A piggyBac transposon- and gateway-enhanced system for efficient BAC transgenesis

Developmental Dynamics

Volumn 243, Issue 9, 2014, Pages 1086-1094

  Zhao, Liang ^a   Ng, Ee Ting ^a   Koopman, Peter ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Heart development; Kidney development; Sex determination; Testis development; Transgenic mice; Wt1

Indexed keywords

GENOMIC DNA; MESSENGER RNA; TRANSPOSASE; WT1 PROTEIN; TRANSPOSON;

ANIMAL EXPERIMENT; ARTICLE; BACTERIAL ARTIFICIAL CHROMOSOME; DNA TRANSPOSITION; EMBRYO; GATEWAY ENHANCED SYSTEM; GENE EXPRESSION; GENE TRANSFER; GENE VECTOR; GENETIC ENGINEERING; GENETIC RECOMBINATION; GENOTYPE; IN VITRO STUDY; MOUSE; NONHUMAN; PIGGYBAC TRANSPOSASE; PRIORITY JOURNAL; TRANSGENICS; TRANSPOSON; ANIMAL; MICROINJECTION; TRANSGENE; TRANSGENIC MOUSE;

ANIMALS; DNA TRANSPOSABLE ELEMENTS; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; MICE; MICE, TRANSGENIC; MICROINJECTIONS; TRANSGENES;

EID: 84906313434     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.24153     Document Type: Article

References (50)

