Fork head controls the timing and tissue selectivity of steroid-induced developmental cell death

Journal of Cell Biology

Volumn 176, Issue 6, 2007, Pages 843-852

  Cao, Chike ^a   Liu, Yanling ^a   Lehmann, Michael ^a  

^a UNIVERSITY OF ARKANSAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ECDYSTERONE; HEPATOCYTE NUCLEAR FACTOR; PROTEIN FORK HEAD; STEROID; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL DEATH; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; METAMORPHOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SALIVARY GLAND;

ANIMALS; APOPTOSIS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ECDYSTERONE; INHIBITOR OF APOPTOSIS PROTEINS; LIFE CYCLE STAGES; MODELS, BIOLOGICAL; MUTATION; NEUROPEPTIDES; NUCLEAR PROTEINS; RNA, MESSENGER; SALIVARY GLANDS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

DROSOPHILA MELANOGASTER;

EID: 33947255439     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200611155     Document Type: Article

References (58)

1. Abrams, J.M. 1996. Molecular and genetic control of apoptosis in Drosophila. In Apoptosis in Normal Development and Cancer. M. Sluyser, editor. Taylor and Francis, London. 171-187.
2. Abrams, E.W., W.K. Mihoulides, and D.J. Andrew. 2006. Fork head and Sage maintain a uniform and patent salivary gland lumen through regulation of two downstream target genes, PH4alphaSG1 and PH4alphaSG2. Development. 133:3517-3527.
3. Andres, A.J., and C.S. Thummel. 1994. Methods for quantitative analysis of transcription in larvae and prepupae. Methods Cell Biol. 44:565-573.
4. Ashwell, J.D., F.W. Lu, and M.S. Vacchio. 2000. Glucocorticoids in T cell development and function. Annu. Rev. Immunol. 18:309-345.
5. Baehrecke, E.H. 2002. How death shapes life during development. Nat. Rev. Mol. Cell Biol. 3:779-787.
6. Baehrecke, E.H. 2003. Autophagic programmed cell death in Drosophila. Cell Death Differ. 10:940-945.
7. Belyaeva, E.S., M.G. Aizenzon, V.F. Semeshin, I.I. Kiss, K. Koczka, E.M. Baritcheva, T.D. Gorelova, and I.F. Zhimulev. 1980. Cytogenetic analysis of the 2B3-4-2B11 region of the X-chromosome of Drosophila melanogaster. I. Cytology of the region and mutant complementation groups. Chromosoma. 81:281-306.
8. Broadus, J., J.R. McCabe, B. Endrizzi, C.S. Thummel, and C.T. Woodard. 1999. The Drosophila beta FTZ-F1 orphan nuclear receptor provides competence for stage-specific responses to the steroid hormone ecdysone. Mol. Cell. 3:143-149.
9. Cakouros, D., T.J. Daish, and S. Kumar. 2004. Ecdysone receptor directly binds the promoter of the Drosophila caspase dronc, regulating its expression in specific tissues. J. Cell Biol. 165:631-640.
10. Chandrasekaran, V., and S.K. Beckendorf. 2003. senseless is necessary for the survival of embryonic salivary glands in Drosophila. Development. 130:4719-4728.
11. Daish, T.J., K. Mills, and S. Kumar. 2004. Drosophila caspase DRONC is required for specific developmental cell death pathways and stress-induced apoptosis. Dev. Cell. 7:909-915.
12. Du, C., M. Fang, Y. Li, L. Li, and X. Wang. 2000. Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell. 102:33-42.
13. Friedman, J.R., and K.H. Kaestner. 2006. The Foxa family of transcription factors in development and metabolism. Cell Mol. Life Sci. 63:2317-2328.
14. Gajiwala, K.S., and S.K. Burley. 2000. Winged helix proteins. Curr. Opin. Struct. Biol. 10:110-116.
15. Hegde, R., S.M. Srinivasula, Z. Zhang, R. Wassell, R. Mukattash, L. Cilenti, G. DuBois, Y. Lazebnik, A.S. Zervos, T. Fernandes-Alnemri, and E.S. Alnemri. 2002. Identification of Omi/HtrA2 as a mitochondrial apoptotic serine protease that disrupts inhibitor of apoptosis protein-caspase interaction. J. Biol. Chem. 277:432-438.
