Sleeping Beauty Transposon System: Comparison
Please note this is a comparison between Version 2 by Vivi Li and Version 1 by Matthias Thomas Ochmann.

Sleeping Beauty

 (SB) is a transposon system that has been widely used as a genetic engineering tool. Central to the development of any transposon as a research tool is the ability to integrate a foreign piece of DNA into the cellular genome. Driven by the need for efficient transposon-based gene vector systems, extensive studies have largely elucidated the molecular actors and actions taking place during SB transposition. Close transposon relatives and other recombination enzymes, including retroviral integrases, have served as useful models to infer functional information relevant to SB. Recently obtained structural data on the SB transposase enable a direct insight into the workings of this enzyme. These efforts cumulatively allowed the development of novel variants of SB that offer advanced possibilities for genetic engineering due to their hyperactivity, integration deficiency, or targeting capacity. However, many aspects of the process of transposition remain poorly understood and require further investigation. We anticipate that continued investigations into the structure–function relationships of SB transposition will enable the development of new generations of transposition-based vector systems, thereby facilitating the use of SB in preclinical studies and clinical trials.

  • transposon
  • strand transfer
  • excision
  • synaptic complex
  • DNA repair
  • integration
  • DNA binding
  • crystal structure
  • transposase
  • DNA recombination
Please wait, diff process is still running!

References

  1. Seelamgari, A.; Maddukuri, A.; Berro, R.; de La Fuente, C.; Kehn, K.; Deng, L.; Dadgar, S.; Bottazzi, M.E.; Ghedin, E.; Pumfery, A.; et al. Role of viral regulatory and accessory proteins in HIV-1 replication. Front. Biosci. 2004, 9, 2388–2413.
  2. Frankel, A.D.; Young, J.A. HIV-1: Fifteen proteins and an RNA. Annu. Rev. Biochem. 1998, 67, 1–25.
  3. Bannert, N.; Kurth, R. The evolutionary dynamics of human endogenous retroviral families. Annu. Rev. Genom. Hum. Genet. 2006, 7, 149–173.
  4. Jasin, M.; Rothstein, R. Repair of strand breaks by homologous recombination. Cold Spring Harb. Perspect. Biol. 2013, 5, a012740.
  5. McClintock, B. Induction of Instability at Selected Loci in Maize. Genetics 1953, 38, 579–599.
  6. Wicker, T.; Sabot, F.; Hua-Van, A.; Bennetzen, J.L.; Capy, P.; Chalhoub, B.; Flavell, A.; Leroy, P.; Morgante, M.; Panaud, O.; et al. A unified classification system for eukaryotic transposable elements. Nat. Rev. Genet. 2007, 8, 973–982.
  7. Beck, C.R.; Garcia-Perez, J.L.; Badge, R.M.; Moran, J.V. LINE-1 elements in structural variation and disease. Annu. Rev. Genomics Hum. Genet. 2011, 12, 187–215.
  8. Deininger, P. Alu elements: Know the SINEs. Genome Biol. 2011, 12, 236.
  9. Kapitonov, V.V.; Jurka, J. RAG1 core and V(D)J recombination signal sequences were derived from Transib transposons. PLoS Biol. 2005, 3, e181.
  10. Kapitonov, V.V.; Jurka, J. Rolling-circle transposons in eukaryotes. Proc. Natl. Acad. Sci. USA 2001, 98, 8714–8719.
  11. Sarkar, A.; Sim, C.; Hong, Y.S.; Hogan, J.R.; Fraser, M.J.; Robertson, H.M.; Collins, F.H. Molecular evolutionary analysis of the widespread piggyBac transposon family and related “domesticated” sequences. Mol. Genet. Genom. 2003, 270, 173–180.
  12. Jurka, J.; Kapitonov, V.V. PIFs meet Tourists and Harbingers: A superfamily reunion. Proc. Natl. Acad. Sci. USA 2001, 98, 12315–12316.
  13. Shao, H.; Tu, Z. Expanding the diversity of the IS630-Tc1-mariner superfamily: Discovery of a unique DD37E transposon and reclassification of the DD37D and DD39D transposons. Genetics 2001, 159, 1103–1115.
  14. Ivics, Z.; Hackett, P.B.; Plasterk, R.H.; Izsvák, Z. Molecular Reconstruction of Sleeping Beauty, a Tc1-like Transposon from Fish, and Its Transposition in Human Cells. Cell 1997, 91, 501–510.
