High-level genomic integration, epigenetic changes and expression of sleeping beauty transgene

Biochemistry

Volumn 49, Issue 7, 2010, Pages 1507-1521

  Zhu, Jianhui ^a   Park, Chang Won ^a   Sjeklocha, Lucas ^a   Kren, Betsy T ^a   Steer, Clifford J ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CLONES; CELL SORTING; DEACETYLATION; DNA METHYLATION PATTERN; ENDOGENOUS FACTORS; ERYTHROID CELLS; FLUORESCENT REPORTER; GENOMIC ANALYSIS; GENOMIC INTEGRATION; GREEN FLUORESCENT PROTEIN; INTERNAL RIBOSOME ENTRY SITE; K562 CELLS; MAMMALIAN CELLS; MAMMALIAN GENOMES; MEGAKARYOCYTE; NONVIRAL VECTORS; PROMOTER ELEMENTS; SLEEPING BEAUTY; SLEEPING BEAUTY TRANSPOSON; TRANS-GENES; TRANSGENE; TRANSGENE EXPRESSION; TRANSPOSASE;

ACETYLATION; ALKYLATION; CLONE CELLS; FLUORESCENCE; INTEGRATION; MAMMALS; METHYLATION; PROTEINS; SORTING;

GENE EXPRESSION;

GREEN FLUORESCENT PROTEIN; TRANSPOSASE;

ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; EPIGENETICS; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; GENE INSERTION; GENOMICS; HUMAN; HUMAN CELL; MEGAKARYOCYTE; PRIORITY JOURNAL; SLEEPING BEAUTY GENE; TRANSGENE; TRANSPOSON;

5-AMINOLEVULINATE SYNTHETASE; ANIMALS; ANKYRINS; ANTIGENS, CD34; CELL DIFFERENTIATION; CLONING, MOLECULAR; DNA TRANSPOSABLE ELEMENTS; ENHANCER ELEMENTS, GENETIC; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION; GENES, REPORTER; GENETIC MARKERS; GENETIC VECTORS; GENOME, HUMAN; GREEN FLUORESCENT PROTEINS; HEMATOPOIETIC STEM CELLS; HUMANS; K562 CELLS; LUMINESCENT PROTEINS; MICE; TRANSDUCTION, GENETIC; TRANSGENES; TRANSPOSASES;

MAMMALIA;

EID: 77449156754     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi9016846     Document Type: Article

References (61)

