Efficient site-specific transgenesis and enhancer activity tests in medaka using PhiC31 integrase

Development (Cambridge)

Volumn 140, Issue 20, 2013, Pages 4287-4295

  Kirchmaier, Stephan ^a   Höckendorf, Burkhard ^a,b   Möller, Eva Katharina ^a   Bornhorst, Dorothee ^a   Spitz, Francois ^c   Wittbrodt, Joachim ^a,b  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

Fish; In vivo analysis; PhiC31 integrase; Position effects; Regulatory DNA

Indexed keywords

INTEGRASE; PHIC31 INTEGRASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; EMBRYO; EMBRYO DEVELOPMENT; ENHANCER REGION; ENZYME ACTIVITY; GENE LOCUS; GENE VECTOR; GENOMICS; GERM LINE; NONHUMAN; ORYZIAS; POSITION EFFECT; PRIORITY JOURNAL; PROMOTER REGION; TRANSGENE; TRANSGENICS;

FISH; IN VIVO ANALYSIS; PHIC31 INTEGRASE; POSITION EFFECTS; REGULATORY DNA;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; DNA; GENE TRANSFER TECHNIQUES; GREEN FLUORESCENT PROTEINS; HSP70 HEAT-SHOCK PROTEINS; INTEGRASES; ORYZIAS; PROMOTER REGIONS, GENETIC; TRANSGENES; ZEBRAFISH;

EID: 84884934419     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.096081     Document Type: Article

References (50)