  15. Amberger, M.; Ivics, Z. Latest Advances for the Sleeping Beauty Transposon System: 23 Years of Insomnia but Prettier than Ever: Refinement and Recent Innovations of the Sleeping Beauty Transposon System Enabling Novel, Nonviral Genetic Engineering Applications. Bioessays 2020, 42, e2000136.
  16. Izsvák, Z.; Khare, D.; Behlke, J.; Heinemann, U.; Plasterk, R.H.; Ivics, Z. Involvement of a bifunctional, paired-like DNA-binding domain and a transpositional enhancer in Sleeping Beauty transposition. J. Biol. Chem. 2002, 277, 34581–34588.
  17. Pabo, C.O.; Sauer, R.T. Transcription factors: Structural families and principles of DNA recognition. Annu. Rev. Biochem. 1992, 61, 1053–1095.
  18. Czerny, T.; Schaffner, G.; Busslinger, M. DNA sequence recognition by Pax proteins: Bipartite structure of the paired domain and its binding site. Genes Dev. 1993, 7, 2048–2061.
  19. Brennan, R.G.; Matthews, B.W. The helix-turn-helix DNA binding motif. J. Biol. Chem. 1989, 264, 1903–1906.
  20. Aravind, L.; Anantharaman, V.; Balaji, S.; Babu, M.M.; Iyer, L.M. The many faces of the helix-turn-helix domain: Transcription regulation and beyond. FEMS Microbiol. Rev. 2005, 29, 231–262.
  21. Konnova, T.A.; Singer, C.M.; Nesmelova, I.V. NMR solution structure of the RED subdomain of the Sleeping Beauty transposase. Protein Sci. 2017, 26, 1171–1181.
  22. Carpentier, C.E.; Schreifels, J.M.; Aronovich, E.L.; Carlson, D.F.; Hackett, P.B.; Nesmelova, I.V. NMR structural analysis of Sleeping Beauty transposase binding to DNA. Protein Sci. 2014, 23, 23–33.
  23. Voigt, F.; Wiedemann, L.; Zuliani, C.; Querques, I.; Sebe, A.; Mátés, L.; Izsvák, Z.; Ivics, Z.; Barabas, O. Sleeping Beauty transposase structure allows rational design of hyperactive variants for genetic engineering. Nat. Commun. 2016, 7, 11126.
  24. Hickman, A.B.; Chandler, M.; Dyda, F. Integrating prokaryotes and eukaryotes: DNA transposases in light of structure. Crit. Rev. Biochem. Mol. Biol. 2010, 45, 50–69.
  25. Rice, P.A.; Baker, T.A. Comparative architecture of transposase and integrase complexes. Nat. Struct Biol. 2001, 8, 302–307.
  26. Montaño, S.P.; Rice, P.A. Moving DNA around: DNA transposition and retroviral integration. Curr. Opin. Struct. Biol. 2011, 21, 370–378.
  27. Yang, W.; Lee, J.Y.; Nowotny, M. Making and breaking nucleic acids: Two-Mg2+-ion catalysis and substrate specificity. Mol. Cell 2006, 22, 5–13.
  28. Cui, Z.; Geurts, A.M.; Liu, G.; Kaufman, C.D.; Hackett, P.B. Structure–Function Analysis of the Inverted Terminal Repeats of the Sleeping Beauty Transposon. J. Mol. Biol. 2002, 318, 1221–1235.
  29. Liu, G.; Aronovich, E.L.; Cui, Z.; Whitley, C.B.; Hackett, P.B. Excision of Sleeping Beauty transposons: Parameters and applications to gene therapy. J. Gene Med. 2004, 6, 574–583.
  30. Zayed, H.; Izsvák, Z.; Walisko, O.; Ivics, Z. Development of hyperactive sleeping beauty transposon vectors by mutational analysis. Mol. Ther. 2004, 9, 292–304.
  31. Geurts, A.M.; Yang, Y.; Clark, K.J.; Liu, G.; Cui, Z.; Dupuy, A.J.; Bell, J.B.; Largaespada, D.A.; Hackett, P.B. Gene transfer into genomes of human cells by the sleeping beauty transposon system. Mol. Ther. 2003, 8, 108–117.
