Marine Biotechnology

, Volume 7, Issue 3, pp 135–141

Fishing for Answers with Transposons

  • Shannon A. Wadman
  • Karl J. Clark
  • Perry B. Hackett
Review

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.

Keywords

enhancer trap gene trap fish safety Sleeping Beauty transgenesis 

References

  1. 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: 62Google Scholar
  2. Burns, J.C., Friedmann, T., Driever, W., Burrascano, M., Yee, J.K. 1993Vesicular stomatitis virus G glycoprotein pseudotyped retroviral vectors: concentration to very high titer and efficient gene transfer into mammalian and nonmammalian cellsProc Natl Acad Sci USA9080338037PubMedGoogle Scholar
  3. Carlson, C.M., Dupuy, A.J., Fritz, S., Roberg-Perez, K.J., Fletcher, C.F., Largaespada, D.A. 2003Transposon mutagenesis of the mouse germlineGenetics165243256PubMedGoogle Scholar
  4. 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)MathSciNetGoogle Scholar
  5. Clark, K.J., Geurts, A.M., Bell, J.B., Hackett, P.B. 2004Transposon vectors for gene-trap insertional mutagenesis in vertebratesGenesis39225233CrossRefPubMedGoogle Scholar
  6. Cui, Z., Geurts, A.M., Liu, G., Kaufman, C.D., Hackett, P.B. 2002Structure-function analysis of the inverted terminal repeats of the sleeping beauty transposonJ Mol Biol31812211235CrossRefPubMedGoogle Scholar
  7. Davidson, A.E., Balciunas, D., Mohn, D., Shaffer, J., Hermanson, S., Sivasubbu, S., Cliff, M.P., Hackett, P.B., Ekker, S.C. 2003Efficient gene delivery and gene expression in zebrafish using the Sleeping Beauty transposonDev Biol263191202CrossRefPubMedGoogle Scholar
  8. Driever, W., Solnica-Krezel, L., Schier, A.F., Neuhauss, S.C., Malicki, J., Stemple, D.L., Stainier, D.Y., Zwartkruis, F., Abdelilah, S., Rangini, Z.,  et al. 1996A genetic screen for mutations affecting embryogenesis in zebrafishDevelopment1233746PubMedGoogle Scholar
  9. Dupuy, A.J., Fritz, S., Largaespada, D.A. 2001Transposition and gene disruption in the male germline of the mouseGenesis308288CrossRefPubMedGoogle Scholar
  10. Dupuy, A.J., Clark, K., Carlson, C.M., Fritz, S., Davidson, A.E., Markley, K.M., Finley, K., Fletcher, C.F., Ekker, S.C., Hackett, P.B.,  et al. 2002Mammalian germ-line transgenesis by transpositionProc Natl Acad Sci U S A9944954499CrossRefPubMedGoogle Scholar
  11. Eisen, J.S. 1996Zebrafish make a big splashCell87969977CrossRefPubMedGoogle Scholar
  12. Evans, M.J., Carlton, M.B., Russ, A.P. 1997Gene trapping and functional genomicsTrends Genet13370374CrossRefPubMedGoogle Scholar
  13. Fischer, S.E., Wienholds, E., Plasterk, R.H. 2001Regulated transposition of a fish transposon in the mouse germ lineProc Natl Acad Sci U S A9867596764CrossRefPubMedGoogle Scholar
  14. Friedrich, G., Soriano, P. 1991Promoter traps in embryonic stem cells: a genetic screen to identify and mutate developmental genes in miceGenes Dev515131523PubMedGoogle Scholar
  15. Gaiano, N., Allende, M., Amsterdam, A., Kawakami, K., Hopkins, N. 1996Highly efficient germ-line transmission of proviral insertions in zebrafishProc Natl Acad Sci USA9377777782CrossRefPubMedGoogle Scholar
  16. Geurts, A.M., Yang, Y., Clark, K.J., Liu, G., Cui, Z., Dupuy, A.J., Bell, J.B., Largaespada, D.A., Hackett, P.B. 2003Gene transfer into genomes of human cells by the sleeping beauty transposon systemMol Ther8108117CrossRefPubMedGoogle Scholar
  17. Golling, G., Amsterdam, A., Sun, Z., Antonelli, M., Maldonado, E., Chen, W., Burgess, S., Haldi, M., Artzt, K., Farrington, S.,  et al. 2002Insertional mutagenesis in zebrafish rapidly identifies genes essential for early vertebrate developmentNat Genet31135140CrossRefPubMedGoogle Scholar
