Developmentally programmed cell death in Drosophila

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1833, Issue 12, 2013, Pages 3499-3506

  Denton, Donna ^a,b,c   Aung Htut, May T ^a   Kumar, Sharad ^a,b,c  

^a CENTRE FOR CANCER BIOLOGY   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

Author keywords

Apoptosis; Autophagy; Caspases; Development; Drosophila; Programmed cell death

Indexed keywords

CASPASE; INHIBITOR OF APOPTOSIS PROTEIN; PROTEIN BCL 2;

APOPTOSIS; AUTOPHAGY; CAENORHABDITIS ELEGANS; CELL ACTIVATION; CELL COMPONENT; CELL DIFFERENTIATION; CELL FUNCTION; CELL MATURATION; CELL SURVIVAL; DROSOPHILA; ENZYME ACTIVITY; GENETIC TRANSCRIPTION; GERM CELL; INSECT CELL; INSECT DEVELOPMENT; LARVAL STAGE; METAMORPHOSIS; MIDGUT; NONHUMAN; OOCYTE DEVELOPMENT; PAEDOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SALIVARY GLAND; SPERMATOGENESIS; TRANSCRIPTION REGULATION;

CAENORHABDITIS ELEGANS; DROSOPHILA MELANOGASTER; MAMMALIA; METAZOA;

EID: 84887619826     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2013.06.014     Document Type: Review

References (150)

1. Kerr J.F., Wyllie A.H., Currie A.R. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 1972, 26:239-257.
2. Baehrecke E.H. How death shapes life during development. Nat. Rev. Mol. Cell Biol. 2002, 3:779-787.
3. Denton D., Nicolson S., Kumar S. Cell death by autophagy: facts and apparent artefacts. Cell Death Differ. 2012, 19:87-95.
4. Abrams J.M., White K., Fessler L.I., Steller H. Programmed cell death during Drosophila embryogenesis. Development 1993, 117:29-43.
5. Rusconi J.C., Hays R., Cagan R.L. Programmed cell death and patterning in Drosophila. Cell Death Differ. 2000, 7:1063-1070.
6. Brachmann C.B., Cagan R.L. Patterning the fly eye: the role of apoptosis. Trends Genet. 2003, 19:91-96.
7. Cagan R.L., Ready D.F. The emergence of order in the Drosophila pupal retina. Dev. Biol. 1989, 136:346-362.
8. Wolff T., Ready D.F. Cell death in normal and rough eye mutants of Drosophila. Development 1991, 113:825-839.
9. Baehrecke E.H. Steroid regulation of programmed cell death during Drosophila development. Cell Death Differ. 2000, 7:1057-1062.
10. Buszczak M., Cooley L. Eggs to die for: cell death during Drosophila oogenesis. Cell Death Differ. 2000, 7:1071-1074.
11. Yuan J., Shaham S., Ledoux S., Ellis H.M., Horvitz H.R. The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1 beta-converting enzyme. Cell 1993, 75:641-652.
12. Ellis H.M., Horvitz H.R. Genetic control of programmed cell death in the nematode C. elegans. Cell 1986, 44:817-829.
13. Hengartner M.O., Ellis R.E., Horvitz H.R. Caenorhabditis elegans gene ced-9 protects cells from programmed cell death. Nature 1992, 356:494-499.
14. Yuan J., Horvitz H.R. The Caenorhabditis elegans cell death gene ced-4 encodes a novel protein and is expressed during the period of extensive programmed cell death. Development 1992, 116:309-320.
15. Conradt B., Horvitz H.R. The C. elegans protein EGL-1 is required for programmed cell death and interacts with the Bcl-2-like protein CED-9. Cell 1998, 93:519-529.
16. del Peso L., Gonzalez V.M., Nunez G. Caenorhabditis elegans EGL-1 disrupts the interaction of CED-9 with CED-4 and promotes CED-3 activation. J. Biol. Chem. 1998, 273:33495-33500.
17. del Peso L., Gonzalez V.M., Inohara N., Ellis R.E., Nunez G. Disruption of the CED-9.CED-4 complex by EGL-1 is a critical step for programmed cell death in Caenorhabditis elegans. J. Biol. Chem. 2000, 275:27205-27211.
18. Yang X., Chang H.Y., Baltimore D. Essential role of CED-4 oligomerization in CED-3 activation and apoptosis. Science 1998, 281:1355-1357.