  32. Walisko, O.; Schorn, A.; Rolfs, F.; Devaraj, A.; Miskey, C.; Izsvák, Z.; Ivics, Z. Transcriptional activities of the Sleeping Beauty transposon and shielding its genetic cargo with insulators. Mol. Ther. 2008, 16, 359–369.
  33. Moldt, B.; Yant, S.R.; Andersen, P.R.; Kay, M.A.; Mikkelsen, J.G. Cis-acting gene regulatory activities in the terminal regions of sleeping beauty DNA transposon-based vectors. Hum. Gene Ther. 2007, 18, 1193–1204.
  34. Izsvák, Z.; Ivics, Z.; Plasterk, R.H. Sleeping Beauty, a wide host-range transposon vector for genetic transformation in vertebrates. J. Mol. Biol. 2000, 302, 93–102.
  35. Zayed, H.; Izsvák, Z.; Khare, D.; Heinemann, U.; Ivics, Z. The DNA-bending protein HMGB1 is a cellular cofactor of Sleeping Beauty transposition. Nucleic Acids Res. 2003, 31, 2313–2322.
  36. Wang, Y.; Pryputniewicz-Dobrinska, D.; Nagy, E.É.; Kaufman, C.D.; Singh, M.; Yant, S.; Wang, J.; Dalda, A.; Kay, M.A.; Ivics, Z.; et al. Regulated complex assembly safeguards the fidelity of Sleeping Beauty transposition. Nucleic Acids Res. 2017, 45, 311–326.
  37. Richardson, J.M.; Colloms, S.D.; Finnegan, D.J.; Walkinshaw, M.D. Molecular architecture of the Mos1 paired-end complex: The structural basis of DNA transposition in a eukaryote. Cell 2009, 138, 1096–1108.
  38. Watkins, S.; van Pouderoyen, G.; Sixma, T.K. Structural analysis of the bipartite DNA-binding domain of Tc3 transposase bound to transposon DNA. Nucleic Acids Res. 2004, 32, 4306–4312.
  39. Bouuaert, C.C.; Liu, D.; Chalmers, R. A simple topological filter in a eukaryotic transposon as a mechanism to suppress genome instability. Mol. Cell. Biol. 2011, 31, 317–327.
  40. Wang, Y.; Wang, J.; Devaraj, A.; Singh, M.; Jimenez Orgaz, A.; Chen, J.-X.; Selbach, M.; Ivics, Z.; Izsvák, Z. Suicidal autointegration of sleeping beauty and piggyBac transposons in eukaryotic cells. PLoS Genet. 2014, 10, e1004103.
  41. West, R.B.; Lieber, M.R. The RAG-HMG1 complex enforces the 12/23 rule of V(D)J recombination specifically at the double-hairpin formation step. Mol. Cell. Biol. 1998, 18, 6408–6415.
  42. Van Gent, D.C.; Hiom, K.; Paull, T.T.; Gellert, M. Stimulation of V(D)J cleavage by high mobility group proteins. EMBO J. 1997, 16, 2665–2670.
  43. Agrawal, A.; Eastman, Q.M.; Schatz, D.G. Transposition mediated by RAG1 and RAG2 and its implications for the evolution of the immune system. Nature 1998, 394, 744–751.
  44. Jones, J.M.; Gellert, M. Ordered assembly of the V(D)J synaptic complex ensures accurate recombination. EMBO J. 2002, 21, 4162–4171.
  45. Mizuuchi, K. Polynucleotidyl transfer reactions in transpositional DNA recombination. J. Biol. Chem. 1992, 267, 21273–21276.
  46. Craig, N.L. Unity in transposition reactions. Science 1995, 270, 253–254.
  47. Hickman, A.B.; Dyda, F. Mechanisms of DNA Transposition. Microbiol. Spectr. 2015, 3, 531–553.
  48. Hencken, C.G.; Li, X.; Craig, N.L. Functional characterization of an active Rag-like transposase. Nat. Struct. Mol. Biol. 2012, 19, 834–836.
  49. Zhou, L.; Mitra, R.; Atkinson, P.W.; Hickman, A.B.; Dyda, F.; Craig, N.L. Transposition of hAT elements links transposable elements and V(D)J recombination. Nature 2004, 432, 995–1001.
  50. Mitra, R.; Fain-Thornton, J.; Craig, N.L. piggyBac can bypass DNA synthesis during cut and paste transposition. EMBO J. 2008, 27, 1097–1109.
