Serial specification of diverse neuroblast identities from a neurogenic placode by Notch and Egfr signaling

Development

Volumn 138, Issue 14, 2011, Pages 2883-2893

  Hwang, Helen J ^a,b   Rulifson, Eric ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Drosophila; Egfr; Insulin; Neuroblast; Neurogenesis; Notch

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; INSULIN; MUTANT PROTEIN; NOTCH RECEPTOR;

APOPTOSIS; ARTICLE; BRAIN CELL; CELL COUNT; CELL EXPANSION; CELL LINEAGE; CELL SURVIVAL; DROSOPHILA; LOSS OF FUNCTION MUTATION; NERVE CELL; NEUROBLAST; NEUROECTODERM; NONHUMAN; PRIORITY JOURNAL; PROTEIN PURIFICATION;

ANIMALS; BRAIN; BROMODEOXYURIDINE; CELL DIFFERENTIATION; CELL LINEAGE; DNA PRIMERS; DROSOPHILA; DROSOPHILA PROTEINS; IMMUNOHISTOCHEMISTRY; NEURAL PLATE; NEURONS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, INVERTEBRATE PEPTIDE; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; TEMPERATURE;

EID: 79959400233     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.055681     Document Type: Article

References (78)

1. Bello, B. C., Izergina, N., Caussinus, E. and Reichert, H. (2008). Amplification of neural stem cell proliferation by intermediate progenitor cells in Drosophila brain development. Neural Dev. 3, 5.
2. Bergmann, A., Agapite, J., McCall, K. and Steller, H. (1998). The Drosophila gene hid is a direct molecular target of Ras-dependent survival signaling. Cell 95, 331-341.
3. Bhat, K. M. (1999). Segment polarity genes in neuroblast formation and identity specification during Drosophila neurogenesis. BioEssays 21, 472-485.
4. Bier, E., Jan, L. Y. and Jan, Y. N. (1990). rhomboid, a gene required for dorsoventral axis establishment and peripheral nervous system development in Drosophila melanogaster. Genes Dev. 4, 190-203.
5. Bier, E., Vaessin, H., Younger-Shepherd, S., Jan, L. Y. and Jan, Y. N. (1992). deadpan, an essential pan-neural gene in Drosophila, encodes a helix-loop-helix protein similar to the hairy gene product. Genes Dev. 6, 2137-2151.
6. Boone, J. Q. and Doe, C. Q. (2008). Identification of Drosophila type II neuroblast lineages containing transit amplifying ganglion mother cells. Dev. Neurobiol. 68, 1185-1195.
7. Bowman, S. K., Rolland, V., Betschinger, J., Kinsey, K. A., Emery, G. and Knoblich, J. A. (2008). The tumor suppressors Brat and Numb regulate transitamplifying neuroblast lineages in Drosophila. Dev. Cell 14, 535-546.
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. Cagan, R. L. and Ready, D. F. (1989). Notch is required for successive cell decisions in the developing Drosophila retina. Genes Dev. 3, 1099-1112.
10. Campos-Ortega, J. A. and Hartenstein, V. (1985). The Embryonic Development of Drosophila melanogaster. Berlin: Springer-Verlag.
11. Castro, B., Barolo, S., Bailey, A. M. and Posakony, J. W. (2005). Lateral inhibition in proneural clusters: cis-regulatory logic and default repression by Suppressor of Hairless. Development 132, 3333-3344.
12. Chang, T., Mazotta, J., Dumstrei, K., Dumitrescu, A. and Hartenstein, V. (2001). Dpp and Hh signaling in the Drosophila embryonic eye field. Development 128, 4691-4704.
13. Clifford, R. J. and Schupbach, T. (1989). Coordinately and differentially mutable activities of torpedo, the Drosophila melanogaster homolog of the vertebrate EGF receptor gene. Genetics 123, 771-787.
14. Cui, X. and Doe, C. Q. (1992). ming is expressed in neuroblast sublineages and regulates gene expression in the Drosophila central nervous system. Development 116, 943-952.
15. Culi, J., Martin-Blanco, E. and Modolell, J. (2001). The EGF receptor and N signalling pathways act antagonistically in Drosophila mesothorax bristle patterning. Development 128, 299-308.
16. de Velasco, B., Mandal, L., Mkrtchyan, M. and Hartenstein, V. (2006). Subdivision and developmental fate of the head mesoderm in Drosophila melanogaster. Dev. Genes Evol. 216, 39-51.
