Unexpectedly high copy number of random integration but low frequency of persistent expression of the sleeping beauty transposase after trans delivery in primary human T cells

Human Gene Therapy

Volumn 21, Issue 11, 2010, Pages 1577-1590

  Huang, Xin ^a,b   Haley, Kari ^c   Wong, Marianna ^a,b   Guo, Hongfeng ^a,b   Lu, Changming ^a,b   Wilber, Andrew ^d   Zhou, Xianzheng ^a,b  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

^d SOUTHERN ILLINOIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA; SLEEPING BEAUTY TRANSPOSASE; TRANSPOSASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHROMOSOME ANALYSIS; COMPARATIVE GENOMIC HYBRIDIZATION; CONTROLLED STUDY; DNA EXTRACTION; DNA TRANSPOSITION; EPISOME; FEMALE; GENE DOSAGE; GENE SEQUENCE; GENETIC TRANSFECTION; GENOME ANALYSIS; HUMAN; HUMAN CELL; LYMPHOCYTE SUBPOPULATION; MOLECULAR CLONING; MOUSE; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; PERIPHERAL LYMPHOCYTE; PLASMID; POLYMERASE CHAIN REACTION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOUTHERN BLOTTING; STABLE EXPRESSION; T LYMPHOCYTE; TRANSGENE; TRANSPOSON; WESTERN BLOTTING;

ANIMALS; FEMALE; GENE DOSAGE; GENE EXPRESSION; HUMANS; MICE; MICE, INBRED BALB C; MICE, NUDE; MUTAGENESIS, INSERTIONAL; PLASMIDS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; T-LYMPHOCYTES; TRANSFECTION; TRANSGENES; TRANSPOSASES;

MUS MUSCULUS;

EID: 78649344779     PISSN: 10430342     EISSN: None     Source Type: Journal    
DOI: 10.1089/hum.2009.138     Document Type: Article

References (35)

