Insertional mutagenesis by the Tol2 transposon-mediated enhancer trap approach generated mutations in two developmental genes: tcf7 and synembryn-like

Development

Volumn 135, Issue 1, 2008, Pages 159-169

  Nagayoshi, Saori ^a   Hayashi, Eriko ^b   Abe, Gembu ^a   Osato, Naoki ^c   Asakawa, Kazuhide ^a   Urasaki, Akihiro ^a   Horikawa, Kazuki ^b,e   Ikeo, Kazuho ^c,d   Takeda, Hiroyuki ^b   Kawakami, Koichi ^a,d  

^a NATIONAL INSTITUTE OF GENETICS   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c NATIONAL INSTITUTE OF GENETICS   (Japan)

^d GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^e HOKKAIDO UNIVERSITY   (Japan)

Author keywords

Enhancer trapping; Insertional mutagenesis; Synembryn; tcf7; Zebrafish

Indexed keywords

ADENYLATE CYCLASE; DNA; FORSKOLIN; GREEN FLUORESCENT PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; HEAT SHOCK PROTEIN 70; SYNEMBRYN; T CELL FACTOR PROTEIN; T CELL FACTOR PROTEIN 7; TRANSPOSASE; UNCLASSIFIED DRUG; WNT PROTEIN;

ANIMAL TISSUE; ARTICLE; CELL SPECIFICITY; CONTROLLED STUDY; DEVELOPMENTAL GENETICS; ECTODERM; EMBRYO; EMBRYO DEATH; EMBRYO DEVELOPMENT; ENHANCER REGION; EXON; GENE DISRUPTION; GENE EXPRESSION PROFILING; GENE INSERTION; GENE MAPPING; GENETIC SCREENING; GENOME; HETEROZYGOSITY; INTRON; MUTAGENESIS; MUTATIONAL ANALYSIS; NONHUMAN; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; TISSUE SPECIFICITY; TRANSPOSON; VERTEBRATE; ZEBRA FISH;

ANIMALS; CLONING, MOLECULAR; DNA TRANSPOSABLE ELEMENTS; EMBRYO, NONMAMMALIAN; ENHANCER ELEMENTS (GENETICS); FORSKOLIN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MUTAGENESIS, INSERTIONAL; MUTATION; NUCLEAR PROTEINS; PHENOTYPE; PHYLOGENY; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; ZEBRAFISH; ZEBRAFISH PROTEINS;

CAENORHABDITIS ELEGANS; DANIO RERIO; VERTEBRATA;

EID: 38849083900     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.009050     Document Type: Article

References (48)

