Dual role for drosophila lethal of scute in CNS midline precursor formation and dopaminergic neuron and motoneuron cell fate

Development

Volumn 138, Issue 11, 2011, Pages 2171-2183

  Stagg, Stephanie B ^a   Guardiola, Amaris R ^a,b   Crews, Stephen T ^a,c  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b ANGELO STATE UNIVERSITY   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

bHLH; Dopamine; Drosophila; Lethal of scute; Neural cell fate; Tailup

Indexed keywords

NEUROTRANSMITTER; NOTCH RECEPTOR; TRANSCRIPTION FACTOR;

ARTICLE; CELL FATE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DROSOPHILA; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; LETHAL GENE; MOTONEURON; NERVOUS SYSTEM DEVELOPMENT; NEUROBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; VENTRAL ROOT;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CENTRAL NERVOUS SYSTEM; DNA-BINDING PROTEINS; DOPAMINE; DROSOPHILA; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IN SITU HYBRIDIZATION; MOTOR NEURONS; NEUROGENESIS; NEURONS; RECEPTORS, NEUROTRANSMITTER; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; SOX TRANSCRIPTION FACTORS; TRANSCRIPTION FACTORS;

EID: 79956317657     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.056507     Document Type: Article

References (53)

1. Alonso, M. C. and Cabrera, C. V. (1988). The achaete-scute gene complex of Drosophila melanogaster comprises four homologous genes. EMBO J. 7, 2585-2591.
2. Ashraf, S. I. and Ip, Y. T. (2001). The Snail protein family regulates neuroblast expression of inscuteable and string, genes involved in asymmetry and cell division in Drosophila. Development 128, 4757-4767.
3. Ashraf, S. I., Hu, X., Roote, J. and Ip, Y. T. (1999). The mesoderm determinant snail collaborates with related zinc-finger proteins to control Drosophila neurogenesis. EMBO J. 18, 6426-6438.
4. Bertrand, N., Castro, D. S. and Guillemot, F. (2002). Proneural genes and the specification of neural cell types. Nat. Rev. Neurosci. 3, 517-530.
5. Bossing, T. and Technau, G. M. (1994). The fate of the CNS midline progenitors in Drosophila as revealed by a new method for single cell labelling. Development 120, 1895-1906.
6. Bossing, T. and Brand, A. H. (2006). Determination of cell fate along the anteroposterior axis of the Drosophila ventral midline. Development 133, 1001-1012.
7. Brand, M., Jarman, A. P., Jan, L. Y. and Jan, Y. N. (1993). Asense is a Drosophila neural precursor gene and is capable of initiating sense organ formation. Development 119, 1-17.
8. 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.
9. Budnik, V. and White, K. (1988). Catecholamine-containing neurons in Drosophila melanogaster: distribution and development. J. Comp. Neurol. 268, 400-413.
10. Buescher, M., Yeo, S. L., Udolph, G., Zavortink, M., Yang, X., Tear, G. and Chia, W. (1998). Binary sibling neuronal cell fate decisions in the Drosophila embryonic central nervous system are nonstochastic and require inscuteable-mediated asymmetry of ganglion mother cells. Genes Dev. 12, 1858-1870.
11. Buescher, M., Hing, F. S. and Chia, W. (2002). Formation of neuroblasts in the embryonic central nervous system of Drosophila melanogaster is controlled by SoxNeuro. Development 129, 4193-4203.
12. Cai, Y., Chia, W. and Yang, X. (2001). A family of snail-related zinc finger proteins regulates two distinct and parallel mechanisms that mediate Drosophila neuroblast asymmetric divisions. EMBO J. 20, 1704-1714.
13. Campuzano, S. and Modolell, J. (1992). Patterning of the Drosophila nervous system: the achaete-scute gene complex. Trends Genet. 8, 202-208.
