Genome-Wide Manipulations of Drosophila melanogaster with Transposons, Flp Recombinase, and ΦC31 Integrase

Protocol
Part of the Methods in Molecular Biology book series (MIMB, volume 859)

Abstract

Transposable elements, the Flp recombinase, and the ΦC31 integrase are used in Drosophila melanogaster for numerous genome-wide manipulations. Often, their use is combined in a synergistic fashion to alter and engineer the fruit fly genome. Transposons are the foundation for all transgenic technologies in flies and hence almost all innovations in the fruit fly. They have been instrumental in the generation of genome-wide collections of insertions for gene disruption and manipulation. Many important transgenic strains of these collections are available from public repositories. The Flp protein is the most widely used recombinase to induce mitotic clones to study individual gene function. However, Flp has also been used to generate chromosome- and genome-wide collections of precise deletions, inversions, and duplications. Similarly, transposons that contain attP attachment sites for the ΦC31 integrase can be used for numerous applications. This integrase was incorporated into a transgenesis system that allows the integration of small to very large DNA fragments that can be easily manipulated through recombineering. This system allowed the creation of genomic DNA libraries for genome-wide gene manipulations and X chromosome duplications. Moreover, the attP sites are being used to create libraries of tens of thousands of RNAi constructs and tissue-specific GAL4 lines. This chapter focuses on genome-wide applications of transposons, Flp recombinase, and ΦC31 integrase that greatly facilitate experimental manipulation of Drosophila.

Key words

P element transposon piggyBac transposon Minos transposon Flp recombinase ΦC31 integrase Deletion Duplication Recombineering GAL4/UAS RNAi 

References

  1. 1.
    Adams, M. D., Celniker, S. E., Holt, R. A., Evans, C. A., Gocayne, J. D., Amanatides, P. G., Scherer, S. E., Li, P. W., Hoskins, R. A., Galle, R. F., George, R. A., Lewis, S. E., Richards, S., Ashburner, M., Henderson, S. N., Sutton, G. G., Wortman, J. R., Yandell, M. D., Zhang, Q., Chen, L. X., Brandon, R. C., Rogers, Y. H., Blazej, R. G., Champe, M., Pfeiffer, B. D., Wan, K. H., Doyle, C., Baxter, E. G., Helt, G., Nelson, C. R., Gabor, G. L., Abril, J. F., Agbayani, A., An, H. J., Andrews-Pfannkoch, C., Baldwin, D., Ballew, R. M., Basu, A., Baxendale, J., Bayraktaroglu, L., Beasley, E. M., Beeson, K. Y., Benos, P. V., Berman, B. P., Bhandari, D., Bolshakov, S., Borkova, D., Botchan, M. R., Bouck, J., Brokstein, P., Brottier, P., Burtis, K. C., Busam, D. A., Butler, H., Cadieu, E., Center, A., Chandra, I., Cherry, J. M., Cawley, S., Dahlke, C., Davenport, L. B., Davies, P., de, P. B., Delcher, A., Deng, Z., Mays, A. D., Dew, I., Dietz, S. M., Dodson, K., Doup, L. E., Downes, M., Dugan-Rocha, S., Dunkov, B. C., Dunn, P., Durbin, K