Gene transfer efficiency and genome-wide integration profiling of sleeping beauty, Tol2, and PiggyBac transposons in human primary t cells

Molecular Therapy

Volumn 18, Issue 10, 2010, Pages 1803-1813

  Huang, Xin ^a,b   Guo, Hongfeng ^a,b   Tammana, Syam ^c   Jung, Yong Chul ^d   Mellgren, Emil ^e   Bassi, Preetinder ^c   Cao, Qing ^b   Tu, Zheng Jin ^c   Kim, Yeong C ^d   Ekker, Stephen C ^f   Wu, Xiaolin ^g   Wang, San Ming ^d   Zhou, Xianzheng ^a,b,c  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

^d NORTHWESTERN UNIVERSITY   (United States)

^e MACALESTER COLLEGE   (United States)

^f MAYO GRADUATE SCHOOL   (United States)

^g SAIC FREDERICK INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYRIBONUCLEASE I; PIGGYBAC PROTEIN; PROTEIN TOL2; SLEEPING BEAUTY PROTEIN; TRANSPOSASE; UNCLASSIFIED DRUG;

ARTICLE; CHROMOSOME; CPG ISLAND; GENE DELIVERY SYSTEM; GENE EXPRESSION; GENE LOCATION; HUMAN; HUMAN CELL; ONCOGENE; PERIPHERAL LYMPHOCYTE; SOUTHERN BLOTTING; T LYMPHOCYTE; TRANSCRIPTION INITIATION; TRANSPOSON; UMBILICAL CORD BLOOD;

EID: 77957579849     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2010.141     Document Type: Article

References (45)