19. Chen P., Abrams J.M. Drosophila apoptosis and Bcl-2 genes: outliers fly in. J. Cell Biol. 2000, 148:625-627.
20. Chen P., Rodriguez A., Erskine R., Thach T., Abrams J.M. Dredd, a novel effector of the apoptosis activators reaper, grim, and hid in Drosophila. Dev. Biol. 1998, 201:202-216.
21. Dorstyn L., Colussi P.A., Quinn L.M., Richardson H., Kumar S. DRONC, an ecdysone-inducible Drosophila caspase. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:4307-4312.
22. Dorstyn L., Read S.H., Quinn L.M., Richardson H., Kumar S. DECAY, a novel Drosophila caspase related to mammalian caspase-3 and caspase-7. J. Biol. Chem. 1999, 274:30778-30783.
23. Doumanis J., Quinn L., Richardson H., Kumar S. STRICA, a novel Drosophila melanogaster caspase with an unusual serine/threonine-rich prodomain, interacts with DIAP1 and DIAP2. Cell Death Differ. 2001, 8:387-394.
24. Fraser A.G., Evan G.I. Identification of a Drosophila melanogaster ICE/CED-3-related protease, drICE. EMBO J. 1997, 16:2805-2813.
25. Inohara N., Koseki T., Hu Y., Chen S., Nunez G. CLARP, a death effector domain-containing protein interacts with caspase-8 and regulates apoptosis. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:10717-10722.
26. Song Z., McCall K., Steller H. DCP-1, a Drosophila cell death protease essential for development. Science 1997, 275:536-540.
27. Harvey N.L., Daish T., Mills K., Dorstyn L., Quinn L.M., Read S.H., Richardson H., Kumar S. Characterization of the Drosophila caspase, DAMM. J. Biol. Chem. 2001, 276:25342-25350.
28. Kumar S., Doumanis J. The fly caspases. Cell Death Differ. 2000, 7:1039-1044.
29. Yu X., Wang L., Acehan D., Wang X., Akey C.W. Three-dimensional structure of a double apoptosome formed by the Drosophila Apaf-1 related killer. J. Mol. Biol. 2006, 355:577-589.
30. Yuan S., Yu X., Topf M., Dorstyn L., Kumar S., Ludtke S.J., Akey C.W. Structure of the Drosophila apoptosome at 6.9 a resolution. Structure 2011, 19:128-140.
31. Chew S.K., Akdemir F., Chen P., Lu W.J., Mills K., Daish T., Kumar S., Rodriguez A., Abrams J.M. The apical caspase dronc governs programmed and unprogrammed cell death in Drosophila. Dev. Cell 2004, 7:897-907.
32. Daish T.J., Mills K., Kumar S. Drosophila caspase DRONC is required for specific developmental cell death pathways and stress-induced apoptosis. Dev. Cell 2004, 7:909-915.
33. Waldhuber M., Emoto K., Petritsch C. The Drosophila caspase DRONC is required for metamorphosis and cell death in response to irradiation and developmental signals. Mech. Dev. 2005, 122:914-927.
34. Xu D., Li Y., Arcaro M., Lackey M., Bergmann A. The CARD-carrying caspase Dronc is essential for most, but not all, developmental cell death in Drosophila. Development 2005, 132:2125-2134.
35. Kondo S., Senoo-Matsuda N., Hiromi Y., Miura M. DRONC coordinates cell death and compensatory proliferation. Mol. Cell Biol. 2006, 26:7258-7268.
36. Quinn L.M., Dorstyn L., Mills K., Colussi P.A., Chen P., Coombe M., Abrams J., Kumar S., Richardson H. An essential role for the caspase dronc in developmentally programmed cell death in Drosophila. J. Biol. Chem. 2000, 275:40416-40424.
37. Kuranaga E. Beyond apoptosis: caspase regulatory mechanisms and functions in vivo. Genes Cells 2012, 17:83-97.
38. Yi C.H., Yuan J. The Jekyll and Hyde functions of caspases. Dev. Cell 2009, 16:21-34.
39. Dorstyn L., Kumar S. A biochemical analysis of the activation of the Drosophila caspase DRONC. Cell Death Differ. 2008, 15:461-470.
40. Dorstyn L., Mills K., Lazebnik Y., Kumar S. The two cytochrome c species, DC3 and DC4, are not required for caspase activation and apoptosis in Drosophila cells. J. Cell Biol. 2004, 167:405-410.