1. Armstrong JF, Pritchard-Jones K, Bickmore WA, Hastie ND, Bard JB. 1993. The expression of the Wilms' tumour gene, WT1, in the developing mammalian embryo. Mech Dev 40:85-97.
2. Bai DP, Yang MM, Chen YL. 2012. PiggyBac transposon-mediated gene transfer in Cashmere goat fetal fibroblast cells. Biosci Biotechnol Biochem 76:933-937.
3. Bowles J, Cooper L, Berkman J, Koopman P. 1999. Sry requires a CAG repeat domain for male sex determination in Mus musculus. Nat Genet 22:405-408.
4. Carbery ID, Ji D, Harrington A, Brown V, Weinstein EJ, Liaw L, Cui X. 2010. Targeted genome modification in mice using zinc-finger nucleases. Genetics 186:451-459.
5. Chandler K, Chandler R, Broeckelmann E, Hou Y, Southard-Smith EM, Mortlock D. 2007. Relevance of BAC transgene copy number in mice: transgene copy number variation across multiple transgenic lines and correlations with transgene integrity and expression. Mamm Genome 18:693-708.
6. Copeland NG, Jenkins NA, Court DL. 2001. Recombineering: a powerful new tool for mouse functional genomics. Nat Rev Genet 2:769-779.
7. Devon RS, Porteous DJ, Brookes AJ. 1995. Splinkerettes-improved vectorettes for greater efficiency in PCR walking. Nucleic Acids Res 23:1644-1645.
8. 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.
9. Dorer D. 1997. Do transgene arrays form heterochromatin in vertebrates? Transgenic Res 6:3-10.
10. Dupuy AJ, Clark K, Carlson CM, Fritz S, Davidson AE, Markley KM, Finley K, Fletcher CF, Ekker SC, Hackett PB, Horn S, Largaespada DA. 2002. Mammalian germ-line transgenesis by transposition. Proc Natl Acad Sci U S A 99:4495-4499.
11. 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.
12. Frengen E, Weichenhan D, Zhao B, Osoegawa K, van Geel M, de Jong PJ. 1999. A modular, positive selection bacterial artificial chromosome vector with multiple cloning sites. Genomics 58:250-253.
13. Furushima K, Jang CW, Chen DW, Xiao N, Overbeek PA, Behringer RR. 2012. Insertional mutagenesis by a hybrid piggyBac and sleeping beauty transposon in the rat. Genetics 192:1235-1248.
14. Giraldo P, Montoliu L. 2001. Size matters: use of YACs, BACs and PACs in transgenic animals. Transgenic Res 10:83-103.
15. Gong S, Zheng C, Doughty ML, Losos K, Didkovsky N, Schambra UB, Nowak NJ, Joyner A, Leblanc G, Hatten ME, Heintz N. 2003. A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 425:917-925.
16. Inoue T, Inoue YU, Asami J, Izumi H, Nakamura S, Krumlauf R. 2008. Analysis of mouse Cdh6 gene regulation by transgenesis of modified bacterial artificial chromosomes. Dev Biol 315:506-520.
17. Ivics Z, Izsvak Z. 2010. The expanding universe of transposon technologies for gene and cell engineering. Mob DNA 1:25.
18. Keuren M, Gavrilina G, Filipiak W, Zeidler M, Saunders T. 2009. Generating transgenic mice from bacterial artificial chromosomes: transgenesis efficiency, integration and expression outcomes. Transgenic Res 18:769-785.
19. Kreidberg JA, Sariola H, Loring JM, Maeda M, Pelletier J, Housman D, Jaenisch R. 1993. WT-1 is required for early kidney development. Cell 74:679-691.
20. Kunec D, van Haren S, Burgess SC, Hanson LA. 2009. A Gateway recombination herpesvirus cloning system with negative selection that produces vectorless progeny. J Virol Methods 155:82-86.
21. 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.
22. Li R, Zhuang Y, Han M, Xu T, Wu X. 2013. piggyBac as a high-capacity transgenesis and gene-therapy vector in human cells and mice. Dis Model Mech 6:828-833.
23. Li Y, Liu W, Oo TF, Wang L, Tang Y, Jackson-Lewis V, Zhou C, Geghman K, Bogdanov M, Przedborski S, Beal MF, Burke RE, Li C. 2009. Mutant LRRK2R1441G BAC transgenic mice recapitulate cardinal features of Parkinson's disease. Nat Neurosci 12:826-828.
24. Liu X, Li N, Hu X, Zhang R, Li Q, Cao D, Liu T, Zhang Y, Liu X. 2013. Efficient production of transgenic chickens based on piggyBac. Transgenic Res 22:417-423.
25. Marh J, Stoytcheva Z, Urschitz J, Sugawara A, Yamashiro H, Owens JB, Stoytchev I, Pelczar P, Yanagimachi R, Moisyadi S. 2012. Hyperactive self-inactivating piggyBac for transposase-enhanced pronuclear microinjection transgenesis. Proc Natl Acad Sci U S A 109:19184-19189.
26. Mates L, Chuah MKL, Belay E, Jerchow B, Manoj N, Acosta-Sanchez A, Grzela DP, Schmitt A, Becker K, Matrai J, Ma L, Samara-Kuko E, Gysemans C, Pryputniewicz D, Miskey C, Fletcher B, VandenDriessche T, Ivics Z, Izsvak Z. 2009. Molecular evolution of a novel hyperactive Sleeping Beauty transposase enables robust stable gene transfer in vertebrates. Nat Genet 41:753-761.