16. Jacobson, M.D., M. Weil, and M.C. Raff. 1997. Programmed cell death in animal development. Cell. 88:347-354.
17. Jiang, C., E.H. Baehrecke, and C.S. Thummel. 1997. Steroid regulated programmed cell death during Drosophila metamorphosis. Development. 124:4673-4683.
18. Jiang, C., A.F. Lamblin, H. Steller, and C.S. Thummel. 2000. A steroid-triggered transcriptional hierarchy controls salivary gland cell death during Drosophila metamorphosis. Mol. Cell. 5:445-455.
19. Kaestner, K.H., W. Knochel, and D.E. Martinez. 2000. Unified nomenclature for the winged helix/forkhead transcription factors. Genes Dev. 14:142-146.
20. Korge, G. 1977. Larval saliva in Drosophila melanogaster: production, composition, and relationship to chromosome puffs. Dev. Biol. 58:339-355.
21. Kornbluth, S., and K. White. 2005. Apoptosis in Drosophila: neither fish nor fowl (nor man, nor worm). J. Cell Sci. 118:1779-1787.
22. Kuzin, B., S. Tillib, Y. Sedkov, L. Mizrokhi, and A. Mazo. 1994. The Drosophila trithorax gene encodes a chromosomal protein and directly regulates the region-specific homeotic gene fork head. Genes Dev. 8:2478-2490.
23. Lam, G., and C.S. Thummel. 2000. Inducible expression of double-stranded RNA directs specific genetic interference in Drosophila. Curr. Biol. 10:957-963.
24. Lee, C.Y., D.P. Wendel, P. Reid, G. Lam, C.S. Thummel, and E.H. Baehrecke. 2000. E93 directs steroid-triggered programmed cell death in Drosophila. Mol. Cell. 6:433-443.
25. Lee, C.Y., C.R. Simon, C.T. Woodard, and E.H. Baehrecke. 2002. Genetic mechanism for the stage- and tissue-specific regulation of steroid triggered programmed cell death in Drosophila. Dev. Biol. 252:138-148.
26. Lee, H.H., and M. Frasch. 2004. Survey of forkhead domain encoding genes in the Drosophila genome: classification and embryonic expression patterns. Dev. Dyn. 229:357-366.
27. Lehmann, M., and G. Korge. 1996. The fork head product directly specifies the tissue-specific hormone responsiveness of the Drosophila Sgs-4 gene. EMBO J. 15:4825-4834.
28. Lehmann, M., C. Jiang, Y.T. Ip, and C.S. Thummel. 2002. AP-1, but not NF-kB, is required for efficient steroid-triggered cell death in Drosophila. Cell Death Differ. 9:581-590.
29. Li, C., and W.H. Wong. 2001. Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc. Natl. Acad. Sci. USA. 98:31-36.
30. Li, T.R., and K.P. White. 2003. Tissue-specific gene expression and ecdysone-regulated genomic networks in Drosophila. Dev. Cell. 5:59-72.
31. Liu, Y., and M. Lehmann. 2006. FOXO-independent suppression of programmed cell death by the PI3K/Akt signaling pathway in Drosophila. Dev. Genes Evol. 216:531-535.
32. Mach, V., K. Ohno, H. Kokubo, and Y. Suzuki. 1996. The Drosophila fork head factor directly controls larval salivary gland-specific expression of the glue protein gene Sgs3. Nucleic Acids Res. 24:2387-2394.
33. Mazet, F., J.K. Yu, D.A. Liberles, L.Z. Holland, and S.M. Shimeld. 2003. Phylogenetic relationships of the Fox (Forkhead) gene family in the Bilateria. Gene. 316:79-89.
34. Meier, P., and J. Silke. 2003. Programmed cell death: Superman meets Dr Death. Nat. Cell Biol. 5:1035-1038.
35. Mills, K., T. Daish, K.F. Harvey, C.M. Pfleger, I.K. Hariharan, and S. Kumar. 2006. The Drosophila melanogaster Apaf-1 homologue ARK is required for most, but not all, programmed cell death. J. Cell Biol. 172:809-815.
36. Myat, M.M., and D.J. Andrew. 2000. Fork head prevents apoptosis and promotes cell shape change during formation of the Drosophila salivary glands. Development. 127:4217-4226.
37. Nash, D., and W. Plaut. 1964. On the denaturation of chromosomal DNA in situ. Proc. Natl. Acad. Sci. USA. 51:731-735.