1. Abe, G., Ide, H. and Tamura, K. (2007). Function of FGF signaling in the developmental process of the median fin fold in zebrafish. Dev. Biol. 304, 355-366.
2. Agarwal, P., Wylie, J. N., Galceran, J., Arkhitko, O., Li, C., Deng, C., Grosschedl, R. and Bruneau, B. G. (2003). Tbx5 is essential for forelimb bud initiation following patterning of the limb field in the mouse embryo. Development 130, 623-633.
3. Akimenko, M. A., Ekker, M., Wegner, J., Lin, W. and Westerfield, M. (1994). Combinatorial expression of three zebrafish genes related to distal-less: part of a homeobox gene code for the head. J. Neurosci. 14, 3475-3486.
4. Amsterdam, A. and Becker, T. S. (2005). Transgenes as screening tools to probe and manipulate the zebrafish genome. Dev. Dyn. 234, 255-268.
5. Amsterdam, A., Burgess, S., Golling, G., Chen, W., Sun, Z., Townsend, K., Farrington, S., Haldi, M. and Hopkins, N. (1999). A large-scale insertional mutagenesis screen in zebrafish. Genes Dev. 13, 2713-2724.
6. Amsterdam, A., Nissen, R. M., Sun, Z., Swindell, E. C., Farrington, S. and Hopkins, N. (2004). Identification of 315 genes essential for early zebrafish development. Proc. Natl. Acad. Sci. USA 101, 12792-12797.
7. Balciunas, D., Davidson, A. E., Sivasubbu, S., Hermanson, S. B., Welle, Z. and Ekker, S. C. (2004). Enhancer trapping in zebrafish using the Sleeping Beauty transposon. BMC Genomics 5, 62.
8. Barresi, M. J., Stickney, H. L. and Devoto, S. H. (2000). The zebrafish slow-muscle-omitted gene product is required for Hedgehog signal transduction and the development of slow muscle identity. Development 127, 2189-2199.
9. Blackshear, P. J., Graves, J. P., Stumpo, D. J., Cobos, I., Rubenstein, J. L. and Zeldin, D. C. (2003). Graded phenotypic response to partial and complete deficiency of a brain-specific transcript variant of the winged helix transcription factor RFX4. Development 130, 4539-4552.
10. Brown, S. A., Imbalzano, A. N. and Kingston, R. E. (1996). Activator-dependent regulation of transcriptional pausing on nucleosomal templates. Genes Dev. 10, 1479-1490.
11. 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. (1996). A genetic screen for mutations affecting embryogenesis in zebrafish. Development 123, 37-46.
12. Ellingsen, S., Laplante, M. A., Konig, 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. Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783-791.
14. Fischer, S., Draper, B. W. and Neumann, C. J. (2003). The zebrafish fgf24 mutant identifies an additional level of Fgf signaling involved in vertebrate forelimb initiation. Development 130, 3515-3524.
15. Gaiano, N., Amsterdam, A., Kawakami, K., Allende, M., Becker, T. and Hopkins, N. (1996). Insertional mutagenesis and rapid cloning of essential genes in zebrafish. Nature 383, 829-832.
16. Galceran, J., Farinas, I., Depew, M. J., Clevers, H. and Grosschedl, R. (1999). Wnt3a-/-like phenotype and limb deficiency in Lef1 (-/ -)Tcf1(-/-) mice. Genes Dev. 13, 709-717.
17. Haffter, P., Granato, M., Brand, M., Mullins, M. C., Hammerschmidt, M., Kane, D. A., Odenthal, J., van Eeden, F. J., Jiang, Y. J., Heisenberg, C. P. et al. (1996). The identification of genes with unique and essential functions in the development of the zebrafish, Danio rerio. Development 123, 1-36.
18. Halloran, M. C., Sato-Maeda, M., Warren, J. T., Su, F., Lele, Z., Krone, P. H., Kuwada, J. Y. and Shoji, W. (2000). Laser-induced gene expression in specific cells of transgenic zebrafish. Development 127, 1953-1960.
19. Kawakami, K. (2004). Transgenesis and gene trap methods in zebrafish by using the Tol2 transposable element. Methods Cell Biol. 77, 201-222.
20. Kawakami, K. (2005). Transposon tools and methods in zebrafish. Dev. Dyn. 234, 244-254.
21. Kawakami, K. and Shima, A. (1999). Identification 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.
22. Kawakami, K., Koga, A., Hori, H. and Shima, A. (1998). Excision of the Tol2 transposable element of the medaka fish, Oryzias latipes, in zebrafish, Danio rerio. Gene 225, 17-22.
23. Kawakami, K., Shima, A. and Kawakami, N. (2000). Identification 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.
24. Kawakami, Y., Capdevila, J., Buscher, D., Itoh, T., Rodriguez Esteban, C. and Izpisua Belmonte, J. C. (2001). WNT signals control FGF-dependent limb initiation and AER induction in the chick embryo. Cell 104, 891-900.
25. Kawakami, K., Takeda, H., Kawakami, N., Kobayashi, M., Matsuda, N. and Mishina, M. (2004). A transposon-mediated gene trap approach identifies developmentally regulated genes in zebrafish. Dev. Cell 7, 133-144.