41. Dorstyn L., Kumar S. A cytochrome c-free fly apoptosome. Cell Death Differ. 2006, 13:1049-1051.
42. Kanuka H., Sawamoto K., Inohara N., Matsuno K., Okano H., Miura M. Control of the cell death pathway by Dapaf-1, a Drosophila Apaf-1/CED-4-related caspase activator. Mol. Cell 1999, 4:757-769.
43. Rodriguez A., Oliver H., Zou H., Chen P., Wang X., Abrams J.M. Dark is a Drosophila homologue of Apaf-1/CED-4 and functions in an evolutionarily conserved death pathway. Nat. Cell Biol. 1999, 1:272-279.
44. Zhou L., Song Z., Tittel J., Steller H. HAC-1, a Drosophila homolog of APAF-1 and CED-4 functions in developmental and radiation-induced apoptosis. Mol. Cell 1999, 4:745-755.
45. Akdemir F., Farkas R., Chen P., Juhasz G., Medved'ova L., Sass M., Wang L., Wang X., Chittaranjan S., Gorski S.M., Rodriguez A., Abrams J.M. Autophagy occurs upstream or parallel to the apoptosome during histolytic cell death. Development 2006, 133:1457-1465.
46. Mills K., Daish T., Harvey K.F., Pfleger C.M., Hariharan I.K., Kumar S. The Drosophila melanogaster Apaf-1 homologue ARK is required for most, but not all, programmed cell death. J. Cell Biol. 2006, 172:809-815.
47. Srivastava M., Scherr H., Lackey M., Xu D., Chen Z., Lu J., Bergmann A. ARK, the Apaf-1 related killer in Drosophila, requires diverse domains for its apoptotic activity. Cell Death Differ. 2007, 14:92-102.
48. Denton D., Shravage B., Simin R., Mills K., Berry D.L., Baehrecke E.H., Kumar S. Autophagy, not apoptosis, is essential for midgut cell death in Drosophila. Curr. Biol. 2009, 19:1741-1746.
49. Hu S., Yang X. dFADD, a novel death domain-containing adapter protein for the Drosophila caspase DREDD. J. Biol. Chem. 2000, 275:30761-30764.
50. Leulier F., Rodriguez A., Khush R.S., Abrams J.M., Lemaitre B. The Drosophila caspase Dredd is required to resist gram-negative bacterial infection. EMBO Rep. 2000, 1:353-358.
51. Stoven S., Ando I., Kadalayil L., Engstrom Y., Hultmark D. Activation of the Drosophila NF-kappaB factor Relish by rapid endoproteolytic cleavage. EMBO Rep. 2000, 1:347-352.
52. Stoven S., Silverman N., Junell A., Hedengren-Olcott M., Erturk D., Engstrom Y., Maniatis T., Hultmark D. Caspase-mediated processing of the Drosophila NF-kappaB factor Relish. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:5991-5996.
53. Huh J.R., Vernooy S.Y., Yu H., Yan N., Shi Y., Guo M., Hay B.A. Multiple apoptotic caspase cascades are required in nonapoptotic roles for Drosophila spermatid individualization. PLoS Biol. 2004, 2:E15.
54. Baum J.S., Arama E., Steller H., McCall K. The Drosophila caspases Strica and Dronc function redundantly in programmed cell death during oogenesis. Cell Death Differ. 2007, 14:1508-1517.
55. Lee G., Wang Z., Sehgal R., Chen C.H., Kikuno K., Hay B., Park J.H. Drosophila caspases involved in developmentally regulated programmed cell death of peptidergic neurons during early metamorphosis. J. Comp. Neurol. 2011, 519:34-48.
56. Muro I., Berry D.L., Huh J.R., Chen C.H., Huang H., Yoo S.J., Guo M., Baehrecke E.H., Hay B.A. The Drosophila caspase Ice is important for many apoptotic cell deaths and for spermatid individualization, a nonapoptotic process. Development 2006, 133:3305-3315.
57. Xu D., Wang Y., Willecke R., Chen Z., Ding T., Bergmann A. The effector caspases drICE and dcp-1 have partially overlapping functions in the apoptotic pathway in Drosophila. Cell Death Differ. 2006, 13:1697-1706.
58. Laundrie B., Peterson J.S., Baum J.S., Chang J.C., Fileppo D., Thompson S.R., McCall K. Germline cell death is inhibited by P-element insertions disrupting the dcp-1/pita nested gene pair in Drosophila. Genetics 2003, 165:1881-1888.