. J., Evangelista, C. C., Ferraz, C., Ferriera, S., Fleischmann, W., Fosler, C., Gabrielian, A. E., Garg, N. S., Gelbart, W. M., Glasser, K., Glodek, A., Gong, F., Gorrell, J. H., Gu, Z., Guan, P., Harris, M., Harris, N. L., Harvey, D., Heiman, T. J., Hernandez, J. R., Houck, J., Hostin, D., Houston, K. A., Howland, T. J., Wei, M. H., Ibegwam, C., Jalali, M., Kalush, F., Karpen, G. H., Ke, Z., Kennison, J. A., Ketchum, K. A., Kimmel, B. E., Kodira, C. D., Kraft, C., Kravitz, S., Kulp, D., Lai, Z., Lasko, P., Lei, Y., Levitsky, A. A., Li, J., Li, Z., Liang, Y., Lin, X., Liu, X., Mattei, B., McIntosh, T. C., McLeod, M. P., McPherson, D., Merkulov, G., Milshina, N. V., Mobarry, C., Morris, J., Moshrefi, A., Mount, S. M., Moy, M., Murphy, B., Murphy, L., Muzny, D. M., Nelson, D. L., Nelson, D. R., Nelson, K. A., Nixon, K., Nusskern, D. R., Pacleb, J. M., Palazzolo, M., Pittman, G. S., Pan, S., Pollard, J., Puri, V., Reese, M. G., Reinert, K., Remington, K., Saunders, R. D., Scheeler, F., Shen, H., Shue, B. C., Siden-Kiamos, I., Simpson, M., Skupski, M. P., Smith, T., Spier, E., Spradling, A. C., Stapleton, M., Strong, R., Sun, E., Svirskas, R., Tector, C., Turner, R., Venter, E., Wang, A. H., Wang, X., Wang, Z. Y., Wassarman, D. A., Weinstock, G. M., Weissenbach, J., Williams, S. M., WoodageT, Worley, K. C., Wu, D., Yang, S., Yao, Q. A., Ye, J., Yeh, R. F., Zaveri, J. S., Zhan, M., Zhang, G., Zhao, Q., Zheng, L., Zheng, X. H., Zhong, F. N., Zhong, W., Zhou, X., Zhu, S., Zhu, X., Smith, H. O., Gibbs, R. A., Myers, E. W., Rubin, G. M., and Venter, J. C. (2000) Science 287, 2185–2195.Google Scholar
  2. 2.
    Venken, K. J. and Bellen, H. J. (2007) Development 134, 3571–3584.PubMedCrossRefGoogle Scholar
  3. 3.
    Venken, K. J. and Bellen, H. J. (2005) Nat. Rev. Genet. 6, 167–178.PubMedCrossRefGoogle Scholar
  4. 4.
    Rubin, G. M. and Spradling, A. C. (1982) Science 218, 348–353.PubMedCrossRefGoogle Scholar
  5. 5.
    Bellen, H. J., Levis, R. W., Liao, G., He, Y., Carlson, J. W., Tsang, G., Evans-Holm, M., Hiesinger, P. R., Schulze, K. L., Rubin, G. M., Hoskins, R. A., and Spradling, A. C. (2004) Genetics 167, 761–781.PubMedCrossRefGoogle Scholar
  6. 6.
    Handler, A. M. and Harrell, R. A. (1999) Insect Mol. Biol. 8, 449–457.Google Scholar
  7. 7.
    Loukeris, T. G., Arca, B., Livadaras, I., Dialektaki, G., and Savakis, C. (1995) Proc. Natl. Acad. Sci. U. S. A 92, 9485–9489.CrossRefGoogle Scholar
  8. 8.
    Cook, K. R., Parks, A. L., Jacobus, L. M., Kaufman, T. C., and Matthews, K. A. (2010) Fly. (Austin. ) 4, 88–91.Google Scholar
  9. 9.
    Yamamoto, M. T. (2010) Exp. Anim 59, 125–138.Google Scholar
  10. 10.
    Bischof, J. and Basler, K. (2008) Methods Mol. Biol. 420, 175–195.Google Scholar
  11. 11.
    Gong, W. J. and Golic, K. G. (2003) Proc. Natl. Acad. Sci. U. S. A 100, 2556–2561.CrossRefGoogle Scholar
  12. 12.
    Rong, Y. S. and Golic, K. G. (2000) Science 288, 2013–2018.PubMedCrossRefGoogle Scholar
  13. 13.
