Multiple Notch signaling events control Drosophila CNS midline neurogenesis, gliogenesis and neuronal identity

Development

Volumn 135, Issue 18, 2008, Pages 3071-3079

  Wheeler, Scott R ^a   Stagg, Stephanie B ^a   Crews, Stephen T ^a  

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

Author keywords

CNS midline; Drosophila; Glia; Neuroblast; Neuron; Notch

Indexed keywords

BETA GALACTOSIDASE; CELL PROTEIN; NOTCH RECEPTOR; PROTEIN NUMB; PROTEIN SPDO; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL COUNT; CELL DIFFERENTIATION; CELL DIVISION; CELL FATE; CELL MATURATION; CELL MOTION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; DEVELOPMENTAL STAGE; DROSOPHILA; GENE ACTIVATION; GENE EXPRESSION; GENE FUNCTION; GENE LOCATION; GENE MAPPING; GLIA CELL; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; ANIMAL; ANIMAL EMBRYO; BIOLOGICAL MODEL; CENTRAL NERVOUS SYSTEM; CYTOLOGY; GENETICS; GLIA; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; METABOLISM; PHYSIOLOGY; PRENATAL DEVELOPMENT; SIGNAL TRANSDUCTION;

ANIMALS; CELL DIVISION; CENTRAL NERVOUS SYSTEM; DROSOPHILA; EMBRYO, NONMAMMALIAN; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MODELS, BIOLOGICAL; NEUROGLIA; NEURONS; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION;

EID: 58149111207     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.022343     Document Type: Article

References (48)