  18. Gossler, A., Joyner, A.L., Rossant, J., Skarnes, W.C. 1989Mouse embryonic stem cells and reporter constructs to detect developmentally regulated genesScience244463465PubMedGoogle Scholar
  19. Grabher, C., Henrich, T., Sasado, T., Arenz, A., Wittbrodt, J., Furutani-Seiki, M. 2003Transposon-mediated enhancer trapping in medakaGene3225766CrossRefPubMedGoogle Scholar
  20. Grabher, C., Wittbrodt, J. (2004) “Efficient activation of gene expression using a heat-shock inducible Gal4/Vp16-UAS system in medaka” BMC Biotechnol 4: 26Google Scholar
  21. Hackett, P.B., Alvarez, M.C. 2000The molecular genetics of transgenic fishRecent Adv Mar Biotech477145Google Scholar
  22. Haffter, P., Granato, M., Brand, M., Mullins, M.C., Hammerschmidt, M., Kane, D.A., Odenthal, J., Eeden, F.J., Jiang, Y.J., Heisenberg, C.P.,  et al. 1996The identification of genes with unique and essential functions in the development of the zebrafish, Danio rerio.Development123136PubMedGoogle Scholar
  23. Hamada, H. 1986Random isolation of gene activator elements from the human genomeMol Cell Biol641854194PubMedGoogle Scholar
  24. Horie, K., Kuroiwa, A., Ikawa, M., Okabe, M., Kondoh, G., Matsuda, Y., Takeda, J. 2001Efficient chromosomal transposition of a Tcl/mariner-like transposon Sleeping Beauty in miceProc Natl Acad Sci USA9891919196CrossRefPubMedGoogle Scholar
  25. Ivics, Z., Izsvak, Z. 2004Transposable elements for transgenesis and insertional mutagenesis in vertebrates: a contemporary review of experimental strategiesMethods Mol Biol260255276PubMedGoogle Scholar
  26. Ivics, Z., Izsvak, Z., Hackett, P.B. 1993Enhanced incorporation of transgenic DNA into zebrafish chromosomes by a retroviral integration proteinMol Mar Biol Biotechnol2 162173PubMedGoogle Scholar
  27. Ivics, Z., Hackett, P.B., Plasterk, R.H., Izsvak, Z. 1997Molecular reconstruction of Sleeping Beauty, a Tc1-like transposon from fish, and its transposition in human cellsCell91501510CrossRefPubMedGoogle Scholar
  28. Izsvak, Z., Ivics, Z., Shimoda, N., Mohn, D., Okamoto, H., Hackett, P.B. 1999Short inverted-repeat transposable elements in teleost fish and implications for a mechanism of their amplificationJ Mol Evol481321PubMedGoogle Scholar
  29. Izsvak, Z., Stuwe, E.E., Fiedler, D., Katzer, A., Jeggo, P.A., Ivics, Z. 2004Healing the wounds inflicted by Sleeping Beauty transposition by double-strand break repair in mammalian somatic cellsMol Cell13279290CrossRefPubMedGoogle Scholar
  30. Kapuscinski, A.R., Hallerman, E.M. 1990Transgenic fish and public policy: regulatory concernsFisheries751220Google Scholar
  31. Kawakami, K., Shima, A. 1999Identification of the Tol2 transposase of the medaka fish Oryzias latipes that catalyzes excision of a nonautonomous Tol2 element in zebrafish Danio rerioGene240239244CrossRefPubMedGoogle Scholar
  32. Kawakami, K., Koga, A., Hori, H., Shima, A. 1998Excision of the Tol2 transposable element of the medaka fish, Oryzias latipes, in zebrafish, Danio rerioGene2251722CrossRefPubMedGoogle Scholar
  33. Kawakami, K., Shima, A., Kawakami, N. 2000Identification of a functional transposase of the Tol2 element, an Ac-like element from the Japanese medaka fish, and its transposition in the zebrafish germ lineageProc Natl Acad Sci USA971140311408CrossRefPubMedGoogle Scholar
  34. Kazazian, H.H. 2004Mobile elements: drivers of genome evolutionScience30316261632CrossRefPubMedGoogle Scholar
  35. Koga, A., Hori, H. 1997Albinism due to transposable element insertion in fishPigment Cell Res10377381PubMedGoogle Scholar
