Coordinated expression of cell death genes regulates neuroblast apoptosis

Development

Volumn 138, Issue 11, 2011, Pages 2197-2206

  Tan, Ying ^a   Yamada Mabuchi, Megumu ^a   Arya, Richa ^a   Pierre, Susan St ^a,c   Tang, Wei ^a,d   Tosa, Marie ^a   Brachmannspi Sup, Carrie ^b   White, Kristin ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c HARVARD UNIVERSITY   (United States)

^d BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

Apoptosis; Drosophila; Neuroblast

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL SURVIVAL; CHROMOSOME; DROSOPHILA; EMBRYO; EMBRYO DEVELOPMENT; GENE; GENE ACTIVITY; GENE CLUSTER; GENE DELETION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GRIM GENE; NEUROBLAST; NEUROPATHY; NONHUMAN; PRIORITY JOURNAL; REAPER GENE; SICKLE GENE; VENTRAL ROOT;

ANIMALS; APOPTOSIS; CELL SURVIVAL; CENTRAL NERVOUS SYSTEM; DROSOPHILA; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE KNOCKOUT TECHNIQUES; IN SITU HYBRIDIZATION, FLUORESCENCE; NEURAL STEM CELLS; NEUROPEPTIDES; POLYMERASE CHAIN REACTION; PROMOTER REGIONS, GENETIC;

EID: 79956297118     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.058826     Document Type: Article

References (51)

