Transcription activator like effector (TALE)-directed piggyBac transposition in human cells

Nucleic Acids Research

Volumn 41, Issue 19, 2013, Pages 9197-9207

  Owens, Jesse B ^a   Mauro, Damiano ^a   Stoytchev, Ilko ^a   Bhakta, Mital S ^b   Kim, Moon Soo ^b   Segal, David J ^b   Moisyadi, Stefan ^a,c  

^a UNIVERSITY OF HAWAII   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Manoa BioSciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEASE; TRANSCRIPTION ACTIVATOR LIKE EFFECTOR; TRANSCRIPTION FACTOR GAL4; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CCR5 GENE; CONTROLLED STUDY; DNA INTEGRATION; ENZYME ACTIVITY; GENE; GENE EXPRESSION; GENE INSERTION; GENE LOCATION; GENE TARGETING; HUMAN; HUMAN CELL; INTRON; PRIORITY JOURNAL; PROTEIN DNA BINDING; REPORTER GENE; ROSA26 GENE; TALC1 GENE; TRANSCRIPTION INITIATION; TRANSPOSON;

DNA TRANSPOSABLE ELEMENTS; DNA-BINDING PROTEINS; GENE TARGETING; HEK293 CELLS; HUMANS; RECEPTORS, CCR5; RECOMBINANT FUSION PROTEINS; TRANSPOSASES;

EID: 84886048819     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt677     Document Type: Article

References (61)

