Recombineering Hunchback identifies two conserved domains required to maintain neuroblast competence and specify early-born neuronal identity

Development

Volumn 137, Issue 9, 2010, Pages 1421-1430

  Tran, Khoa D ^a   Miller, Michael R ^a   Doe, Chris Q ^a  

^a UNIVERSITY OF OREGON   (United States)

Author keywords

Competence; Drosophila; Hunchback; Ikaros; Neurogenesis; Temporal identity; Transcription

Indexed keywords

IKAROS TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PDM2; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; DROSOPHILA PROTEIN; HOMEODOMAIN PROTEIN; HUNCHBACK PROTEIN, DROSOPHILA; PDM2 PROTEIN, DROSOPHILA; TRANSCRIPTION FACTOR POU;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DROSOPHILA; EMBRYO; GENE CONTROL; GENE DELETION; GENE EXPRESSION; GENE REPRESSION; GENE SILENCING; GENE TARGETING; GENETIC RECOMBINATION; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; IMMUNOHISTOCHEMISTRY; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NEUROBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; ANIMAL; CENTRAL NERVOUS SYSTEM; CONFOCAL MICROSCOPY; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PRENATAL DEVELOPMENT; PROTEIN TERTIARY STRUCTURE;

HEXAPODA; MAMMALIA;

ANIMALS; CENTRAL NERVOUS SYSTEM; DNA-BINDING PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; MICROSCOPY, CONFOCAL; NEUROGENESIS; NEURONS; POU DOMAIN FACTORS; PROTEIN STRUCTURE, TERTIARY; TRANSCRIPTION FACTORS;

EID: 77951249368     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.048678     Document Type: Article

References (54)