1. Ivics, Z., Hackett, P. B., Plasterk, R. H., and Izsvák, Z. (1997) Molecular reconstruction of Sleeping Beauty, a Tc1-like transposon from fish, and its transposition in human cells, Cell 91, 501-510.
2. Yant, S. R., Meuse, L., Chiu, W., Ivics, Z., Izsvák, Z., and Kay, M. A. (2000) Somatic integration and long-term transgene expression in normal and haemophilic mice using a DNA transposon system. Nat. Genet. 25, 35-41.
3. Ivics, Z., and Izsvák, Z. (2006) Transposons for gene therapy!. Curr. Gene Ther. 6, 593-607.
4. 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.
5. Yant, S. R., Huang, Y., Akache, B., and Kay, M. A. (2007) Sitedirected transposon integration in human cells, Nucleic Acids Res. 35, e50.
6. Ivics, Z., Katzer, A., Stuwe, E. E., Fiedler, D., Knespel, S., and Izsvák, Z. (2007) Targeted Sleeping Beauty transposition in human cells, Mol. Ther. 15, 1137-1144. (Pubitemid 46813616)
7. Park, C. W., Park, J., Kren, B. T., and Steer, C. J. (2006) Sleeping Beauty transposition in the mouse genome is associated with changes in DNA methylation at the site of insertion, Genomics 88, 204-213. (Pubitemid 44062275)
8. Sorrentino, B. P., and Nienhuis, A. W. (2001) Gene therapy for hematopoietic diseases, in The Molecular Basis of Blood Diseases (Stamatoyannopoulous, G., Majerus, P. W., Perlmutter, R. M., and Varmus, H., Eds.) 3rd ed., pp 969-1003, Saunders, Philadelphia, PA.
9. Ingram, V. M. (1957) Gene mutations in human, haemoglobin: the chemical difference between normal and sickle cell haemoglobin. Nature 180, 326-328.
10. 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., Macintyre, 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.
11. Zhu, J., Kren, B. T., Park, C. W., Bilgim, R., Wong, P. Y., and Steer, C. J. (2007) Erythroid-specific expression of β-globin by the Sleeping Beauty transposon for sickle cell disease. Biochemistry 46, 6844-6858. (Pubitemid 46906414)
12. Moreau-Gaudry, F., Xia, P., Jiang, G., Perelman, N. P., Bauer, G., Ellis, J., Surinya, K. H., Mavilio, F., Shen, C. K., and Malik, P. (2001) High-level erythroid-specific gene expression in primary human and murine hematopoietic cells with self-inactivating lentiviral vectors. Blood 98, 2664-2672.
13. Gallagher,P.G.,Romana,M.,Tse,W.T.,Lux,S.E.,andForget,B.G.(2000) Thehumanankyrin- 1geneisselectivelytranscribedinerythroidcelllinesdespitethepresenceofahou sekeeping-likepromoter,Blood96,1136-1143.(Pubitemid30616885)
14. Pelletier, J., and Sonenberg, N. (1988) Internal initiation of translation of eukaryotic mRNA directed by a sequence derived from poliovirus RNA, Nature 334, 320-325. (Pubitemid 18177659)
15. Jang, S. K., Krausslich, H. G., Nicklin, M. J., Duke, G. M., Palmenberg, A. C., and Wimmer, E. (1988) A segment of the 5′ nontranslated region of encephalomyocarditis virus RNA directs internal entry of ribosomes during in vitro translation. J. Virol. 62, 2636-2643.
16. Michalowsky, L. A., and Jones, P. A. (1987) Differential nuclear protein binding to 5-azacytosine-containing DNA as a potential mechanism for 5-aza-2′-deoxycytidine resistance, Mol. Cell. Biol. 7, 3076-3083.
17. Frommer, M., McDonald, L. E., Millar, D. S., Collis, C. M., Watt, F., Grigg, G. W., Molloy, P. L., and Paul, C. L. (1992) A genomic sequencing protocol that yields a positive display of 5-methylcytosine residues in individual DNA strands, Proc. Natl. Acad. Sci. U.S.A. 89, 1827-1831.
18. Grunau, C., Clark, S. J., and Rosenthal, A. (2001) Bisulfite genomic sequencing: systematic investigation of critical experimental parameters, Nucleic Acids Res. 29, e65.
19. Gross-Bellard, M., Oudet, P., and Chambon, P. (1973) Isolation of high-molecular-weight DNA from mammalian cells, Eur. J. Biochem. 36, 32-38.
20. Li, L. C., and Dahiya, R. (2002) MethPrimer: designing primers for methylation PCRs. Bioinformatics 18, 1427-1431.
21. Xiong, Z., and Laird, P. W. (1997) COBRA: a sensitive and quantitative DNA methylation assay. Nucleic Acids Res. 25, 2532-2534. (Pubitemid 27303718)
22. Yant, S. R., Wu, X., Huang, Y., Garrison, B., Burgess, S. M., and Kay, M. A. (2005) High-resolution genome-wide mapping of transposon integration in mammals. Mol. Cell. Biol. 25, 2085-2094. (Pubitemid 40354609)