1. Di Matteo, M., Matrai, J., Belay, E., Firdissa, T., Vandendriessche, T. and Chuah, M.K. (2012) PiggyBac toolbox. Methods Mol. Biol., 859, 241-254.
2. Ding, S., Wu, X., Li, G., Han, M., Zhuang, Y. and Xu, T. (2005) Efficient transposition of the piggyBac (PB) transposon in mammalian cells and mice. Cell, 122, 473-483.
3. Feschotte, C. (2006) The piggyBac transposon holds promise for human gene therapy. Proc. Natl Acad. Sci. USA, 103, 14981-14982.
4. Wu, S.C., Meir, Y.J., Coates, C.J., Handler, A.M., Pelczar, P., Moisyadi, S. and Kaminski, J.M. (2006) PiggyBac is a flexible and highly active transposon as compared to sleeping beauty, Tol2, and Mos1 in mammalian cells. Proc. Natl Acad. Sci. USA, 103, 15008-15013.
5. Daniel, R. and Smith, J.A. (2008) Integration site selection by retroviral vectors: molecular mechanism and clinical consequences. Hum. Gene Ther., 19, 557-568.
6. Di Matteo, M., Belay, E., Chuah, M.K. and Vandendriessche, T. (2012) Recent developments in transposon-mediated gene therapy. Expert Opin. Biol. Ther., 12, 841-858.
7. Mitchell, R.S., Beitzel, B.F., Schroder, A.R., Shinn, P., Chen, H., Berry, C.C., Ecker, J.R. and Bushman, F.D. (2004) Retroviral DNA integration: ASLV, HIV, and MLV show distinct target site preferences. PLoS Biol., 2, E234.
8. 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.
9. Baum, C. (2007) Insertional mutagenesis in gene therapy and stem cell biology. Curr. Opin. Hematol., 14, 337-342.
10. Fan, H. and Johnson, C. (2011) Insertional oncogenesis by non-acute retroviruses: implications for gene therapy. Viruses, 3, 398-422.
11. Fehse, B. and Roeder, I. (2008) Insertional mutagenesis and clonal dominance: biological and statistical considerations. Gene Ther., 15, 143-153.
12. Romano, G., Marino, I.R., Pentimalli, F., Adamo, V. and Giordano, A. (2009) Insertional mutagenesis and development of malignancies induced by integrating gene delivery systems: implications for the design of safer gene-based interventions in patients. Drug News Perspect., 22, 185-196.
13. Li, T., Huang, S., Jiang, W.Z., Wright, D., Spalding, M.H., Weeks, D.P. and Yang, B. (2011) TAL nucleases (TALNs) : hybrid proteins composed of TAL effectors and FokI DNA-cleavage domain. Nucleic Acids Res., 39, 359-372.
14. Perez, E.E., Wang, J., Miller, J.C., Jouvenot, Y., Kim, K.A., Liu, O., Wang, N., Lee, G., Bartsevich, V.V., Lee, Y.L. et al. (2008) Establishment of HIV-1 resistance in CD4+T cells by genome editing using zinc-finger nucleases. Nat. Biotechnol., 26, 808-816.
15. Porteus, M.H. and Baltimore, D. (2003) Chimeric nucleases stimulate gene targeting in human cells. Science, 300, 763.
16. Cong, L., Ran, F.A., Cox, D., Lin, S., Barretto, R., Habib, N., Hsu, P.D., Wu, X., Jiang, W., Marraffini, L.A. et al. (2013) Multiplex genome engineering using CRISPR/Cas systems. Science, 339, 819-823.
17. Mali, P., Yang, L., Esvelt, K.M., Aach, J., Guell, M., DiCarlo, J.E., Norville, J.E. and Church, G.M. (2013) RNA-guided human genome engineering via Cas9. Science, 339, 823-826.
18. Olsen, P.A., Gelazauskaite, M., Randol, M. and Krauss, S. (2010) Analysis of illegitimate genomic integration mediated by zincfinger nucleases: implications for specificity of targeted gene correction. BMC Mol. Biol., 11, 35.
19. Pruett-Miller, S.M., Connelly, J.P., Maeder, M.L., Joung, J.K. and Porteus, M.H. (2008) Comparison of zinc finger nucleases for use in gene targeting in mammalian cells. Mol. Ther., 16, 707-717.
20. Cornu, T.I., Thibodeau-Beganny, S., Guhl, E., Alwin, S., Eichtinger, M., Joung, J.K. and Cathomen, T. (2008) DNA-binding specificity is a major determinant of the activity and toxicity of zinc-finger nucleases. Mol. Ther., 16, 352-358.
21. Bohne, J. and Cathomen, T. (2008) Genotoxicity in gene therapy: an account of vector integration and designer nucleases. Curr. Opin. Mol. Ther., 10, 214-223.
22. Cornu, T.I. and Cathomen, T. (2010) Quantification of zinc finger nuclease-associated toxicity. Methods Mol. Biol., 649, 237-245.
23. Pattanayak, V., Ramirez, C.L., Joung, J.K. and Liu, D.R. (2011) Revealing off-target cleavage specificities of zinc-finger nucleases by in vitro selection. Nat. Methods, 8, 765-770.
24. Gabriel, R., Lombardo, A., Arens, A., Miller, J.C., Genovese, P., Kaeppel, C., Nowrouzi, A., Bartholomae, C.C., Wang, J., Friedman, G. et al. (2011) An unbiased genome-wide analysis of zinc-finger nuclease specificity. Nat. Biotechnol., 29, 816-823.
