;134:C3.
86. Yant SR, Ehrhardt A, Mikkelsen JG, Meuse L, Pham T, Kay MA. Transposition from a gutless adeno-transposon vector stabilizes transgene expression in vivo. Nat Biotechnol 2002;20:999-1005.
87. Maragathavally KJ, Kaminski JM, Coates CJ. Chimeric Mos1 and piggyBac transposases result in site-directed integration. FASEB J 2006;20:1880-2.
88. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, Devon K, Dewar K, Doyle M, FitzHugh W. Initial sequencing and analysis of the human genome. Nature 2001;409:860-921.
89. Shi X, Harrison RL, Hollister JR, Mohammed A, Fraser MJ, Jarvis DL. Construction and characterization of new piggyBac vectors for constitutive or inducible expression of heterologous gene pairs and the identification of a previously unrecognized activator sequence in piggyBac. BMC Biotechnol 2007;7:5.