    Parks, A. L., Cook, K. R., Belvin, M., Dompe, N. A., Fawcett, R., Huppert, K., Tan, L. R., Winter, C. G., Bogart, K. P., Deal, J. E., alHerr, M. E., Grant, D., Marcinko, M., Miyazaki, W. Y., Robertson, S., Shaw, K. J., Tabios, M., Vysotskaia, V., Zhao, L., Andrade, R. S., Edgar, K. A., Howie, E., Killpack, K., Milash, B., Norton, A., Thao, D., Whittaker, K., Winner, M. A., Friedman, L., Margolis, J., Singer, M. A., Kopczynski, C., Curtis, D., Kaufman, T. C., Plowman, G. D., Duyk, G., and Francis-Lang, H. L. (2004) Nat. Genet. 36, 288–292.Google Scholar
  14. 14.
    Ryder, E., Blows, F., Ashburner, M., Bautista-Llacer, R., Coulson, D., Drummond, J., Webster, J., Gubb, D., Gunton, N., Johnson, G., O’Kane, C. J., Huen, D., Sharma, P., Asztalos, Z., Baisch, H., Schulze, J., Kube, M., Kittlaus, K., Reuter, G., Maroy, P., Szidonya, J., Rasmuson-Lestander, A., Ekstrom, K., Dickson, B., Hugentobler, C., Stocker, H., Hafen, E., Lepesant, J. A., Pflugfelder, G., Heisenberg, M., Mechler, B., Serras, F., Corominas, M., Schneuwly, S., Preat, T., Roote, J., and Russell, S. (2004) Genetics 167, 797–813.PubMedCrossRefGoogle Scholar
  15. 15.
    Ryder, E., Ashburner, M., Bautista-Llacer, R., Drummond, J., Webster, J., Johnson, G., Morley, T., Chan, Y. S., Blows, F., Coulson, D., Reuter, G., Baisch, H., Apelt, C., Kauk, A., Rudolph, T., Kube, M., Klimm, M., Nickel, C., Szidonya, J., Maroy, P., Pal, M., Rasmuson-Lestander, A., Ekstrom, K., Stocker, H., Hugentobler, C., Hafen, E., Gubb, D., Pflugfelder, G., Dorner, C., Mechler, B., Schenkel, H., Marhold, J., Serras, F., Corominas, M., Punset, A., Roote, J., and Russell, S. (2007) Genetics 177, 615–629.PubMedCrossRefGoogle Scholar
  16. 16.
    Groth, A. C., Fish, M., Nusse, R., and Calos, M. P. (2004) Genetics 166, 1775–1782.PubMedCrossRefGoogle Scholar
  17. 17.
    Bischof, J., Maeda, R. K., Hediger, M., Karch, F., and Basler, K. (2007) Proc. Natl. Acad. Sci. U. S. A 104, 3312–3317.CrossRefGoogle Scholar
  18. 18.
    Venken, K. J., He, Y., Hoskins, R. A., and Bellen, H. J. (2006) Science 314, 1747–1751.PubMedCrossRefGoogle Scholar
  19. 19.
    Markstein, M., Pitsouli, C., Villalta, C., Celniker, S. E., and Perrimon, N. (2008) Nat. Genet. 40, 476–483.PubMedCrossRefGoogle Scholar
  20. 20.
    Ni, J. Q., Liu, L. P., Binari, R., Hardy, R., Shim, H. S., Cavallaro, A., Booker, M., Pfeiffer, B. D., Markstein, M., Wang, H., Villalta, C., Laverty, T. R., Perkins, L. A., and Perrimon, N. (2009) Genetics 182, 1089–1100.PubMedCrossRefGoogle Scholar
  21. 21.
    Pfeiffer, B. D., Jenett, A., Hammonds, A. S., Ngo, T. T., Misra, S., Murphy, C., Scully, A., Carlson, J. W., Wan, K. H., Laverty, T. R., Mungall, C., Svirskas, R., Kadonaga, J. T., Doe, C. Q., Eisen, M. B., Celniker, S. E., and Rubin, G. M. (2008) Proc. Natl. Acad. Sci. U. S. A 105, 9715–9720.CrossRefGoogle Scholar
  22. 22.
