Abstract
Transposons are one means that nature has used to introduce new genetic material into chromosomes of organisms from every kingdom. They have been extensively used in prokaryotic and lower eukaryotic systems, but until recently there was no transposon that had significant activity in vertebrates. The Sleeping Beauty (SB) transposon system was developed to direct the integration of precise DNA sequences into chromosomes. The SB system was derived from salmonid sequences that had been inactive for more than 10 million years. SB transposons have been used for two principle uses – as a vector for transgenesis and as a method for introducing various trap vectors into (gene-trap) or in the neighborhood of (enhancer-trap) genes to identify their functions. Results of these studies show that SB-mediated transgenesis is more efficient than that by injection of simple plasmids and that expression of transgenesis is stable and reliable following passage through the germline.
Similar content being viewed by others
References
Balciunas, D., Davidson, A.E., Sivasubbu, S., Hermanson, S.B., Welle, Z., Ekker, S.C. (2004) “Enhancer trapping in zebrafish using the Sleeping Beauty transposon” BMC Genomics 5: 62
J.C. Burns T. Friedmann W. Driever M. Burrascano J.K. Yee (1993) ArticleTitleVesicular stomatitis virus G glycoprotein pseudotyped retroviral vectors: concentration to very high titer and efficient gene transfer into mammalian and nonmammalian cells Proc Natl Acad Sci USA 90 8033–8037 Occurrence Handle8396259
C.M. Carlson A.J. Dupuy S. Fritz K.J. Roberg-Perez C.F. Fletcher D.A. Largaespada (2003) ArticleTitleTransposon mutagenesis of the mouse germline Genetics 165 243–256 Occurrence Handle14504232
Choi, C.Q., and Nash, S. (2004). GloFish draw suit: watchdog groups want FDA to regulate first genetically modified pet in US. The Scientist: Daily News, 7 January (http://www.biomedcentral.com/news/20040107/01)
K.J. Clark A.M. Geurts J.B. Bell P.B. Hackett (2004) ArticleTitleTransposon vectors for gene-trap insertional mutagenesis in vertebrates Genesis 39 225–233 Occurrence Handle10.1002/gene.20049 Occurrence Handle15286994
Z. Cui A.M. Geurts G. Liu C.D. Kaufman P.B. Hackett (2002) ArticleTitleStructure-function analysis of the inverted terminal repeats of the sleeping beauty transposon J Mol Biol 318 1221–1235 Occurrence Handle10.1016/S0022-2836(02)00237-1 Occurrence Handle12083513
A.E. Davidson D. Balciunas D. Mohn J. Shaffer S. Hermanson S. Sivasubbu M.P. Cliff P.B. Hackett S.C. Ekker (2003) ArticleTitleEfficient gene delivery and gene expression in zebrafish using the Sleeping Beauty transposon Dev Biol 263 191–202 Occurrence Handle10.1016/j.ydbio.2003.07.013 Occurrence Handle14597195
W. Driever L. Solnica-Krezel A.F. Schier S.C. Neuhauss J. Malicki D.L. Stemple D.Y. Stainier F. Zwartkruis S. Abdelilah Z. Rangini et al. (1996) ArticleTitleA genetic screen for mutations affecting embryogenesis in zebrafish Development 123 37–46 Occurrence Handle9007227
A.J. Dupuy S. Fritz D.A. Largaespada (2001) ArticleTitleTransposition and gene disruption in the male germline of the mouse Genesis 30 82–88 Occurrence Handle10.1002/gene.1037 Occurrence Handle11416868
A.J. Dupuy K. Clark C.M. Carlson S. Fritz A.E. Davidson K.M. Markley K. Finley C.F. Fletcher S.C. Ekker P.B. Hackett et al. (2002) ArticleTitleMammalian germ-line transgenesis by transposition Proc Natl Acad Sci U S A 99 4495–4499 Occurrence Handle10.1073/pnas.062630599 Occurrence Handle11904379
