Optimization of the piggyBac transposon using mRNA and insulators: Toward a more reliable gene delivery system

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Bire, Solenne ^a,b,c   Ley, Déborah ^b   Casteret, Sophie ^c   Mermod, Nicolas ^b   Bigot, Yves ^c   Rouleux Bonnin, Florence ^a  

^a UNIVERSITÉ DE TOURS   (France)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c UMR85 PHYSIOLOGIE DE LA REPRODUCTION ET DES COMPORTEMENTS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA; MESSENGER RNA; TRANSPOSASE;

ARTICLE; CELL VIABILITY; CONTROLLED STUDY; DNA CLEAVAGE; DNA TRANSPOSITION; DNA VECTOR; GENE EXPRESSION; GENOTOXICITY; HELA CELL; INSULATOR ELEMENT; NUCLEOTIDE SEQUENCE; PIGGYBAC TRANSPOSON; REGULATORY SEQUENCE; TRANSGENE; TRANSPOSON; GENE TRANSFER; GENE VECTOR; GENETICS; HELA CELL LINE; HUMAN; METABOLISM; WESTERN BLOTTING;

BLOTTING, WESTERN; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; HELA CELLS; HUMANS; RNA, MESSENGER; TRANSPOSASES;

EID: 84891608276     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0082559     Document Type: Article

References (42)