    Ejsmont, R. K., Sarov, M., Winkler, S., Lipinsk, K. A., and Tomancak, P. (2009) Nat. Methods 6, 435–437.Google Scholar
  23. 23.
    Venken, K. J., Carlson, J. W., Schulze, K. L., Pan, H., He, Y., Spokony, R., Wan, K. H., Koriabine, M., de Jong, P. J., White, K. P., Bellen, H. J., and Hoskins, R. A. (2009) Nat. Methods 6, 431–434.Google Scholar
  24. 24.
    Ryder, E. and Russell, S. (2003) Brief. Funct. Genomic. Proteomic. 2, 57–71.PubMedCrossRefGoogle Scholar
  25. 25.
    Castro, J. P. and Carareto, C. M. (2004) Genetica 121, 107–118.PubMedCrossRefGoogle Scholar
  26. 26.
    Cooley, L., Kelley, R., and Spradling, A. (1988) Science 239, 1121–1128.PubMedCrossRefGoogle Scholar
  27. 27.
    Robertson, H. M., Preston, C. R., Phillis, R. W., Johnson-Schlitz, D. M., Benz, W. K., and Engels, W. R. (1988) Genetics 118, 461–470.PubMedGoogle Scholar
  28. 28.
    Bellen, H. J., O’Kane, C. J., Wilson, C., Grossniklaus, U., Pearson, R. K., and Gehring, W. J. (1989) Genes Dev. 3, 1288–1300.PubMedCrossRefGoogle Scholar
  29. 29.
    Bier, E., Vaessin, H., Shepherd, S., Lee, K., McCall, K., Barbel, S., Ackerman, L., Carretto, R., Uemura, T., and Grell, E. (1989) Genes Dev. 3, 1273–1287.PubMedCrossRefGoogle Scholar
  30. 30.
    Spradling, A. C., Stern, D., Beaton, A., Rhem, E. J., Laverty, T., Mozden, N., Misra, S., and Rubin, G. M. (1999) Genetics 153, 135–177.PubMedGoogle Scholar
  31. 31.
    Ochman, H., Gerber, A. S., and Hartl, D. L. (1988) Genetics 120, 621–623.PubMedGoogle Scholar
  32. 32.
    Hui, E. K., Wang, P. C., and Lo, S. J. (1998) Cell Mol. Life Sci. 54, 1403–1411.PubMedCrossRefGoogle Scholar
  33. 33.
    Voelker, R. A., Greenleaf, A. L., Gyurkovics, H., Wisely, G. B., Huang, S. M., and Searles, L. L. (1984) Genetics 107, 279–294.PubMedGoogle Scholar
  34. 34.
    Gloor, G. B., Nassif, N. A., Johnson-Schlitz, D. M., Preston, C. R., and Engels, W. R. (1991) Science 253, 1110–1117.PubMedCrossRefGoogle Scholar
  35. 35.
    Sepp, K. J. and Auld, V. J. (1999) Genetics 151, 1093–1101.PubMedGoogle Scholar
  36. 36.
    Norga, K. K., Gurganus, M. C., Dilda, C. L., Yamamoto, A., Lyman, R. F., Patel, P. H., Rubin, G. M., Hoskins, R. A., Mackay, T. F., and Bellen, H. J. (2003) Curr. Biol. 13, 1388–1396.PubMedCrossRefGoogle Scholar
  37. 37.
    Buszczak, M., Paterno, S., Lighthouse, D., Bachman, J., Planck, J., Owen, S., Skora, A. D., Nystul, T. G., Ohlstein, B., Allen, A., Wilhelm, J. E., Murphy, T. D., Levis, R. W., Matunis, E., Srivali, N., Hoskins, R. A., and Spradling, A. C. (2007) Genetics 175, 1505–1531.PubMedCrossRefGoogle Scholar
  38. 38.
    Quinones-Coello, A. T., Petrella, L. N., Ayers, K., Melillo, A., Mazzalupo, S., Hudson, A. M., Wang, S., Castiblanco, C., Buszczak, M., Hoskins, R. A., and Cooley, L. (2007) Genetics 175, 1089–1104.PubMedCrossRefGoogle Scholar
  39. 39.
