The piggybac transposon displays local and distant reintegration preferences and can cause mutations at noncanonical integration sites

Molecular and Cellular Biology

Volumn 33, Issue 7, 2013, Pages 1317-1330

  Li, Meng Amy ^a,b   Pettitt, Stephen J ^a,c   Eckert, Sabine ^a   Ning, Zemin ^a   Rice, Stephen ^a   Cadiñanos, Juan ^a,d   Yusa, Kosuke ^a   Conte, Nathalie ^a   Bradley, Allan ^a  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b Berkeley   (United States)

^c INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^d Instituto de Medicina Oncologica y Molecular de Asturias   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; CELL REGENERATION; CHROMATIN STRUCTURE; CONTROLLED STUDY; DNA FLANKING REGION; DNA SEQUENCE; DNA TRANSPOSITION; EMBRYONIC STEM CELL; GENE EXPRESSION; GENE FREQUENCY; GENE INSERTION; GENE INSERTION SEQUENCE; GENE LOCUS; GENOME; HETEROCHROMATIN; HOST CELL; MOUSE; NONHUMAN; PLASMID; POINT MUTATION; PRIORITY JOURNAL; TRANSPOSON;

ANIMALS; CELLS, CULTURED; CHROMATIN; DNA TRANSPOSABLE ELEMENTS; EMBRYONIC STEM CELLS; GENETIC LOCI; GENOME; MICE; MUTAGENESIS, INSERTIONAL; PLASMIDS; POINT MUTATION;

EID: 84875260104     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00670-12     Document Type: Article

References (46)