1. Alwin, S., Gere, M.B., Guhl, E., Effertz, K., Barbas, C.F., III, Segal, D.J., Weitzman, M.D., and Cathomen, T. (2005). Custom zinc-finger nucleases for use in human cells. Mol. Ther. 12, 610-617.
2. Carlson, C.M., Frandsen, J.L., Kirchhof, N., McIvor, R.S., and Largaespada, D.A. (2005). Somatic integration of an oncogene-harboring Sleeping Beauty transposon models liver tumor development in the mouse. Proc. Natl. Acad. Sci. U.S.A. 102, 17059-17064.
3. Collier, L.S., Carlson, C.M., Ravimohan, S., Dupuy, A.J., and Largaespada, D.A. (2005). Cancer gene discovery in solid tumors using transposon-based somatic mutagenesis in the mouse. Nature 436, 272-276.
4. Converse, A.D., Belur, L.R., Gori, J., Liu, G., Amaya, F., Aguilar-Cordova, E., Hackett, P.B., and McIvor, R.S. (2005). Counter-selection and co-delivery of transposon and transposase functions for Sleeping Beauty-mediated transposition in cultured mammalian cells. Biosci. Rep. 24, 577-594.
5. de Wit, T., Drabek, D., and Grosveld, F. (1998). Microinjection of Cre recombinase RNA induces site-specific recombination of a transgene in mouse oocytes. Nucleic Acids Res. 26, 676-678.
6. Doetschman, T., Maeda, N., and Smithies, O. (1988). Targeted mutation of the Hprt gene in mouse embryonic stem cells. Proc. Natl. Acad. Sci. U.S.A. 85, 8583-8587.
7. Dupuy, A,J, Akagi, K., Largaespada, D.A., Copeland, N.G., and Jenkins, N.A. (2005). Mammalian mutagenesis using a highly mobile somatic Sleeping Beauty transposon system. Nature 436, 221-226. (Pubitemid 41021267)
8. Galla, M., Will, E., Kraunus, J., Chen, L., and Baum, C. (2004). Retroviral pseudotransduction for targeted cell manipulation. Mol. Cell 16, 309-315.
9. Hacein-Bey-Abina, S., Von Kalle, C., Schmidt, M., McCormack, M.P., Wulffraat, N., Leboulch, P., Lim, A., Osborne, C.S., Pawliuk, R., Morillon, E., Sorensen, R., Forster, A., Fraser, P., Cohen, J.I., 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., Ma-cintyre, E., Sigaux, F., Soulier, J., Leiva, L.E., Wissler, M., Prinz, C., Rabbitts, T.H., Le Deist, F., Fischer, A., and Cavazzana-Calvo, M. (2003). LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1. Science 302, 415-419.
10. 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.
11. Hirt, B (1967). Selective extraction of polyoma DNA from infected mouse cell cultures. J. Mol. Biol. 26, 365-369.
12. Huang, X., Wilber, A.C., Bao, L., Tuong, D., Tolar, J., Orchard, P.J., Levine, B.L., June, C.H., McIvor, R.S., Blazar, B.R., and Zhou, X. (2006). Stable gene transfer and expression in human primary T cells by the Sleeping Beauty transposon system. Blood 107, 483-491.
13. \+ lymphoid malignancies. Mol. Ther. 16, 580-589.
14. 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.
15. Huang, X., Guo, H., Tammana, S., Jung, Y.C., Mellgren, E., Bassi, P., Cao, Q., Tu, Z.J., Kim, Y.C., Ekker, S.C., Wu, X., Wang, S.M., and Zhou, X. (2010). Gene transfer efficiency and genome-wide integration profiling of Sleeping Beauty, Tol2, and PiggyBac transposons in human primary T cells. Mol. Ther. 18, 1803- 1813.
16. Ivics, Z., Hackett, P.B., Plsterk, 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.
17. Izsvak, Z., and Ivics, Z. (2004). Sleeping Beauty transposon: Biology and applications for molecular therapy. Mol. Ther. 9, 147-156.
18. Keng, V.W., Villanueva, A., Chiang, D.Y., Dupuy, A.J., Ryan, B.J., Matise, I, Silverstein, K.A.T., Sarver, A., Starr, T.K., Akagi, E., Tessarollo, L., Collier, L.S., Powers, S., Lowe, S.W., Jenkins, N.A., Copeland, N.G., Llovet, J.M., and Largaespada, D.A. (2009). A conditional transposon-based insertional mutagen-esis screen for genes associated with mouse hepatocellular carcinoma. Nat. Biotechnol. 27, 264-274.
19. \+ T cells induces expansion of peripheral T cells and decreased CCR5 expression in HIV infection. Nat. Med. 8, 47-53.