17. de Velasco, B., Erclik, T., Shy, D., Sclafani, J., Lipshitz, H., McInnes, R. and Hartenstein, V. (2007). Specification and development of the pars intercerebralis and pars lateralis, neuroendocrine command centers in the Drosophila brain. Dev. Biol. 302, 309-323.
18. Dickson, B. and Hafen, E. (1993). Genetic dissection of eye development in Drosophila. In The Development of Drosophila melanogaster, Vol. 2. (ed. M. Bate and A. Martinez Arias), pp. 1327-1362. Plainview, NY: Cold Spring Harbor Laboratory Press.
19. Dickson, B. J., Dominguez, M., van der Straten, A. and Hafen, E. (1995). Control of Drosophila photoreceptor cell fates by phyllopod, a novel nuclear protein acting downstream of the Raf kinase. Cell 80, 453-462.
20. Dominguez, M., Wasserman, J. D. and Freeman, M. (1998). Multiple functions of the EGF receptor in Drosophila eye development. Curr. Biol. 8, 1039-1048.
21. 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.
22. Dumstrei, K., Nassif, C., Abboud, G., Aryai, A. and Hartenstein, V. (1998). EGFR signaling is required for the differentiation and maintenance of neural progenitors along the dorsal midline of the Drosophila embryonic head. Development 125, 3417-3426.
23. Erclik, T., Hartenstein, V., Lipshitz, H. D. and McInnes, R. R. (2008). Conserved role of the Vsx genes supports a monophyletic origin for bilaterian visual systems. Curr. Biol. 18, 1278-1287.
24. Escudero, L. M., Caminero, E., Schulze, K. L., Bellen, H. J. and Modolell, J. (2005). Charlatan, a Zn-finger transcription factor, establishes a novel level of regulation of the proneural achaete/scute genes of Drosophila. Development 132, 1211-1222.
25. Grether, M. E., Abrams, J. M., Agapite, J., White, K. and Steller, H. (1995). The head involution defective gene of Drosophila melanogaster functions in programmed cell death. Genes Dev. 9, 1694-1708.
26. Heitzler, P. and Simpson, P. (1991). The choice of cell fate in the epidermis of Drosophila. Cell 64, 1083-1092.
27. Hewes, R. S., Park, D., Gauthier, S. A., Schaefer, A. M. and Taghert, P. H. (2003). The bHLH protein Dimmed controls neuroendocrine cell differentiation in Drosophila. Development 130, 1771-1781.
28. Izergina, N., Balmer, J., Bello, B. and Reichert, H. (2009). Postembryonic development of transit amplifying neuroblast lineages in the Drosophila brain. Neural Dev. 4, 44.
29. Jarman, A. P., Grell, E. H., Ackerman, L., Jan, L. Y. and Jan, Y. N. (1994). Atonal is the proneural gene for Drosophila photoreceptors. Nature 369, 398-400.
30. Kawamura, K., Kouki, T., Kawahara, G. and Kikuyama, S. (2002). Hypophyseal development in vertebrates from amphibians to mammals. Gen. Comp. Endocrinol. 126, 130-135.
31. Klaes, A., Menne, T., Stollewerk, A., Scholz, H. and Klambt, C. (1994). The Ets transcription factors encoded by the Drosophila gene pointed direct glial cell differentiation in the embryonic CNS. Cell 78, 149-160.
32. Kumar, J. P., Tio, M., Hsiung, F., Akopyan, S., Gabay, L., Seger, R., Shilo, B. Z. and Moses, K. (1998). Dissecting the roles of the Drosophila EGF receptor in eye development and MAP kinase activation. Development 125, 3875-3885.
33. Kurada, P. and White, K. (1998). Ras promotes cell survival in Drosophila by downregulating hid expression. Cell 95, 319-329.
34. Lage, P., Jan, Y. N. and Jarman, A. P. (1997). Requirement for EGF receptor signalling in neural recruitment during formation of Drosophila chordotonal sense organ clusters. Curr. Biol. 7, 166-175.
35. Larkin, M. K., Holder, K., Yost, C., Giniger, E. and Ruohola-Baker, H. (1996). Expression of constitutively active Notch arrests follicle cells at a precursor stage during Drosophila oogenesis and disrupts the anterior-posterior axis of the oocyte. Development 122, 3639-3650.