1. Abdelwahid, E., Yokokura, T., Krieser, R. J., Balasundaram, S., Fowle, W. H. and White, K. (2007). Mitochondrial disruption in Drosophila apoptosis. Dev. Cell 12, 793-806.
2. Bangs, P. and White, K. (2000). Regulation and execution of apoptosis during Drosophila development. Dev. Dyn. 218, 68-79.
3. Bello, B. C., Hirth, F. and Gould, A. P. (2003). A pulse of the Drosophila Hox protein Abdominal-A schedules the end of neural proliferation via neuroblast apoptosis. Neuron 37, 209-219.
4. 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.
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. Brodsky, M. H., Nordstrom, W., Tsang, G., Kwan, E., Rubin, G. M. and Abrams, J. M. (2000). Drosophila p53 binds a damage response element at the reaper locus. Cell 101, 103-113.
8. Buss, R. R., Sun, W. and Oppenheim, R. W. (2006). Adaptive roles of programmed cell death during nervous system development. Annu. Rev. Neurosci. 29, 1-35.
9. Cashio, P., Lee, T. V. and Bergmann, A. (2005). Genetic control of programmed cell death in Drosophila melanogaster. Semin. Cell Dev. Biol. 16, 225-235.
10. Celniker, S. E., Dillon, L. A., Gerstein, M. B., Gunsalus, K. C., Henikoff, S., Karpen, G. H., Kellis, M., Lai, E. C., Lieb, J. D., MacAlpine, D. M. et al. (2009). Unlocking the secrets of the genome. Nature 459, 927-930.
11. Chen, P., Nordstrom, W., Gish, B. and Abrams, J. M. (1996). Grim, a novel cell death gene in Drosophila. Genes Dev. 10, 1773-1782.
12. Clark, A. G., Eisen, M. B., Smith, D. R., Bergman, C. M., Oliver, B., Markow, T. A., Kaufman, T. C., Kellis, M., Gelbart, W., Iyer, V. N. et al. (2007). Evolution of genes and genomes on the Drosophila phylogeny. Nature 450, 203-218.
13. De Zio, D., Giunta, L., Corvaro, M., Ferraro, E. and Cecconi, F. (2005). Expanding roles of programmed cell death in mammalian neurodevelopment. Semin. Cell Dev. Biol. 16, 281-294.
14. Dietzl, G., Chen, D., Schnorrer, F., Su, K. C., Barinova, Y., Fellner, M., Gasser, B., Kinsey, K., Oppel, S., Scheiblauer, S. et al. (2007). A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448, 151-156.
15. Flybase (2003). The FlyBase database of the Drosophila genome projects and community literature. Nucleic Acids Res. 31, 172-175.
16. 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.
17. Hortsch, M., Patel, N. H., Bieber, A. J., Traquina, Z. R. and Goodman, C. S. (1990). Drosophila neurotactin, a surface glycoprotein with homology to serine esterases, is dynamically expressed during embryogenesis. Development 110, 1327-1340.
18. Huet, F., Lu, J. T., Myrick, K. V., Baugh, L. R., Crosby, M. A. and Gelbart, W. M. (2002). A deletion-generator compound element allows deletion saturation analysis for genomewide phenotypic annotation. Proc. Natl. Acad. Sci. USA 99, 9948-9953.
19. Ito, K., Awano, W., Suzuki, K., Hiromi, Y. and Yamamoto, D. (1997). The Drosophila mushroom body is a quadruple structure of clonal units each of which contains a virtually identical set of neurones and glial cells. Development 124, 761-771.
20. Jiang, C., Baehrecke, E. and Thummel, C. (1997). Steroid regulated programmed cell death during Drosophila metamorphosis. Development 124, 4673-4683.
21. Jiang, C. A., Lamblin, A. F. J., Steller, H. and Thummel, C. S. (2000). A steroid-triggered transcriptional hierarchy controls salivary gland cell death during Drosophila metamorphosis. Mol. Cell 5, 445-455.
22. Kornbluth, S. and White, K. (2005). Apoptosis in Drosophila: neither fish nor fowl (nor man, nor worm). J. Cell Sci. 118, 1779-1787.
23. Kurada, P. and White, K. (1998). Ras promotes cell survival in Drosophila by downregulating hid expression. Cell 95, 319-329.
24. Lecuyer, E., Parthasarathy, N. and Krause, H. M. (2008). Fluorescent in situ hybridization protocols in Drosophila embryos and tissues. Methods Mol. Biol. 420, 289-302.
25. Lin, M. F., Carlson, J. W., Crosby, M. A., Matthews, B. B., Yu, C., Park, S., Wan, K. H., Schroeder, A. J., Gramates, L. S., St Pierre, S. E. et al. (2007). Revisiting the protein-coding gene catalog of Drosophila melanogaster using 12 fly genomes. Genome Res. 17, 1823-1836.
26. Lohmann, I., McGinnis, N., Bodmer, M. and McGinnis, W. (2002). The Drosophila Hox gene deformed sculpts head morphology via direct regulation of the apoptosis activator reaper. Cell 110, 457-466.
27. Moon, N. S., Frolov, M. V., Kwon, E. J., Di Stefano, L., Dimova, D. K., Morris, E. J., Taylor-Harding, B., White, K. and Dyson, N. J. (2005). Drosophila E2F1 has context-specific pro- and antiapoptotic properties during development. Dev. Cell 9, 463-475.