1. Allen, B. G. and Weeks, D. L. (2005). Transgenic Xenopus laevis embryos can be generated using phiC31 integrase. Nat. Methods 2, 975-979.
2. Auman, H. J., Coleman, H., Riley, H. E., Olale, F., Tsai, H.-J. and Yelon, D. (2007). Functional modulation of cardiac form through regionally confined cell shape changes. PLoS Biol. 5, e53.
3. Barolo, S. (2006). Transgenic Wnt/TCF pathway reporters: all you need is Lef? Oncogene 25, 7505-7511.
4. Bateman, J. R., Johnson, J. E. and Locke, M. N. (2012). Comparing enhancer action in cis and in trans. Genetics 191, 1143-1155.
5. Bedell, V. M., Wang, Y., Campbell, J. M., Poshusta, T. L., Starker, C. G., Krug, R. G., 2nd, Tan, W., Penheiter, S. G., Ma, A. C., Leung, A. Y. H. et al. (2012). In vivo genome editing using a high-efficiency TALEN system. Nature 491, 114-118.
6. Belteki, G., Gertsenstein, M., Ow, D. W. and Nagy, A. (2003). Site-specific cassette exchange and germline transmission with mouse ES cells expressing phiC31 integrase. Nat. Biotechnol. 21, 321-324.
7. Bernstein, B. E., Birney, E., Dunham, I., Green, E. D., Gunter, C., Snyder, M. et al.; ENCODE Project Consortium (2012). An integrated encyclopedia of DNA elements in the human genome. Nature 489, 57-74.
8. Bischof, J., Maeda, R. K., Hediger, M., Karch, F. and Basler, K. (2007). An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc. Natl. Acad. Sci. USA 104, 3312-3317.
9. Blechinger, S. R., Evans, T. G., Tang, P. T., Kuwada, J. Y., Warren, J. T., Jr and Krone, P. H. (2002). The heat-inducible zebrafish hsp70 gene is expressed during normal lens development under non-stress conditions. Mech. Dev. 112, 213-215.
10. Branda, C. S. and Dymecki, S. M. (2004). Talking about a revolution: The impact of site-specific recombinases on genetic analyses in mice. Dev. Cell 6, 7-28.
11. Eichenlaub, M. P. and Ettwiller, L. (2011). De novo genesis of enhancers in vertebrates. PLoS Biol. 9, e1001188.
12. Ellingsen, S., Laplante, M. A., König, M., Kikuta, H., Furmanek, T., Hoivik, E. A. and Becker, T. S. (2005). Large-scale enhancer detection in the zebrafish genome. Development 132, 3799-3811.
13. Emelyanov, A. and Parinov, S. (2008). Mifepristone-inducible LexPR system to drive and control gene expression in transgenic zebrafish. Dev. Biol. 320, 113-121.
14. Grabher, C. and Wittbrodt, J. (2007). Meganuclease and transposon mediated transgenesis in medaka. Genome Biol. 8 Suppl., S10.
15. Groth, A. C., Olivares, E. C., Thyagarajan, B. and Calos, M. P. (2000). A phage integrase directs efficient site-specific integration in human cells. Proc. Natl. Acad. Sci. USA 97, 5995-6000.
16. Groth, A. C., Fish, M., Nusse, R. and Calos, M. P. (2004). Construction of transgenic Drosophila by using the site-specific integrase from phage phiC31. Genetics 166, 1775-1782.
17. Hu, G., Goll, M. G. and Fisher, S. (2011). ΦC31 integrase mediates efficient cassette exchange in the zebrafish germline. Dev. Dyn. 240, 2101-2107.
18. Huang, C.-J., Tu, C.-T., Hsiao, C.-D., Hsieh, F.-J. and Tsai, H.-J. (2003). Germ-line transmission of a myocardium-specific GFP transgene reveals critical regulatory elements in the cardiac myosin light chain 2 promoter of zebrafish. Dev. Dyn. 228, 30-40.
19. Ivics, Z., Hackett, P. B., Plasterk, R. H. and Izsvák, Z. (1997). Molecular reconstruction of Sleeping Beauty, a Tc1-like transposon from fish, and its transposition in human cells. Cell 91, 501-510.
20. Kapusi, E., Kempe, K., Rubtsova, M., Kumlehn, J. and Gils, M. (2012). phiC31 integrase-mediated site-specific recombination in barley. PLoS ONE 7, e45353.
21. Koster, R., Stick, R., Loosli, F. and Wittbrodt, J. (1997). Medaka spalt acts as a target gene of hedgehog signaling. Development 124, 3147-3156.
22. Lee, T. and Luo, L. (2001). Mosaic analysis with a repressible cell marker (MARCM) for Drosophila neural development. Trends Neurosci. 24, 251-254.
23. Leneuve, P., Colnot, S., Hamard, G., Francis, F., Niwa-Kawakita, M., Giovannini, M. and Holzenberger, M. (2003). Cre-mediated germline mosaicism: a new transgenic mouse for the selective removal of residual markers from tri-lox conditional alleles. Nucleic Acids Res. 31, e21.
24. Lister, J. A. (2010). Transgene excision in zebrafish using the phiC31 integrase. Genesis 48, 137-143.
25. Lu, J., Maddison, L. A. and Chen, W. (2011). PhiC31 integrase induces efficient site-specific excision in zebrafish. Transgenic Res. 20, 183-189.
26. Luo, L. (2007). Fly MARCM and mouse MADM: genetic methods of labeling and manipulating single neurons. Brain Res. Rev. 55, 220-227.
27. Mátés, L., Chuah, M. K. L., Belay, E., Jerchow, B., Manoj, N., Acosta-Sanchez, A., Grzela, D. P., Schmitt, A., Becker, K., Matrai, J. et al. (2009). Molecular evolution of a novel hyperactive Sleeping Beauty transposase enables robust stable gene transfer in vertebrates. Nat. Genet. 41, 753-761.