    Handler, A. M., Gomez, S. P., and O’Brochta, D. A. (1993) Arch. Insect Biochem. Physiol 22, 373–384.PubMedCrossRefGoogle Scholar
  40. 40.
    Pirrotta, V. (1988) Biotechnology 10, 437–456.PubMedGoogle Scholar
  41. 41.
    Patton, J. S., Gomes, X. V., and Geyer, P. K. (1992) Nucleic Acids Res. 20, 5859–5860.PubMedCrossRefGoogle Scholar
  42. 42.
    Berghammer, A. J., Klingler, M., and Wimmer, E. A. (1999) Nature 402, 370–371.PubMedCrossRefGoogle Scholar
  43. 43.
    Horn, C. and Wimmer, E. A. (2000) Dev. Genes Evol. 210, 630–637.PubMedCrossRefGoogle Scholar
  44. 44.
    Rorth, P., Szabo, K., Bailey, A., Laverty, T., Rehm, J., Rubin, G. M., Weigmann, K., Milan, M., Benes, V., Ansorge, W., and Cohen, S. M. (1998) Development 125, 1049–1057.PubMedGoogle Scholar
  45. 45.
    Metaxakis, A., Oehler, S., Klinakis, A., and Savakis, C. (2005) Genetics 171, 571–581.PubMedCrossRefGoogle Scholar
  46. 46.
    Hacker, U., Nystedt, S., Barmchi, M. P., Horn, C., and Wimmer, E. A. (2003) Proc. Natl. Acad. Sci. U. S. A 100, 7720–7725.CrossRefGoogle Scholar
  47. 47.
    Horn, C., Offen, N., Nystedt, S., Hacker, U., and Wimmer, E. A. (2003) Genetics 163, 647–661.PubMedGoogle Scholar
  48. 48.
    Thibault, S. T., Singer, M. A., Miyazaki, W. Y., Milash, B., Dompe, N. A., Singh, C. M., Buchholz, R., Demsky, M., Fawcett, R., Francis-Lang, H. L., Ryner, L., Cheung, L. M., Chong, A., Erickson, C., Fisher, W. W., Greer, K., Hartouni, S. R., Howie, E., Jakkula, L., Joo, D., Killpack, K., Laufer, A., Mazzotta, J., Smith, R. D., Stevens, L. M., Stuber, C., Tan, L. R., Ventura, R., Woo, A., Zakrajsek, I., Zhao, L., Chen, F., Swimmer, C., Kopczynski, C., Duyk, G., Winberg, M. L., and Margolis, J. (2004) Nat. Genet. 36, 283–287.PubMedCrossRefGoogle Scholar
  49. 49.
    Golic, K. G. and Lindquist, S. (1989) Cell 59, 499–509.PubMedCrossRefGoogle Scholar
  50. 50.
    Heidmann, D. and Lehner, C. F. (2001) Dev. Genes Evol. 211, 458–465.PubMedCrossRefGoogle Scholar
  51. 51.
    McLeod, M., Craft, S., and Broach, J. R. (1986) Mol. Cell Biol. 6, 3357–3367.PubMedGoogle Scholar
  52. 52.
    Groth, A. C., Olivares, E. C., Thyagarajan, B., and Calos, M. P. (2000) Proc. Natl. Acad. Sci. U. S. A 97, 5995–6000.CrossRefGoogle Scholar
  53. 53.
    Golic, M. M., Rong, Y. S., Petersen, R. B., Lindquist, S. L., and Golic, K. G. (1997) Nucleic Acids Res. 25, 3665–3671.PubMedCrossRefGoogle Scholar
  54. 54.
    Golic, K. G. and Golic, M. M. (1996) Genetics 144, 1693–1711.PubMedGoogle Scholar
  55. 55.