1. Kumar M, Keller B, Makalou N, Sutton, RE (2001) Systematic determination of the packaging limit of lentiviral vectors. Hum Gene Ther 12: 1893-1905
2. Ding S, Wu X, Li G, Han M, Zhuang Y et al. (2005) Efficient transposition of the piggyBac (PB) transposon in mammalian cells and mice. Cell 122: 473-483. doi:10.1016/j.cell.2005.07.013. PubMed: 16096065.
3. Ivics Z, Izsvák Z (2010) The expanding universe of transposon technologies for gene and cell engineering. Mob DNA 1: 25. doi: 10.1186/1759-8753-1-25. PubMed: 21138556.
4. Bire S, Rouleux-Bonnin F (2012) Transposable elements as tools for reshaping the genome: it is a huge world after all! Methods Mol Biol 859: 1-28. doi:10.1007/978-1-61779-603-6-1. PubMed: 22367863.
5. Ivics Z, Hackett PB, Plasterk RH, Izsvák Z (1997) Molecular reconstruction of Sleeping Beauty, a Tc1-like transposon from fish, and its transposition in human cells. Cell 91: 501-510. doi:10.1016/S0092-8674(00)80436- 5. PubMed: 9390559.
6. Horie K, Kuroiwa A, Ikawa M, Okabe M, Kondoh G et al. (2001) Efficient chromosomal transposition of a Tc1/mariner- like transposon Sleeping Beauty in mice. Proc Natl Acad Sci U S A 98: 9191-9196. doi: 10.1073/pnas.161071798. PubMed: 11481482.
7. Huls M, Figliola M, Dawson M, Olivares S, Kebriaei P et al. (2013) Clinical Application of Sleeping Beauty and Artificial Antigen Presenting Cells to Genetically Modify T Cells from Peripheral and Umbilical Cord. Blood - J Vis Exp 72: e50070.
8. Di Matteo M, Mátrai J, Belay E, Firdissa T, Vandendriessche T et al. (2012) PiggyBac toolbox. Methods Mol Biol 859: 241-254. doi: 10.1007/978-1-61779-603-6-14. PubMed: 22367876.
9. Le Fourn V, Girod PA, Buceta M, Regamey A, Mermod N (2013) CHO cell engineering to prevent polypeptide aggregation and improve therapeutic protein secretion. Metab Eng pii: S1096-7176(13)00002-5
10. Ley D, Harraghy N, Le Fourn V, Bire S, Girod PA et al. (2013) MAR elements and transposons for improved transgene integration and expression. PLOS ONE 8: e62784. doi:10.1371/journal.pone.0062784. PubMed: 23646143.
11. Wu SC, Meir YJ, Coates CJ, Handler AM, Pelczar P 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 U S A 103: 15008-15013. doi:10.1073/pnas.0606979103. PubMed: 17005721.
12. Palazzoli F, Testu FX, Merly F, Bigot Y (2010) Transposon tools: worldwide landscape of intellectual property and technological developments. Genetica 138: 285-299. doi:10.1007/s10709-009-9426-3. PubMed: 19957019.
13. Nakanishi H, Higuchi Y, Kawakami S, Yamashita F, Hashida M (2010) piggyBac transposon-mediated long-term gene expression in mice. Mol Ther 18: 707-714. doi:10.1038/mt.2009.302. PubMed: 20104210.
14. Lacoste A, Berenshteyn F, Brivanlou AH (2009) An efficient and reversible transposable system for gene delivery and lineage-specific differentiation in human embryonic stem cells. Cell Stem Cell 5: 332-342. doi:10.1016/j.stem.2009. 07.011. PubMed: 19733544.
15. Woltjen K, Michael IP, Mohseni P, Desai R, Mileikovsky M et al. (2009) piggyBac transposition reprograms fibroblasts to induced pluripotent stem cells. Nature 458: 766-770. doi:10.1038/nature07863. PubMed: 19252478.
16. Cadiñanos J, Bradley A (2007) Generation of an inducible and optimized piggyBac transposon system. Nucleic Acids Res 35: e87. doi:10.1093/nar/gkm446. PubMed: 17576687.
17. Yusa K, Zhou L, Li MA, Bradley A, Craig NL (2011) A hyperactive piggyBac transposase for mammalian applications. Proc Natl Acad Sci U S A 108: 1531-1536. doi:10.1073/pnas.1008322108. PubMed: 21205896.
18. Huang X, Guo H, Tammana S, Jung YC, Mellgren E et al. (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. doi:10.1038/mt.2010.141. PubMed: 20606646.
19. Van Tendeloo VF, Ponsaerts P, Berneman ZN (2007) mRNA-based gene transfer as a tool for gene and cell therapy. Curr Opin Mol Ther 9: 423-431. PubMed: 17932806.
20. Furushima K, Jang CW, Chen DW, Xiao N, Overbeek PA et al. (2012) Insertional mutagenesis by a hybrid piggyBac and sleeping beauty transposon in the rat. Genetics 192: 1235-1248. doi:10.1534/genetics. 112.140855. PubMed: 23023007.
21. Wilber A, Frandsen JL, Geurts JL, Largaespada DA, Hackett PB et al. (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. doi:10.1016/j.ymthe.2005.10.014. PubMed: 16368272.
22. Garrison BS, Yant SR, Mikkelsen JG, Kay MA (2007) Postintegrative gene silencing within the Sleeping Beauty transposition system. Mol Cell Biol 27: 8824-8833. doi:10.1128/MCB.00498-07. PubMed: 17938204.
23. Recillas-Targa F, Valadez-Graham V, Farrell CM (2004) Prospects and implications of using chromatin insulators in gene therapy and transgenesis. Bioessays 26: 796-807. doi:10.1002/bies.20059. PubMed: 15221861.