1. Albertson, R., Chabu, C., Sheehan, A. and Doe, C. Q. (2004). Scribble protein domain mapping reveals a multistep localization mechanism and domains necessary for establishing cortical polarity. J. Cell Sci. 117, 6061-6070. (Pubitemid 40123972)
2. Baumgardt, M., Karlsson, D., Terriente, J., Diaz-Benjumea, F. J. and Thor, S. (2009). Neuronal subtype specification within a lineage by opposing temporal feed-forward loops. Cell 139, 969-982.
3. Berman, B. P., Nibu, Y., Pfeiffer, B. D., Tomancak, P., Celniker, S. E., Levine, M., Rubin, G. M. and Eisen, M. B. (2002). Exploiting transcription factor binding site clustering to identify cis-regulatory modules involved in pattern formation in the Drosophila genome. Proc. Natl. Acad. Sci. USA 99, 757-762. (Pubitemid 34106583)
4. Berman, B. P., Pfeiffer, B. D., Laverty, T. R., Salzberg, S. L., Rubin, G. M., Eisen, M. B. and Celniker, S. E. (2004). Computational identification of developmental enhancers: conservation and function of transcription factor binding-site clusters in Drosophila melanogaster and Drosophila pseudoobscura. Genome Biol. 5, R61.
5. 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. (Pubitemid 46364156)
6. Bossing, T., Udolph, G., Doe, C. Q. and Technau, G. M. (1996). The embryonic central nervous system lineages of Drosophila melanogaster. I. Neuroblast lineages derived from the ventral half of the neuroectoderm. Dev. Biol. 179, 41-64. (Pubitemid 26363246)
7. Brand, A. H. and Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415.
8. Broadus, J., Skeath, J. B., Spana, E. P., Bossing, T., Technau, G. and Doe, C. Q. (1995). New neuroblast markers and the origin of the aCC/pCC neurons in the Drosophila central nervous system. Mech. Dev. 53, 393-402.
9. Cepko, C. L. (1999). The roles of intrinsic and extrinsic cues and bHLH genes in the determination of retinal cell fates. Curr. Opin. Neurobiol. 9, 37-46.
10. Cleary, M. D. and Doe, C. Q. (2006). Regulation of neuroblast competence: multiple temporal identity factors specify distinct neuronal fates within a single early competence window. Genes Dev. 20, 429-434.
11. Desai, A. R. and McConnell, S. K. (2000). Progressive restriction in fate potential by neural progenitors during cerebral cortical development. Development 127, 2863-2872.
12. Doe, C. Q. and Skeath, J. B. (1996). Neurogenesis in the insect central nervous system. Curr. Opin. Neurobiol. 6, 18-24. (Pubitemid 26102962)
13. Elliott, J., Jolicoeur, C., Ramamurthy, V. and Cayouette, M. (2008). Ikaros confers early temporal competence to mouse retinal progenitor cells. Neuron 60, 26-39.
14. Gaul, U., Seifert, E., Schuh, R. and Jackle, H. (1987). Analysis of Kruppel protein distribution during early Drosophila development reveals posttranscriptional regulation. Cell 50, 639-647.
15. Grosskortenhaus, R., Pearson, B. J., Marusich, A. and Doe, C. Q. (2005). Regulation of temporal identity transitions in Drosophila neuroblasts. Dev. Cell 8, 193-202. (Pubitemid 40197736)
16. Grosskortenhaus, R., Robinson, K. J. and Doe, C. Q. (2006). Pdm and Castor specify late-born motor neuron identity in the NB7-1 lineage. Genes Dev. 20, 2618-2627. (Pubitemid 44396845)
17. Han, K. and Manley, J. L. (1993). Functional domains of the Drosophila Engrailed protein. EMBO J. 12, 2723-2733. (Pubitemid 23218322)
18. Hanashima, C., Li, S. C., Shen, L., Lai, E. and Fishell, G. (2004). Foxg1 suppresses early cortical cell fate. Science 303, 56-59. (Pubitemid 38055766)
19. Harrison, D. A., Binari, R., Nahreini, T. S., Gilman, M. and Perrimon, N. (1995). Activation of a Drosophila Janus kinase (JAK) causes hematopoietic neoplasia and developmental defects. EMBO J. 14, 2857-2865.
20. Hoch, M., Seifert, E. and Jackle, H. (1991). Gene expression mediated by cis-acting sequences of the Kruppel gene in response to the Drosophila morphogens bicoid and hunchback. EMBO J. 10, 2267-2278. (Pubitemid 21905700)
21. Hulskamp, M., Pfeifle, C. and Tautz, D. (1990). A morphogenetic gradient of hunchback protein organizes the expression of the gap genes Kruppel and knirps in the early Drosophila embryo. Nature 346, 577-580. (Pubitemid 20238812)
22. Hulskamp, M., Lukowitz, W., Beermann, A., Glaser, G. and Tautz, D. (1994). Differential regulation of target genes by different alleles of the segmentation gene hunchback in Drosophila. Genetics 138, 125-134. (Pubitemid 24262185)
23. Isshiki, T., Pearson, B., Holbrook, S. and Doe, C. Q. (2001). Drosophila neuroblasts sequentially express transcription factors which specify the temporal identity of their neuronal progeny. Cell 106, 511-521. (Pubitemid 32786994)
24. Jaynes, J. B. and O'Farrell, P. H. (1991). Active repression of transcription by the engrailed homeodomain protein. EMBO J. 10, 1427-1433. (Pubitemid 21905608)
25. Kambadur, R., Koizumi, K., Stivers, C., Nagle, J., Poole, S. J. and Odenwald, W. F. (1998). Regulation of POU genes by castor and hunchback establishes layered compartments in the Drosophila CNS. Genes Dev. 12, 246-260. (Pubitemid 28060454)
26. Kehle, J., Beuchle, D., Treuheit, S., Christen, B., Kennison, J. A., Bienz, M. and Muller, J. (1998). dMi-2, a hunchback-interacting protein that functions in polycomb repression. Science 282, 1897-1900. (Pubitemid 28555270)