    Schlake, T. and Bode, J. (1994) Biochemistry 33, 12746–12751.PubMedCrossRefGoogle Scholar
  56. 56.
    Bateman, J. R., Lee, A. M., and Wu, C. T. (2006) Genetics 173, 769–777.PubMedCrossRefGoogle Scholar
  57. 57.
    Horn, C. and Handler, A. M. (2005) Proc. Natl. Acad. Sci. U. S. A 102, 12483–12488.CrossRefGoogle Scholar
  58. 58.
    Oberstein, A., Pare, A., Kaplan, L., and Small, S. (2005) Nat. Methods 2, 583–585.Google Scholar
  59. 59.
    St Johnston, D. (2002) Nat. Rev. Genet. 3, 176–188.CrossRefGoogle Scholar
  60. 60.
    Zhai, R. G., Hiesinger, P. R., Koh, T. W., Verstreken, P., Schulze, K. L., Cao, Y., Jafar-Nejad, H., Norga, K. K., Pan, H., Bayat, V., Greenbaum, M. P., and Bellen, H. J. (2003) Proc. Natl. Acad. Sci. U. S. A 100, 10860–10865.CrossRefGoogle Scholar
  61. 61.
    Mamanova, L., Coffey, A. J., Scott, C. E., Kozarewa, I., Turner, E. H., Kumar, A., Howard, E., Shendure, J., and Turner, D. J. (2010) Nat. Methods 7, 111–118.Google Scholar
  62. 62.
    Cook, R. K., Deal, M. E., Deal, J. A., Garton, R. D., Brown, C. A., Ward, M. E., Andrade, R. S., Spana, E. P., Kaufman, T. C., and Cook, K. R. (2010) Genetics 186, 1095–1109.PubMedCrossRefGoogle Scholar
  63. 63.
    Xu, T. and Rubin, G. M. (1993) Development 117, 1223–1237.PubMedGoogle Scholar
  64. 64.
    Newsome, T. P., Asling, B., and Dickson, B. J. (2000) Development 127, 851–860.PubMedGoogle Scholar
  65. 65.
    Stowers, R. S. and Schwarz, T. L. (1999) Genetics 152, 1631–1639.PubMedGoogle Scholar
  66. 66.
    Verstreken, P., Koh, T. W., Schulze, K. L., Zhai, R. G., Hiesinger, P. R., Zhou, Y., Mehta, S. Q., Cao, Y., Roos, J., and Bellen, H. J. (2003) Neuron 40, 733–748.PubMedCrossRefGoogle Scholar
  67. 67.
    Tien, A. C., Rajan, A., Schulze, K. L., Ryoo, H. D., Acar, M., Steller, H., and Bellen, H. J. (2008) J. Cell Biol. 182, 1113–1125.PubMedCrossRefGoogle Scholar
  68. 68.
    Kango-Singh, M., Nolo, R., Tao, C., Verstreken, P., Hiesinger, P. R., Bellen, H. J., and Halder, G. (2002) Development 129, 5719–5730.PubMedCrossRefGoogle Scholar
  69. 69.
    Menut, L., Vaccari, T., Dionne, H., Hill, J., Wu, G., and Bilder, D. (2007) Genetics 177, 1667–1677.PubMedCrossRefGoogle Scholar
  70. 70.
    Mehta, S. Q., Hiesinger, P. R., Beronja, S., Zhai, R. G., Schulze, K. L., Verstreken, P., Cao, Y., Zhou, Y., Tepass, U., Crair, M. C., and Bellen, H. J. (2005) Neuron 46, 219–232.PubMedCrossRefGoogle Scholar
  71. 71.
    Hiesinger, P. R., Fayyazuddin, A., Mehta, S. Q., Rosenmund, T., Schulze, K. L., Zhai, R. G., Verstreken, P., Cao, Y., Zhou, Y., Kunz, J., and Bellen, H. J. (2005) Cell 121, 607–620.PubMedCrossRefGoogle Scholar
  72. 72.