59. Hou Y.C., Chittaranjan S., Barbosa S.G., McCall K., Gorski S.M. Effector caspase Dcp-1 and IAP protein Bruce regulate starvation-induced autophagy during Drosophila melanogaster oogenesis. J. Cell Biol. 2008, 182:1127-1139.
60. Hawkins C.J., Yoo S.J., Peterson E.P., Wang S.L., Vernooy S.Y., Hay B.A. The Drosophila caspase DRONC cleaves following glutamate or aspartate and is regulated by DIAP1, HID, and GRIM. J. Biol. Chem. 2000, 275:27084-27093.
61. Leulier F., Ribeiro P.S., Palmer E., Tenev T., Takahashi K., Robertson D., Zachariou A., Pichaud F., Ueda R., Meier P. Systematic in vivo RNAi analysis of putative components of the Drosophila cell death machinery. Cell Death Differ. 2006, 13:1663-1674.
62. Crook N.E., Clem R.J., Miller L.K. An apoptosis-inhibiting baculovirus gene with a zinc finger-like motif. J. Virol. 1993, 67:2168-2174.
63. Vaux D.L., Silke J. IAPs, RINGs and ubiquitylation. Nat. Rev. Mol. Cell Biol. 2005, 6:287-297.
64. Orme M., Meier P. Inhibitor of apoptosis proteins in Drosophila: gatekeepers of death. Apoptosis 2009, 14:950-960.
65. Wang S.L., Hawkins C.J., Yoo S.J., Muller H.A., Hay B.A. The Drosophila caspase inhibitor DIAP1 is essential for cell survival and is negatively regulated by HID. Cell 1999, 98:453-463.
66. Meier P., Silke J., Leevers S.J., Evan G.I. The Drosophila caspase DRONC is regulated by DIAP1. EMBO J. 2000, 19:598-611.
67. Muro I., Hay B.A., Clem R.J. The Drosophila DIAP1 protein is required to prevent accumulation of a continuously generated, processed form of the apical caspase DRONC. J. Biol. Chem. 2002, 277:49644-49650.
68. Chai J., Yan N., Huh J.R., Wu J.W., Li W., Hay B.A., Shi Y. Molecular mechanism of Reaper-Grim-Hid-mediated suppression of DIAP1-dependent Dronc ubiquitination. Nat. Struct. Biol. 2003, 10:892-898.
69. Wilson R., Goyal L., Ditzel M., Zachariou A., Baker D.A., Agapite J., Steller H., Meier P. The DIAP1 RING finger mediates ubiquitination of Dronc and is indispensable for regulating apoptosis. Nat. Cell Biol. 2002, 4:445-450.
70. Lee T.V., Fan Y., Wang S., Srivastava M., Broemer M., Meier P., Bergmann A. Drosophila IAP1-mediated ubiquitylation controls activation of the initiator caspase DRONC independent of protein degradation. PLoS Genet. 2011, 7:e1002261.
71. Ditzel M., Broemer M., Tenev T., Bolduc C., Lee T.V., Rigbolt K.T., Elliott R., Zvelebil M., Blagoev B., Bergmann A., Meier P. Inactivation of effector caspases through nondegradative polyubiquitylation. Mol. Cell 2008, 32:540-553.
72. Li X., Wang J., Shi Y. Structural mechanisms of DIAP1 auto-inhibition and DIAP1-mediated inhibition of drICE. Nat. Commun. 2011, 2:408.
73. Arama E., Bader M., Rieckhof G.E., Steller H. A ubiquitin ligase complex regulates caspase activation during sperm differentiation in Drosophila. PLoS Biol. 2007, 5:e251.
74. Kaplan Y., Gibbs-Bar L., Kalifa Y., Feinstein-Rotkopf Y., Arama E. Gradients of a ubiquitin E3 ligase inhibitor and a caspase inhibitor determine differentiation or death in spermatids. Dev. Cell 2010, 19:160-173.
75. Nezis I.P., Lamark T., Velentzas A.D., Rusten T.E., Bjorkoy G., Johansen T., Papassideri I.S., Stravopodis D.J., Margaritis L.H., Stenmark H., Brech A. Cell death during Drosophila melanogaster early oogenesis is mediated through autophagy. Autophagy 2009, 5:298-302.
76. Huh J.R., Foe I., Muro I., Chen C.H., Seol J.H., Yoo S.J., Guo M., Park J.M., Hay B.A. The Drosophila inhibitor of apoptosis (IAP) DIAP2 is dispensable for cell survival, required for the innate immune response to gram-negative bacterial infection, and can be negatively regulated by the reaper/hid/grim family of IAP-binding apoptosis inducers. J. Biol. Chem. 2007, 282:2056-2068.