1. Ivics Z, Hackett PB, Plasterk RH, Izsvàk Z. 1997. Molecular reconstruction of Sleeping Beauty, a Tc1-like transposon from fish, and its transposition in human cells. Cell 91:501-510.
2. Fraser MJ, Ciszczon T, Elick T, Bauser C. 1996. Precise excision of TTAA-specific lepidopteran transposons piggyBac (IFP2) and tagalong (TFP3) from the baculovirus genome in cell lines from two species of Lepidoptera. Insect Mol. Biol. 5:141-151.
3. Ding S, Wu X, Li G, Han M, Zhuang Y, Xu T. 2005. Efficient transposition of the piggyBac (PB) transposon in mammalian cells and mice. Cell 122:473-483.
4. Li MA, Turner DJ, Ning Z, Yusa K, Liang Q, Eckert S, Rad L, Fitzgerald TW, Craig NL, Bradley A. 2011. Mobilization of giant piggyBac transposons in the mouse genome. Nucleic Acids Res. 39:e148. doi:10.1093/nar /gkr764.
5. Cadiñanos J, Bradley A. 2007. Generation of an inducible and optimized piggyBac transposon system. Nucleic Acids Res. 35:e87. doi:10.1093/nar /gkm446.
6. Maragathavally KJ. 2006. Chimeric MosI and piggyBac transposases result in site-directed integration. FASEB J. 20:1880-1882.
7. Woltjen K, Michael IP, Mohseni P, Desai R, Mileikovsky M, Hämäläinen R, Cowling R, Wang W, Liu P, Gertsenstein M, Kaji K, Sung H-K, Nagy A. 2009. piggyBac transposition reprograms fibroblasts to induced pluripotent stem cells. Nature 458:766-770.
8. Yusa K, Rad R, Takeda J, Bradley A. 2009. Generation of transgene-free induced pluripotent mouse stem cells by the piggyBac transposon. Nat. Methods 6:363-369.
9. Ivics Z, Li MA, Mátés L, Boeke JD, Nagy A, Bradley A, Izsvàk Z. 2009. Transposon-mediated genome manipulation in vertebrates. Nat. Methods 6:415-422.
10. Bouwman P, Aly A, Escandell JM, Pieterse M, Bartkova J, Gulden H, Hiddingh S, Thanasoula M, Kulkarni A, Yang Q, Haffty BG, Tommiska J, Blomqvist C, Drapkin R, Adams DJ, Nevanlinna H, Bartek J, Tarsounas M, Ganesan S, Jonkers J. 2010. 53BP1 loss rescues BRCA1 deficiency and is associated with triple-negative and BRCA-mutated breast cancers. Nat. Struct. Mol. Biol. 17:688-695.
11. Guo G, Huang Y, Humphreys P, Wang X, Smith A. 2011. A piggyBacbased recessive screening method to identify pluripotency regulators. PLoS One 6:e18189. doi:10.1371/journal.pone.0018189.
12. Huang Y, Pettitt SJ, Guo G, Liu G, Li MA, Yang F, Bradley A. 2012. Isolation of homozygous mutant mouse embryonic stem cells using a dual selection system. Nucleic Acids Res. 40:e21. doi:10.1093/nar/gkr908.
13. Kong J, Wang F, Brenton JD, Adams DJ. 2010. Slingshot: a piggyBac based transposon system for tamoxifen-inducible 'self-inactivating' insertional mutagenesis. Nucleic Acids Res. 38:e173. doi:10.1093/nar/gkq658.
14. Li MA, Pettitt SJ, Yusa K, Bradley A. 2010. Genome-wide forward genetic screens in mouse ES cells. Methods Enzymol. 477:217-242.
15. Rad R, Rad L, Wang W, Cadiñanos J, Vassiliou Rice S, Campos LS, Yusa K, Banerjee R, Li MA, de la Rosa J, Strong A, Lu D, Ellis P, Conte N, Yang FT, Liu P, Bradley A. 2010. PiggyBac transposon mutagenesis: a tool for cancer gene discovery in mice. Science 330:1104-1107.
16. Wang W, Bradley A. 2007. A recessive genetic screen for host factors required for retroviral infection in a library of insertionally mutated Blmdeficient embryonic stem cells. Genome Biol. 8:R48. doi:10.1186/gb-2007-8-4-r48.
17. Liang Q, Kong J, Stalker J, Bradley A. 2009. Chromosomal mobilization and reintegration of Sleeping Beauty and piggyBac transposons. Genesis 47:404-408.
18. Wang W, Lin C, Lu D, Ning Z, Cox T, Melvin D, Wang X, Bradley A, Liu P. 2008. Chromosomal transposition of piggyBac in mouse embryonic stem cells. Proc. Natl. Acad. Sci. U. S. A. 105:9290-9295.
19. Meir Y, Weirauch M, Yang H, Chung P, Yu R, Wu S. 2011. Genomewide 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.
20. Wang H, Mayhew D, Chen X, Johnston M, Mitra RD. 2012. "Calling cards" for DNA-binding proteins in mammalian cells. Genetics 190:941-949.
21. van der Weyden L, Adams DJ, Harris LW, Tannahill D, Arends MJ, Bradley A. 2005. Null and conditional semaphorin 3B alleles using a flexible puroDeltatk loxP/FRT vector. Genesis 41:171-178.
22. Ramírez-Solis R, Davis AC, Bradley A. 1993. Gene targeting in embryonic stem cells. Methods Enzymol. 225:855-878.
23. Guo G, Wang W, Bradley A. 2004. Mismatch repair genes identified using genetic screens in Blm-deficient embryonic stem cells. Nature 429: 891-895.