J.S. Eisen (1996) ArticleTitleZebrafish make a big splash Cell 87 969–977 Occurrence Handle10.1016/S0092-8674(00)81792-4 Occurrence Handle8978602
M.J. Evans M.B. Carlton A.P. Russ (1997) ArticleTitleGene trapping and functional genomics Trends Genet 13 370–374 Occurrence Handle10.1016/S0168-9525(97)01240-7 Occurrence Handle9287493
S.E. Fischer E. Wienholds R.H. Plasterk (2001) ArticleTitleRegulated transposition of a fish transposon in the mouse germ line Proc Natl Acad Sci U S A 98 6759–6764 Occurrence Handle10.1073/pnas.121569298 Occurrence Handle11381141
G. Friedrich P. Soriano (1991) ArticleTitlePromoter traps in embryonic stem cells: a genetic screen to identify and mutate developmental genes in mice Genes Dev 5 1513–1523 Occurrence Handle1653172
N. Gaiano M. Allende A. Amsterdam K. Kawakami N. Hopkins (1996) ArticleTitleHighly efficient germ-line transmission of proviral insertions in zebrafish Proc Natl Acad Sci USA 93 7777–7782 Occurrence Handle10.1073/pnas.93.15.7777 Occurrence Handle8755552
A.M. Geurts Y. Yang K.J. Clark G. Liu Z. Cui A.J. Dupuy J.B. Bell D.A. Largaespada P.B. Hackett (2003) ArticleTitleGene transfer into genomes of human cells by the sleeping beauty transposon system Mol Ther 8 108–117 Occurrence Handle10.1016/S1525-0016(03)00099-6 Occurrence Handle12842434
G. Golling A. Amsterdam Z. Sun M. Antonelli E. Maldonado W. Chen S. Burgess M. Haldi K. Artzt S. Farrington et al. (2002) ArticleTitleInsertional mutagenesis in zebrafish rapidly identifies genes essential for early vertebrate development Nat Genet 31 135–140 Occurrence Handle10.1038/ng896 Occurrence Handle12006978
A. Gossler A.L. Joyner J. Rossant W.C. Skarnes (1989) ArticleTitleMouse embryonic stem cells and reporter constructs to detect developmentally regulated genes Science 244 463–465 Occurrence Handle2497519
C. Grabher T. Henrich T. Sasado A. Arenz J. Wittbrodt M. Furutani-Seiki (2003) ArticleTitleTransposon-mediated enhancer trapping in medaka Gene 322 57–66 Occurrence Handle10.1016/j.gene.2003.09.009 Occurrence Handle14644497
Grabher, C., Wittbrodt, J. (2004) “Efficient activation of gene expression using a heat-shock inducible Gal4/Vp16-UAS system in medaka” BMC Biotechnol 4: 26
P.B. Hackett M.C. Alvarez (2000) ArticleTitleThe molecular genetics of transgenic fish Recent Adv Mar Biotech 4 77–145
P. Haffter M. Granato M. Brand M.C. Mullins M. Hammerschmidt D.A. Kane J. Odenthal F.J. Eeden Particlevan Y.J. Jiang C.P. Heisenberg et al. (1996) ArticleTitleThe identification of genes with unique and essential functions in the development of the zebrafish, Danio rerio. Development 123 1–36 Occurrence Handle9007226
H. Hamada (1986) ArticleTitleRandom isolation of gene activator elements from the human genome Mol Cell Biol 6 4185–4194 Occurrence Handle3025643
K. Horie A. Kuroiwa M. Ikawa M. Okabe G. Kondoh Y. Matsuda J. Takeda (2001) ArticleTitleEfficient chromosomal transposition of a Tcl/mariner-like transposon Sleeping Beauty in mice Proc Natl Acad Sci USA 98 9191–9196 Occurrence Handle10.1073/pnas.161071798 Occurrence Handle11481482
Z. Ivics Z. Izsvak (2004) ArticleTitleTransposable elements for transgenesis and insertional mutagenesis in vertebrates: a contemporary review of experimental strategies Methods Mol Biol 260 255–276 Occurrence Handle15020812
Z. Ivics Z. Izsvak P.B. Hackett (1993) ArticleTitleEnhanced incorporation of transgenic DNA into zebrafish chromosomes by a retroviral integration protein Mol Mar Biol Biotechnol 2 162–173 Occurrence Handle8364694