24. Palazzoli F, Bire S, Bigot Y, Bonnin-Rouleux F (2011) Landscape of chromatin control element patents: positioning effects in pharmaceutical bioproduction. Nat Biotechnol 29: 593-597. doi: 10.1038/nbt.1907. PubMed: 21747382.
25. Dalsgaard T, Moldt B, Sharma N, Wolf G, Schmitz A et al. (2009) Shielding of sleeping beauty DNA transposon-delivered transgene cassettes by heterologous insulators in early embryonal cells. Mol Ther 17: 121-130. doi:10.1038/mt.2008. 224. PubMed: 18985029.
26. Esnault G, Majocchi S, Martinet D, Besuchet-Schmutz N, Beckmann JS et al. (2009) Transcription factor CTF1 acts as a chromatin domain boundary that shields human telomeric genes from silencing. Mol Cell Biol 29: 2409-2418. doi:10.1128/MCB.00779-08. PubMed: 19273604.
27. Gaussin A, Modlich U, Bauche C, Niederländer NJ, Schambach A et al. (2012) CTF/NF1 transcription factors act as potent genetic insulators for integrating gene transfer vectors. Gene Ther 19: 15-24. doi: 10.1038/gt.2011.70. PubMed: 21562592.
28. Ottaviani A, Rival-Gervier S, Boussouar A, Foerster AM, Rondier D et al. (2009) The D4Z4 macrosatellite repeat acts as a CTCF and A-type lamins-dependent insulator in facio-scapulo-humeral dystrophy. PLoS Genet 5: e1000394. PubMed: 19247430.
29. Wang G, Levy DD, Seidman MM, Glazer PM (1995) Targeted mutagenesis in mammalian cells mediated by intracellular triple helix formation. Mol Cell Biol 15: 1759-1768. PubMed: 7862165.
30. Geurts AM, Collier LS, Geurts JL, Oseth LL, Bell ML et al. (2006) Gene mutations and genomic rearrangements in the mouse as a result of transposon mobilization from chromosomal concatemers. PLoS Genet 2: e156. doi:10.1371/journal.pgen.0020156. PubMed: 17009875.
31. Urschitz J, Kawasumi M, Owens J, Morozumi K, Yamashiro H et al. (2010) Helper-independent piggyBac plasmids for gene delivery approaches: strategies for avoiding potential genotoxic effects. Proc Natl Acad Sci U S A 107: 8117-8122. doi:10.1073/pnas.1003674107. PubMed: 20404201.
32. Suganuma R, Pelczar P, Spetz JF, Hohn B, Yanagimachi R et al. (2005) Tn5 transposase-mediated mouse transgenesis. Biol Reprod 73: 1157-1163. doi:10.1095/biolreprod.105.044669. PubMed: 16079303.
33. Sumiyama K, Kawakami K, Yagita K (2010) Simple and highly efficient transgenesis method in mice with the Tol2 transposon system and cytoplasmic microinjection. Genomics 95: 306-311. doi:10.1016/ j.ygeno.2010.02.006. PubMed: 20219670.
34. Yang E, van Nimwegen E, Zavolan M, Rajewsky N, Schroeder M et al. (2003) Decay rates of human mRNAs:correlation with functional characteristics and sequence attributes. Genome Res 13: 1863-1872. PubMed: 12902380.
35. Bire S, Gosset D, Jégot G, Midoux P, Pichon C et al. (2013) Exogenous mRNA delivery and bioavailability in gene transfer mediated by piggyBac transposition. BMC Biotechnol 13: 75. doi: 10.1186/1472-6750-13-75. PubMed: 24070093.
36. Buzdin A, Gogvadze E, Kovalskaya E, Volchkov P, Ustyugova S et al. (2003) The human genome contains many types of chimeric retrogenes generated through in vivo RNA recombination. Nucleic Acids Res 31: 4385-4390. doi:10.1093/nar/ gkg496. PubMed: 12888497.
37. Steiniger M, Adams CD, Marko JF, Reznikoff WS (2006) Defining characteristics of Tn5 Transposase non-specific DNA binding. Nucleic Acids Res 34: 2820-2832. doi:10.1093/nar/gkl179. PubMed: 16717287.
38. Mousnier A, Kubat N, Massias-Simon A, Ségéral E, Rain JC et al. (2007) von Hippel Lindau binding protein 1-mediated degradation of integrase affects HIV-1 gene expression at a postintegration step. Proc Natl Acad Sci U S A 104: 13615-13620. doi:10.1073/pnas.0705162104. PubMed: 17698809.
39. Liu J, Skjørringe T, Gjetting T, Jensen TG (2009) PhiC31 integrase induces a DNA damage response and chromosomal rearrangements in human adult fibroblasts. BMC Biotechnol 9: 31. doi: 10.1186/1472-6750-9-31. PubMed: 19341467.
40. Meir YJ, Weirauch MT, Yang HS, Chung PC, Yu RK et al. (2011) Genome-wide target profiling of piggyBac and Tol2 in HEK 293:pros and cons for gene discovery and gene therapy. BMC Biotechnol 11: 28. doi:10.1186/1472-6750-11-28. PubMed: 21447194.
41. Bire S, Rouleux-Bonnin F (2013) Transgene site specific integration: problems and solutions. In: S RenaultP Duchateau. Topics in Current Genetics. Netherlands: Springer. pp. 3-39.
42. Hollister JD, Gaut BS (2009) Epigenetic silencing of transposable elements:a trade-off between reduced transposition and deleterious effects on neighboring gene expression. Genome Res 19: 1419-1428. doi:10.1101/gr.091678. 109. PubMed: 19478138.