24. Pettitt SJ, Liang Q, Rairdan XY, Moran JL, Prosser HM, Beier DR, Lloyd KC, Bradley A, Skarnes WC. 2009. Agouti C57BL/6N embryonic stem cells for mouse genetic resources. Nat. Methods 6:493-495.
25. 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.
26. Ning Z, Cox AJ, Mullikin JC. 2001. SSAHA: a fast search method for large DNA databases. Genome Res. 11:1725-1729.
27. Dixon JR, Selvaraj S, Yue F, Kim A, Li Y, Shen Y, Hu M, Liu JS, Ren B. 2012. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485:376-380.
28. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, Alvarez P, Brockman W, Kim T, Koche RP, Lee W, Mendenhall E, O'Donovan A, Presser A, Russ C, Xie X, Meissner A, Wernig M, Jaenisch R, Nusbaum C, Lander ES, Bernstein BE. 2007. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448:553-560.
29. Peric-Hupkes D, Meuleman W, Pagie L, Bruggeman SWM, Solovei I, Brugman W, Gräf S, Flicek P, Kerkhoven RM, van Lohuizen M, Reinders M, Wessels L, van Steensel B. 2010. Molecular maps of the reorganization of genome-nuclear lamina interactions during differentiation. Mol. Cell 38:603-613.
30. Marson A, Levine SS, Cole MF, Frampton GM, Brambrink T, Johnstone S, Guenther MG, Johnston WK, Wernig M, Newman J, Calabrese JM, Dennis LM, Volkert TL, Gupta S, Love J, Hannett N, Sharp PA, Bartel DP, Jaenisch R, Young RA. 2008. Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells. Cell 134:521-533.
31. Hiratani I, Ryba T, Itoh M, Yokochi T, Schwaiger M, Chang C-W, Lyou Y, Townes TM, Schübeler D, Gilbert DM. 2008. Global reorganization of replication domains during embryonic stem cell differentiation. PLoS Biol. 6:e245. doi:10.1371/journal.pbio.0060245.
32. Olshen AB, Venkatraman ES, Lucito R, Wigler M. 2004. Circular binary segmentation for the analysis of array-based DNA copy number data. Biostatistics 5:557-572.
33. Tang F, Barbacioru C, Bao S, Lee C, Nordman E, Wang X, Lao K, Surani MA. 2010. Tracing the derivation of embryonic stem cells from the inner cell mass by single-cell RNA-Seq analysis. Cell Stem Cell 6:468-478.
34. Down TA. 2005. NestedMICA: sensitive inference of over-represented motifs in nucleic acid sequence. Nucleic Acids Res. 33:1445-1453.
35. Feil R, Wagner J, Metzger D, Chambon P. 1997. Regulation of Cre recombinase activity by mutated estrogen receptor ligand-binding domains. Biochem. Biophys. Res. Commun. 237:752-757.
36. Gilbert DM. 2002. Replication timing and transcriptional control: beyond cause and effect. Curr. Opin. Cell Biol. 14:377-383.
37. Mitra R, Fain-Thornton J, Craig NL. 2008. piggyBac can bypass DNA synthesis during cut and paste transposition. EMBO J. 27:1097-1109.
38. Abuin A, Zhang H, Bradley A. 2000. Genetic analysis of mouse embry-onic stem cells bearing Msh3 and Msh2 single and compound mutations. Mol. Cell. Biol. 20:149-157.
39. Bellen HJ, Levis RW, He Y, Carlson JW, Evans-Holm M, Bae E, Kim J, Metaxakis A, Savakis C, Schulze KL, Hoskins RA, Spradling AC. 2011. The Drosophila gene disruption project: progress using transposons with distinctive site specificities. Genetics 188:731-743.
40. Bellen HJ, Levis RW, Liao G, He Y, Carlson JW, Tsang G, Evans-Holm M, Hiesinger PR, Schulze KL, Rubin GM, Hoskins RA, Spradling AC. 2004. The BDGP gene disruption project: single transposon insertions associated with 40% of Drosophila genes. Genetics 167:761-781.
41. Ikeda R, Kokubu C, Yusa K, Keng VW, Horie K, Takeda J. 2007. Sleeping Beauty transposase has an affinity for heterochromatin conformation. Mol. Cell. Biol. 27:1665-1676.
42. Ma Y, Pannicke U, Schwarz K, Lieber MR. 2002. Hairpin opening and overhang processing by an Artemis/DNA-dependent protein kinase complex in nonhomologous end joining and V(D)J recombination. Cell 108: 781-794.
43. Wiebauer K, Jiricny J. 1990. Mismatch-specific thymine DNA glycosylase andDNApolymerase beta mediate the correction ofG.Tmispairs in nuclear extracts from human cells. Proc. Natl. Acad. Sci. U. S. A. 87:5842-5845.
44. Brown TC, Jiricny J. 1988. Different base/base mispairs are corrected with different efficiencies and specificities in monkey kidney cells. Cell 54:705-711.
45. Tichy ED, Liang L, Deng L, Tischfield J, Schwemberger S, Babcock G, Stambrook PJ. 2011. Mismatch and base excision repair proficiency in murine embryonic stem cells. DNA Repair 10:445-451.
46. Hansen G, Markesich D, Burnett M, Zhu Q, Dionne K, Richter L, Finnell R, Sands A, Zambrowicz B, Abuin A. 2008. Large-scale gene trapping in C57BL/6N mouse embryonic stem cells. Genome Res. 18:1670-1679.