    Lee, T. and Luo, L. (1999) Neuron 22, 451–461.PubMedCrossRefGoogle Scholar
  73. 73.
    Awasaki, T. and Lee, T. (2011) Glia 59, 1377–1386.Google Scholar
  74. 74.
    Duffy, J. B., Harrison, D. A., and Perrimon, N. (1998) Development 125, 2263–2271.PubMedGoogle Scholar
  75. 75.
    Hoskins, R. A., Carlson, J. W., Kennedy, C., Acevedo, D., Evans-Holm, M., Frise, E., Wan, K. H., Park, S., Mendez-Lago, M., Rossi, F., Villasante, A., Dimitri, P., Karpen, G. H., and Celniker, S. E. (2007) Science 316, 1625–1628.PubMedCrossRefGoogle Scholar
  76. 76.
    Sharan, S. K., Thomason, L. C., Kuznetsov, S. G., and Court DL (2009) Nat. Protoc. 4, 206–223.CrossRefGoogle Scholar
  77. 77.
    Wild, J., Hradecna, Z., and Szybalski, W. (2002) Genome Res. 12, 1434–1444.PubMedCrossRefGoogle Scholar
  78. 78.
    Pepple, K. L., Atkins, M., Venken, K., Wellnitz, K., Harding, M., Frankfort, B., and Mardon, G. (2008) Development 135, 4071–4079.PubMedCrossRefGoogle Scholar
  79. 79.
    Venken, K. J., Kasprowicz, J., Kuenen, S., Yan, J., Hassan, B. A., and Verstreken, P. (2008) Nucleic Acids Res. 36, e114.PubMedCrossRefGoogle Scholar
  80. 80.
    Venken, K. J., Popodi, E., Holtzman, S. L., Schulze, K. L., Park, S., Carlson, J. W., Hoskins, R. A., Bellen, H. J., and Kaufman, T. C. (2010) Genetics 186, 1111–1125.PubMedCrossRefGoogle Scholar
  81. 81.
    Fire, A., Xu, S., Montgomery, M. K., Kostas, S. A., Driver, S. E., and Mello, C. C. (1998) Nature 391, 806–811.PubMedCrossRefGoogle Scholar
  82. 82.
    Kennerdell, J. R. and Carthew, R. W. (1998) Cell 95, 1017–1026.PubMedCrossRefGoogle Scholar
  83. 83.
    Fortier, E. and Belote, J. M. (2000) Genesis. 26, 240–244.PubMedCrossRefGoogle Scholar
  84. 84.
    Lam, G. and Thummel, C. S. (2000) Curr. Biol. 10, 957–963.PubMedCrossRefGoogle Scholar
  85. 85.
    Kennerdell, J. R. and Carthew, R. W. (2000) Nat. Biotechnol. 18, 896–898.PubMedCrossRefGoogle Scholar
  86. 86.
    Dietzl, G., Chen, D., Schnorrer, F., Su, K. C., Barinova, Y., Fellner, M., Gasser, B., Kinsey, K., Oppel, S., Scheiblauer, S., Couto, A., Marra, V., Keleman, K., and Dickson, B. J. (2007) Nature 448, 151–156.PubMedCrossRefGoogle Scholar
  87. 87.
    Neumuller, R. A. and Perrimon, N. (2011) Wiley. Interdiscip. Rev. Syst. Biol. Med. 3, 471–478.Google Scholar
  88. 88.
    Neely, G. G., Hess, A., Costigan, M., Keene, A. C., Goulas, S., Langeslag, M., Griffin, R. S., Belfer, I., Dai, F., Smith, S. B., Diatchenko, L., Gupta, V., Xia, C. P., Amann, S., Kreitz, S., Heindl-Erdmann, C., Wolz, S., Ly, C. V., Arora, S., Sarangi, R., Dan, D., Novatchkova, M., Rosenzweig, M., Gibson, D. G., Truong, D., Schramek, D., Zoranovic, T., Cronin, S. J., Angjeli, B., Brune, K., Dietzl, G., Maixner, W., Meixner, A., Thomas, W., Pospisilik, J. A., Alenius, M., Kress, M., Subramaniam, S., Garrity, P. A., Bellen, H. J., Woolf, C. J., and Penninger, J. M. (2010) Cell 143, 628–638.PubMedCrossRefGoogle Scholar
  89. 89.
