Abstract
Drosophila has served as a particularly attractive model to study cell death due to the vast array of tools for genetic manipulation under defined spatial and temporal conditions in vivo as well as in cultured cells. These genetic methods have been well supplemented by enzymatic assays and a panel of antibodies recognizing cell death markers. This chapter discusses reporters, mutants, and assays used by various laboratories to study cell death in the context of development and in response to external insults.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Chen P, Rodriguez A, Erskine R et al (1998) Dredd, a novel effector of the apoptosis activators reaper, grim, and hid in Drosophila. Dev Biol 201:202–216. doi:10.1006/dbio.1998.9000
Dorstyn L, Colussi PA, Quinn LM et al (1999) DRONC, an ecdysone-inducible Drosophila caspase. Proc Natl Acad Sci U S A 96:4307–4312. doi:10.1073/pnas.96.8.4307
Doumanis J, Quinn L, Richardson H, Kumar S (2001) STRICA, a novel Drosophila melanogaster caspase with an unusual serine/threonine-rich prodomain, interacts with DIAP1 and DIAP2. Cell Death Differ 8:387–394. doi:10.1038/sj.cdd.4400864
Fraser AG, Evan GI (1997) Identification of a Drosophila melanogaster ICE/CED-3-related protease, drICE. EMBO J 16:2805–2813. doi:10.1093/emboj/16.10.2805
Song Z, McCall K, Steller H (1997) DCP-1, a Drosophila cell death protease essential for development. Science 275:536–540. doi:10.1126/science.275.5299.536
Dorstyn L, Read SH, Quinn LM et al (1999) DECAY, a novel Drosophila caspase related to mammalian caspase-3 and caspase-7. J Biol Chem 274:30778–30783. doi:10.1074/jbc.274.43.30778
Harvey NL, Daish T, Mills K et al (2001) Characterization of the Drosophila caspase, DAMM. J Biol Chem 276:25342–25350. doi:10.1074/jbc.M009444200
Hay BA, Wassarman DA, Rubin GM (1995) Drosophila homologs of baculovirus inhibitor of apoptosis proteins function to block cell death. Cell 83:1253–1262. doi:10.1016/0092-8674(95)90150-7
Leulier F, Ribeiro PS, Palmer E et al (2006) Systematic in vivo RNAi analysis of putative components of the Drosophila cell death machinery. Cell Death Differ 13:1663–1674. doi:10.1038/sj.cdd.4401868
Vucic D, Kaiser WJ, Harvey AJ, Miller LK (1997) Inhibition of reaper-induced apoptosis by interaction with inhibitor of apoptosis proteins (IAPs). Proc Natl Acad Sci U S A 94:10183–10188. doi:10.1073/pnas.94.19.10183
Vernooy SY, Copeland J, Ghaboosi N et al (2000) Cell death regulation in Drosophila: conservation of mechanism and unique insights. J Cell Biol 150:F69–F76. doi:10.1083/jcb.150.2.F69
Domingues C, Ryoo HD (2012) Drosophila BRUCE inhibits apoptosis through non-lysine ubiquitination of the IAP-antagonist REAPER. Cell Death Differ 19:470–477. doi:10.1038/cdd.2011.116
Arama E, Agapite J, Steller H (2003) Caspase activity and a specific cytochrome C are required for sperm differentiation in Drosophila. Dev Cell 4:687–697
Orme M, Meier P (2009) Inhibitor of apoptosis proteins in Drosophila: gatekeepers of death. Apoptosis 14:950–960. doi:10.1007/s10495-009-0358-2
Kumar S (2007) Caspase function in programmed cell death. Cell Death Differ 14:32–43. doi:10.1038/sj.cdd.4402060
Ryoo HD, Baehrecke EH (2010) Distinct death mechanisms in Drosophila development. Curr Opin Cell Biol 22:889–895. doi:10.1016/j.ceb.2010.08.022
Grether ME, Abrams JM, Agapite J et al (1995) The head involution defective gene of Drosophila melanogaster functions in programmed cell death. Genes Dev 9:1694–1708