28. Moon, N. S., Di Stefano, L., Morris, E. J., Patel, R., White, K. and Dyson, N. J. (2008). E2F and p53 induce apoptosis independently during Drosophila development but intersect in the context of DNA damage. PLoS Genet. 4, e1000153.
29. Ollmann, M., Young, L. M., Di Como, C. J., Karim, F., Belvin, M., Robertson, S., Whittaker, K., Demsky, M., Fisher, W. W., Buchman, A. et al. (2000). Drosophila p53 is a structural and functional homolog of the tumor suppressor p53. Cell 101, 91-101.
30. Parks, A. L., Cook, K. R., Belvin, M., Dompe, N. A., Fawcett, R., Huppert, K., Tan, L. R., Winter, C. G., Bogart, K. P., Deal, J. E. et al. (2004). Systematic generation of high-resolution deletion coverage of the Drosophila melanogaster genome. Nat. Genet. 36, 288-292.
31. Peterson, C., Carney, G. E., Taylor, B. J. and White, K. (2002). Reaper is required for neuroblast apoptosis during Drosophila development. Development 129, 1467-1476.
32. Robinow, S. and White, K. (1991). Characterization and spatial distribution of the ELAV protein during Drosophila melanogaster development. J. Neurobiol. 22, 443-461.
33. Sandu, C., Ryoo, H. D. and Steller, H. (2010). Drosophila IAP antagonists form multimeric complexes to promote cell death. J. Cell Biol. 190, 1039-1052.
34. Siegrist, S. E., Haque, N. S., Chen, C. H., Hay, B. A. and Hariharan, I. K. (2010). Inactivation of both foxo and reaper promotes long-term adult neurogenesis in Drosophila. Curr. Biol. 20, 643-648.
35. Srinivasula, S. M., Datta, P., Kobayashi, M., Wu, J. W., Fujioka, M., Hegde, R., Zhang, Z., Mukattash, R., Fernandes-Alnemri, T., Shi, Y. et al. (2002). Sickle, a novel Drosophila death gene in the reaper/hid/grim region, encodes an IAP-inhibitory protein. Curr. Biol. 12, 125-130.
36. Thomenius, M. and Kornbluth, S. (2006). Multifunctional reaper: sixty-five amino acids of fury. Cell Death Differ. 13, 1305-1309.
37. Thress, K., Henzel, W., Shillinglaw, W. and Kornbluth, S. (1998). Scythe: a novel reaper-binding apoptotic regulator. EMBO J. 17, 6135-6143.
38. Truman, J. W. and Bate, M. (1988). Spatial and temporal patterns of neurogenesis in the central nervous system of Drosophila melanogaster. Dev. Biol. 125, 145-157.
39. 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.
40. Vernooy, S. Y., Chow, V., Su, J., Verbrugghe, K., Yang, J., Cole, S., Olson, M. R. and Hay, B. A. (2002). Drosophila Bruce can potently suppress Rpr- andGrim-dependent but not Hid-dependent cell death. Curr. Biol. 12, 1164-1168.
41. White, K., Grether, M. E., Abrams, J. M., Young, L., Farrell, K. and Steller, H. (1994). Genetic control of programmed cell death in Drosophila. Science 264, 677-683.
42. White, K., Tahaoglu, E. and Steller, H. (1996). Cell killing by the Drosophila gene reaper. Science 271, 805-807.
43. Wing, J. P., Karres, J. S., Ogdahl, J. L., Zhou, L., Schwartz, L. M. and Nambu, J. R. (2002). Drosophila sickle is a novel grim-reaper cell death activator. Curr. Biol. 12, 131-135.
44. Wu, J. N., Nguyen, N., Aghazarian, M., Tan, Y., Sevrioukov, E. A., Mabuchi, M., Tang, W., Monserrate, J. P., White, K. and Brachmann, C. B. (2010). Grim promotes programmed cell death of Drosophila microchaete glial cells. Mech. Dev. 127, 407-417.
45. Wu, J. W., Cocina, A. E., Chai, J., Hay, B. A. and Shi, Y. (2001). Structural analysis of a functional DIAP1 fragment bound to grim and hid peptides. Mol. Cell 8, 95-104.
46. Yokokura, T., Dresnek, D., Huseinovic, N., Lisi, S., Abdelwahid, E., Bangs, P. and White, K. (2004). Dissection of DIAP1 functional domains via a mutant replacement strategy. J. Biol. Chem. 279, 52603-52612.
47. Yoo, S. J., Huh, J. R., Muro, I., Yu, H., Wang, L., Wang, S. L., Feldman, R. M., Clem, R. J., Muller, H. A. and Hay, B. A. (2002). Hid, Rpr and Grim negatively regulate DIAP1 levels through distinct mechanisms. Nat. Cell Biol. 4, 416-424.
48. Yuan, J. and Yankner, B. A. (2000). Apoptosis in the nervous system. Nature 407, 802-809.
49. Zachariou, A., Tenev, T., Goyal, L., Agapite, J., Steller, H. and Meier, P. (2003). IAP-antagonists exhibit non-redundant modes of action through differential DIAP1 binding. EMBO J. 22, 6642-6652.
50. Zhang, Y., Lin, N., Carroll, P. M., Chan, G., Guan, B., Xiao, H., Yao, B., Wu, S. S. and Zhou, L. (2008). Epigenetic blocking of an enhancer region controls irradiation-induced proapoptotic gene expression in Drosophila embryos. Dev. Cell 14, 481-493.
51. Zhou, L., Jiang, G., Chan, G., Santos, C. P., Severson, D. W. and Xiao, L.(2005). Michelob_x is the missing inhibitor of apoptosis protein antagonist in mosquito genomes. EMBO Rep. 6, 769-774.