Abstract
It is now well established that the mitochondrion is a central regulator of mammalian cell apoptosis. However, the importance of this organelle in non-mammalian apoptosis has long been regarded as minor, mainly because of the absence of a crucial role for cytochrome c in caspase activation. Recent results indicate that the control of caspase activation and cell death in Drosophila occurs at the mitochondrial level. Numerous proteins, including RHG proteins and proteins of the Bcl-2 family that are key regulators of Drosophila apoptosis, constitutively or transiently localize in mitochondria. These proteins participate in the cell death process at different levels such as degradation of Diap1, a Drosophila IAP, production of mitochondrial reactive oxygen species or stimulation of the mitochondrial fission machinery. Here, we review these mitochondrial events that might have their counterpart in human.
Similar content being viewed by others
References
Connolly PF, Jager R, Fearnhead HO (2014) New roles for old enzymes: killer caspases as the engine of cell behavior changes. Front Physiol 5:149
Cooper DM, Granville DJ, Lowenberger C (2009) The insect caspases. Apoptosis 14:247–256
Kumar S, Doumanis J (2000) The fly caspases. Cell Death Differ 7:1039–1044
Mignotte B, Colin J, Brun S, Guénal I (2005) Apoptosis: the fly point of view. In: Scovassi AI (ed) Apoptosis. Research Signpost, Kerala, pp 169–186
Wajant H (2002) The Fas signaling pathway: more than a paradigm. Science 296:1635–1636
Darding M, Meier P (2012) IAPs: guardians of RIPK1. Cell Death Differ 19:58–66
Khosravi-Far R, Esposti MD (2004) Death receptor signals to mitochondria. Cancer Biol Ther 3:1051–1057
Desagher S, Martinou JC (2000) Mitochondria as the central control point of apoptosis. Trends Cell Biol 10:369–377
Cosentino K, Garcia-Saez AJ (2014) Mitochondrial alterations in apoptosis. Chem Phys Lipids 181:62–75
Varkey J, Chen P, Jemmerson R, Abrams JM (1999) Altered cytochrome c display precedes apoptotic cell death in Drosophila. J Cell Biol 144:701–710
Abdelwahid E, Yokokura T, Krieser RJ, Balasundaram S, Fowle WH, White K (2007) Mitochondrial disruption in Drosophila apoptosis. Dev Cell 12:793–806
Challa M, Malladi S, Pellock BJ, Dresnek D, Varadarajan S, Yin YW et al (2007) Drosophila Omi, a mitochondrial-localized IAP antagonist and proapoptotic serine protease. EMBO J 26:3144–3156
Dorstyn L, Read S, Cakouros D, Huh JR, Hay BA, Kumar S (2002) The role of cytochrome c in caspase activation in Drosophila melanogaster cells. J Cell Biol 156:1089–1098
Kanuka H, Sawamoto K, Inohara N, Matsuno K, Okano H, Miura M (1999) Control of the cell death pathway by Dapaf-1, a Drosophila Apaf-1/Ced-4-related caspase activator. Mol Cell 4:757–769
Zimmermann KC, Ricci JE, Droin NM, Green DR (2002) The role of ARK in stress-induced apoptosis in Drosophila cells. J Cell Biol 156:1077–1087
Rodriguez A, Oliver H, Zou H, Chen P, Wang X, Abrams JM (1999) Dark is a Drosophila homologue of Apaf-1/CED-4 and functions in an evolutionarily conserved death pathway. Nat Cell Biol 1:272–279
Zhou L, Song Z, Tittel J, Steller H (1999) HAC-1, a Drosophila homolog of Apaf-1 and Ced-4, functions in developmental and radiation-induced apoptosis. Mol Cell 4:745–755
D’Brot A, Chen P, Vaishnav M, Yuan S, Akey CW, Abrams JM (2013) Tango7 directs cellular remodeling by the Drosophila apoptosome. Genes Dev 27:1650–1655
Yu X, Wang L, Acehan D, Wang X, Akey CW (2006) Three-dimensional structure of a double apoptosome formed by the Drosophila Apaf-1 related killer. J Mol Biol 355:577–589
Yuan S, Yu X, Topf M, Dorstyn L, Kumar S, Ludtke SJ et al (2011) Structure of the Drosophila apoptosome at 6.9 a resolution. Structure 19:128–140
Dorstyn L, Kumar S (2006) A cytochrome c-free fly apoptosome. Cell Death Differ 13:1049–1051
Dorstyn L, Mills K, Lazebnik Y, Kumar S (2004) The two cytochrome c species, DC3 and DC4, are not required for caspase activation and apoptosis in Drosophila cells. J Cell Biol 167:405–410
Kiessling S, Green DR (2006) Cell survival and proliferation in Drosophila S2 cells following apoptotic stress in the absence of the APAF-1 homolog, ARK, or downstream caspases. Apoptosis 11:497–507
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
Arama E, Bader M, Srivastava M, Bergmann A, Steller H (2006) The two Drosophila cytochrome C proteins can function in both respiration and caspase activation. EMBO J 25:232–243
Huh JR, Vernooy SY, Yu H, Yan N, Shi Y, Guo M et al (2004) Multiple apoptotic caspase cascades are required in nonapoptotic roles for Drosophila spermatid individualization. PLoS Biol 2:E15
Feinstein-Rotkopf Y, Arama E (2009) Can’t live without them, can live with them: roles of caspases during vital cellular processes. Apoptosis 14:980–995