77. Gesellchen V., Kuttenkeuler D., Steckel M., Pelte N., Boutros M. An RNA interference screen identifies Inhibitor of Apoptosis Protein 2 as a regulator of innate immune signalling in Drosophila. EMBO Rep. 2005, 6:979-984.
78. Leulier F., Lhocine N., Lemaitre B., Meier P. The Drosophila inhibitor of apoptosis protein DIAP2 functions in innate immunity and is essential to resist gram-negative bacterial infection. Mol. Cell Biol. 2006, 26:7821-7831.
79. Kleino A., Valanne S., Ulvila J., Kallio J., Myllymaki H., Enwald H., Stoven S., Poidevin M., Ueda R., Hultmark D., Lemaitre B., Ramet M. Inhibitor of apoptosis 2 and TAK1-binding protein are components of the Drosophila Imd pathway. EMBO J. 2005, 24:3423-3434.
80. Jones G., Jones D., Zhou L., Steller H., Chu Y. Deterin, a new inhibitor of apoptosis from Drosophila melanogaster. J. Biol. Chem. 2000, 275:22157-22165.
81. White K., Grether M.E., Abrams J.M., Young L., Farrell K., Steller H. Genetic control of programmed cell death in Drosophila. Science 1994, 264:677-683.
82. Chen P., Nordstrom W., Gish B., Abrams J.M. Grim, a novel cell death gene in Drosophila. Genes Dev. 1996, 10:1773-1782.
83. Grether M.E., Abrams J.M., Agapite J., White K., Steller H. The head involution defective gene of Drosophila melanogaster functions in programmed cell death. Genes Dev. 1995, 9:1694-1708.
84. Wing J.P., Schwartz L.M., Nambu J.R. The RHG motifs of Drosophila Reaper and Grim are important for their distinct cell death-inducing abilities. Mech. Dev. 2001, 102:193-203.
85. Foley K., Cooley L. Apoptosis in late stage Drosophila nurse cells does not require genes within the H99 deficiency. Development 1998, 125:1075-1082.
86. Tenev T., Zachariou A., Wilson R., Paul A., Meier P. Jafrac2 is an IAP antagonist that promotes cell death by liberating Dronc from DIAP1. EMBO J. 2002, 21:5118-5129.
87. Christich A., Kauppila S., Chen P., Sogame N., Ho S.I., Abrams J.M. The damage-responsive Drosophila gene sickle encodes a novel IAP binding protein similar to but distinct from reaper, grim, and hid. Curr. Biol. 2002, 12:137-140.
88. Wing J.P., Karres J.S., Ogdahl J.L., Zhou L., Schwartz L.M., Nambu J.R. Drosophila sickle is a novel grim-reaper cell death activator. Curr. Biol. 2002, 12:131-135.
89. Challa M., Malladi S., Pellock B.J., Dresnek D., Varadarajan S., Yin Y.W., White K., Bratton S.B. Drosophila Omi, a mitochondrial-localized IAP antagonist and proapoptotic serine protease. EMBO J. 2007, 26:3144-3156.
90. Igaki T., Suzuki Y., Tokushige N., Aonuma H., Takahashi R., Miura M. Evolution of mitochondrial cell death pathway: Proapoptotic role of HtrA2/Omi in Drosophila. Biochem. Biophys. Res. Commun. 2007, 356:993-997.
91. Khan F.S., Fujioka M., Datta P., Fernandes-Alnemri T., Jaynes J.B., Alnemri E.S. The interaction of DIAP1 with dOmi/HtrA2 regulates cell death in Drosophila. Cell Death Differ. 2008, 15:1073-1083.
92. Srinivasula S.M., Datta P., Kobayashi M., Wu J.W., Fujioka M., Hegde R., Zhang Z., Mukattash R., Fernandes-Alnemri T., Shi Y., Jaynes J.B., Alnemri E.S. Sickle, a novel Drosophila death gene in the reaper/hid/grim region, encodes an IAP-inhibitory protein. Curr. Biol. 2002, 12:125-130.
93. Hays R., Wickline L., Cagan R. Morgue mediates apoptosis in the Drosophila melanogaster retina by promoting degradation of DIAP1. Nat. Cell Biol. 2002, 4:425-431.