36. Lehmann, R., Jimenez, F., Dietrich, U. and Camposortega, J. A. (1983). On the phenotype and development of mutants of early neurogenesis in Drosophilamelanogaster. Roux's Arch. Dev. Biol. 192, 62-74.
37. Lichtneckert, R. and Reichert, H. (2008). Anteroposterior regionalization of the brain: genetic and comparative aspects. Adv. Exp. Med. Biol. 628, 32-41.
38. Markakis, E. A. (2002). Development of the neuroendocrine hypothalamus. Front. Neuroendocrinol. 23, 257-291.
39. 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.
40. Nagaraj, R. and Banerjee, U. (2009). Regulation of Notch and Wingless signalling by phyllopod, a transcriptional target of the EGFR pathway. EMBO J. 28, 337-346.
41. Park, D., Veenstra, J. A., Park, J. H. and Taghert, P. H. (2008). Mapping peptidergic cells in Drosophila: where DIMM fits in. PLoS ONE 3, e1896.
42. Parks, A. L., Stout, J. R., Shepard, S. B., Klueg, K. M., Dos Santos, A. A., Parody, T. R., Vaskova, M. and Muskavitch, M. A. (2006). Structure-function analysis of delta trafficking, receptor binding and signaling in Drosophila. Genetics 174, 1947-1961.
43. Pereanu, W. and Hartenstein, V. (2006). Neural lineages of the Drosophila brain: a three-dimensional digital atlas of the pattern of lineage location and projection at the late larval stage. J. Neurosci. 26, 5534-5553.
44. Pi, H., Huang, S. K., Tang, C. Y., Sun, Y. H. and Chien, C. T. (2004). phyllopod is a target gene of proneural proteins in Drosophila external sensory organ development. Proc. Natl. Acad. Sci. USA 101, 8378-8383.
45. Qian, X., Goderie, S. K., Shen, Q., Stern, J. H. and Temple, S. (1998). Intrinsic programs of patterned cell lineages in isolated vertebrate CNS ventricular zone cells. Development 125, 3143-3152.
46. Rogge, R., Green, P. J., Urano, J., Horn-Saban, S., Mlodzik, M., Shilo, B. Z., Hartenstein, V. and Banerjee, U. (1995). The role of yan in mediating the choice between cell division and differentiation. Development 121, 3947-3958.
47. Rulifson, E. J. and Blair, S. S. (1995). Notch regulates wingless expression and is not required for reception of the paracrine wingless signal during wing margin neurogenesis in Drosophila. Development 121, 2813-2824.
48. Rulifson, E. J., Kim, S. K. and Nusse, R. (2002). Ablation of insulin-producing neurons in flies: growth and diabetic phenotypes. Science 296, 1118-1120.
49. Schlosser, G. (2006). Induction and specification of cranial placodes. Dev. Biol. 294, 303-351.
50. Schnepp, B., Grumbling, G., Donaldson, T. and Simcox, A. (1996). Vein is a novel component in the Drosophila epidermal growth factor receptor pathway with similarity to the neuregulins. Genes Dev. 10, 2302-2313.
51. Scholz, H., Deatrick, J., Klaes, A. and Klämbt, C. (1993). Genetic dissection of pointed, a Drosophila gene encoding two ETS related proteins. Genetics 135, 455-468.
52. Siegmund, T. and Korge, G. (2001). Innervation of the ring gland of Drosophila melanogaster. J. Comp. Neurol. 431, 481-491.
53. Skeath, J. B. (1999). At the nexus between pattern formation and cell-type specification: the generation of individual neuroblast fates in the Drosophila embryonic central nervous system. BioEssays 21, 922-931.
54. Skeath, J. B. and Carroll, S. B. (1992). Regulation of proneural gene expression and cell fate during neuroblast segregation in the Drosophila embryo. Development 114, 939-946.
55. Skeath, J. B. and Thor, S. (2003). Genetic control of Drosophila nerve cord development. Curr. Opin. Neurobiol. 13, 8-15.
56. Spencer, S. A., Powell, P. A., Miller, D. T. and Cagan, R. L. (1998). Regulation of EGF receptor signaling establishes pattern across the developing Drosophila retina. Development 125, 4777-4790.
57. Sprecher, S. G., Reichert, H. and Hartenstein, V. (2007). Gene expression patterns in primary neuronal clusters of the Drosophila embryonic brain. Gene Expr. Patterns 7, 584-595.