38. Peterson, C., G.E. Carney, B.J. Taylor, and K. White. 2002. reaper is required for neuroblast apoptosis during Drosophila development. Development. 129:1467-1476.
39. Renault, N., K. King-Jones, and M. Lehmann. 2001. Downregulation of the tissue-specific transcription factor Fork head by Broad-Complex mediates a stage-specific hormone response. Development. 128:3729-3737.
40. Restifo, L.L., and K. White. 1992. Mutations in a steroid hormone-regulated gene disrupt the metamorphosis of internal tissues in Drosophila: salivary glands, muscle, and gut. Roux's Arch. Dev. Biol. 201:221-234.
41. Rintelen, F., H. Stocker, G. Thomas, and E. Hafen. 2001. PDK1 regulates growth through Akt and S6K in Drosophila. Proc. Natl. Acad. Sci. USA. 98:15020-15025.
42. Roth, G.E., S. Wattler, H. Bornschein, M. Lehmann, and G. Korge. 1999. Structure and regulation of the salivary gland secretion protein gene Sgs-1 of Drosophila melanogaster. Genetics. 153:753-762.
43. Shi, Y.B., L. Fu, S.C. Hsia, A. Tomita, and D. Buchholz. 2001. Thyroid hormone regulation of apoptotic tissue remodeling during anuran metamorphosis. Cell Res. 11:245-252.
44. Tata, J.R. 1994. Hormonal regulation of programmed cell death during amphibian metamorphosis. Biochem. Cell Biol. 72:581-588.
45. Tenev, T., A. Zachariou, R. Wilson, A. Paul, and P. Meier. 2002. Jafrac2 is an IAP antagonist that promotes cell death by liberating Dronc from DIAP1. EMBO J. 21:5118-5129.
46. Thummel, C.S., A.M. Boulet, and H.D. Lipshitz. 1988. Vectors for Drosophila P-element-mediated transformation and tissue culture transfection. Gene. 74:445-456.
47. Vaux, D.L., and S.J. Korsmeyer. 1999. Cell death in development. Cell. 96:245-254.
48. Verhagen, A.M., P.G. Ekert, M. Pakusch, J. Silke, L.M. Connolly, G.E. Reid, R.L. Moritz, R.J. Simpson, and D.L. Vaux. 2000. Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell. 102:43-53.
49. Waldhuber, M., K. Emoto, and C. Petritsch. 2005. The Drosophila caspase DRONC is required for metamorphosis and cell death in response to irradiation and developmental signals. Mech. Dev. 122:914-927.
50. Wang, J., L. Kean, J. Yang, A.K. Allan, S.A. Davies, P. Herzyk, and J.A. Dow. 2004. Function-informed transcriptome analysis of Drosophila renal tubule. Genome Biol. 5:R69.
51. Weigel, D., H.J. Bellen, G. Jürgens, and H. Jäckle. 1989. Primordium specific requirement of the homeotic gene fork head in the developing gut of the Drosophila embryo. Roux's Arch. Dev. Biol. 198:201-210.
52. Weigel, D., and H. Jäckle. 1990. The Fork head domain: a novel DNA binding motif of eukaryotic transcription factors? Cell. 63:455-456.
53. White, K., M.E. Grether, J.M. Abrams, L. Young, K. Farrell, and H. Steller. 1994. Genetic control of programmed cell death in Drosophila. Science. 264:677-683.
54. Woodard, C.T., E.H. Baehrecke, and C.S. Thummel. 1994. A molecular mechanism for the stage specificity of the Drosophila prepupal genetic response to ecdysone. Cell. 79:607-615.
55. Yamada, M., T. Murata, S. Hirose, G. Lavorgna, E. Suzuki, and H. Ueda. 2000. Temporally restricted expression of transcription factor betaFTZ-F1: significance for embryogenesis, molting and metamorphosis in Drosophila melanogaster. Development. 127:5083-5092.
56. Yin, V.P., and C.S. Thummel. 2004. A balance between the diap1 death inhibitor and reaper and hid death inducers controls steroid-triggered cell death in Drosophila. Proc. Natl. Acad. Sci. USA. 101:8022-8027.
57. Yin, V.P., and C.S. Thummel. 2005. Mechanisms of steroid-triggered programmed cell death in Drosophila. Semin. Cell Dev. Biol. 16:237-243.
58. Zuzarte-Luis, V., and J.M. Hurle. 2005. Programmed cell death in the embryonic vertebrate limb. Semin. Cell Dev. Biol. 16:261-269.