94. Ryoo H.D., Bergmann A., Gonen H., Ciechanover A., Steller H. Regulation of Drosophila IAP1 degradation and apoptosis by reaper and ubcD1. Nat. Cell Biol. 2002, 4:432-438.
95. Yoo S.J., Huh J.R., Muro I., Yu H., Wang L., Wang S.L., Feldman R.M., Clem R.J., Muller H.A., Hay B.A. Hid, Rpr and Grim negatively regulate DIAP1 levels through distinct mechanisms. Nat. Cell Biol. 2002, 4:416-424.
96. Willis S.N., Adams J.M. Life in the balance: how BH3-only proteins induce apoptosis. Curr. Opin. Cell Biol. 2005, 17:617-625.
97. Igaki T., Kanuka H., Inohara N., Sawamoto K., Nunez G., Okano H., Miura M. Drob-1, a Drosophila member of the Bcl-2/CED-9 family that promotes cell death. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:662-667.
98. Colussi P.A., Quinn L.M., Huang D.C., Coombe M., Read S.H., Richardson H., Kumar S. Debcl, a proapoptotic Bcl-2 homologue, is a component of the Drosophila melanogaster cell death machinery. J. Cell Biol. 2000, 148:703-714.
99. Brachmann C.B., Jassim O.W., Wachsmuth B.D., Cagan R.L. The Drosophila bcl-2 family member dBorg-1 functions in the apoptotic response to UV-irradiation. Curr. Biol. 2000, 10:547-550.
100. Zhang H., Huang Q., Ke N., Matsuyama S., Hammock B., Godzik A., Reed J.C. Drosophila pro-apoptotic Bcl-2/Bax homologue reveals evolutionary conservation of cell death mechanisms. J. Biol. Chem. 2000, 275:27303-27306.
101. Quinn L., Coombe M., Mills K., Daish T., Colussi P., Kumar S., Richardson H. Buffy, a Drosophila Bcl-2 protein, has anti-apoptotic and cell cycle inhibitory functions. EMBO J. 2003, 22:3568-3579.
102. Adams J.M., Cory S. The Bcl-2 protein family: arbiters of cell survival. Science 1998, 281:1322-1326.
103. Zhang H., Holzgreve W., De Geyter C. Evolutionarily conserved Bok proteins in the Bcl-2 family. FEBS Lett. 2000, 480:311-313.
104. Doumanis J., Dorstyn L., Kumar S. Molecular determinants of the subcellular localization of the Drosophila Bcl-2 homologues DEBCL and BUFFY. Cell Death Differ. 2007, 14:907-915.
105. Senoo-Matsuda N., Igaki T., Miura M. Bax-like protein Drob-1 protects neurons from expanded polyglutamine-induced toxicity in Drosophila. EMBO J. 2005, 24:2700-2713.
106. Sevrioukov E.A., Burr J., Huang E.W., Assi H.H., Monserrate J.P., Purves D.C., Wu J.N., Song E.J., Brachmann C.B. Drosophila Bcl-2 proteins participate in stress-induced apoptosis, but are not required for normal development. Genesis 2007, 45:184-193.
107. Galindo K.A., Lu W.J., Park J.H., Abrams J.M. The Bax/Bak ortholog in Drosophila, Debcl, exerts limited control over programmed cell death. Development 2009, 136:275-283.
108. Yacobi-Sharon K., Namdar Y., Arama E. Alternative germ cell death pathway in Drosophila involves HtrA2/Omi, lysosomes, and a caspase-9 counterpart. Dev. Cell 2013, 25:29-42.
109. Wu J.N., Nguyen N., Aghazarian M., Tan Y., Sevrioukov E.A., Mabuchi M., Tang W., Monserrate J.P., White K., Brachmann C.B. grim promotes programmed cell death of Drosophila microchaete glial cells. Mech. Dev. 2010, 127:407-417.
110. Galluzzi L., Vitale I., Abrams J.M., Alnemri E.S., Baehrecke E.H., Blagosklonny M.V., Dawson T.M., Dawson V.L., El-Deiry W.S., Fulda S., Gottlieb E., Green D.R., Hengartner M.O., Kepp O., Knight R.A., Kumar S., Lipton S.A., Lu X., Madeo F., Malorni W., Mehlen P., Nunez G., Peter M.E., Piacentini M., Rubinsztein D.C., Shi Y., Simon H.U., Vandenabeele P., White E., Yuan J., Zhivotovsky B., Melino G., Kroemer G. Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death 2012. Cell Death Differ. 2012, 19:107-120.