Z. Ivics P.B. Hackett R.H. Plasterk Z. Izsvak (1997) ArticleTitleMolecular reconstruction of Sleeping Beauty, a Tc1-like transposon from fish, and its transposition in human cells Cell 91 501–510 Occurrence Handle10.1016/S0092-8674(00)80436-5 Occurrence Handle9390559
Z. Izsvak Z. Ivics N. Shimoda D. Mohn H. Okamoto P.B. Hackett (1999) ArticleTitleShort inverted-repeat transposable elements in teleost fish and implications for a mechanism of their amplification J Mol Evol 48 13–21 Occurrence Handle9873073
Z. Izsvak E.E. Stuwe D. Fiedler A. Katzer P.A. Jeggo Z. Ivics (2004) ArticleTitleHealing the wounds inflicted by Sleeping Beauty transposition by double-strand break repair in mammalian somatic cells Mol Cell 13 279–290 Occurrence Handle10.1016/S1097-2765(03)00524-0 Occurrence Handle14759372
A.R. Kapuscinski E.M. Hallerman (1990) ArticleTitleTransgenic fish and public policy: regulatory concerns Fisheries 75 12–20
K. Kawakami A. Shima (1999) ArticleTitleIdentification of the Tol2 transposase of the medaka fish Oryzias latipes that catalyzes excision of a nonautonomous Tol2 element in zebrafish Danio rerio Gene 240 239–244 Occurrence Handle10.1016/S0378-1119(99)00444-8 Occurrence Handle10564832
K. Kawakami A. Koga H. Hori A. Shima (1998) ArticleTitleExcision of the Tol2 transposable element of the medaka fish, Oryzias latipes, in zebrafish, Danio rerio Gene 225 17–22 Occurrence Handle10.1016/S0378-1119(98)00537-X Occurrence Handle9931412
K. Kawakami A. Shima N. Kawakami (2000) ArticleTitleIdentification of a functional transposase of the Tol2 element, an Ac-like element from the Japanese medaka fish, and its transposition in the zebrafish germ lineage Proc Natl Acad Sci USA 97 11403–11408 Occurrence Handle10.1073/pnas.97.21.11403 Occurrence Handle11027340
H.H. Kazazian (2004) ArticleTitleMobile elements: drivers of genome evolution Science 303 1626–1632 Occurrence Handle10.1126/science.1089670 Occurrence Handle15016989
A. Koga H. Hori (1997) ArticleTitleAlbinism due to transposable element insertion in fish Pigment Cell Res 10 377–381 Occurrence Handle9428004
A. Koga H. Hori (2001) ArticleTitleThe Tol2 transposable element of the medaka fish: an active DNA-based element naturally occurring in a vertebrate genome Genes Genet Syst 76 1–8 Occurrence Handle10.1266/ggs.76.1 Occurrence Handle11376546
A. Koga M. Suzuki H. Inagaki Y. Bessho H. Hori (1996) ArticleTitleTransposable element in fish Nature 383 30 Occurrence Handle10.1038/383030a0
A. Koga M. Suzuki Y. Maruyama M. Tsutsumi H. Hori (1999) ArticleTitleAmino acid sequence of a putative transposase protein of the medaka fish transposable element Tol2 deduced from mRNA nucleotide sequences FEBS Lett 461 295–298 Occurrence Handle10.1016/S0014-5793(99)01479-9 Occurrence Handle10567714
A. Koga A. Shimada A. Shima M. Sakaizumi H. Tachida H. Hori (2000) ArticleTitleEvidence for recent invasion of the medaka fish genome by the Tol2 transposable element Genetics 755 273–281
K. Kurita S.M. Burgess N. Sakai (2004) ArticleTitleTransgenic zebrafish produced by retroviral infection of in vitro-cultured sperm Proc Natl Acad Sci USA 101 1263–1267 Occurrence Handle10.1073/pnas.0304265101 Occurrence Handle14745028
Lander, E.S., Linton, L.M., Birren, B., Nusbaum, C., Zody, M.C., Baldwin, J., Devon, K., Dewar, K., Doyle, M., FitzHugh, W., et al. (2001) “Initial sequencing and analysis of the human genome” Nature 409: 860-921
U. Langheinrich (2003) ArticleTitleZebrafish: a new model on the pharmaceutical catwalk Bioessays 25 904–912 Occurrence Handle10.1002/bies.10326 Occurrence Handle12938180