14. Campuzano, S., Carramolino, L., Cabrera, C. V., Ruiz-Gomez, M., Villares, R., Boronat, A. and Modolell, J. (1985). Molecular genetics of the achaete-scute gene complex of D. melanogaster. Cell 40, 327-338.
15. Cremazy, F., Berta, P. and Girard, F. (2000). Sox neuro, a new Drosophila Sox gene expressed in the developing central nervous system. Mech. Dev. 93, 215-219.
16. Crews, S. T. (1998). Control of cell lineage-specific development and transcription by bHLH-PAS proteins. Genes Dev. 12, 607-620.
17. Dambly-Chaudiere, C. and Vervoort, M. (1998). The bHLH genes in neural development. Int. J. Dev. Biol. 42, 269-273.
18. Dominguez, M. and Campuzano, S. (1993). Asense, a member of the Drosophila achaete-scute complex, is a proneural and neural differentiation gene. EMBO J. 12, 2049-2060.
19. Flames, N. and Hobert, O. (2009). Gene regulatory logic of dopamine neuron differentiation. Nature 458, 885-889.
20. Fortini, M. E., Lai, Z. C. and Rubin, G. M. (1991). The Drosophila zfh-1 and zfh-2 genes encode novel proteins containing both zinc-finger and homeodomain motifs. Mech. Dev. 34, 113-122.
21. Gomez-Skarmeta, J. L., Rodriguez, I., Martinez, C., Culi, J., Ferres-Marco, D., Beamonte, D. and Modolell, J. (1995). Cis-regulation of achaete and scute: shared enhancer-like elements drive their coexpression in proneural clusters of the imaginal discs. Genes Dev. 9, 1869-1882.
22. Gonzalez, F., Romani, S., Cubas, P., Modolell, J. and Campuzano, S. (1989). Molecular analysis of the asense gene, a member of the achaete-scute complex of Drosophila melanogaster, and its novel role in optic lobe development. EMBO J. 8, 3553-3562.
23. Goodman, C. S., Bate, M. and Spitzer, N. C. (1981). Embryonic development of identified neurons: origin and transformation of the H cell. J. Neurosci. 1, 94-102.
24. Guillemot, F. (2007). Spatial and temporal specification of neural fates by transcription factor codes. Development 134, 3771-3780.
25. Hatakeyama, J. and Kageyama, R. (2004). Retinal cell fate determination and bHLH factors. Semin. Cell Dev. Biol. 15, 83-89.
26. Jimenez, F. and Campos-Ortega, J. A. (1990). Defective neuroblast commitment in mutants of the achaete-scute complex and adjacent genes of D. melanogaster. Neuron 5, 81-89.
27. 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.
28. Kearney, J. B., Wheeler, S. R., Estes, P., Parente, B. and Crews, S. T. (2004). Gene expression profiling of the developing Drosophila CNS midline cells. Dev. Biol. 275, 473-492.
29. Kele, J., Simplicio, N., Ferri, A. L., Mira, H., Guillemot, F., Arenas, E. and Ang, S. L. (2006). Neurogenin 2 is required for the development of ventral midbrain dopaminergic neurons. Development 133, 495-505.
30. Koushika, S. P., Lisbin, M. J. and White, K. (1996). ELAV, a Drosophila neuron-specific protein, mediates the generation of an alternatively spliced neural protein isoform. Curr. Biol. 6, 1634-1641.
31. Lundell, M. J., Lee, H. K., Perez, E. and Chadwell, L. (2003). The regulation of apoptosis by Numb/Notch signaling in the serotonin lineage of Drosophila. Development 130, 4109-4121.
32. Martin-Bermudo, M. D., Martinez, C., Rodriguez, A. and Jimenez, F. (1991). Distribution and function of the lethal of scute gene product during early neurogenesis in Drosophila. Development 113, 445-454.
33. Mesce, K. A., DeLorme, A. W., Brelje, T. C. and Klukas, K. A. (2001). Dopamine-synthesizing neurons include the putative H-cell homologue in the moth Manduca sexta. J. Comp. Neurol. 430, 501-517.