23. Michalkiewicz, M., Michalkiewicz, T., Geurts, A. M., Roman, R. J., Slocum, G. R., Singer, O., Weihrauch, D., Greene, A. S., Kaldunski, M., Verma, I. M., Jacob, H. J., and Cowley, A. W., Jr. (2007) Efficient transgenic rat production by a lentiviral vector. Am. J. Physiol. Heart Circ. Physiol. 293, H881-H894.
24. Rutherford, T. R., Clegg, J. B., and Weatherall, D. J. (1979) K562 human leukaemic cells synthesise embryonic haemoglobin in response to haemin. Nature 280, 164-165.
25. Lozzio, C. B., Lozzio, B. B., Machado, E. A., Fuhr, J. E., Lair, S. V., and Bamberger, E. G. (1979) Effects of sodium butyrate on human chronic myelogenous leukaemia cell line K562. Nature 281, 709-710.
26. Singh, M. K., and Yu, J. (1984) Accumulation of a heat shock-like protein during differentiation of human erythroid cell line K562. Nature 309, 631-633.
27. Villeval, J. L., Pelicci, P. G., Tabilio, A., Titeux, M., Henri, A., Houesche, F., Thomopoulos, P., Vainchenker, W., Garbaz, M., Rochant, H., Breton-Gorius, J., Edwards, P. A., and Testa, U. (1983) Erythroid properties of K562 cells. Effect of hemin, butyrate and TPA induction. Exp. Cell Res. 146, 428-435.
28. Whalen,A.M.,Galasinski,S.C.,Shapiro,P.S.,Nahreini,T.S.,andAhn,N.G.(1997) Megakaryocyticdifferentiationinducedbyconstitutiveactivationofmitogen- activatedproteinkinasekinase.Mol.Cell.Biol.17,1947-1958.(Pubitemid27133279)
29. Mignotte, V., Vigon, I., Boucher de Crevecoeur, E., Romeo, P. H., Lemarchandel, V., and Chretien, S. (1994) Structure and transcription of the human c-mpl gene (MPL). Genomics 20, 5-12. (Pubitemid 24100913)
30. Meshkini,A.,andYazdanparast,R.(2007) InductionofmegakaryocyticdifferentiationinchronicmyelogenousleukemiacellK562by3- hydrogenkwadaphnin.J.Biochem.Mol.Biol.40,944-951.(Pubitemid350242280)
31. Jokinen, M., Gahmberg, C. G., and Andersson, L. C. (1979) Biosynthesis of the major human red cell sialoglycoprotein, glycophorin A, in a continuous cell line. Nature 279, 604-607. (Pubitemid 9198856)
32. Chénais,B.,Molle,I.,Trentesaux,C.,andJeannesson,P.(1997) Time-courseofbutyricacid-induceddifferentiationinhumanK562leukemiccellline: rapidincreaseinγ-globin,porphobilinogen,deaminaseandNF-E2mRNAlevels. Leukemia11,1575-1579.(Pubitemid27404402)
33. Chénais, B., Andriollo, M., Guiraud, P., Belhoussine, R., and Jeannesson, P. (2000) Oxidative stress involvement in chemically induced differentiation of K562 cells, Free Radical Biol. Med. 28, 18-27. (Pubitemid 30045569)
34. Williams, M. J., Du, X., Loftus, J. C., and Ginsberg, M. H. (1995) Platelet adhesion receptors, Semin. Cell Biol. 6, 305-314.
35. van Pampus, E. C., Denkers, I. A., van Geel, B. J., Huijgens, P. C., Zevenbergen, A., Ossenkoppele, G. J., and Langenhuijsen, M. M. (1992) Expression of adhesion antigens of human bone marrow megakaryocytes, circulating megakaryocytes and blood platelets. Eur. J. Haematol. 49, 122-127.
36. Whitelaw, E., Sutherland, H., Kearns, M., Morgan, H., Weaving, L., and Garrick, D. (2001) Epigenetic effects on transgene expression. Mathods Mol. Biol. 158, 351-368.
37. Yoshida, M., Horinouchi, S., and Beppu, T. (1995) Trichostatin A. and trapoxin: novel chemical probes for the role of histone acetylation in chromatin structure and function. Bio Essays 17, 423-430.
38. Fuks, F. (2005) DNA methylation and histone modifications: teaming up to silence genes, Curr. Opin. Genet. Dev. 15, 490-495.
39. Cameron, E. E., Bachman, K. E., Myohanen, S., Herman, J. G., and Baylin, S. B. (1999) Synergy of demethylation and histone deacetylase inhibition in the re-expression of genes silenced in cancer. Nat. Genet. 21, 103-107. (Pubitemid 29036293)
40. Moldt, B., Yant, S. R., Andersen, P. R., Kay, M. A., and Mikkelsen, J. G. (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)
41. Walisko, O., Schorn, A., Rolfs, F., Devaraj, A., Miskey, C., Izsvák, Z., and Ivics, Z. (2008) Transcriptional activities of the Sleeping Beauty transposon and shielding its genetic cargo with insulators. Mol. Ther. 16, 359-369. (Pubitemid 351168045)
42. Geurts, A. M., Yang, Y., Clark, K. J., Liu, G., Cui, Z., Dupuy, A. J., Bell, J. B., Largaespada, D. A., and Hackett, P. B. (2003) Gene transfer into genomes of human cells by the Sleeping Beauty transposon system, Mol. Ther. 8, 108-117. (Pubitemid 36939302)