  36. Koga, A., Hori, H. 2001The Tol2 transposable element of the medaka fish: an active DNA-based element naturally occurring in a vertebrate genomeGenes Genet Syst7618CrossRefPubMedGoogle Scholar
  37. Koga, A., Suzuki, M., Inagaki, H., Bessho, Y., Hori, H. 1996Transposable element in fishNature38330CrossRefGoogle Scholar
  38. Koga, A., Suzuki, M., Maruyama, Y., Tsutsumi, M., Hori, H. 1999Amino acid sequence of a putative transposase protein of the medaka fish transposable element Tol2 deduced from mRNA nucleotide sequencesFEBS Lett461295298CrossRefPubMedGoogle Scholar
  39. Koga, A., Shimada, A., Shima, A., Sakaizumi, M., Tachida, H., Hori, H. 2000Evidence for recent invasion of the medaka fish genome by the Tol2 transposable elementGenetics755273281Google Scholar
  40. Kurita, K., Burgess, S.M., Sakai, N. 2004Transgenic zebrafish produced by retroviral infection of in vitro-cultured spermProc Natl Acad Sci USA10112631267CrossRefPubMedGoogle Scholar
  41. 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: 860-921Google Scholar
  42. Langheinrich, U. 2003Zebrafish: a new model on the pharmaceutical catwalkBioessays25904912CrossRefPubMedGoogle Scholar
  43. Leaver, M.J. 2001A family of Tcl-like transposons from the genomes of fishes and frogs: evidence for horizontal transmissionGene271203214CrossRefPubMedGoogle Scholar
  44. Lin, S., Gaiano, N., Culp, P., Burns, J.C., Friedmann, T., Yee, J.K., Hopkins, N. 1994Integration and germ-line transmission of a pseudotyped retroviral vector in zebrafishScience265666669PubMedGoogle Scholar
  45. Lindblad-Toh, K. 2004Genome sequencing: three’s companyNature428475476CrossRefPubMedGoogle Scholar
  46. Liu, G., Aronovich, E.L., Cui, Z., Whitley, C.B., Hackett, P.B. 2004Excision of Sleeping Beauty transposons: parameters and applications to gene therapyJ Gene Med6574583CrossRefPubMedGoogle Scholar
  47. March, J.C., Rao, G., Bentley, W.E. 2003Biotechnological applications of green fluorescent proteinAppl Microbiol Biotechnol62303315CrossRefPubMedGoogle Scholar
  48. Miskey, C., Izsvak, Z., Plasterk, R.H., Ivics, Z. 2003The Frog Prince: a reconstructed transposon from Rana pipiens with high transpositional activity in vertebrate cellsNucleic Acids Res3168736881CrossRefPubMedGoogle Scholar
  49. Moav, B., Liu, Z., Caldovic, L.D., Gross, M.L., Faras, A.J., Hackett, P.B. 1993Regulation of expression of transgenes in developing fishTransgenic Res2153161CrossRefPubMedGoogle Scholar
  50. Muir, W.M., Howard, R.M. 1999Possible ecological risks of transgenic organism release when transgenes affect mating success: sexual selection and the Trojan gene hypothesisProc Natl Acad Sci U S A951385313856CrossRefGoogle Scholar
  51. Muir, W.M., Howard, R.M. 2002Assessment of possible ecolognical risks and hazards of transgenic fish with implications for other sexually reproducing organismsTransgenic Res11101114CrossRefPubMedGoogle Scholar
  52. O’Kane, C.J., Gehring, W.J. 1987Detection in situ of genomic regulatory elements in DrosophilaProc Natl Acad Sci U S A8491239127PubMedGoogle Scholar
  53. Plasterk, R.H., Izsvak, Z., Ivics, Z. 1999Resident aliens: the Tc1/mariner superfamily of transposable elementsTrends Genet15326332CrossRefPubMedGoogle Scholar
  54. Postlethwait, J., Amores, A., Force, A., Yan, Y.L. 1999The zebrafish genomeMethods Cell Biol60149163PubMedCrossRefGoogle Scholar
  55. Ray, P., Bauer, E., Iyer, M., Barrio, J.R., Satyamurthy, N., Phelps, M.E., Herschman, H.R., Gambhir, S.S. 2001Monitoring gene therapy with reporter gene imagingSemin Nucl Med31312320PubMedGoogle Scholar