1. Ivics, Z, Hackett, PB, Plasterk, RH and Izsvak, Z (1997). Molecular reconstruction of Sleeping Beauty, a Tc1-like transposon from fish, and its transposition in human cells. Cell 91: 501-510.
2. Hackett, PB, Ekker, SC, Largaespada, DA and McIvor, RS (2005). Sleeping Beauty transposon-mediated gene therapy for prolonged expression. Adv Genet 54: 189-232.
3. Ivics, Z and Izsvak, Z (2006). Transposons for gene therapy! Curr Gene Ther 6: 593-607.
4. Huang, X, Wilber, AC, Bao, L, Tuong, D, Tolar, J, Orchard, PJ et al. (2006). Stable gene transfer and expression in human primary T cells by the Sleeping Beauty transposon system. Blood 107: 483-491.
5. Huang, X, Wilber, A, McIvor, RS and Zhou, X (2009). DNA transposons for modification of human primary T lymphocytes. Methods Mol Biol 506: 115-126.
6. Huang, X, Guo, H, Kang, J, Choi, S, Zhou, TC, Tammana, S et al. (2008). Sleeping Beauty transposon-mediated engineering of human primary T cells for therapy of CD19+ lymphoid malignancies. Mol Ther 16: 580-589.
7. Hackett, PB (2007). Integrating DNA vectors for gene therapy. Mol Ther 15: 10-12.
8. Geurts, AM, Yang, Y, Clark, KJ, Liu, G, Cui, Z, Dupuy, AJ et al. (2003). Gene transfer into genomes of human cells by the Sleeping Beauty transposon system. Mol Ther 8: 108-117.
9. Cary, LC, Goebel, M, Corsaro, BG, Wang, HG, Rosen, E and Fraser, MJ (1989). Transposon mutagenesis of baculoviruses: analysis of Trichoplusia ni transposon IFP2 insertions within the FP-locus of nuclear polyhedrosis viruses. Virology 172: 156-169.
10. 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.
11. Wu, SC, Meir, YJ, Coates, CJ, Handler, AM, Pelczar, P, Moisyadi, S et al. (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.
12. Wilson, MH, Coates, CJ and George, AL Jr (2007). PiggyBac transposon-mediated gene transfer in human cells. Mol Ther 15: 139-145.
13. Wang, W, Lin, C, Lu, D, Ning, Z, Cox, T, Melvin, D et al. (2008). Chromosomal transposition of PiggyBac in mouse embryonic stem cells. Proc Natl Acad Sci USA 105: 9290-9295.
14. Kaji, K, Norrby, K, Paca, A, Mileikovsky, M, Mohseni, P and Woltjen, K (2009). Virusfree induction of pluripotency and subsequent excision of reprogramming factors. Nature 458: 771-775.
15. Woltjen, K, Michael, IP, Mohseni, P, Desai, R, Mileikovsky, M, Hamalainen, R et al. (2009). piggyBac transposition reprograms fibroblasts to induced pluripotent stem cells. Nature 458: 766-770.
16. Koga, A, Inagaki, H, Bessho, Y and Hori, H (1995). Insertion of a novel transposable element in the tyrosinase gene is responsible for an albino mutation in the medaka fish, Oryzias latipes. Mol Gen Genet 249: 400-405.
17. Balciunas, D, Wangensteen, KJ, Wilber, A, Bell, J, Geurts, A, Sivasubbu, S et al. (2006). Harnessing a high cargo-capacity transposon for genetic applications in vertebrates. PLoS Genet 2: e169.
18. Tosi, LR and Beverley, SM (2000). cis and trans factors affecting Mos1 mariner evolution and transposition in vitro, and its potential for functional genomics. Nucleic Acids Res 28: 784-790.
19. Wilson, MH, Kaminski, JM and George, AL Jr (2005). Functional zinc finger/Sleeping Beauty transposase chimeras exhibit attenuated overproduction inhibition. FEBS Lett 579: 6205-6209.
20. Ivics, Z, Katzer, A, Stuwe, EE, Fiedler, D, Knespel, S and Izsvak, Z (2007). Targeted Sleeping Beauty transposition in human cells. Mol Ther 15: 1137-1144.
21. Yant, SR, Huang, Y, Akache, B and Kay, MA (2007). Site-directed transposon integration in human cells. Nucleic Acids Res 35: e50.
22. Feschotte, C (2006). The piggyBac transposon holds promise for human gene therapy. Proc Natl Acad Sci USA 103: 14981-14982.
23. Yant, SR, Wu, X, Huang, Y, Garrison, B, Burgess, SM and Kay, MA (2005). Highresolution genome-wide mapping of transposon integration in mammals. Mol Cell Biol 25: 2085-2094.
24. Singh, H, Manuri, PR, Olivares, S, Dara, N, Dawson, MJ, Huls, H et al. (2008). Redirecting specificity of T-cell populations for CD19 using the Sleeping Beauty system. Cancer Res 68: 2961-2971.
25. Peng, PD, Cohen, CJ, Yang, S, Hsu, C, Jones, S, Zhao, Y 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.