White K, Tahaoglu E, Steller H (1996) Cell killing by the Drosophila gene reaper. Science 271:805–807
Chen P, Nordstrom W, Gish B, Abrams JM (1996) grim, a novel cell death gene in Drosophila. Genes Dev 10:1773–1782. doi:10.1101/gad.10.14.1773
Christich A, Kauppila S, Chen P et al (2002) The damage-responsive Drosophila gene sickle encodes a novel IAP binding protein similar to but distinct from reaper, grim, and hid. Curr Biol 12:137–140. doi:10.1016/S0960-9822(01)00658-3
Srinivasula SM, Datta P, Kobayashi M 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. doi:10.1016/S0960-9822(01)00657-1
Wing JP, Karres JS, Ogdahl JL et al (2002) Drosophila sickle is a novel grim-reaper cell death activator. Curr Biol 12:131–135
Yu X, Wang L, Acehan D et al (2006) Three-dimensional structure of a double apoptosome formed by the Drosophila Apaf-1 related killer. J Mol Biol 355:577–589. doi:10.1016/j.jmb.2005.10.040
Shapiro PJ, Hsu HH, Jung H et al (2008) Regulation of the Drosophila apoptosome through feedback inhibition. Nat Cell Biol 10:1440–1446. doi:10.1038/ncb1803
Handler A (1982) Ecdysteroid titers during pupal and adult development in Drosophila melanogaster. Dev Biol 93:73–82. doi:10.1016/0012-1606(82)90240-8
Warren JT, Yerushalmi Y, Shimell MJ et al (2006) Discrete pulses of molting hormone, 20-hydroxyecdysone, during late larval development of Drosophila melanogaster: correlations with changes in gene activity. Dev Dyn 235:315–326. doi:10.1002/dvdy.20626
Baehrecke EH (2000) Steroid regulation of programmed cell death during Drosophila development. Cell Death Differ 7:1057–1062. doi:10.1038/sj.cdd.4400753
Denton D, Aung-Htut MT, Kumar S (2013) Developmentally programmed cell death in Drosophila. Biochim Biophys Acta. doi:10.1016/j.bbamcr.2013.06.014
Abbott MK, Lengyel JA (1991) Embryonic head involution and rotation of male terminalia require the Drosophila locus head involution defective. Genetics 129:783–789
Miguel-Aliaga I, Thor S (2004) Segment-specific prevention of pioneer neuron apoptosis by cell-autonomous, postmitotic Hox gene activity. Development 131:6093–6105. doi:10.1242/dev.01521
Fichelson P, Gho M (2003) The glial cell undergoes apoptosis in the microchaete lineage of Drosophila. Development 130:123–133
MacÃas A, Romero NM, MartÃn F et al (2004) PVF1/PVR signaling and apoptosis promotes the rotation and dorsal closure of the Drosophila male terminalia. Int J Dev Biol 48:1087–1094. doi:10.1387/ijdb.041859am
Wichmann A, Jaklevic B, Su TT (2006) Ionizing radiation induces caspase-dependent but Chk2- and p53-independent cell death in Drosophila melanogaster. Proc Natl Acad Sci U S A 103:9952–9957. doi:10.1073/pnas.0510528103
Choi YJ, Lee G, Park JH (2006) Programmed cell death mechanisms of identifiable peptidergic neurons in Drosophila melanogaster. Development 133:2223–2232. doi:10.1242/dev.02376
White K, Grether ME, Abrams JM et al (1994) Genetic control of programmed cell death in Drosophila. Science 264:677–683
Brodsky MH, Nordstrom W, Tsang G et al (2000) Drosophila p53 binds a damage response element at the reaper locus. Cell 101:103–113. doi:10.1016/S0092-8674(00)80627-3
Thomas SE, Malzer E, Ordóñez A et al (2013) p53 and translation attenuation regulate distinct cell cycle checkpoints during endoplasmic reticulum (ER) stress. J Biol Chem 288:7606–7617. doi:10.1074/jbc.M112.424655
Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401–415