43. Zayed, H., Izsvák, Z., Walisko, O., and Ivics, Z. (2004) Development of hyperactive Sleeping Beauty transposon vectors by mutational analysis. Mol. Ther. 9, 292-304. (Pubitemid 38256555)
44. Yant, S. R., Park, J., Huang, Y., Mikkelsen, J. G., and Kay, M. A. (2004) Mutational analysis of the N-terminal DNA-binding domain of Sleeping Beauty transposase: critical residues for DNA binding and hyperactivity in mammalian cells. Mol. Cell. Biol. 24, 9239-9247. (Pubitemid 39313924)
45. 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., Pryputniewicz, 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.
46. Kustikova, O. S., Wahlers, A., Kuhlcke, K., Stahle, B., Zander, A. R., Baum, C., and Fehse, B. (2003) Dose finding with retroviral vectors: correlation of retroviral vector copy numbers in single cells with gene transfer efficiency in a cell population. Blood 102, 3934-3937. (Pubitemid 37486973)
47. Woltjen, K., Michael, I. P., Mohseni, P., Desai, R., Mileikovsky, M., Hämäläinen, R., Cowling, R., Wang, W., Liu, P., Gertsenstein, M., Kaji, K., Sung, H.-K., and Nagy, A. (2009) piggy Bac transposition reprograms fibroblasts to induced pluripotent stem cells. Nature 458, 766-770.
48. + hematopoietic stem and progenitor cells by a hyperactive Sleeping Beauty transposon system. Blood 114, 1319-1330.
49. Higgs,D.R.,Wood,W.G.,Jarman,A.P.,Sharpe,J.,Lida,J.,Pretorius,I.M., andAyyub,H.(1990) Amajorpositiveregulatoryregionlocatedfarupstreamofthehumanα- globingenelocus.GenesDev.4,1588-1601.(Pubitemid20310078)
50. Morishita, K., Parker, D. S., Mucenski, M. L., Jenkins, N. A., Copeland, N. G., and Ihle, J. N. (1988) Retroviral activation of a novel gene encoding a zinc finger protein in IL-3-dependent myeloid leukemia cell lines, Cell 54, 831-840. (Pubitemid 18215352)
51. Lazo, P. A., Lee, J. S., and Tsichlis, P. N. (1990) Long-distance activation of the Myc protooncogene by provirus insertion in Mlvi-1 or Mivi-4 in rat T-cell lymphomas, Proc. Natl. Acad. Sci. U.S.A. 87, 170-173. (Pubitemid 20033029)
52. Saitoh,N.,Bell,A.C.,Recillas-Targa,F.,West,A.G.,Simpson,M.,Pikaart,M., andFelsenfeld,G.(2000)Structuralandfunctionalconservation, attheboundariesofthechickenβ-globindomain.EMBOJ.19,2315-2322. (Pubitemid30259012)
53. Weber, E. L., and Cannon, P. M. (2007) Promoter choice for retroviral vectors: transcriptional strength versus trans-activation potential. Hum. Gene Ther. 18, 849-860.
54. Doerfler, W., Schubbert, R., Heller, H., Kammer, C., Hilger-Eversheim, K., Knoblauch, M., and Remus, R. (1997) Integration of foreign DNA and its consequences in mammalian systems. Trends Biotechnol. 15, 297-301. (Pubitemid 27330624)
55. Jaenisch, R., and Bird, A. (2003) Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals, Nat. Genet. 33 (Suppl.), 245-254. (Pubitemid 36278835)
56. Chevalier-Mariette, C., Henry, I., Montfort, L., Capgras, S., Forlani, S., Miuschler, J., and Nicolas, J. F. (2003) CpG content affects gene scilencing in mice: evidence from novel transgenes. Genome Biol. 4, R53.
57. Yoder, J. A., Walsh, C. P., and Bestor, T. H. (1997) Cytosine methylation and the ecology of intragenomic parasites. Trends Genet. 13, 335-340.
58. Park, C. W., Kren, B. T., Largaespada, D. A., and Steer, C. J. (2005) DNA methylation of Sleeping Beauty with transposition into the mouse genome. Genes Cells 10, 763-776.
59. Chen, Z. Y., Rui, E., He, C. Y., Xu, H., and Kay, M. A. (2008) Silencing of episomal expression in liver by plasmid bacterial backbone DNA is independent of CpG methylation. Mol. Ther. 16, 548-556. (Pubitemid 351314995)
60. von Levetzow, G., Spanholtz, J., Beckmann, J., Fischer, J., Kogler, G., Wernet, P., Punzel, M., and Giebel, B. (2006) Nucleofection, an efficient nonviral method to transfer genes into human hematopoietic stem, and progenitor cells. Stem Cells Dev. 15, 278-285. (Pubitemid 43726506)
61. Mikkelson, J. G., Yant, S. R., Meuse, L., Huang, Z., Xu, H., and Kay, M. A. (2003) Helper-independent Sleeping Beauty transposon-transposase vectors for efficient nonviral gene delivery and persistent gene expression in vivo. Mol. Ther. 8, 654-665. (Pubitemid 37321695)