25. Gupta, A., Meng, X., Zhu, L.J., Lawson, N.D. and Wolfe, S.A. (2011) Zinc finger protein-dependent and -independent contributions to the in vivo off-target activity of zinc finger nucleases. Nucleic Acids Res., 39, 381-392.
26. Radecke, S., Radecke, F., Cathomen, T. and Schwarz, K. (2010) Zinc-finger nuclease-induced gene repair with oligodeoxynucleotides: wanted and unwanted target locus modifications. Mol. Ther., 18, 743-753.
27. Mitra, R., Fain-Thornton, J. and Craig, N.L. (2008) piggyBac can bypass DNA synthesis during cut and paste transposition. EMBO J., 27, 1097-1109.
28. Owens, J.B., Urschitz, J., Stoytchev, I., Dang, N.C., Stoytcheva, Z., Belcaid, M., Maragathavally, K.J., Coates, C.J., Segal, D.J. and Moisyadi, S. (2012) Chimeric piggyBac transposases for genomic targeting in human cells. Nucleic Acids Res., 40, 6978-6991.
29. Lombardo, A., Cesana, D., Genovese, P., Di Stefano, B., Provasi, E., Colombo, D.F., Neri, M., Magnani, Z., Cantore, A., Lo Riso, P. et al. (2011) Site-specific integration and tailoring of cassette design for sustainable gene transfer. Nat. Methods, 8, 861-869.
30. van Rensburg, R., Beyer, I., Yao, X.Y., Wang, H., Denisenko, O., Li, Z.Y., Russell, D.W., Miller, D.G., Gregory, P., Holmes, M. et al. (2013) Chromatin structure of two genomic sites for targeted transgene integration in induced pluripotent stem cells and hematopoietic stem cells. Gene Ther., 20, 201-214.
31. Lobritz, M.A., Ratcliff, A.N. and Arts, E.J. (2010) HIV-1 entry, inhibitors, and resistance. Viruses, 2, 1069-1105.
32. Maier, D.A., Brennan, A.L., Jiang, S., Binder-Scholl, G.K., Lee, G., Plesa, G., Zheng, Z., Cotte, J., Carpenito, C., Wood, T. et al. (2013) Efficient clinical scale gene modification via zinc finger nucleasetargeted disruption of the HIV co-receptor CCR5. Hum. Gene Ther., 24, 245-258.
33. Urschitz, J., Kawasumi, M., Owens, J., Morozumi, K., Yamashiro, H., Stoytchev, I., Marh, J., Dee, J.A., Kawamoto, K., Coates, C.J. et al. (2010) Helper-independent piggyBac plasmids for gene delivery approaches: strategies for avoiding potential genotoxic effects. Proc. Natl Acad. Sci. USA, 107, 8117-8122.
34. Marh, J., Stoytcheva, Z., Urschitz, J., Sugawara, A., Yamashiro, H., Owens, J.B., Stoytchev, I., Pelczar, P., Yanagimachi, R. and Moisyadi, S. (2012) Hyperactive self-inactivating piggyBac for transposase-enhanced pronuclear microinjection transgenesis. Proc. Natl Acad. Sci. USA, 109, 19184-19189.
35. Yusa, K., Zhou, L., Li, M.A., Bradley, A. and Craig, N.L. (2011) A hyperactive piggyBac transposase for mammalian applications. Proc. Natl Acad. Sci. USA, 108, 1531-1536.
36. Meckler, J.F., Bhakta, M.S., Kim, M.S., Ovadia, R., Habrian, C.H., Zykovich, A., Yu, A., Lockwood, S.H., Morbitzer, R., Elsaesser, J. et al. (2013) Quantitative analysis of TALE-DNA interactions suggests polarity effects. Nucleic Acids Res., 41, 4118-4128.
37. Doherty, J.E., Huye, L.E., Yusa, K., Zhou, L., Craig, N.L. and Wilson, M.H. (2012) Hyperactive piggyBac gene transfer in human cells and in vivo. Hum. Gene Ther., 23, 311-320.
38. Herzog, R.W., Cao, O. and Srivastava, A. (2010) Two decades of clinical gene therapy-success is finally mounting. Discov. Med., 9, 105-111.
39. Papapetrou, E.P., Lee, G., Malani, N., Setty, M., Riviere, I., Tirunagari, L.M., Kadota, K., Roth, S.L., Giardina, P., Viale, A. et al. (2011) Genomic safe harbors permit high beta-globin transgene expression in thalassemia induced pluripotent stem cells. Nat. Biotechnol., 29, 73-78.
40. Tan, W., Dong, Z., Wilkinson, T.A., Barbas, C.F. 3rd and Chow, S.A. (2006) Human immunodeficiency virus type 1 incorporated with fusion proteins consisting of integrase and the designed polydactyl zinc finger protein E2C can bias integration of viral DNA into a predetermined chromosomal region in human cells. J. Virol., 80, 1939-1948.
41. Gaj, T., Mercer, A.C., Sirk, S.J., Smith, H.L. and Barbas, C.F. 3rd (2013) A comprehensive approach to zinc-finger recombinase customization enables genomic targeting in human cells. Nucleic Acids Res., 41, 3937-3946.
42. Ammar, I., Gogol-Doring, A., Miskey, C., Chen, W., Cathomen, T., Izsvak, Z. and Ivics, Z. (2012) Retargeting transposon insertions by the adeno-associated virus Rep protein. Nucleic Acids Res., 40, 6693-6712.