McGuire SE, Le PT, Osborn AJ et al (2003) Spatiotemporal rescue of memory dysfunction in Drosophila. Science 302:1765–1768. doi:10.1126/science.1089035
Osterwalder T, Yoon KS, White BH, Keshishian H (2001) A conditional tissue-specific transgene expression system using inducible GAL4. Proc Natl Acad Sci U S A 98:12596–12601. doi:10.1073/pnas.221303298
Lee T, Luo L (1999) Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22:451–461
Del Valle RA, Didiano D, Desplan C (2012) Power tools for gene expression and clonal analysis in Drosophila. Nat Methods 9:47–55. doi:10.1038/nmeth.1800
Kanuka H, Hisahara S, Sawamoto K et al (1999) Proapoptotic activity of Caenorhabditis elegans CED-4 protein in Drosophila: implicated mechanisms for caspase activation. Proc Natl Acad Sci U S A 96:145–150
Juhász G, Sass M (2005) Hid can induce, but is not required for autophagy in polyploid larval Drosophila tissues. Eur J Cell Biol 84:491–502. doi:10.1016/j.ejcb.2004.11.010
Abdelwahid E, Yokokura T, Krieser RJ et al (2007) Mitochondrial disruption in Drosophila apoptosis. Dev Cell 12:793–806. doi:10.1016/j.devcel.2007.04.004
Zhou L, Steller H (2003) Distinct pathways mediate UV-induced apoptosis in Drosophila embryos. Dev Cell 4:599–605
Means JC, Muro I, Clem RJ (2006) Lack of involvement of mitochondrial factors in caspase activation in a Drosophila cell-free system. Cell Death Differ 13:1222–1234. doi:10.1038/sj.cdd.4401821
Nordstrom W, Chen P, Steller H, Abrams JM (1996) Activation of the reaper gene during ectopic cell killing in Drosophila. Dev Biol 180:213–226. doi:10.1006/dbio.1996.0296
Jiang C, Lamblin AF, Steller H, Thummel CS (2000) A steroid-triggered transcriptional hierarchy controls salivary gland cell death during Drosophila metamorphosis. Mol Cell 5:445–455
Fan Y, Lee TV, Xu D et al (2010) Dual roles of Drosophila p53 in cell death and cell differentiation. Cell Death Differ 17:912–921. doi:10.1038/cdd.2009.182
Steller H (2008) Regulation of apoptosis in Drosophila. Cell Death Differ 15:1132–1138. doi:10.1038/cdd.2008.50
Dorstyn L, Read S, Cakouros D et al (2002) The role of cytochrome c in caspase activation in Drosophila melanogaster cells. J Cell Biol 156:1089–1098. doi:10.1083/jcb.200111107
Robbins E, Marcus PI (1963) Dynamics of acridine orange-cell interaction. I. interrelationships of acridine orange particles and cytoplasmic reddening. J Cell Biol 18:237–250
Bonini NM, Leiserson WM, Benzer S (1993) The eyes absent gene: genetic control of cell survival and differentiation in the developing Drosophila eye. Cell 72:379–395
Riss TL, Moravec RA, Niles AL, et al. (2004) Cell viability assays. Assay Guidance Manual
Morishita J, Kang MJ, Fidelin K, Ryoo HD (2013) CDK7 regulates the mitochondrial localization of a Tail-anchored proapoptotic protein, hid. Cell Rep 5:1481–1488. doi:10.1016/j.celrep.2013.11.030
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2016 Springer Science+Business Media New York
About this protocol
Cite this protocol
Vasudevan, D., Ryoo, H.D. (2016). Detection of Cell Death in Drosophila Tissues. In: Puthalakath, H., Hawkins, C. (eds) Programmed Cell Death. Methods in Molecular Biology, vol 1419. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-3581-9_11
Download citation
DOI: https://doi.org/10.1007/978-1-4939-3581-9_11
Published:
Publisher Name: Humana Press, New York, NY
Print ISBN: 978-1-4939-3579-6
Online ISBN: 978-1-4939-3581-9
eBook Packages: Springer Protocols