  51. Bischerour, J.; Chalmers, R. Base flipping in tn10 transposition: An active flip and capture mechanism. PLoS ONE 2009, 4, e6201.
  52. Bischerour, J.; Lu, C.; Roth, D.B.; Chalmers, R. Base flipping in V(D)J recombination: Insights into the mechanism of hairpin formation, the 12/23 rule, and the coordination of double-strand breaks. Mol. Cell. Biol. 2009, 29, 5889–5899.
  53. Richardson, J.M.; Dawson, A.; O’Hagan, N.; Taylor, P.; Finnegan, D.J.; Walkinshaw, M.D. Mechanism of Mos1 transposition: Insights from structural analysis. EMBO J. 2006, 25, 1324–1334.
  54. Izsvák, Z.; Stüwe, E.E.; Fiedler, D.; Katzer, A.; Jeggo, P.A.; Ivics, Z. Healing the Wounds Inflicted by Sleeping Beauty Transposition by Double-Strand Break Repair in Mammalian Somatic Cells. Mol. Cell 2004, 13, 279–290.
  55. Claeys Bouuaert, C.; Chalmers, R. A single active site in the mariner transposase cleaves DNA strands of opposite polarity. Nucleic Acids Res. 2017, 45, 11467–11478.
  56. Dawson, A.; Finnegan, D.J. Excision of the Drosophila Mariner Transposon Mos1. Mol. Cell 2003, 11, 225–235.
  57. Miskey, C.; Papp, B.; Mátés, L.; Sinzelle, L.; Keller, H.; Izsvák, Z.; Ivics, Z. The ancient mariner sails again: Transposition of the human Hsmar1 element by a reconstructed transposase and activities of the SETMAR protein on transposon ends. Mol. Cell. Biol. 2007, 27, 4589–4600.
  58. Lampe, D.J.; Churchill, M.E.; Robertson, H.M. A purified mariner transposase is sufficient to mediate transposition in vitro. EMBO J. 1996, 15, 5470–5479.
  59. Lohe, A.R.; Timmons, C.; Beerman, I.; Lozovskaya, E.R.; Hartl, D.L. Self-inflicted wounds, template-directed gap repair and a recombination hotspot. Effects of the mariner transposase. Genetics 2000, 154, 647–656.
  60. Engels, W.R.; Johnson-Schlitz, D.M.; Eggleston, W.B.; Sved, J. High-frequency P element loss in Drosophila is homolog dependent. Cell 1990, 62, 515–525.
  61. Luo, G.; Ivics, Z.; Izsvák, Z.; Bradley, A. Chromosomal transposition of a Tc1/mariner-like element in mouse embryonic stem cells. Proc. Natl. Acad. Sci. USA 1998, 95, 10769–10773.
  62. Daniel, R.; Katz, R.A.; Skalka, A.M. A role for DNA-PK in retroviral DNA integration. Science 1999, 284, 644–647.
  63. Jackson, S.P.; Jeggo, P.A. DNA double-strand break repair and V(D)J recombination: Involvement of DNA-PK. Trends Biochem. Sci. 1995, 20, 412–415.
  64. Miskey, C.; Izsvák, Z.; Kawakami, K.; Ivics, Z. DNA transposons in vertebrate functional genomics. Cell. Mol. Life Sci. 2005, 62, 629–641.
  65. Yoder, J.A.; Walsh, C.P.; Bestor, T.H. Cytosine methylation and the ecology of intragenomic parasites. Trends Genet. 1997, 13, 335–340.
  66. Yusa, K.; Takeda, J.; Horie, K. Enhancement of Sleeping Beauty transposition by CpG methylation: Possible role of heterochromatin formation. Mol. Cell. Biol. 2004, 24, 4004–4018.
  67. Jursch, T.; Miskey, C.; Izsvák, Z.; Ivics, Z. Regulation of DNA transposition by CpG methylation and chromatin structure in human cells. Mob. DNA 2013, 4, 15.
  68. Li, X.; Ewis, H.; Hice, R.H.; Malani, N.; Parker, N.; Zhou, L.; Feschotte, C.; Bushman, F.D.; Atkinson, P.W.; Craig, N.L. A resurrected mammalian hAT transposable element and a closely related insect element are highly active in human cell culture. Proc. Natl. Acad. Sci. USA 2013, 110, E478–E487.