  56. Stanford, W.L., Cohn, J.B., Cordes, S.P. 2001Gene-trap mutagenesis: past, present and beyondNat Rev Genet2756768CrossRefPubMedGoogle Scholar
  57. Streisinger, G., Walker, C., Dower, N., Knauber, D., Singer, F. 1981Production of clones of homozygous diploid zebra fish (Brachydanio rerio)Nature297293296CrossRefGoogle Scholar
  58. Stuart, G.W., McMurray, J.R., Westerfield, M. 1988Replication, integration and stable germ-line transmission of foreign sequences injected into early zebrafish embryosDevelopment103403412PubMedGoogle Scholar
  59. Stuart, G.W., Vielkind, J.R., McMurray, J.V., Westerfield, M. 1990Stable lines of transgenic zebrafish exhibit reproducible patterns of transgene expressionDevelopment109577584PubMedGoogle Scholar
  60. Tsutsumi, M., Koga, A., Hori, H. 2003Long and short mRNAs transcribed from the medaka fish transposon Tol2 respectively exert positive and negative effects on excisionGenet Res823340CrossRefPubMedGoogle Scholar
  61. Udvadia, A.J., Linney, E. 2003Windows into development: historic, current, and future perspectives on transgenic zebrafishDev Biol256117CrossRefPubMedGoogle Scholar
  62. 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: 1304-1351Google Scholar
  63. von Melchner, H., Ruley, H.E. 1989Identification of cellular promoters by using a retrovirus promoter trapJ Virol6332273233PubMedGoogle Scholar
  64. Westerfield, M., Wegner, J., Jegalian, B.G., DeRobertis, E.M., Puschel, A.W. 1992Specific activation of mammalian Hox promoters in mosaic transgenic zebrafishGenes Dev6591598PubMedGoogle Scholar
  65. Wu, X., Li, Y., Crise, B., Burgess, S.M. 2003Transcription start regions in the human genome are favored targets for MLV integrationScience30017491751CrossRefPubMedGoogle Scholar
  66. Yant, S.R., Kay, M.A. 2003Nonhomologous-end-joining factors regulate DNA repair fidelity during Sleeping Beauty element transposition in mammalian cellsMol Cell Biol2385058518CrossRefPubMedGoogle Scholar
  67. Yoshida, M., Yagi, T., Furuta, Y., Takayanagi, K., Kominami, R., Takeda, N., Tokunaga, T., Chiba, J., Ikawa, Y., Aizawa, S. 1995A new strategy of gene trapping in ES cells using 3’RACETransgenic Res4277287CrossRefPubMedGoogle Scholar
  68. Yu, Y.A., Oberg, K., Wang, G., Szalay, A.A. 2003Visualization of molecular and cellular events with green fluorescent proteins in developing embryos: a reviewLuminescence18118CrossRefPubMedGoogle Scholar
  69. Zambrowicz, B.P., Sands, A.T. 2003Knockouts model the 100 best-selling drugs-will they model the next 100?Nat Rev Drag Discov23851CrossRefGoogle Scholar
  70. Zambrowicz, B.P., Friedrich, G.A., Buxton, E.C., Lilleberg, S.L., Person, C., Sands, A.T. 1998Disruption and sequence identification of 2,000 genes in mouse embryonic stem cellsNature392608611CrossRefPubMedGoogle Scholar
  71. Zayed, H., Izsvak, Z., Khare, D., Heinemann, U., Ivics, Z. 2003The DNA-bending protein HMGB1 is a cellular cofactor of Sleeping Beauty transpositionNucleic Acids Res3123132322CrossRefPubMedGoogle Scholar
  72. Zayed, H., Izsvak, Z., Walisko, O., Ivics, Z. 2004Development of hyperactive Sleeping Beauty transposon vectors by mutational analysisMol Ther9292304CrossRefPubMedGoogle Scholar
  73. Zhang, J., Campbell, R.E., Ting, A.Y., Tsien, R.Y. 2002Creating new fluorescent probes for cell biologyNat Rev Mol Cell Biol3906918CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2005

Authors and Affiliations

  • Shannon A. Wadman
    • 1
  • Karl J. Clark
    • 1
  • Perry B. Hackett
    • 1
    • 2
  1. 1.Discovery Genomics, Inc.MinneapolisUSA.
  2. 2.Department of Genetics, Cell Biology and DevelopmentUniversity of MinnesotaMinneapolisUSA

Personalised recommendations