Even-skipped, acting as a repressor, regulates axonal projections in Drosophila

Development

Volumn 130, Issue 22, 2003, Pages 5385-5400

  Fujioka, Miki ^a   Lear, Bridget C ^b,d   Landgraf, Matthias ^c   Yusibova, Galina L ^a   Zhou, Jian ^a   Riley, Kristen M ^a   Patel, Nipam H ^b,e   Jaynes, James B ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d NORTHWESTERN UNIVERSITY   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Atrophin; Axon guidance; Eve; Evx; Groucho; Grunge; Hb9; Homeodomian; Nervous system; Transcriptional repressor

Indexed keywords

CHIMERIC PROTEIN; DNA BINDING PROTEIN; DROSOPHILA PROTEIN; HOMEODOMAIN PROTEIN; HYBRID PROTEIN; PROTEIN EVE; PROTEIN HB9; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; CORRELATION COEFFICIENT; DNA BINDING; DROSOPHILA; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; GENE MUTATION; GENE REPRESSION; GENE TARGETING; GENETIC CONSERVATION; GENETIC VARIABILITY; MUSCLE INNERVATION; NERVE FIBER; NERVE PROJECTION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; NULL ALLELE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; REPORTER GENE; SEQUENCE HOMOLOGY; SPECIES DIVERSITY; TRANSGENE; WILD TYPE;

ANIMALS; AXONS; CENTRAL NERVOUS SYSTEM; DROSOPHILA; DROSOPHILA PROTEINS; HOMEODOMAIN PROTEINS; NEURONS; TRANSCRIPTION FACTORS;

ARACHNIDA; HEXAPODA; INSECTA;

EID: 0344033617     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.00770     Document Type: Article

References (52)