1. Abramoff, M. D., Magelhaes, P. J. and Ram, S. J. (2004). Image processing with ImageJ. Biophotonics Int. 11, 36-42.
2. Almeida, M. S. and Bray, S. J. (2005). Regulation of post-embryonic neuroblasts by Drosophila Grainyhead. Mech. Dev. 122, 1282-1293.
3. Bate, C. M. and Grunewald, E. B. (1981). Embryogenesis of an insect nervous system II: a second class of neuron precursor cells and the origin of the intersegmental connectives. J. Embryol. Exp. Morphol. 61, 317-330.
4. 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.
5. Bossing, T. and Brand, A. H. (2006). Determination of cell fate along the anteroposterior axis of the Drosophila ventral midline. Development 133, 1001-1012.
6. Brand, A. (1995). GFP in Drosophila. Trends Genet. 11, 324-325.
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. Campos-Ortega, J. A. (1993). Early neurogenesis in Drosophila melanogaster. In The Development of Drosophila melanogaster, vol. 2 (ed. M. Bate and A. M. Arias), pp. 1091-1129. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
9. Crews, S. T. (2003). Drosophila bHLH-PAS developmental regulatory proteins. In PAS Proteins: Regulators and Sensors of Development and Physiology (ed. S. T. Crews), pp. 69-108. New York: Kluwer Academic Publishers.
10. Doroquez, D. B. and Rebay, I. (2006). Signal integration during development: mechanisms of EGFR and Notch pathway function and cross-talk. Crit. Rev. Biochem. Mol. Biol. 41, 339-385.
11. Foe, V. E. (1989). Mitotic domains reveal early commitment of cells in Drosophila embryos. Development 107, 1-22.
12. Furriols, M. and Bray, S. (2001). A model Notch response element detects Suppressor of Hairless-dependent molecular switch. Curr. Biol. 11, 60-64.
13. Gaiano, N., Nye, J. S. and Fishell, G. (2000). Radial glial identity is promoted by Notch1 signaling in the murine forebrain. Neuron 26, 395-404.
14. Go, M. J., Eastman, D. S. and Artavanis-Tsakonas, S. (1998). Cell proliferation control by Notch signaling in Drosophila development. Development 125, 2031-2040.
15. 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.
16. Hutterer, A. and Knoblich, J. A. (2005). Numb and alpha-Adaptin regulate Sanpodo endocytosis to specify cell fate in Drosophila external sensory organs. EMBO Rep. 6, 836-842.
17. 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.
18. Jacobs, J. R. (2000). The midline glia of Drosophila: a molecular genetic model for the developmental functions of glia. Prog. Neurobiol. 62, 475-508.
19. Jia, X. X. and Siegler, M. V. (2002). Midline lineages in grasshopper produce neuronal siblings with asymmetric expression of Engrailed. Development 129, 5181-5193.
20. 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.
21. 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.
22. Kidd, S., Lieber, T. and Young, M. W. (1998). Ligand-induced cleavage and regulation of nuclear entry of Notch in Drosophila melanogaster embryos. Genes Dev. 12, 3728-3740.
23. Klambt, C., Jacobs, J. R. and Goodman, C. S. (1991). The midline of the Drosophila central nervous system: a model for the genetic analysis of cell fate, cell migration, and growth cone guidance. Cell 64, 801-815.
24. 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.
25. Kuwada, J. Y. and Goodman, C. S. (1985). Neuronal determination during embryonic development of the grasshopper nervous system. Dev. Biol. 110, 114-126.
26. Lee, C. Y., Andersen, R. O., Cabernard, C., Manning, L., Tran, K. D., Lanskey, M. J., Bashirullah, A. and Doe, C. Q. (2006). Drosophila Aurora-A kinase inhibits neuroblast self-renewal by regulating aPKC/Numb cortical polarity and spindle orientation. Genes Dev. 20, 3464-3474.
27. Liu, X., Zwiebel, L. J., Hinton, D., Benzer, S., Hall, J. C. and Rosbash, M. (1992). The period gene encodes a predominantly nuclear protein in adult Drosophila. J. Neurosci. 12, 2735-2744.
28. Ma, Y., Certel, K., Gao, Y., Niemitz, E., Mosher, J., Mukherjee, A., Mutsuddi, M., Huseinovic, N., Crews, S. T., Johnson, W. A. et al. (2000). Functional interactions between Drosophila bHLH/PAS, Sox, and POU transcription factors regulate CNS midline expression of the slit gene. J. Neurosci. 20, 4596-4605.
29. Menne, T. V. and Klambt, C. (1994). The formation of commissures in the Drosophila CNS depends on the midline cells and on the Notch gene. Development 120, 123-133.
30. Morrison, S. J., Perez, S. E., Qiao, Z., Verdi, J. M., Hicks, C., Weinmaster, G. and Anderson, D. J. (2000). Transient Notch activation initiates an irreversible switch from neurogenesis to gliogenesis by neural crest stem cells. Cell 101, 499-510.
31. 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.
32. 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.
33. 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.
34. 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.
35. Spana, E. P. and Doe, C. Q. (1996). Numb antagonizes Notch signaling to specify sibling neuron cell fates. Neuron 17, 21-26.
36. Spana, E. P., Kopczynski, C., Goodman, C. S. and Doe, C. Q. (1995). Asymmetric localization of numb autonomously determines sibling neuron identity in the Drosophila CNS. Development 121, 3489-3494.
37. Thomas, J. B., Crews, S. T. and Goodman, C. S. (1988). Molecular genetics of the single-minded locus: a gene involved in the development of the Drosophila nervous system. Cell 52, 133-141.
38. Truman, J. W., Schuppe, H., Shepherd, D. and Williams, D. W. (2004). Developmental architecture of adult-specific lineages in the ventral CNS of Drosophila. Development 131, 5167-5184.
39. Udolph, G., Rath, P. and Chia, W. (2001). A requirement for Notch in the genesis of a subset of glial cells in the Drosophila embryonic central nervous system which arise through asymmetric divisions. Development 128, 1457-1466.
40. Uemura, T., Shepherd, S., Ackerman, L., Jan, L. Y. and Jan, Y. N. (1989). numb, a gene required in determination of cell fate during sensory organ formation in Drosophila embryos. Cell 58, 349-360.
41. Wang, H., Ouyang, Y., Somers, W. G., Chia, W. and Lu, B. (2007). Polo inhibits progenitor self-renewal and regulates Numb asymmetry by phosphorylating Pon. Nature 449, 96-100.
42. Wang, S., Younger-Shepherd, S., Jan, L. Y. and Jan, Y. N. (1997). Only a subset of the binary cell fate decisions mediated by Numb/Notch signaling in Drosophila sensory organ lineage requires Suppressor of Hairless. Development 124, 4435-4446.
43. Ward, E. J. and Skeath, J. B. (2000). Characterization of a novel subset of cardiac cells and their progenitors in the Drosophila embryo. Development 127, 4959-4969.
44. Ward, M. P., Mosher, J. T. and Crews, S. T. (1998). Regulation of bHLH-PAS protein subcellular localization during Drosophila embryogenesis. Development 125, 1599-1608.
45. Wech, I., Bray, S., Delidakis, C. and Preiss, A. (1999). Distinct expression patterns of different enhancer of split bHLH genes during embryogenesis of Drosophila melanogaster. Dev. Genes Evol. 209, 370-375.
46. Wharton, K. A., Jr, Franks, R. G., Kasai, Y. and Crews, S. T. (1994). Control of CNS midline transcription by asymmetric E-box-like elements: similarity to xenobiotic responsive regulation. Development 120, 3563-3569.
47. Wheeler, S. R., Kearney, J. B., Guardiola, A. R. and Crews, S. T. (2006). Single-cell mapping of neural and glial gene expression in the developing Drosophila CNS midline cells. Dev. Biol. 294, 509-524.
48. 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.