Specification of Droscophila aCC motoneuron identity by a genetic cascade involving even-skipped, grain and zfh1

Development

Volumn 133, Issue 8, 2006, Pages 1445-1455

  Garces, Alain ^a   Thor, Stefan ^b  

^a HÔPITAL SAINT ELOI   (France)

^b LINKÖPING UNIVERSITY   (Sweden)

Author keywords

Axon pathfinding; Combinatorial code; Drosophila; Even skipped; Grain; Neuronal fate specification

Indexed keywords

TRANSCRIPTION FACTOR; ZINC FINGER PROTEIN; DNA BINDING PROTEIN; DROSOPHILA PROTEIN; EVEN SKIPPED PROTEIN, DROSOPHILA; EVEN-SKIPPED PROTEIN, DROSOPHILA; GRN PROTEIN, DROSOPHILA; HOMEODOMAIN PROTEIN; NOTCH PROTEIN, DROSOPHILA; NOTCH RECEPTOR; REPRESSOR PROTEIN; TRANSCRIPTION FACTOR GATA; ZFH1 PROTEIN, DROSOPHILA;

ANIMAL TISSUE; ARTICLE; CELL FATE; CONTROLLED STUDY; DROSOPHILA; EMBRYO; GENE EXPRESSION; GENE FUNCTION; HOMEOBOX; MOTONEURON; MOTOR NERVE; MUTANT; NERVE CELL; NERVE FIBER; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; REGULATOR GENE; ANIMAL; CELL DIFFERENTIATION; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; INTERNEURON; METABOLISM; PHYSIOLOGY; PRENATAL DEVELOPMENT; SIGNAL TRANSDUCTION;

ANIMALIA;

ANIMALS; AXONS; CELL DIFFERENTIATION; DNA-BINDING PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; GATA TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; INTERNEURONS; MOTOR NEURONS; RECEPTORS, NOTCH; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 33646686875     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.02321     Document Type: Article

References (59)