M.J. Leaver (2001) ArticleTitleA family of Tcl-like transposons from the genomes of fishes and frogs: evidence for horizontal transmission Gene 271 203–214 Occurrence Handle10.1016/S0378-1119(01)00530-3 Occurrence Handle11418241
S. Lin N. Gaiano P. Culp J.C. Burns T. Friedmann J.K. Yee N. Hopkins (1994) ArticleTitleIntegration and germ-line transmission of a pseudotyped retroviral vector in zebrafish Science 265 666–669 Occurrence Handle8036514
K. Lindblad-Toh (2004) ArticleTitleGenome sequencing: three’s company Nature 428 475–476 Occurrence Handle10.1038/428475a Occurrence Handle15057812
G. Liu E.L. Aronovich Z. Cui C.B. Whitley P.B. Hackett (2004) ArticleTitleExcision of Sleeping Beauty transposons: parameters and applications to gene therapy J Gene Med 6 574–583 Occurrence Handle10.1002/jgm.486 Occurrence Handle15133768
J.C. March G. Rao W.E. Bentley (2003) ArticleTitleBiotechnological applications of green fluorescent protein Appl Microbiol Biotechnol 62 303–315 Occurrence Handle10.1007/s00253-003-1339-y Occurrence Handle12768245
C. Miskey Z. Izsvak R.H. Plasterk Z. Ivics (2003) ArticleTitleThe Frog Prince: a reconstructed transposon from Rana pipiens with high transpositional activity in vertebrate cells Nucleic Acids Res 31 6873–6881 Occurrence Handle10.1093/nar/gkg910 Occurrence Handle14627820
B. Moav Z. Liu L.D. Caldovic M.L. Gross A.J. Faras P.B. Hackett (1993) ArticleTitleRegulation of expression of transgenes in developing fish Transgenic Res 2 153–161 Occurrence Handle10.1007/BF01972609 Occurrence Handle8353534
W.M. Muir R.M. Howard (1999) ArticleTitlePossible ecological risks of transgenic organism release when transgenes affect mating success: sexual selection and the Trojan gene hypothesis Proc Natl Acad Sci U S A 95 13853–13856 Occurrence Handle10.1073/pnas.96.24.13853
W.M. Muir R.M. Howard (2002) ArticleTitleAssessment of possible ecolognical risks and hazards of transgenic fish with implications for other sexually reproducing organisms Transgenic Res 11 101–114 Occurrence Handle10.1023/A:1015203812200 Occurrence Handle12054344
C.J. O’Kane W.J. Gehring (1987) ArticleTitleDetection in situ of genomic regulatory elements in Drosophila Proc Natl Acad Sci U S A 84 9123–9127 Occurrence Handle2827169
R.H. Plasterk Z. Izsvak Z. Ivics (1999) ArticleTitleResident aliens: the Tc1/mariner superfamily of transposable elements Trends Genet 15 326–332 Occurrence Handle10.1016/S0168-9525(99)01777-1 Occurrence Handle10431195
J. Postlethwait A. Amores A. Force Y.L. Yan (1999) ArticleTitleThe zebrafish genome Methods Cell Biol 60 149–163 Occurrence Handle9891335 Occurrence Handle10.1016/S0091-679X(08)61898-1
P. Ray E. Bauer M. Iyer J.R. Barrio N. Satyamurthy M.E. Phelps H.R. Herschman S.S. Gambhir (2001) ArticleTitleMonitoring gene therapy with reporter gene imaging Semin Nucl Med 31 312–320 Occurrence Handle11710773
W.L. Stanford J.B. Cohn S.P. Cordes (2001) ArticleTitleGene-trap mutagenesis: past, present and beyond Nat Rev Genet 2 756–768 Occurrence Handle10.1038/35093548 Occurrence Handle11584292
G. Streisinger C. Walker N. Dower D. Knauber F. Singer (1981) ArticleTitleProduction of clones of homozygous diploid zebra fish (Brachydanio rerio) Nature 297 293–296 Occurrence Handle10.1038/291293a0
G.W. Stuart J.R. McMurray M. Westerfield (1988) ArticleTitleReplication, integration and stable germ-line transmission of foreign sequences injected into early zebrafish embryos Development 103 403–412 Occurrence Handle2852096
G.W. Stuart J.R. Vielkind J.V. McMurray M. Westerfield (1990) ArticleTitleStable lines of transgenic zebrafish exhibit reproducible patterns of transgene expression Development 109 577–584 Occurrence Handle2401211