  69. Liu, G.; Geurts, A.M.; Yae, K.; Srinivasan, A.R.; Fahrenkrug, S.C.; Largaespada, D.A.; Takeda, J.; Horie, K.; Olson, W.K.; Hackett, P.B. Target-site preferences of Sleeping Beauty transposons. J. Mol. Biol. 2005, 346, 161–173.
  70. Voigt, K.; Gogol-Döring, A.; Miskey, C.; Chen, W.; Cathomen, T.; Izsvák, Z.; Ivics, Z. Retargeting sleeping beauty transposon insertions by engineered zinc finger DNA-binding domains. Mol. Ther. 2012, 20, 1852–1862.
  71. Moldt, B.; Miskey, C.; Staunstrup, N.H.; Gogol-Döring, A.; Bak, R.O.; Sharma, N.; Mátés, L.; Izsvák, Z.; Chen, W.; Ivics, Z.; et al. Comparative genomic integration profiling of Sleeping Beauty transposons mobilized with high efficacy from integrase-defective lentiviral vectors in primary human cells. Mol. Ther. 2011, 19, 1499–1510.
  72. de Jong, J.; Akhtar, W.; Badhai, J.; Rust, A.G.; Rad, R.; Hilkens, J.; Berns, A.; van Lohuizen, M.; Wessels, L.F.A.; de Ridder, J. Chromatin landscapes of retroviral and transposon integration profiles. PLoS Genet. 2014, 10, e1004250.
  73. Montaño, S.P.; Pigli, Y.Z.; Rice, P.A. The μ transpososome structure sheds light on DDE recombinase evolution. Nature 2012, 491, 413–417.
  74. Morris, E.R.; Grey, H.; McKenzie, G.; Jones, A.C.; Richardson, J.M. A bend, flip and trap mechanism for transposon integration. Elife 2016, 5.
  75. Passos, D.O.; Li, M.; Yang, R.; Rebensburg, S.V.; Ghirlando, R.; Jeon, Y.; Shkriabai, N.; Kvaratskhelia, M.; Craigie, R.; Lyumkis, D. Cryo-EM structures and atomic model of the HIV-1 strand transfer complex intasome. Science 2017, 355, 89–92.
  76. Yin, Z.; Shi, K.; Banerjee, S.; Pandey, K.K.; Bera, S.; Grandgenett, D.P.; Aihara, H. Crystal structure of the Rous sarcoma virus intasome. Nature 2016, 530, 362–366.
  77. Maertens, G.N.; Hare, S.; Cherepanov, P. The mechanism of retroviral integration from X-ray structures of its key intermediates. Nature 2010, 468, 326–329.
  78. Maskell, D.P.; Renault, L.; Serrao, E.; Lesbats, P.; Matadeen, R.; Hare, S.; Lindemann, D.; Engelman, A.N.; Costa, A.; Cherepanov, P. Structural basis for retroviral integration into nucleosomes. Nature 2015, 523, 366–369.
  79. Yanagihara, K.; Mizuuchi, K. Mismatch-targeted transposition of Mu: A new strategy to map genetic polymorphism. Proc. Natl. Acad. Sci. USA 2002, 99, 11317–11321.
  80. Fuller, J.R.; Rice, P.A. Target DNA bending by the Mu transpososome promotes careful transposition and prevents its reversal. Elife 2017, 6.
  81. Kuduvalli, P.N.; Rao, J.E.; Craig, N.L. Target DNA structure plays a critical role in Tn7 transposition. EMBO J. 2001, 20, 924–932.
  82. Pribil, P.A.; Haniford, D.B. Target DNA Bending is an Important Specificity Determinant in Target Site Selection in Tn10 Transposition. J. Mol. Biol. 2003, 330, 247–259.
  83. Benjamin, H.W.; Kleckner, N. Intramolecular transposition by Tn10. Cell 1989, 59, 373–383.
  84. Maxwell, A.; Craigie, R.; Mizuuchi, K. B protein of bacteriophage mu is an ATPase that preferentially stimulates intermolecular DNA strand transfer. Proc. Natl. Acad. Sci. USA 1987, 84, 699–703.
  85. Karsi, A.; Moav, B.; Hackett, P.; Liu, Z. Effects of insert size on transposition efficiency of the sleeping beauty transposon in mouse cells. Mar. Biotechnol. 2001, 3, 241–245.
  86. Lampe, D.J.; Grant, T.E.; Robertson, H.M. Factors affecting transposition of the Himar1 mariner transposon in vitro. Genetics 1998, 149, 179–187.