26. Kengaku, M., Capdevila, J., Rodriguez-Esteban, C., De La Pena, J., Johnson, R. L., Belmonte, J. C. and Tabin, C. J. (1998). Distinct WNT pathways regulating AER formation and dorsoventral polarity in the chick limb bud. Science 280, 1274-1277.
27. Kent, W. J. (2002). BLAT-the BLAST-like alignment tool. Genome Res. 12, 656-664.
28. Kikuta, H., Laplante, M., Navratilova, P., Komisarczuk, A. Z., Engstrom, P. G., Fredman, D., Akalin, A., Caccamo, M., Sealy, I., Howe, K. et al. (2007). Genomic regulatory blocks encompass multiple neighboring genes and maintain conserved synteny in vertebrates. Genome Res. 17, 545-555.
29. Klattenhoff, C., Montecino, M., Soto, X., Guzman, L., Romo, X., Garcia, M. A., Mellstrom, B., Naranjo, J. R., Hinrichs, M. V. and Olate, J. (2003). Human brain synembryn interacts with Gsalpha and Gqalpha and is translocated to the plasma membrane in response to isoproterenol and carbachol. J. Cell. Physiol. 195, 151-157.
30. Kotani, T., Nagayoshi, S., Urasaki, A. and Kawakami, K. (2006). Transposon-mediated gene trapping in zebrafish. Methods 39, 199-206.
31. Logan, D. W., Burn, S. F. and Jackson, I. J. (2006). Regulation of pigmentation in zebrafish melanophores. Pigment Cell Res. 19, 206-213.
32. Miller, K. G., Emerson, M. D., McManus, J. R. and Rand, J. B. (2000). RIC-8 (Synembryn): a novel conserved protein that is required for G (q)alpha signaling in the C. elegans nervous system. Neuron 27, 289-299.
33. Mlodzik, M. and Hiromi, Y. (1992). Enhancer trap method in Drosophila: its application to neurobiology. In Methods in Neurosciences. Vol. 9 (ed. P. M. Conn), pp. 397-414. San Diego: Academic Press.
34. Ng, J. K., Kawakami, Y., Buscher, D., Raya, A., Itoh, T., Koth, C. M., Rodriguez Esteban, C., Rodriguez-Leon, J., Garrity, D. M., Fishman, M. C. et al. (2002). The limb identity gene Tbx5 promotes limb initiation by interacting with Wnt2b and Fgf10. Development 129, 5161-5170.
35. Norton, W. H., Ledin, J., Grandel, H. and Neumann, C. J. (2005). HSPG synthesis by zebrafish Ext2 and Ext13 is required for Fgf10 signalling during limb development. Development 132, 4963-4973.
36. Parinov, S., Kondrichin, I., Korzh, V. and Emelyanov, A. (2004). Tol2 transposon-mediated enhancer trap to identify developmentally regulated zebrafish genes in vivo. Dev. Dyn. 231, 449-459.
37. Reifers, F., Bohli, H., Walsh, E. C., Crossley, P. H., Stainier, D. Y. and Brand, M. (1998). Fgf8 is mutated in zebrafish acerebellar (ace) mutants and is required for maintenance of midbrain-hindbrain boundary development and somitogenesis. Development 125, 2381-2395.
38. Rougvie, A. E. and Lis, J. T. (1988). The RNA polymerase II molecule at the 5′ end of the uninduced hsp70 gene of D. melanogaster is transcriptionally engaged. Cell 54, 795-804.
39. Rzhetsky, A. and Nei, M. (1992). Statistical properties of the ordinary least-squares, generalized least-squares, and minimum-evolution methods of phylogenetic inference. J. Mol. Evol. 35, 367-375.
40. Saitou, N. and Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425.
41. Schade, M. A., Reynolds, N. K., Dollins, C. M. and Miller, K. G. (2005). Mutations that rescue the paralysis of Caenorhabditis elegans ric-8 (synembryn) mutants activate the G alpha (s) pathway and define a third major branch of the synaptic signaling network. Genetics 169, 631-649.
42. Scott, E. K., Mason, L., Arrenberg, A. B., Ziv, L., Gosse, N. J., Xiao, T., Chi, N. C., Asakawa, K., Kawakami, K. and Baier, H. (2007). Targeting neural circuitry in zebrafish using GAL4 enhancer trapping. Nat. Methods 4, 323-326.
43. Seamon, K. B., Padgett, W. and Daly, J. W. (1981). Forskolin: unique diterpene activator of adenylate cyclase in membranes and in intact cells. Proc. Natl. Acad. Sci. USA 78, 3363-3367.
44. Tall, G. G., Krumins, A. M. and Gilman, A. G. (2003). Mammalian Ric-8A (synembryn) is a heterotrimeric Galpha protein guanine nucleotide exchange factor. J. Biol. Chem. 278, 8356-8362.
45. Thompson, J. D., Higgins, D. G. and Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680.
46. Uemura, O., Okada, Y., Ando, H., Guedj, M., Higashijima, S., Shimazaki, T., Chino, N., Okano, H. and Okamoto, H. (2005). Comparative functional genomics revealed conservation and diversification of three enhancers of the isl1 gene for motor and sensory neuron-specific expression. Dev. Biol. 278, 587-606.
47. Urasaki, A., Morvan, G. and Kawakami, K. (2006). Functional dissection of the Tol2 transposable element identified the minimal cis-sequence and a highly repetitive sequence in the subterminal region essential for transposition. Genetics 174, 639-649.
48. Veien, E. S., Grierson, M. J., Saund, R. S. and Dorsky, R. I. (2005). Expression pattern of zebrafish tcf7 suggests unexplored domains of Wnt/beta-catenin activity. Dev. Dyn. 233, 233-239.