43. Feng, X., Bednarz, A.L. and Colloms, S.D. (2010) Precise targeted integration by a chimaeric transposase zinc-finger fusion protein. Nucleic Acids Res., 38, 1204-1216.
44. Brady, T.L., Schmidt, C.L. and Voytas, D.F. (2008) Targeting integration of the Saccharomyces Ty5 retrotransposon. Methods Mol. Biol., 435, 153-163.
45. Yant, S.R., Huang, Y., Akache, B. and Kay, M.A. (2007) Sitedirected transposon integration in human cells. Nucleic Acids Res., 35, e50.
46. Ivics, Z., Katzer, A., Stuwe, E.E., Fiedler, D., Knespel, S. and Izsvak, Z. (2007) Targeted sleeping beauty transposition in human cells. Mol. Ther., 15, 1137-1144.
47. Maragathavally, K.J., Kaminski, J.M. and Coates, C.J. (2006) Chimeric Mos1 and piggyBac transposases result in site-directed integration. FASEB J., 20, 1880-1882.
48. Szabo, M., Muller, F., Kiss, J., Balduf, C., Strahle, U. and Olasz, F. (2003) Transposition and targeting of the prokaryotic mobile element IS30 in zebrafish. FEBS Lett., 550, 46-50.
49. Kettlun, C., Galvan, D.L., George, A.L. Jr, Kaja, A. and Wilson, M.H. (2011) Manipulating piggyBac transposon chromosomal integration site selection in human cells. Mol. Ther., 19, 1636-1644.
50. Kim, Y., Kweon, J., Kim, A., Chon, J.K., Yoo, J.Y., Kim, H.J., Kim, S., Lee, C., Jeong, E., Chung, E. et al. (2013) A library of TAL effector nucleases spanning the human genome. Nat. Biotechnol., 31, 251-258.
51. Lombardo, A., Genovese, P., Beausejour, C.M., Colleoni, S., Lee, Y.L., Kim, K.A., Ando, D., Urnov, F.D., Galli, C., Gregory, P.D. et al. (2007) Gene editing in human stem cells using zinc finger nucleases and integrase-defective lentiviral vector delivery. Nat. Biotechnol., 25, 1298-1306.
52. Li, X., Burnight, E.R., Cooney, A.L., Malani, N., Brady, T., Sander, J.D., Staber, J., Wheelan, S.J., Joung, J.K., McCray, P.B. Jr et al. (2013) piggyBac transposase tools for genome engineering. Proc. Natl Acad. Sci. USA., 18, E2279-E2287.
53. Benabdallah, B.F., Allard, E., Yao, S., Friedman, G., Gregory, P.D., Eliopoulos, N., Fradette, J., Spees, J.L., Haddad, E., Holmes, M.C. et al. (2010) Targeted gene addition to human mesenchymal stromal cells as a cell-based plasma-soluble protein delivery platform. Cytotherapy, 12, 394-399.
54. Zou, J., Maeder, M.L., Mali, P., Pruett-Miller, S.M., Thibodeau-Beganny, S., Chou, B.K., Chen, G., Ye, Z., Park, I.H., Daley, G.Q. et al. (2009) Gene targeting of a disease-related gene in human induced pluripotent stem and embryonic stem cells. Cell Stem Cell, 5, 97-110.
55. Zou, J., Sweeney, C.L., Chou, B.K., Choi, U., Pan, J., Wang, H., Dowey, S.N., Cheng, L. and Malech, H.L. (2011) Oxidase-deficient neutrophils from X-linked chronic granulomatous disease iPS cells: functional correction by zinc finger nuclease-mediated safe harbor targeting. Blood, 117, 5561-5572.
56. DeKelver, R.C., Choi, V.M., Moehle, E.A., Paschon, D.E., Hockemeyer, D., Meijsing, S.H., Sancak, Y., Cui, X., Steine, E.J., Miller, J.C. et al. (2010) Functional genomics, proteomics, and regulatory DNA analysis in isogenic settings using zinc finger nuclease-driven transgenesis into a safe harbor locus in the human genome. Genome Res., 20, 1133-1142.
57. Hockemeyer, D., Soldner, F., Beard, C., Gao, Q., Mitalipova, M., DeKelver, R.C., Katibah, G.E., Amora, R., Boydston, E.A., Zeitler, B. et al. (2009) Efficient targeting of expressed and silent genes in human ESCs and iPSCs using zinc-finger nucleases. Nat. Biotechnol., 27, 851-857.
58. Perez-Pinera, P., Ousterout, D.G., Brown, M.T. and Gersbach, C.A. (2012) Gene targeting to the ROSA26 locus directed by engineered zinc finger nucleases. Nucleic Acids Res., 40, 3741-3752.
59. Bedell, V.M., Wang, Y., Campbell, J.M., Poshusta, T.L., Starker, C.G., Krug, R.G. 2nd, Tan, W., Penheiter, S.G., Ma, A.C., Leung, A.Y. et al. (2012) In vivo genome editing using a highefficiency TALEN system. Nature, 491, 114-118.
60. Tong, C., Huang, G., Ashton, C., Wu, H., Yan, H. and Ying, Q.L. (2012) Rapid and cost-effective gene targeting in rat embryonic stem cells by TALENs. J. Genet Genomics, 39, 275-280.
61. Li, M.A., Turner, D.J., Ning, Z., Yusa, K., Liang, Q., Eckert, S., Rad, L., Fitzgerald, T.W., Craig, N.L. and Bradley, A. (2011) Mobilization of giant piggyBac transposons in the mouse genome. Nucleic Acids Res., 39, e148.