34. Monastirioti, M. (1999). Biogenic amine systems in the fruit fly Drosophila melanogaster. Microsc. Res. Tech. 45, 106-121.
35. Overton, P. M., Meadows, L. A., Urban, J. and Russell, S. (2002). Evidence for differential and redundant function of the Sox genes Dichaete and SoxN during CNS development in Drosophila. Development 129, 4219-4228.
36. Parras, C., Garcia-Alonso, L. A., Rodriguez, I. and Jimenez, F. (1996). Control of neural precursor specification by proneural proteins in the CNS of Drosophila. EMBO J. 15, 6394-6399.
37. Powell, L. M. and Jarman, A. P. (2008). Context dependence of proneural bHLH proteins. Curr. Opin. Genet. Dev. 18, 411-417.
38. Reig, G., Cabrejos, M. E. and Concha, M. L. (2007). Functions of BarH transcription factors during embryonic development. Dev. Biol. 302, 367-375.
39. 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.
40. Skeath, J. B. and Carroll, S. B. (1991). Regulation of achaete-scute gene expression and sensory organ pattern formation in the Drosophila wing. Genes Dev. 5, 984-995.
41. Skeath, J. B. and Doe, C. Q. (1996). The achaete-scute complex proneural genes contribute to neural precursor specification in the Drosophila CNS. Curr. Biol. 6, 1146-1152.
42. Skeath, J. B., Panganiban, G., Selegue, J. and Carroll, S. B. (1992). Gene regulation in two dimensions: the proneural achaete and scute genes are controlled by combinations of axis-patterning genes through a common intergenic control region. Genes Dev. 6, 2606-2619.
43. Smidt, M. P. and Burbach, J. P. (2007). How to make a mesodiencephalic dopaminergic neuron. Nat. Rev. Neurosci. 8, 21-32.
44. Stollewerk, A. (2000). Changes in cell shape in the ventral neuroectoderm of Drosophila melanogaster depend on the activity of the achaete-scute complex genes. Dev. Genes Evol. 210, 190-199.
45. Sugimori, M., Nagao, M., Bertrand, N., Parras, C. M., Guillemot, F. and Nakafuku, M. (2007). Combinatorial actions of patterning and HLH transcription factors in the spatiotemporal control of neurogenesis and gliogenesis in the developing spinal cord. Development 134, 1617-1629.
46. Thor, S. and Thomas, J. B. (1997). The Drosophila islet gene governs axon pathfinding and neurotransmitter identity. Neuron 18, 397-409.
47. Tsuchida, T., Ensini, M., Morton, S. B., Baldassare, M., Edlund, T., Jessell, T. M. and Pfaff, S. L. (1994). Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes. Cell 79, 957-970.
48. Vierbuchen, T., Ostermeier, A., Pang, Z. P., Kokubu, Y., Sudhof, T. C. and Wernig, M. (2010). Direct conversion of fibroblasts to functional neurons by defined factors. Nature 463, 1035-1041.
49. Villares, R. and Cabrera, C. V. (1987). The achaete-scute gene complex of D. melanogaster: conserved domains in a subset of genes required for neurogenesis and their homology to myc. Cell 50, 415-424.
50. Wheeler, S. R., Kearney, J. B., Guardiola, A. R. and Crews, S. T. (2006). Single-cell apping of neural and glial gene expression in the developing Drosophila CNS midline cells. Dev. Biol. 294, 509-524.
51. Wheeler, S. R., Stagg, S. B. and Crews, S. T. (2008). Multiple Notch signaling events control Drosophila CNS midline neurogenesis, gliogenesis and neuronal identity. Development 135, 3071-3079.
52. Younossi-Hartenstein, A., Green, P., Liaw, G. J., Rudolph, K., Lengyel, J. and artenstein, V. (1997). Control of early neurogenesis of the Drosophila brain by the head gap genes tll, otd, ems, and btd. Dev. Biol. 182, 270-283.
53. Xiao, H., Hrdlicka, L. A. and Nambu, J. R. (1996). Alternate functions of the single-minded and rhomboid genes in development of the Drosophila ventral neuroectoderm. Mech. Dev. 58, 65-74.