27. Kosman, D., Small, S. and Reinitz, J. (1998). Rapid preparation of a panel of polyclonal antibodies to Drosophila segmentation proteins. Dev. Genes Evol. 208, 290-294. (Pubitemid 28388897)
28. Lai, S. L. and Lee, T. (2006). Genetic mosaic with dual binary transcriptional systems in Drosophila. Nat. Neurosci. 9, 703-709.
29. Lai, Z. C., Fortini, M. E. and Rubin, G. M. (1991). The embryonic expression patterns of zfh-1 and zfh-2, two Drosophila genes encoding novel zinc-finger homeodomain proteins. Mech. Dev. 34, 123-134.
30. Markstein, M., Pitsouli, C., Villalta, C., Celniker, S. E. and Perrimon, N. (2008). Exploiting position effects and the gypsy retrovirus insulator to engineer precisely expressed transgenes. Nat. Genet. 40, 476-483. (Pubitemid 351450875)
31. Maurange, C., Cheng, L. and Gould, A. P. (2008). Temporal transcription factors and their targets schedule the end of neural proliferation in Drosophila. Cell 133, 891-902. (Pubitemid 351707683)
32. Miller, M. R., Robinson, K. J., Cleary, M. D. and Doe, C. Q. (2009). TU-tagging: cell type-specific RNA isolation from intact complex tissues. Nat. Methods 6, 439-441.
33. Novotny, T., Eiselt, R. and Urban, J. (2002). Hunchback is required for the specification of the early sublineage of neuroblast 7-3 in the Drosophila central nervous system. Development 129, 1027-1036. (Pubitemid 34874126)
34. Odenwald, W. F., Rasband, W., Kuzin, A. and Brody, T. (2005). EVOPRINTER, a multigenomic comparative tool for rapid identification of functionally important DNA. Proc. Natl. Acad. Sci. USA 102, 14700-14705. (Pubitemid 41457119)
35. Pankratz, M. J., Busch, M., Hoch, M., Seifert, E. and Jackle, H. (1992). Spatial control of the gap gene knirps in the Drosophila embryo by posterior morphogen system. Science 255, 986-989.
36. Papatsenko, D. and Levine, M. S. (2008). Dual regulation by the Hunchback gradient in the Drosophila embryo. Proc. Natl. Acad. Sci. USA 105, 2901-2906. (Pubitemid 351723641)
37. Patel, N. H., Martin-Blanco, E., Coleman, K. G., Poole, S. J., Ellis, M. C., Kornberg, T. B. and Goodman, C. S. (1989). Expression of engrailed proteins in arthropods, annelids, and chordates. Cell 58, 955-968.
38. Patel, N. H., Condron, B. G. and Zinn, K. (1994). Pair-rule expression patterns of even-skipped are found in both short- and long-germ beetles. Nature 367, 429-434. (Pubitemid 24984611)
39. Pearson, B. J. and Doe, C. Q. (2003). Regulation of neuroblast competence in Drosophila. Nature 425, 624-628.
40. Pelegri, F. and Lehmann, R. (1994). A role of polycomb group genes in the regulation of gap gene expression in Drosophila. Genetics 136, 1341-1353. (Pubitemid 24097863)
41. Rapaport, D. H., Patheal, S. L. and Harris, W. A. (2001). Cellular competence plays a role in photoreceptor differentiation in the developing Xenopus retina. J. Neurobiol. 49, 129-141.
42. Rivera-Pomar, R., Lu, X., Perrimon, N., Taubert, H. and Jackle, H. (1995). Activation of posterior gap gene expression in the Drosophila blastoderm. Nature 376, 253-256.
43. Schmid, A., Chiba, A. and Doe, C. Q. (1999). Clonal analysis of Drosophila embryonic neuroblasts: neural cell types, axon projections and muscle targets. Development 126, 4653-4689.
44. Schulz, C. and Tautz, D. (1994). Autonomous concentration-dependent activation and repression of Kruppel by hunchback in the Drosophila embryo. Development 120, 3043-3049. (Pubitemid 24312070)
45. Siegrist, S. E. and Doe, C. Q. (2005). Microtubule-induced Pins/Galphai cortical polarity in Drosophila neuroblasts. Cell 123, 1323-1335. (Pubitemid 41821788)
46. Struhl, G., Johnston, P. and Lawrence, P. A. (1992). Control of Drosophila body pattern by the hunchback morphogen gradient. Cell 69, 237-249.
47. Sun, L., Liu, A. and Georgopoulos, K. (1996). Zinc finger-mediated protein interactions modulate Ikaros activity, a molecular control of lymphocyte development. EMBO J. 15, 5358-5369. (Pubitemid 26336218)
48. Tautz, D., Lehman, R., Schnurh, H., Schuh, R., Seifert, E., Kienlin, A., Jones, K. and Jäckle, H. (1987). Finger protein of novel structure encoded by hunchback, a second member of the gap class of Drosophila segmentation genes. Nature 327, 383-389. (Pubitemid 17075810)
49. Tran, K. D. and Doe, C. Q. (2008). Pdm and Castor close successive temporal identity windows in the NB3-1 lineage. Development 135, 3491-3499.
50. Treisman, J. and Desplan, C. (1989). The products of the Drosophila gap genes hunchback and Kruppel bind to the hunchback promoters. Nature 341, 335-337. (Pubitemid 20102103)
51. Triezenberg, S. J., Kingsbury, R. C. and McKnight, S. L. (1988). Functional dissection of VP16, the trans-activator of herpes simplex virus immediate early gene expression. Genes Dev. 2, 718-729.
52. Walsh, C. and Reid, C. (1995). Cell lineage and patterns of migration in the developing cortex. Ciba Found. Symp. 193, 21-40. (Pubitemid 20331707)
53. Warming, S., Costantino, N., Court, D. L., Jenkins, N. A. and Copeland, N. G. (2005). Simple and highly efficient BAC recombineering using galK selection. Nucleic Acids Res. 33, e36. (Pubitemid 41439937)
54. Wimmer, E. A., Carleton, A., Harjes, P., Turner, T. and Desplan, C. (2000). Bicoid-independent formation of thoracic segments in Drosophila. Science 287, 2476-2479. (Pubitemid 30185441)