27. Matsuoka K, Saito M, Shibata K, Sekine M, Shitara H, Taya C, Zhang X, Takahashi TA, Kohno K, Kikkawa Y, Yonekawa H. 2013. Generation of mouse models for type 1 diabetes by selective depletion of pancreatic beta cells using toxin receptor-mediated cell knockout. Biochem Biophys Res Commun 436:400-405.
28. Nel-Themaat L, Jang C-W, Stewart MD, Akiyama H, Viger RS, Behringer RR. 2011. Sertoli cell behaviors in developing testis cords and postnatal seminiferous tubules of the mouse. Biol Reprod 84:342-350.
29. Osterwalder M, Galli A, Rosen B, Skarnes WC, Zeller R, Lopez-Rios J. 2010. Dual RMCE for efficient re-engineering of mouse mutant alleles. Nat Methods 7:893-895.
30. Polanco JC, Wilhelm D, Davidson T-L, Knight D, Koopman P. 2010. Sox10 gain-of-function causes XX sex reversal in mice: implications for human 22q-linked disorders of sex development. Hum Mol Genet 19:506-516.
31. Rostovskaya M, Fu J, Obst M, Baer I, Weidlich S, Wang H, Smith AJH, Anastassiadis K, Stewart AF. 2012. Transposon-mediated BAC transgenesis in human ES cells. Nucleic Acids Res 40:e150.
32. Rostovskaya M, Naumann R, Fu J, Obst M, Mueller D, Stewart AF, Anastassiadis K. 2013. Transposon mediated BAC transgenesis via pronuclear injection of mouse zygotes. Genesis 51:135-141.
33. Schmeisser F, Weir J. 2007. Incorporation of a lambda phage recombination system and EGFP detection to simplify mutagenesis of Herpes simplex virus bacterial artificial chromosomes. BMC Biotechnol 7:22.
34. Sekido R, Lovell-Badge R. 2008. Sex determination involves synergistic action of SRY and SF1 on a specific Sox9 enhancer. Nature 453:930-934.
35. Sharan SK, Thomason LC, Kuznetsov SG, Court DL. 2009. Recombineering: a homologous recombination-based method of genetic engineering. Nat Protoc 4:206-223.
36. Sumiyama K, Kawakami K, Yagita K. 2010. A simple and highly efficient transgenesis method in mice with the Tol2 transposon system and cytoplasmic microinjection. Genomics 95:306-311.
37. Suster M, Sumiyama K, Kawakami K. 2009. Transposon-mediated BAC transgenesis in zebrafish and mice. BMC Genomics 10:477.
38. Suster ML, Abe G, Schouw A, Kawakami K. 2011. Transposon-mediated BAC transgenesis in zebrafish. Nat Protocols 6:1998-2021.
39. Svingen T, Spiller CM, Kashimada K, Harley VR, Koopman P. 2009. Identification of suitable normalizing genes for quantitative real-time RT-PCR analysis of gene expression in fetal mouse gonads. Sex Dev 3:194-204.
40. Vidal VPI, Chaboissier M-C, de Rooij DG, Schedl A. 2001. Sox9 induces testis development in XX transgenic mice. Nat Genet 28:216-217.
41. Wainwright EN, Jorgensen JS, Kim Y, Truong V, Bagheri-Fam S, Davidson T, Svingen T, Fernandez-Valverde SL, McClelland KS, Taft RJ, Harley VR, Koopman P, Wilhelm D. 2013. SOX9 regulates microRNA miR-202-5p/3p expression during mouse testis differentiation. Biol Reprod 89:34.
42. Walhout AJ, Temple GF, Brasch MA, Hartley JL, Lorson MA, van den Heuvel S, Vidal M. 2000. GATEWAY recombinational cloning: application to the cloning of large numbers of open reading frames or ORFeomes. Methods Enzymol 328:575-592.
43. Wang H, Yang H, Shivalila Chikdu S, Dawlaty Meelad M, Cheng Albert W, Zhang F, Jaenisch R. 2013. One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell 153:910-918.
44. Warming SR, Costantino N, Court DL, Jenkins NA, Copeland NG. 2005. Simple and highly efficient BAC recombineering using galK selection. Nucleic Acids Res 33:e36.
45. Wefers B, Meyer M, Ortiz O, Hrabé de Angelis M, Hansen J, Wurst W, Kühn R. 2013. Direct production of mouse disease models by embryo microinjection of TALENs and oligodeoxynucleotides. Proc Natl Acad Sci U S A 110:3782-3787.
46. Wolfe D, Craft AM, Cohen JB, Glorioso JC. 2010. A herpes simplex virus vector system for expression of complex cellular cDNA libraries. J Virol 84:7360-7368.
47. Wu Z, Xu Z, Zou X, Zeng F, Shi J, Liu D, Urschitz J, Moisyadi S, Li Z. 2013. Pig transgenesis by piggyBac transposition in combination with somatic cell nuclear transfer. Transgenic Res 22:1107-1118.
48. 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.
49. 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.
50. Zeng C, Kouprina N, Zhu B, Cairo A, Hoek M, Cross G, Osoegawa K, Larionov V, de Jong P. 2001. Large-Insert BAC/YAC Libraries for Selective Re-isolation of Genomic Regions by Homologous Recombination in Yeast. Genomics 77:27-34.