    Kondo, S., Booker, M., and Perrimon, N. (2009) Genetics 183, 1165–1173.PubMedCrossRefGoogle Scholar
  90. 90.
    Langer, C. C., Ejsmont, R. K., Schonbauer, C., Schnorrer, F., and Tomancak, P. (2010) PLoS. ONE. 5, e8928.CrossRefGoogle Scholar
  91. 91.
    Richards, S., Liu, Y., Bettencourt, B. R., Hradecky, P., Letovsky, S., Nielsen, R., Thornton, K., Hubisz, M. J., Chen, R., Meisel, R. P., Couronne, O., Hua, S., Smith, M. A., Zhang, P., Liu, J., Bussemaker, H. J., van Batenburg, M. F., Howells, S. L., Scherer, S. E., Sodergren, E., Matthews, B. B., Crosby, M. A., Schroeder, A. J., Ortiz-Barrientos, D., Rives, C. M., Metzker, M. L., Muzny, D. M., Scott, G., Steffen, D., Wheeler, D. A., Worley, K. C., Havlak, P., Durbin, K. J., Egan, A., Gill, R., Hume, J., Morgan, M. B., Miner, G., Hamilton, C., Huang, Y., Waldron, L., Verduzco, D., Clerc-Blankenburg, K. P., Dubchak, I., Noor, M. A., Anderson, W., White, K. P., Clark, A. G., Schaeffer, S. W., Gelbart, W., Weinstock, G. M., and Gibbs, R. A. (2005) Genome Res. 15, 1–18.PubMedCrossRefGoogle Scholar
  92. 92.
    Wang, Z., Engler, P., Longacre, A., and Storb, U. (2001) Genome Res. 11, 137–142.PubMedCrossRefGoogle Scholar
  93. 93.
    Schulz, J. G., David, G., and Hassan, B. A. (2009) Nucleic Acids Res. 37, e93.PubMedCrossRefGoogle Scholar
  94. 94.
    Brand, A. H. and Perrimon, N. (1993) Development 118, 401–415.PubMedGoogle Scholar
  95. 95.
    Bellen, H. J., Levis, R. W., He, Y., Carlson, J. W., Evans-Holm, M., Bae, E., Kim, J., Metaxakis, A., Savakis, C., Schulze, K. L., Hoskins, R. A., and Spradling, A. C. (2011) The Drosophila gene disruption ­project: progress using transposons with ­distinctive site specificities. Genetics 188, 731–743.PubMedGoogle Scholar
  96. 96.
    Spradling, A. C., Bellen, H. J., and Hoskins, R. A. (2011) Drosophila P elements preferentially transpose to replication origins. Proc. Natl. Acad. Sci. U. S. A. 108, 15948–15953.PubMedGoogle Scholar
  97. 97.
    Venken, K. J., Schulze, K. L., Haelterman, N. A., Pan, H., He, Y., Evans-Holm, M., Carlson, J. W., Levis, R. W., Spradling, A. C., Hoskins, R. A., and Bellen, H. J. (2011) MiMIC: a highly versatile transposon insertion resource for engineering Drosophila melanogaster genes. Nat. Methods 8, 737–743.PubMedGoogle Scholar
  98. 98.
    Venken, K. J., Simpson, J. H., and Bellen, H. J. (2011) Genetic manipulation of genes and cells in the nervous system of the fruit fly. Neuron 72, 202–230.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  1. 1.Department of Molecular and Human GeneticsHoward Hughes Medical Institute, Baylor College of MedicineHoustonUSA
  2. 2.Department of Molecular and Human GeneticsHoward Hughes Medical Institute Program in Developmental Biology, Baylor College of MedicineHoustonUSA

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