28. Maurano, M. T., Wang, H., Kutyavin, T. and Stamatoyannopoulos, J. A. (2012). Widespread site-dependent buffering of human regulatory polymorphism. PLoS Genet. 8, e1002599.
29. Mongin, E., Auer, T. O., Bourrat, F., Gruhl, F., Dewar, K., Blanchette, M., Wittbrodt, J. and Ettwiller, L. (2011). Combining computational prediction of cis-regulatory elements with a new enhancer assay to efficiently label neuronal structures in the medaka fish. PLoS ONE 6, e19747.
30. Mosimann, C., Puller, A. C., Lawson, K. L., Tschopp, P., Amsterdam, A. and Zon, L. I. (2013). Site-directed zebrafish transgenesis into single landing sites with the phiC31 integrase system. Dev. Dyn. 242, 949-963.
31. Neumann, C. J. and Nuesslein-Volhard, C. (2000). Patterning of the zebrafish retina by a wave of sonic hedgehog activity. Science 289, 2137-2139.
32. Ni, J.-Q., Liu, L.-P., Binari, R., Hardy, R., Shim, H.-S., Cavallaro, A., Booker, M., Pfeiffer, B. D., Markstein, M., Wang, H. et al. (2009). A Drosophila resource of transgenic RNAi lines for neurogenetics. Genetics 182, 1089-1100.
33. Pastinen, T. and Hudson, T. J. (2004). Cis-acting regulatory variation in the human genome. Science 306, 647-650.
34. Preibisch, S., Saalfeld, S. and Tomancak, P. (2009). Globally optimal stitching of tiled 3D microscopic image acquisitions. Bioinformatics 25, 1463-1465.
35. Rausch, H. and Lehmann, M. (1991). Structural analysis of the actinophage phi C31 attachment site. Nucleic Acids Res. 19, 5187-5189.
36. Raymond, C. S. and Soriano, P. (2007). High-efficiency FLP and PhiC31 sitespecific recombination in mammalian cells. PLoS ONE 2, e162.
37. Rembold, M., Lahiri, K., Foulkes, N. S. and Wittbrodt, J. (2006). Transgenesis in fish: efficient selection of transgenic fish by co-injection with a fluorescent reporter construct. Nat. Protoc. 1, 1133-1139.
38. Ritter, D. I., Dong, Z., Guo, S. and Chuang, J. H. (2012). Transcriptional enhancers in protein-coding exons of vertebrate developmental genes. PLoS ONE 7, e35202.
39. Ruf, S., Symmons, O., Uslu, V. V., Dolle, D., Hot, C., Ettwiller, L. and Spitz, F. (2011). Large-scale analysis of the regulatory architecture of the mouse genome with a transposon-associated sensor. Nat. Genet. 43, 379-386.
40. Shakes, L. A., Du, H., Wolf, H. M., Hatcher, C., Norford, D. C., Precht, P., Sen, R. and Chatterjee, P. K. (2012). Using BAC transgenesis in zebrafish to identify regulatory sequences of the amyloid precursor protein gene in humans. BMC Genomics 13, 451.
41. Thiel, C., Schwarz, M., Peng, J., Grzmil, M., Hasilik, M., Braulke, T., Kohlschütter, A., von Figura, K., Lehle, L. and Körner, C. (2003). A new type of congenital disorders of glycosylation (CDG-Ii) provides new insights into the early steps of dolichol-linked oligosaccharide biosynthesis. J. Biol. Chem. 278, 22498-22505.
42. Thomson, J. G., Chan, R., Thilmony, R., Yau, Y.-Y. and Ow, D. W. (2010). PhiC31 recombination system demonstrates heritable germinal transmission of sitespecific excision from the Arabidopsis genome. BMC Biotechnol. 10, 17.
43. Thyagarajan, B., Olivares, E. C., Hollis, R. P., Ginsburg, D. S. and Calos, M. P. (2001). Site-specific genomic integration in mammalian cells mediated by phage phiC31 integrase. Mol. Cell. Biol. 21, 3926-3934.
44. Venken, K. J., He, Y., Hoskins, R. A. and Bellen, H. J. (2006). P[acman]: a BAC transgenic platform for targeted insertion of large DNA fragments in D. melanogaster. Science 314, 1747-1751.
45. Venken, K. J. T., 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. et al. (2011). MiMIC: a highly versatile transposon insertion resource for engineering Drosophila melanogaster genes. Nat. Methods 8, 737-743.
46. Visel, A., Blow, M. J., Li, Z., Zhang, T., Akiyama, J. A., Holt, A., Plajzer-Frick, I., Shoukry, M., Wright, C., Chen, F. et al. (2009a). ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 457, 854-858.
47. Vooijs, M., Jonkers, J. and Berns, A. (2001). A highly efficient ligand-regulated Cre recombinase mouse line shows that LoxP recombination is position dependent. EMBO Rep. 2, 292-297.
48. Wu, X., Li, Y., Crise, B. and Burgess, S. M. (2003). Transcription start regions in the human genome are favored targets for MLV integration. Science 300, 1749-1751.
49. Yergeau, D. A., Kelley, C. M., Kuliyev, E., Zhu, H., Johnson Hamlet, M. R., Sater, A. K., Wells, D. E. and Mead, P. E. (2011). Remobilization of Sleeping Beauty transposons in the germline of Xenopus tropicalis. Mobile DNA 2, 15.
50. Yonemura, N., Tamura, T., Uchino, K., Kobayashi, I., Tatematsu, K., Iizuka, T., Sezutsu, H., Muthulakshmi, M., Nagaraju, J. and Kusakabe, T. (2012). PhiC31 integrase-mediated cassette exchange in silkworm embryos. Mol. Genet. Genomics 287, 731-739.