  87. Fischer, S.E.; van Luenen, H.G.; Plasterk, R.H. Cis requirements for transposition of Tc1-like transposons in C. elegans. Mol. Genet. Genom. 1999, 262, 268–274.
  88. Mansharamani, M.; Graham, D.R.M.; Monie, D.; Lee, K.K.; Hildreth, J.E.K.; Siliciano, R.F.; Wilson, K.L. Barrier-to-autointegration factor BAF binds p55 Gag and matrix and is a host component of human immunodeficiency virus type 1 virions. J. Virol. 2003, 77, 13084–13092.
  89. Suzuki, Y.; Craigie, R. Regulatory mechanisms by which barrier-to-autointegration factor blocks autointegration and stimulates intermolecular integration of Moloney murine leukemia virus preintegration complexes. J. Virol. 2002, 76, 12376–12380.
  90. Lee, M.S.; Craigie, R. A previously unidentified host protein protects retroviral DNA from autointegration. Proc. Natl. Acad. Sci. USA 1998, 95, 1528–1533.
  91. Lee, M.S.; Craigie, R. Protection of retroviral DNA from autointegration: Involvement of a cellular factor. Proc. Natl. Acad. Sci. USA 1994, 91, 9823–9827.
  92. Tower, J.; Karpen, G.H.; Craig, N.; Spradling, A.C. Preferential transposition of Drosophila P elements to nearby chromosomal sites. Genetics 1993, 133, 347–359.
  93. Ruf, S.; Symmons, O.; Uslu, V.V.; Dolle, D.; Hot, C.; Ettwiller, L.; Spitz, F. Large-scale analysis of the regulatory architecture of the mouse genome with a transposon-associated sensor. Nat. Genet. 2011, 43, 379–386.
  94. Dupuy, A.J.; Fritz, S.; Largaespada, D.A. Transposition and gene disruption in the male germline of the mouse. Genesis 2001, 30, 82–88.
  95. Kokubu, C.; Horie, K.; Abe, K.; Ikeda, R.; Mizuno, S.; Uno, Y.; Ogiwara, S.; Ohtsuka, M.; Isotani, A.; Okabe, M.; et al. A transposon-based chromosomal engineering method to survey a large cis-regulatory landscape in mice. Nat. Genet. 2009, 41, 946–952.
  96. Liang, Q.; Kong, J.; Stalker, J.; Bradley, A. Chromosomal mobilization and reintegration of Sleeping Beauty and PiggyBac transposons. Genesis 2009, 47, 404–408.
  97. Horie, K.; Yusa, K.; Yae, K.; Odajima, J.; Fischer, S.E.J.; Keng, V.W.; Hayakawa, T.; Mizuno, S.; Kondoh, G.; Ijiri, T.; et al. Characterization of Sleeping Beauty transposition and its application to genetic screening in mice. Mol. Cell. Biol. 2003, 23, 9189–9207.
  98. Carlson, C.M.; Dupuy, A.J.; Fritz, S.; Roberg-Perez, K.J.; Fletcher, C.F.; Largaespada, D.A. Transposon mutagenesis of the mouse germline. Genetics 2003, 165, 243–256.
  99. Fischer, S.E.; Wienholds, E.; Plasterk, R.H. Regulated transposition of a fish transposon in the mouse germ line. Proc. Natl. Acad. Sci. USA 2001, 98, 6759–6764.
  100. Yergeau, D.A.; Kelley, C.M.; Kuliyev, E.; Zhu, H.; Johnson Hamlet, M.R.; Sater, A.K.; Wells, D.E.; Mead, P.E. Remobilization of Sleeping Beauty transposons in the germline of Xenopus tropicalis. Mob. DNA 2011, 2, 15.
  101. Keng, V.W.; Yae, K.; Hayakawa, T.; Mizuno, S.; Uno, Y.; Yusa, K.; Kokubu, C.; Kinoshita, T.; Akagi, K.; Jenkins, N.A.; et al. Region-specific saturation germline mutagenesis in mice using the Sleeping Beauty transposon system. Nat. Methods 2005, 2, 763–769.
  102. Knapp, S.; Larondelle, Y.; Rossberg, M.; Furtek, D.; Theres, K. Transgenic tomato lines containing Ds elements at defined genomic positions as tools for targeted transposon tagging. Mol. Genet. Genom. 1994, 243, 666–673.
More
ScholarVision Creations