1. Aberle, H., Haghighi, A. P., Fetter, R. D., McCabe, B. D., Magalhaes, T. R. and Goodman, C. S. (2002). wishful thinking encodes a BMP type II receptor that regulates synaptic growth in Drosophila. Neuron 33, 545-558.
2. Allan, D. W., St Pierre, S. E., Miguel-Aliaga, I. and Thor, S. (2003). Specification of neuropeptide cell identity by the integration of retrograde BMP signaling and a combinatorial transcription factor code. Cell 113, 73-86.
3. Amsen, D., Blander, J. M., Lee, G. R., Tanigaki, K., Honjo, T. and Flavell, R. A. (2004). Instruction of distinct CD4 T helper cell fates by different notch ligands on antigen-presenting cells. Cell 117, 515-526.
4. Briscoe, J. and Ericson, J. (2001). Specification of neuronal fates in the ventral neural tube. Curr. Opin. Neurobiol. 11, 43-49.
5. Briscoe, J., Pierani, A., Jessell, T. M. and Ericson, J. (2000). A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell 101, 435-445.
6. 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.
7. 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.
8. Brown, S. and Castelli-Gair Hombria, J. (2000). Drosophila grain encodes a GATA transcription factor required for cell rearrangement during morphogenesis. Development 127, 4867-4876.
9. Craven, S. E., Lim, K. C., Ye, W., Engel, J. D., de Sauvage, F. and Rosenthal, A. (2004). Gata2 specifies serotonergic neurons downstream of sonic hedgehog. Development 131, 1165-1173.
10. Doe, C. Q., Hiromi, Y., Gehring, W. J. and Goodman, C. S. (1988a). Expression and function of the segmentation gene fushi tarazu during Drosophila neurogenesis. Science 239, 170-175.
11. Doe, C. Q., Smouse, D. and Goodman, C. S. (1988b). Control of neuronal fate by the Drosophila segmentation gene even-skipped. Nature 333, 376-378.
12. Doherty, D., Feger, G., Younger-Shepherd, S., Jan, L. Y. and Jan, Y. N. (1996). Delta is a ventral to dorsal signal complementary to Serrate, another Notch ligand, in Drosophila wing formation. Genes Dev 10, 421-434.
13. Fujioka, M., Lear, B. C., Landgraf, M., Yusibova, G. L., Zhou, J., Riley, K. M., Patel, N. H. and Jaynes, J. B. (2003). Even-skipped, acting as a repressor, regulates axonal projections in Drosophila. Development 130, 5385-5400.
14. Grueber, W. B., Jan, L. Y. and Jan, Y. N. (2003). Different levels of the homeodomain protein cut regulate distinct dendrite branching patterns of Drosophila multidendritic neurons. Cell 112, 805-818.
15. Hidalgo, A. and Brand, A. H. (1997). Targeted neuronal ablation: the role of pioneer neurons in guidance and fasciculation in the CNS of Drosophila. Development 124, 3253-3562.
16. Jacobs, J. R. and Goodman, C. S. (1989). Embryonic development of axon pathways in the Drosophila CNS. II. Behavior of pioneer growth cones. J. Neurosci. 9, 2412-2422.
17. Johansen, J., Halpern, M. E. and Keshishian, H. (1989). Axonal guidance and the development of muscle fiber-specific innervation in Drosophila embryos. J. Neurosci. 9, 4318-4332.
18. Karis, A., Pata, I., van Doorninck, J. H., Grosveld, F., de Zeeuw, C. I., de Caprona, D. and Fritzsch, B. (2001). Transcription factor GATA-3 alters pathway selection of olivocochlear neurons and affects morphogenesis of the ear. J. Comp. Neurol. 429, 615-630.
19. Karunaratne, A., Hargrave, M., Poh, A. and Yamada, T. (2002). GATA proteins identify a novel ventral interneuron subclass in the developing chick spinal cord. Dev. Biol. 249, 30-43.
20. Keleman, K. and Dickson, B. J. (2001). Short- and long-range repulsion by the Drosophila Unc5 netrin receptor. Neuron 32, 605-617.
21. Kumano, K., Chiba, S., Shimizu, K., Yamagata, T., Hosoya, N., Saito, T., Takahashi, T., Hamada, Y. and Hirai, H. (2001). Notch 1 inhibits differentiation of hematopoietic cells by sustaining GATA-2 expression. Blood 98, 3283-3289.
22. Labrador, J. P., O'Keefe, D., Yoshikawa, S., McKinnon, R. D., Thomas, J. B. and Bashaw, G. J. (2005). The homeobox transcription factor even-skipped regulates netrin-receptor expression to control dorsal motor-axon projections in Drosophila. Curr. Biol. 15, 1413-1419.
23. 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.
24. 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.
25. 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.
26. Landgraf, M., Jeffrey, V., Fujioka, M., Jaynes, J. B. and Bate, M. (2003). Embryonic origins of a motor system: motor dendrites form a myotopic map in Drosophila. PLoS Biol. 1, E41.
27. Lawoko-Kerali, G., Rivolta, M. N. and Holley, M. (2002). Expression of the transcription factors GATA3 and Pax2 during development of the mammalian inner ear. J. Comp. Neurol. 442, 378-391.
28. Layden, M. J., Odden, J. P., Schmid, A., Garces, A., Thor, S. and Doe, C. Q. (2006). Zfh 1, a somatic motor neuron transcription factor, regulates axon exit from the CNS. Dev. Biol. (in press).
29. Lear, B. C., Skeath, J. B. and Patel, N. H. (1999). Neural cell fate in rca1 and cycA mutants: the roles of intrinsic and extrinsic factors in asymmetric division in the Drosophila central nervous system. Mech. Dev. 88, 207-219.
30. Lin, D. M., Auld, V. J. and Goodman, C. S. (1995a). Targeted neuronal cell ablation in the Drosophila embryo: pathfinding by follower growth cones in the absence of pioneers. Neuron 14, 707-715.
31. Lin, W. H., Huang, L. H., Yeh, J. Y., Hoheisel, J., Lehrach, H., Sun, Y. H. and Tsai, S. F. (1995b). Expression of a Drosophila GATA transcription factor in multiple tissues in the developing embryos. Identification of homozygous lethal mutants with P-element insertion at the promoter region. J. Biol. Chem. 270, 25150-25158.