M. Tsutsumi A. Koga H. Hori (2003) ArticleTitleLong and short mRNAs transcribed from the medaka fish transposon Tol2 respectively exert positive and negative effects on excision Genet Res 82 33–40 Occurrence Handle10.1017/S0016672303006335 Occurrence Handle14621269
A.J. Udvadia E. Linney (2003) ArticleTitleWindows into development: historic, current, and future perspectives on transgenic zebrafish Dev Biol 256 1–17 Occurrence Handle10.1016/S0012-1606(02)00083-0 Occurrence Handle12654288
Venter, J.C., Adams, M.D., Myers, E.W., Li, P.W., Mural, R.J., Sutton, G.G., Smith, H.O., Yandell, M., Evans, C.A., Holt, R.A., et al. (2001) “The sequence of the human genome” Science 291: 1304-1351
H. von Melchner Particlevon H.E. Ruley (1989) ArticleTitleIdentification of cellular promoters by using a retrovirus promoter trap J Virol 63 3227–3233 Occurrence Handle2545900
M. Westerfield J. Wegner B.G. Jegalian E.M. DeRobertis A.W. Puschel (1992) ArticleTitleSpecific activation of mammalian Hox promoters in mosaic transgenic zebrafish Genes Dev 6 591–598 Occurrence Handle1348485
X. Wu Y. Li B. Crise S.M. Burgess (2003) ArticleTitleTranscription start regions in the human genome are favored targets for MLV integration Science 300 1749–1751 Occurrence Handle10.1126/science.1083413 Occurrence Handle12805549
S.R. Yant M.A. Kay (2003) ArticleTitleNonhomologous-end-joining factors regulate DNA repair fidelity during Sleeping Beauty element transposition in mammalian cells Mol Cell Biol 23 8505–8518 Occurrence Handle10.1128/MCB.23.23.8505-8518.2003 Occurrence Handle14612396
M. Yoshida T. Yagi Y. Furuta K. Takayanagi R. Kominami N. Takeda T. Tokunaga J. Chiba Y. Ikawa S. Aizawa (1995) ArticleTitleA new strategy of gene trapping in ES cells using 3’RACE Transgenic Res 4 277–287 Occurrence Handle10.1007/BF01969122 Occurrence Handle7655516
Y.A. Yu K. Oberg G. Wang A.A. Szalay (2003) ArticleTitleVisualization of molecular and cellular events with green fluorescent proteins in developing embryos: a review Luminescence 18 1–18 Occurrence Handle10.1002/bio.701 Occurrence Handle12536374
B.P. Zambrowicz A.T. Sands (2003) ArticleTitleKnockouts model the 100 best-selling drugs-will they model the next 100? Nat Rev Drag Discov 2 38–51 Occurrence Handle10.1038/nrd987
B.P. Zambrowicz G.A. Friedrich E.C. Buxton S.L. Lilleberg C. Person A.T. Sands (1998) ArticleTitleDisruption and sequence identification of 2,000 genes in mouse embryonic stem cells Nature 392 608–611 Occurrence Handle10.1038/33423 Occurrence Handle9560157
H. Zayed Z. Izsvak D. Khare U. Heinemann Z. Ivics (2003) ArticleTitleThe DNA-bending protein HMGB1 is a cellular cofactor of Sleeping Beauty transposition Nucleic Acids Res 31 2313–2322 Occurrence Handle10.1093/nar/gkg341 Occurrence Handle12711676
H. Zayed Z. Izsvak O. Walisko Z. Ivics (2004) ArticleTitleDevelopment of hyperactive Sleeping Beauty transposon vectors by mutational analysis Mol Ther 9 292–304 Occurrence Handle10.1016/j.ymthe.2003.11.024 Occurrence Handle14759813
J. Zhang R.E. Campbell A.Y. Ting R.Y. Tsien (2002) ArticleTitleCreating new fluorescent probes for cell biology Nat Rev Mol Cell Biol 3 906–918 Occurrence Handle10.1038/nrm976 Occurrence Handle12461557
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Wadman, S.A., Clark, K.J. & Hackett, P.B. Fishing for Answers with Transposons. Mar Biotechnol 7, 135–141 (2005). https://doi.org/10.1007/s10126-004-0068-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10126-004-0068-2