26. Lander, ES, Linton, LM, Birren, B, Nusbaum, C, Zody, MC, Baldwin, J et al.; International Human Genome Sequencing Consortium. (2001). Initial sequencing and analysis of the human genome. Nature 409: 860-921.
27. Zayed, H, Izsvak, Z, Khare, D, Heinemann, U and Ivics, Z (2003). The DNA-bending protein HMGB1 is a cellular cofactor of Sleeping Beauty transposition. Nucleic Acids Res 31: 2313-2322.
28. Walisko, O, Izsvak, Z, Szabo, K, Kaufman, CD, Herold, S and Ivics, Z (2006). Sleeping Beauty transposase modulates cell-cycle progression through interaction with Miz-1. Proc Natl Acad Sci USA 103: 4062-4067.
29. Liang, JJ, Wang, H, Rashid, A, Tan, TH, Hwang, RF, Hamilton, SR et al. (2008). Expression of MAP4K4 is associated with worse prognosis in patients with stage II pancreatic ductal adenocarcinoma. Clin Cancer Res 14: 7043-7049.
30. Aouadi, M, Tesz, GJ, Nicoloro, SM, Wang, M, Chouinard, M, Soto, E et al. (2009). Orally delivered siRNA targeting macrophage Map4k4 suppresses systemic inflammation. Nature 458: 1180-1184.
31. Wright, JH, Wang, X, Manning, G, LaMere, BJ, Le, P, Zhu, S et al. (2003). The STE20 kinase HGK is broadly expressed in human tumor cells and can modulate cellular transformation, invasion, and adhesion. Mol Cell Biol 23: 2068-2082.
32. Holterman, CE, Franovic, A, Payette, J and Lee, S (2010). ETS-1 oncogenic activity mediated by transforming growth factor alpha. Cancer Res 70: 730-740.
33. Shibolet, O, Giallourakis, C, Rosenberg, I, Mueller, T, Xavier, RJ and Podolsky, DK (2007). AKAP13, a RhoA GTPase-specific guanine exchange factor, is a novel regulator of TLR2 signaling. J Biol Chem 282: 35308-35317.
34. Sterpetti, P, Marucci, L, Candelaresi, C, Toksoz, D, Alpini, G, Ugili, L et al. (2006). Cell proliferation and drug resistance in hepatocellular carcinoma are modulated by Rho GTPase signals. Am J Physiol Gastrointest Liver Physiol 290: G624-G632.
35. Wu, X, Li, Y, Crise, B and Burgess, SM (2003). Transcription start regions in the human genome are favored targets for MLV integration. Science 300: 1749-1751.
36. Schroder, AR, Shinn, P, Chen, H, Berry, C, Ecker, JR and Bushman, F (2002). HIV-1 integration in the human genome favors active genes and local hotspots. Cell 110: 521-529.
37. Berry, C, Hannenhalli, S, Leipzig, J and Bushman, FD (2006). Selection of target sites for mobile DNA integration in the human genome. PLoS Comput Biol 2: e157.
38. Mates, L, Chuah, MK, Belay, E, Jerchow, B, Manoj, N, Acosta-Sanchez, A et al. (2009). Molecular evolution of a novel hyperactive Sleeping Beauty transposase enables robust stable gene transfer in vertebrates. Nat Genet 41: 753-761.
39. Xue, X, Huang, X, Nodland, SE, Mates, L, Ma, L, Izsvak, Z et al. (2009). Stable gene transfer and expression in cord blood-derived CD34+ hematopoietic stem and progenitor cells by a hyperactive Sleeping Beauty transposon system. Blood 114: 1319-1330.
40. Cadinanos, J and Bradley, A (2007). Generation of an inducible and optimized piggyBac transposon system. Nucleic Acids Res 35: e87.
41. Huang, X, Haley, K, Wong, M, Guo, H, Lu, C, Wilber, A et al. (2010). Unexpectedly high copy number of random integration but low frequency of persistent expression of the Sleeping Beauty transposase following trans delivery in primary T cells. Hum Gene Ther (epub ahead of print).
42. Li, X, Lobo, N, Bauser, CA and Fraser, MJ Jr (2001). The minimum internal and external sequence requirements for transposition of the eukaryotic transformation vector piggyBac. Mol Genet Genomics 266: 190-198.
43. Li, X, Harrell, RA, Handler, AM, Beam, T, Hennessy, K and Fraser, MJ Jr (2005). piggyBac internal sequences are necessary for efficient transformation of target genomes. Insect Mol Biol 14: 17-30.
44. Levine, BL, Bernstein, WB, Aronson, NE, Schlienger, K, Cotte, J, Perfetto, S et al. (2002). Adoptive transfer of costimulated CD4+ T cells induces expansion of peripheral T cells and decreased CCR5 expression in HIV infection. Nat Med 8: 47-53.
45. Riddell, SR and Greenberg, PD (1990). The use of anti-CD3 and anti-CD28 monoclonal antibodies to clone and expand human antigen-specific T cells. J Immunol Methods 128: 189-201.