58. Struhl, G. and Basler, K. (1993). Organizing activity of wingless protein in Drosophila. Cell 72, 527-540.
59. Sullivan, W., Ashburner, M. and Hawley, R. S. (2000). Drosophila protocols. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
60. Sundaram, M. V. (2005). The love-hate relationship between Ras and Notch. Genes Dev. 19, 1825-1839.
61. Technau, G. M. and Campos-Ortega, J. A. (1987). Cell autonomy of expression of neurogenic genes of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 84, 4500-4504.
62. Technau, G. M., Berger, C. and Urbach, R. (2006). Generation of cell diversity and segmental pattern in the embryonic central nervous system of Drosophila. Dev. Dyn. 235, 861-869.
63. Tomancak, P., Beaton, A., Weiszmann, R., Kwan, E., Shu, S., Lewis, S. E., Richards, S., Ashburner, M., Hartenstein, V., Celniker, S. E. et al. (2002). Systematic determination of patterns of gene expression during Drosophila embryogenesis. Genome Biol. 3, RESEARCH0088.
64. Tsuda, L., Kaido, M., Lim, Y. M., Kato, K., Aigaki, T. and Hayashi, S. (2006). An NRSF/REST-like repressor downstream of Ebi/SMRTER/Su(H) regulates eye development in Drosophila. EMBO J. 25, 3191-3202.
65. Urbach, R. and Technau, G. M. (2003). Segment polarity and DV patterning gene expression reveals segmental organization of the Drosophila brain. Development 130, 3607-3620.
66. Urbach, R. and Technau, G. M. (2008). Dorsoventral patterning of the brain: a comparative approach. Adv. Exp. Med. Biol. 628, 42-56.
67. Urbach, R., Schnabel, R. and Technau, G. M. (2003). The pattern of neuroblast formation, mitotic domains and proneural gene expression during early brain development in Drosophila. Development 130, 3589-3606.
68. Urbach, R., Volland, D., Seibert, J. and Technau, G. M. (2006). Segmentspecific requirements for dorsoventral patterning genes during early brain development in Drosophila. Development 133, 4315-4330.
69. Urban, S., Lee, J. R. and Freeman, M. (2002). A family of Rhomboid intramembrane proteases activates all Drosophila membrane-tethered EGF ligands. EMBO J. 21, 4277-4286.
70. Wang, S., Tulina, N., Carlin, D. L. and Rulifson, E. J. (2007). The origin of isletlike cells in Drosophila identifies parallels to the vertebrate endocrine axis. Proc. Natl. Acad. Sci. USA 104, 19873-19878.
71. Whitlock, K. E. (2005). Origin and development of GnRH neurons. Trends Endocrinol. Metab. 16, 145-151.
72. Wolff, T. and Ready, D. F. (1993). Pattern formation in the Drosophila retina. In The Development of Drosophila melanogaster, Vol. 2 (ed. M. Bate and A. Martinez Arias), pp. 1277-1325. Plainview, NY: Cold Spring Harbor Laboratory Press.
73. Yang, L. and Baker, N. E. (2003). Cell cycle withdrawal, progression, and cell survival regulation by EGFR and its effectors in the differentiating Drosophila eye. Dev. Cell 4, 359-369.
74. Yasugi, T., Sugie, A., Umetsu, D. and Tabata, T. (2010). Coordinated sequential action of EGFR and Notch signaling pathways regulates proneural wave progression in the Drosophila optic lobe. Development 137, 3193-3203.
75. Younossi-Hartenstein, A., Nassif, C., Green, P. and Hartenstein, V. (1996). Early neurogenesis of the Drosophila brain. J. Comp. Neurol. 370, 313-329.
76. Younossi-Hartenstein, A., Green, P., Liaw, G. J., Rudolph, K., Lengyel, J. and Hartenstein, 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.
77. zur Lage, P. and Jarman, A. P. (1999). Antagonism of EGFR and notch signalling in the reiterative recruitment of Drosophila adult chordotonal sense organ precursors. Development 126, 3149-3157.
78. zur Lage, P. I., Powell, L. M., Prentice, D. R., McLaughlin, P. and Jarman, A. P. (2004). EGF receptor signaling triggers recruitment of Drosophila sense organ precursors by stimulating proneural gene autoregulation. Dev. Cell 7, 687-696.