111. Igaki T., Kanda H., Yamamoto-Goto Y., Kanuka H., Kuranaga E., Aigaki T., Miura M. Eiger, a TNF superfamily ligand that triggers the Drosophila JNK pathway. EMBO J. 2002, 21:3009-3018.
112. Kanda H., Igaki T., Kanuka H., Yagi T., Miura M. Wengen, a member of the Drosophila tumor necrosis factor receptor superfamily, is required for Eiger signaling. J. Biol. Chem. 2002, 277:28372-28375.
113. Moreno E., Yan M., Basler K. Evolution of TNF signaling mechanisms: JNK-dependent apoptosis triggered by Eiger, the Drosophila homolog of the TNF superfamily. Curr. Biol. 2002, 12:1263-1268.
114. Kauppila S., Maaty W.S., Chen P., Tomar R.S., Eby M.T., Chapo J., Chew S., Rathore N., Zachariah S., Sinha S.K., Abrams J.M., Chaudhary P.M. Eiger and its receptor, Wengen, comprise a TNF-like system in Drosophila. Oncogene 2003, 22:4860-4867.
115. Kanda H., Igaki T., Okano H., Miura M. Conserved metabolic energy production pathways govern Eiger/TNF-induced nonapoptotic cell death. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:18977-18982.
116. Lee C.Y., Baehrecke E.H. Genetic regulation of programmed cell death in Drosophila. Cell Res. 2000, 10:193-204.
117. Jiang C., Baehrecke E.H., Thummel C.S. Steroid regulated programmed cell death during Drosophila metamorphosis. Development 1997, 124:4673-4683.
118. Berry D.L., Baehrecke E.H. Growth arrest and autophagy are required for salivary gland cell degradation in Drosophila. Cell 2007, 131:1137-1148.
119. Thomas H.E., Stunnenberg H.G., Stewart A.F. Heterodimerization of the Drosophila ecdysone receptor with retinoid X receptor and ultraspiracle. Nature 1993, 362:471-475.
120. Yao T.P., Segraves W.A., Oro A.E., McKeown M., Evans R.M. Drosophila ultraspiracle modulates ecdysone receptor function via heterodimer formation. Cell 1992, 71:63-72.
121. Yin V.P., Thummel C.S., Bashirullah A. Down-regulation of inhibitor of apoptosis levels provides competence for steroid-triggered cell death. J. Cell Biol. 2007, 178:85-92.
122. Cao C., Liu Y., Lehmann M. Fork head controls the timing and tissue selectivity of steroid-induced developmental cell death. J. Cell Biol. 2007, 176:843-852.
123. Baehrecke E.H., Thummel C.S. The Drosophila E93 gene from the 93F early puff displays stage- and tissue-specific regulation by 20-hydroxyecdysone. Dev. Biol. 1995, 171:85-97.
124. Burtis K.C., Thummel C.S., Jones C.W., Karim F.D., Hogness D.S. The Drosophila 74EF early puff contains E74, a complex ecdysone-inducible gene that encodes two ets-related proteins. Cell 1990, 61:85-99.
125. Thummel C.S., Burtis K.C., Hogness D.S. Spatial and temporal patterns of E74 transcription during Drosophila development. Cell 1990, 61:101-111.
126. DiBello P.R., Withers D.A., Bayer C.A., Fristrom J.W., Guild G.M. The Drosophila Broad-Complex encodes a family of related proteins containing zinc fingers. Genetics 1991, 129:385-397.
127. Cakouros D., Daish T., Martin D., Baehrecke E.H., Kumar S. Ecdysone-induced expression of the caspase DRONC during hormone-dependent programmed cell death in Drosophila is regulated by Broad-Complex. J. Cell Biol. 2002, 157:985-995.
128. Lee C.Y., Wendel D.P., Reid P., Lam G., Thummel C.S., Baehrecke E.H. E93 directs steroid-triggered programmed cell death in Drosophila. Mol. Cell 2000, 6:433-443.
129. Jiang C., Lamblin A.F., Steller H., Thummel C.S. A steroid-triggered transcriptional hierarchy controls salivary gland cell death during Drosophila metamorphosis. Mol. Cell 2000, 5:445-455.
130. Daish T.J., Cakouros D., Kumar S. Distinct promoter regions regulate spatial and temporal expression of the Drosophila caspase dronc. Cell Death Differ. 2003, 10:1348-1356.