32. Marques, G., Bao, H., Haerry, T. E., Shimell, M. J., Duchek, P., Zhang, B. and O'Connor, M. B. (2002). The Drosophila BMP type II receptor Wishful Thinking regulates neuromuscular synapse morphology and function. Neuron 33, 529-543.
33. McDonald, J. A., Holbrook, S., Isshiki, T., Weiss, J., Doe, C. Q. and Mellerick, D. M. (1998). Dorsoventral patterning in the Drosophila central nervous system: the vnd homeobox gene specifies ventral column identity. Genes Dev. 12, 3603-3612.
34. McDonald, J. A., Fujioka, M., Odden, J. P., Jaynes, J. B. and Doe, C. Q. (2003). Specification of motoneuron fate in Drosophila: integration of positive and negative transcription factor inputs by a minimal eve enhancer. J. Neurobiol. 57, 193-203.
35. Miguel-Aliaga, I. and Thor, S. (2004). Segment-specific prevention of pioneer neuron apoptosis by cell-autonomous, postmitotic Hox gene activity. Development 131, 6093-6105.
36. Muroya, K., Hasegawa, T., Ito, Y., Nagai, T., Isotani, H., Iwata, Y., Yamamoto, K., Fujimoto, S., Seishu, S., Fukushima, Y. et al. (2001). GATA3 abnormalities and the phenotypic spectrum of HDR syndrome. J. Med. Genet. 38, 374-380.
37. Nardelli, J., Thiesson, D., Fujiwara, Y., Tsai, F. Y. and Orkin, S. H. (1999). Expression and genetic interaction of transcription factors GATA-2 and GATA-3 during development of the mouse central nervous system. Dev. Biol. 210, 305-321.
38. O'Connor-Giles, K. M. and Skeath, J. B. (2003). Numb inhibits membrane localization of Sanpodo, a four-pass transmembrane protein, to promote asymmetric divisions in Drosophila. Dev. Cell 5, 231-243.
39. Pandolfi, P. P., Roth, M. E., Karis, A., Leonard, M. W., Dzierzak, E., Grosveld, F. G., Engel, J. D. and Lindenbaum, M. H. (1995). Targeted disruption of the GATA3 gene causes severe abnormalities in the nervous system and in fetal liver haematopoiesis. Nat. Genet. 11, 40-44.
40. Pata, I., Studer, M., van Doorninck, J. H., Briscoe, J., Kuuse, S., Engel, J. D., Grosveld, F. and Karis, A. (1999). The transcription factor GATA3 is a downstream effector of Hoxb1 specification in rhombomere 4. Development 126, 5523-5531.
41. Rivolta, M. N. and Holley, M. C. (1998). GATA3 is downregulated during hair cell differentiation in the mouse cochlea. J. Neurocytol. 27, 637-647.
42. Sanchez-Soriano, N. and Prokop, A. (2005). The influence of pioneer neurons on a growing motor nerve in Drosophila requires the neural cell adhesion molecule homolog Fasciclinll. J. Neurosci. 25, 78-87.
43. Shao, X., Koizumi, K., Nosworthy, N., Tan, D. P., Odenwald, W. and Nirenberg, M. (2002). Regulatory DNA required for vnd/NK-2 homeobox gene expression pattern in neuroblasts. Proc. Natl. Acad. Sci. USA 99, 113-117.
44. Shirasaki, R. and Pfaff, S. L. (2002). Transcriptional codes and the control of neuronal identity Annu. Rev. Neurosci. 25, 251-281.
45. 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.
46. Spradling, A. C., Stern, D., Beaton, A., Rhem, E. J., Laverty, T., Mozden, N., Misra, S. and Rubin, G. M. (1999). The Berkeley Drosophila Genome Project gene disruption project: Single P-element insertions mutating 25% of vital Drosophila genes. Genetics 153, 135-177.
47. St Pierre, S. E., Galindo, M. I., Couso, J. P. and Thor, S. (2002). Control of Drosophila imaginal disc development by rotund and roughened eye: differentially expressed transcripts of the same gene encoding functionally distinct zinc finger proteins. Development 129, 1273-1281.
48. Tanimoto, H., Itoh, S., ten Dijke, P. and Tabata, T. (2000). Hedgehog creates a gradient of DPP activity in Drosophila wing imaginal discs. Mol. Cell 5, 59-71.
49. Thaler, J. P., Koo, S. J., Kania, A., Lettieri, K., Andrews, S., Cox, C., Jessell, T. M. and Plfaff, S. L. (2004). A postmitotic role for Is1-class LIM homeodomain proteins in the assignment of visceral spinal motor neuron identity. Neuron 41, 337-350.
50. Thomas, J. B., Bastiani, M. J., Bate, M. and Goodman, C. S. (1984). From grasshopper to Drosophila: a common plan for neuronal development. Nature 310, 203-207.
51. 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.
52. 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.
53. Tsarovina, K., Pattyn, A., Stubbusch, J., Muller, F., van der Wees, J., Schneider, C., Brunet, J. F. and Rohrer, H. (2004). Essential role of Gata transcription factors in sympathetic neuron development. Development 131, 4775-4786.
54. 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.
55. van Doorninck, J. H., van Der Wees, J., Karis, A., Goedknegt E., Engel, J. D., Coesmans, M., Rutteman, M., Grosveld, F. and De Zeeuw, C. I. (1999). GATA-3 is involved in the development of serotonergic neurons in the caudal raphe nuclei. J. Neurosci. 19, RC 12.
56. Van Doren, M., Mathews, W. R., Samuels, M., Moore, L. A., Broihier, H. T. and Lehmann, R. (2003). fear of intimacy encodes a novel transmembrane protein required for gonad morphogenesis in Drosophila. Development 130, 2355-2364.
57. Van Esch, H., Groenen, P., Nesbit, M. A., Schuffenhauer, S., Lichtner, P., Vanderlinden, G., Harding, B., Beetz, R., Bilous, R. W., Holdaway, I. et al. (2000). GATA3 haplo-insufficiency causes human HDR syndrome. Nature 406, 419-422.
58. Weigmann, K. and Lehner, C. F. (1995) Cell fate specification by even-skipped expression in the Drosophila nervous system is coupled to cell cycle progression. Development 121, 3713-3721.
59. Zhou, Y., Yamamoto, M. and Engel, J. D. (2000). GATA2 is required for the generation of V2 interneurons. Development 127, 3829-3838.