1. Baines, R. A., Robinson, S. G., Fujioka, M., Jaynes, J. B. and Bate, M. (1999). Postsynaptic expression of tetanus toxin light chain blocks synaptogenesis in Drosophila. Curr. Biol. 9, 1267-1270.
2. 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.
3. 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.
4. 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.
5. Broihier, H. T. and Skeath, J. B. (2002). Drosophila homeodomain protein dHb9 directs neuronal fate via crossrepressive and cell-nonautonomous mechanisms. Neuron 35, 39-50.
6. Callahan, C. A., Muralidhar, M. G., Lundgren, S. E., Scully, A. L. and Thomas, J. B. (1995). Control of neuronal pathway selection by a Drosophila receptor protein-tyrosine kinase family member. Nature 376, 171-174.
7. Dickson, B. J. (2002). Molecular mechanisms of axon guidance. Science 298, 1959-1964.
8. Doe, C. Q., Smouse, D. and Goodman, C. S. (1988). Control of neuronal fate by the Drosophila segmentation gene even-skipped. Nature 333, 376-378.
9. Duman-Scheel, M. and Patel, N. H. (1999). Analysis of molecular marker expression reveals neuronal homology in distantly related arthropods. Development 126, 2327-2334.
10. Erkner, A., Roure, A., Charroux, B., Delaage, M., Holway, N., Core, N., Vola, C., Angelats, C., Pages, F., Fasano, L. et al. (2002). Grunge, related to human Atrophin-like proteins, has multiple functions in Drosophila development. Development 129, 1119-1129.
11. Frasch, M., Hoey, T., Rushlow, C., Doyle, H. and Levine, M. (1987). Characterization and localization of the even-skipped protein of Drosophila. EMBO J. 6, 749-759.
12. Frasch, M., Warrior, R., Tugwood, J. and Levine, M. (1988). Molecular analysis of even-skipped mutants in Drosophila development. Genes Dev. 2, 1824-1838.
13. Fujioka, M., Jaynes, J. B. and Goto, T. (1995). Early even-skipped stripes act as morphogenetic gradients at the single cell level to establish engrailed expression. Development 121, 4371-4382.
14. Fujioka, M., Emi-Sarker, Y., Yusibova, G. L., Goto, T. and Jaynes, J. B. (1999). Analysis of an even-skipped rescue transgene reveals both composite and discrete neuronal and early blastoderm enhancers, and multi-stripe positioning by gap gene repressor gradients. Development 126, 2527-2538.
15. Fujioka, M., Jaynes, J. B., Bejsovec, A. and Weir, M. (2000). Production of transgenic Drosophila. Methods Mol. Biol. 136, 353-363.
16. Fujioka, M., Yusibova, G. L., Patel, N. H., Brown, S. J. and Jaynes, J. B. (2002). The repressor activity of Even-skipped is highly conserved, and is sufficient to activate engrailed and to regulate both the spacing and stability of parasegment boundaries. Development 129, 4411-4421.
17. Fujita, S. C., Zipursky, S. L., Benzer, S., Ferrus, A. and Shotwell, S. L. (1982). Monoclonal antibodies against the Drosophila nervous system. Proc. Natl. Acad. Sci. USA 79, 7929-7933.
18. Han, K. and Manley, J. L. (1993). Transcriptional repression by the Drosophila even-skipped protein: definition of a minimal repression domain. Genes Dev. 7, 491-503.
19. Han, Z., Fujioka, M., Su, M., Liu, M., Jaynes, J. B. and Bodmer, R. (2002). Transcriptional integration of competence modulated by mutual repression generates cell-type specificity within the cardiogenic mesoderm. Dev. Biol. 252, 225-240.
20. Harris, R., Sabatelli, L. M. and Seeger, M. A. (1996). Guidance cues at the Drosophila - CNS midline: identification and characterization of two Drosophila Netrin/UNC-6 homologs. Neuron 17, 217-228.
21. Hummel, T., Krukkert, K., Roos, J., Davis, G. and Klambt, C. (2000). Drosophila Futsch/22C10 is a MAP1B-like protein required for dendritic and axonal development. Neuron 26, 357-370.
22. Jaynes, J. B. and O'Farrell, P. H. (1991). Active repression of transcription by the engrailed homeodomain protein. EMBO J. 10, 1427-1433.
23. Jimenez, G., Paroush, Z. and Ish-Horowicz, D. (1997). Groucho acts as a corepressor for a subset of negative regulators, including Hairy and Engrailed. Genes Dev. 11, 3072-3082.
24. Kobayashi, M., Goldstein, R. E., Fujioka, M., Paroush, Z. and Jaynes, J. B. (2001). Groucho augments the repression of multiple Even-skipped target genes in establishing parasegment boundaries. Development 128, 1805-1815.
25. Koide, R., Ikeuchi, T., Onodera, O., Tanaka, H., Igarashi, S., Endo, K., Takahashi, H., Kondo, R., Ishikawa, A., Hayashi, T. et al. (1994). Unstable expansion of CAG repeat in hereditary dentatorubral-pallidoluysian atrophy (DRPLA). Nat. Genet. 6, 9-13.
26. Kolodziej, P. A., Timpe, L. C., Mitchell, K. J., Fried, S. R., Goodman, C. S., Jan, L. Y. and Jan, Y. N. (1996). frazzled encodes a Drosophila member of the DCC immunoglobulin subfamily and is required for CNS and motor axon guidance. Cell 87, 197-204.