131. Cakouros D., Daish T.J., Kumar S. Ecdysone receptor directly binds the promoter of the Drosophila caspase dronc, regulating its expression in specific tissues. J. Cell Biol. 2004, 165:631-640.
132. Broadus J., McCabe J.R., Endrizzi B., Thummel C.S., Woodard C.T. The Drosophila beta FTZ-F1 orphan nuclear receptor provides competence for stage-specific responses to the steroid hormone ecdysone. Mol. Cell 1999, 3:143-149.
133. Yang Z., Klionsky D.J. Eaten alive: a history of macroautophagy. Nat. Cell Biol. 2010, 12:814-822.
134. Lee C.Y., Clough E.A., Yellon P., Teslovich T.M., Stephan D.A., Baehrecke E.H. Genome-wide analyses of steroid- and radiation-triggered programmed cell death in Drosophila. Curr. Biol. 2003, 13:350-357.
135. Gorski S.M., Chittaranjan S., Pleasance E.D., Freeman J.D., Anderson C.L., Varhol R.J., Coughlin S.M., Zuyderduyn S.D., Jones S.J., Marra M.A. A SAGE approach to discovery of genes involved in autophagic cell death. Curr. Biol. 2003, 13:358-363.
136. Kilpatrick Z.E., Cakouros D., Kumar S. Ecdysone-mediated up-regulation of the effector caspase DRICE is required for hormone-dependent apoptosis in Drosophila cells. J. Biol. Chem. 2005, 280:11981-11986.
137. Cakouros D., Daish T.J., Mills K., Kumar S. An arginine-histone methyltransferase, CARMER, coordinates ecdysone-mediated apoptosis in Drosophila cells. J. Biol. Chem. 2004, 279:18467-18471.
138. Cakouros D., Mills K., Denton D., Paterson A., Daish T., Kumar S. dLKR/SDH regulates hormone-mediated histone arginine methylation and transcription of cell death genes. J. Cell Biol. 2008, 182:481-495.
139. Francis V.A., Zorzano A., Teleman A.A. dDOR is an EcR coactivator that forms a feed-forward loop connecting insulin and ecdysone signaling. Curr. Biol. 2010, 20:1799-1808.
140. Lee C.Y., Cooksey B.A., Baehrecke E.H. Steroid regulation of midgut cell death during Drosophila development. Dev. Biol. 2002, 250:101-111.
141. Denton D., Chang T.K., Nicolson S., Shravage B., Simin R., Baehrecke E.H., Kumar S. Relationship between growth arrest and autophagy in midgut programmed cell death in Drosophila. Cell Death Differ. 2012, 19:1299-1307.
142. Cavaliere V., Taddei C., Gargiulo G. Apoptosis of nurse cells at the late stages of oogenesis of Drosophila melanogaster. Dev. Genes Evol. 1998, 208:106-112.
143. Nezis I.P., Stravopodis D.J., Papassideri I., Robert-Nicoud M., Margaritis L.H. Stage-specific apoptotic patterns during Drosophila oogenesis. Eur. J. Cell Biol. 2000, 79:610-620.
144. Peterson J.S., Bass B.P., Jue D., Rodriguez A., Abrams J.M., McCall K. Noncanonical cell death pathways act during Drosophila oogenesis. Genesis 2007, 45:396-404.
145. Peterson J.S., Barkett M., McCall K. Stage-specific regulation of caspase activity in drosophila oogenesis. Dev. Biol. 2003, 260:113-123.
146. Nezis I.P., Shravage B.V., Sagona A.P., Lamark T., Bjorkoy G., Johansen T., Rusten T.E., Brech A., Baehrecke E.H., Stenmark H. Autophagic degradation of dBruce controls DNA fragmentation in nurse cells during late Drosophila melanogaster oogenesis. J. Cell Biol. 2010, 190:523-531.
147. Barth J.M., Szabad J., Hafen E., Kohler K. Autophagy in Drosophila ovaries is induced by starvation and is required for oogenesis. Cell Death Differ. 2011, 18:915-924.
148. Pritchett T.L., Tanner E.A., McCall K. Cracking open cell death in the Drosophila ovary. Apoptosis 2009, 14:969-979.
149. Arama E., Agapite J., Steller H. Caspase activity and a specific cytochrome C are required for sperm differentiation in Drosophila. Dev. Cell 2003, 4:687-697.
150. Arama E., Bader M., Srivastava M., Bergmann A., Steller H. The two Drosophila cytochrome C proteins can function in both respiration and caspase activation. EMBO J. 2006, 25:232-243.