20. Loonstra, A., Vooijs, M., Beverloo, H.B., Allak, B.A., van Drunen, E., Kanaar, R., Berns, A., and Jonkers, J. (2001). Growth inhibition and DNA damage induced by Cre recombinase in mammalian cells. Proc. Natl. Acad. Sci. U.S.A. 98, 9209-9214.
21. Mátés, L., Chuah, M.K., Belay, E., Jerchow, B., Manoj, N., Acosta-Sanchez, A., Grzela, D.P., Schmitt, A., Becker, K., Matrai, J., Ma, L., Samara-Kuko, E., Gysemans, C., Pry-putniewicz, D., Miskey, C., Fletcher, B., Vandendriessche, T., Ivics, Z., and Izsvák, Z. (2009). Molecular evolution of a novel hyperactive Sleeping Beauty transposase enables robust stable gene transfer in vertebrates. Nat. Genet. 41, 753-761.
22. Pfeifer, A., Brandon, E.P., Kootstra, N., Gage, F.H., and Verma, I.M. (2001). Delivery of the Cre recombinase by a self-deleting lentiviral vector: Efficient gene targeting in vivo. Proc. Natl. Acad. Sci. U.S.A. 98, 11450-11455.
23. Ponsaerts, P., Brown, J.P., Van den Plas, D., Van den Eeden, L., Van Bockstaele, D.R., Jorens, P.G., Van Tendeloo, V.F., Mer-regaert, J., Singh, P.B., and Berneman, Z.N. (2004). Messenger RNA electroporation is highly efficient in mouse embryonic stem cells: Successful FLPe- and Cre-mediated recombination. Gene Ther. 11, 1606-1610.
24. Rahrmann, E.P., Collier, L.S., Knutson, T.P., Doyal, M.E., Kuslak, S.L., Green, L.E., Malinowski, R.L., Roethe, L., Akagi, K., Waknitz, M., Huang, W., Largaespada, D.A., and Marker, P.C. (2009). Identification of PDE4D as a proliferation promoting factor in prostate cancer using a Sleeping Beauty transposon-based somatic mutagenesis screen. Cancer Res. 69, 4388-4397.
25. Silver, D.P., and Livingston, D.M. (2001). Self-excising retroviral vectors encoding the Cre recombinase overcome Cre-mediated cellular toxicity. Mol. Cell 8, 233-243.
26. Starr, T.K., Allaei, R., Silverstein, K.A., Staggs, R.A., Sarver, A.L., Bergemann, T.L., Gupta, M., O'Sullivan, M.G., Matise, I., Dupuy, A.J., Collier, L.S., Powers, S., Oberg, A.L., Asmann, Y.W., Thibodeau, S.N., Tessarollo, L., Copeland, N.G., Jenkins, N.A., Cormier, R.T., and Largaespada, D.A. (2009). A transposon-based genetic screen in mice identifies genes altered in colo-rectal cancer. Science 323, 1747-1750.
27. Su, Q., Prosser, H.M., Campos, L.S., Ortiz, M., Nakamura, T., Warren, M., Dupuy, A.J., Jenkins, N.A., Copeland, N.G., Bradley, A., and Liu P. (2008). A DNA transposon-based approach to validate oncogenic mutations in the mouse. Proc. Natl., Acad. Sci. U.S.A. 105, 19904-19909.
28. \+ hematopoietic stem/ progenitor cells, using the Sleeping Beauty transposon system. Hum. Gene Ther. 20, 1607-1626.
29. Thyagarajan, B., Olivares, E.C., Hollis, P., Ginsburg, D.S., and Calos, M.P. (2001). Site-specific genomic integration in mammalian cells mediated by phage FC31 integrase. Mol. Cell. Biol. 21, 3926-3934.
30. VandenDriessche, T., and Chuah, M.K.L. (2009). Moving gene therapy forward with mobile DNA. Hum. Gene Ther. 20, 1559-1561.
31. Van den Plas, D., Ponsaerts, P., Van Tendeloo, V., Van Bockstaele, D.R., Berneman, Z.N., and Merregaert, J. (2003). Efficient removal of LoxP-flanked genes by electroporation of Cre-recombinase mRNA. Biochem. Biophys. Res. Commun. 305, 10-15.
32. Wiesner, S.M., Decker, S.A., Larson, J.D., Erickson, K., Forster, C., Gallardo, J.L., Long, C., Demorest, Z.L., Zamora, E.A., Low, W.C., SantaCruz, K., Largaespada, D.A., and Ohlfest, J.R. (2009). De novo induction of genetically engineered brain tumors in mice using plasmid DNA. Cancer Res. 15, 431-439.
33. Wilber, A., Frandsen, J.L., Geurts, J.L., Largaespada, D.A., Hackett, P.B., and McIvor, R.S. (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.
34. Wilber, A., Wangensteen, K.J., Chen, Y., Zhuo, L., Frandsen, J.L., Bell, J.B., Chen, Z.J., Ekker, S.C., McIvor, R.S., and Wang, X. (2007). Messenger RNA as a source of transposase for Sleeping Beauty transposon-mediated correction of hereditary tyro-sinemia type I. Mol. Ther. 15, 1280-1287.
35. \+ hematopoietic stem and progenitor cells by a hyperactive Sleeping Beauty transposon system. Blood 114, 1319-1330.