27. Landgraf, M., Bossing, T., Technau, G. M. and Bate, M. (1997). The origin, location, and projections of the embryonic abdominal motorneurons of Drosophila. J. Neurosci. 17, 9642-9655.
28. Landgraf, M., Roy, S., Prokop, A., VijayRaghavan, K. and Bate, M. (1999). even-skipped determines the dorsal growth of motor axons in Drosophila. Neuron 22, 43-52.
29. Lee, T. and Luo, L. (1999). Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22, 451-461.
30. Mitchell, K. J., Doyle, J. L., Serafini, T., Kennedy, T. E., Tessier-Lavigne, M., Goodman, C. S. and Dickson, B. J. (1996). Genetic analysis of Netrin genes in Drosophila: Netrins guide CNS commissural axons and peripheral motor axons. Neuron 17, 203-215.
31. Moran-Rivard, L., Kagawa, T., Saueressig, H., Gross, M. K., Burrill, J. and Goulding, M. (2001). Evx1 is a postmitotic determinant of v0 interneuron identity in the spinal cord. Neuron 29, 385-399.
32. Muhr, J., Andersson, E., Persson, M., Jessell, T. M. and Ericson, J. (2001). Groucho-mediated transcriptional repression establishes progenitor cell pattern and neuronal fate in the ventral neural tube. Cell 104, 861-873.
33. Nagafuchi, S., Yanagisawa, H., Ohsaki, E., Shirayama, T., Tadokoro, K., Inoue, T. and Yamada, M. (1994). Structure and expression of the gene responsible for the triplet repeat disorder, dentatorubral and pallidoluysian atrophy (DRPLA). Nat. Genet. 8, 177-182.
34. Nüsslein-Volhard C. and Wieschaus, E. (1980). Mutations affecting segment number and polarity in Drosophila. Nature 287, 795-801.
35. Nüsslein-Volhard, C., Kluding, H. and Jurgens, G. (1985). Genes affecting the segmental subdivision of of the Drosophila embryo. Cold Spring Harb. Symp. Quant. Biol. 50, 145-154.
36. Odden, J. P., Holbrook, S. and Doe, C. Q. (2002). Drosophila HB9 is expressed in a subset of motoneurons and interneurons, where it regulates gene expression and axon pathfinding. J. Neurosci. 22, 9143-9149.
37. Patel, N. H. (1994). Imaging neuronal subsets and other cell types in whole mount Drosophila embryos and larvae using antibody probes. In Methods in Cell Biology Vol. 44 (ed. L. S. B. Goldstein and E. Fyrberg), pp. 445-487. New York: Academic Press.
38. Patel, N. H., Schafer, B., Goodman, C. S. and Holmgren, R. (1989). The role of segment polarity genes during Drosophila neurogenesis. Genes Dev. 3, 890-904.
39. Patel, N. H., Ball, E. E. and Goodman, C. S. (1992). Changing role of even-skipped during the evolution of insect pattern formation. Nature 357, 339-342.
40. 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.
41. Rubin, G. M. and Spradling, A. C. (1982). Genetic transformation of Drosophila with transposable element vectors. Science 218, 348-353.
42. Sackerson, C., Fujioka, M. and Goto, T. (1999). The even-skipped locus is contained in a 16-kb chromatin domain. Dev. Biol. 211, 39-52.
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. Schmidt, H., Rickert, C., Bossing, T., Vef, O., Urban, J. and Technau, G. M. (1997). The embryonic central nervous system lineages of Drosophila melanogaster. II. Neuroblast lineages derived from the dorsal part of the neuroectoderm. Dev. Biol. 189, 186-204.
45. Sink, H. and Whitington, P. M. (1991). Location and connectivity of abdominal motoneurons in the embryo and larva of Drosophila melanogaster. J. Neurobiol. 22, 298-311.
46. Skeath, J. B. and Doe, C. Q. (1998). Sanpodo and Notch act in opposition to Numb to distinguish sibling neuron fates in the Drosophila CNS. Development 125, 1857-1865.
47. Thor, S. and Thomas, J. B. (1997). The Drosophila islet gene governs axon pathfinding and neurotransmitter identity. Neuron 18, 397-409.
48. Thor, S. and Thomas, J. (2002). Motor neuron specification in worms, flies and mice: conserved and 'lost' mechanisms. Curr. Opin. Genet. Dev. 12, 558-564.
49. Thor, S., Andersson, S. G., Tomlinson, A. and Thomas, J. B. (1999). A LIM-homeodomain combinatorial code for motor-neuron pathway selection. Nature 397, 76-80.
50. Vactor, D. V., Sink, H., Fambrough, D., Tsoo, R. and Goodman, C. S. (1993). Genes that control neuromuscular specificity in Drosophila. Cell 73, 1137-1153.
51. Zhang, S., Xu, L., Lee, J. and Xu, T. (2002). Drosophila Atrophin homolog functions as a transcriptional corepressor in multiple developmental processes. Cell 108, 45-56.
52. Zlatic, M., Landgraf, M. and Bate, M. (2003). Genetic specification of axonal arbors: atonal regulates robo3 to position terminal branches in the Drosophila nervous system. Neuron 37, 41-51.