Mendes CS, Arama E, Brown S, Scherr H, Srivastava M, Bergmann A et al (2006) Cytochrome c-d regulates developmental apoptosis in the Drosophila retina. EMBO Rep 7:933–939
Igaki T, Suzuki Y, Tokushige N, Aonuma H, Takahashi R, Miura M (2007) Evolution of mitochondrial cell death pathway: proapoptotic role of HtrA2/Omi in Drosophila. Biochem Biophys Res Commun 356:993–997
Khan FS, Fujioka M, Datta P, Fernandes-Alnemri T, Jaynes JB, Alnemri ES (2008) The interaction of DIAP1 with dOmi/HtrA2 regulates cell death in Drosophila. Cell Death Differ 15:1073–1083
Yacobi-Sharon K, Namdar Y, Arama E (2013) Alternative germ cell death pathway in Drosophila involves HtrA2/Omi, lysosomes, and a caspase-9 counterpart. Dev Cell 25:29–42
Tain LS, Chowdhury RB, Tao RN, Plun-Favreau H, Moisoi N, Martins LM et al (2009) Drosophila HtrA2 is dispensable for apoptosis but acts downstream of PINK1 independently from Parkin. Cell Death Differ 16:1118–1125
Goyal L, McCall K, Agapite J, Hartwieg E, Steller H (2000) Induction of apoptosis by Drosophila reaper, hid and grim through inhibition of IAP function. EMBO J 19:589–597
Leulier F, Ribeiro PS, Palmer E, Tenev T, Takahashi K, Robertson D et al (2006) Systematic in vivo RNAi analysis of putative components of the Drosophila cell death machinery. Cell Death Differ 13:1663–1674
Lisi S, Mazzon I, White K (2000) Diverse domains of THREAD/DIAP1 are required to inhibit apoptosis induced by REAPER and HID in Drosophila. Genetics 154:669–678
Wang ZH, Ding MX, Chew-Cheng SB, Yun JP, Chew EC (1999) Bcl-2 and Bax proteins are nuclear matrix associated proteins. Anticancer Res 19:5445–5449
Yin VP, Thummel CS (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
Yan N, Wu JW, Chai J, Li W, Shi Y (2004) Molecular mechanisms of DrICE inhibition by DIAP1 and removal of inhibition by Reaper, Hid and Grim. Nat Struct Mol Biol 11:420–428
Zachariou A, Tenev T, Goyal L, Agapite J, Steller H, Meier P (2003) IAP-antagonists exhibit non-redundant modes of action through differential DIAP1 binding. EMBO J 22:6642–6652
Chai J, Yan N, Huh JR, Wu JW, Li W, Hay BA et al (2003) Molecular mechanism of Reaper-Grim-Hid-mediated suppression of DIAP1-dependent Dronc ubiquitination. Nat Struct Biol 10:892–898
Meier P, Silke J, Leevers SJ, Evan GI (2000) The Drosophila caspase DRONC is regulated by DIAP1. EMBO J 19:598–611
Muro I, Hay BA, Clem RJ (2002) The Drosophila DIAP1 protein is required to prevent accumulation of a continuously generated, processed form of the apical caspase DRONC. J Biol Chem 277:49644–49650
Shapiro PJ, Hsu HH, Jung H, Robbins ES, Ryoo HD (2008) Regulation of the Drosophila apoptosome through feedback inhibition. Nat Cell Biol 10:1440–1446
Orme M, Meier P (2009) Inhibitor of apoptosis proteins in Drosophila: gatekeepers of death. Apoptosis 14:950–960
Vucic D, Kaiser WJ, Miller LK (1998) Inhibitor of apoptosis proteins physically interact with and block apoptosis induced by Drosophila proteins HID and GRIM. Mol Cell Biol 18:3300–3309
Vucic D, Seshagiri S, Miller LK (1997) Characterization of reaper- and FADD-induced apoptosis in a lepidopteran cell line. Mol Cell Biol 17:667–676
Wing JP, Zhou L, Schwartz LM, Nambu JR (1998) Distinct cell killing properties of the Drosophila reaper, head involution defective, and grim genes. Cell Death Differ 5:930–939
Wing JP, Schwartz LM, Nambu JR (2001) The RHG motifs of Drosophila reaper and Grim are important for their distinct cell death-inducing abilities. Mech Dev 102:193–203
Haining WN, Carboy-Newcomb C, Wei CL, Steller H (1999) The proapoptotic function of Drosophila Hid is conserved in mammalian cells. Proc Natl Acad Sci USA 96:4936–4941
McCarthy JV, Dixit VM (1998) Apoptosis induced by Drosophila reaper and grim in a human system. Attenuation by inhibitor of apoptosis proteins (cIAPs). J Biol Chem 273:24009–24015
Christich A, Kauppila S, Chen P, Sogame N, Ho SI, Abrams JM (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
Srinivasula SM, Datta P, Kobayashi M, Wu JW, Fujioka M, Hegde R 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
Tenev T, Zachariou A, Wilson R, Paul A, Meier P (2002) Jafrac2 is an IAP antagonist that promotes cell death by liberating Dronc from DIAP1. EMBO J 21:5118–5129
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 USA 94:10183–10188
Wu JW, Cocina AE, Chai J, Hay BA, Shi Y (2001) Structural analysis of a functional DIAP1 fragment bound to grim and hid peptides. Mol Cell 8:95–104
Kurada P, White K (1998) Ras promotes cell survival in Drosophila by downregulating hid. Cell 95:319–329
Kang J, Yeom E, Lim J, Choi KW (2014) Bar represses dPax2 and decapentaplegic to regulate cell fate and morphogenetic cell death in Drosophila eye. PLoS ONE 9:e88171
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
Robinow S, Draizen TA, Truman JW (1997) Genes that induce apoptosis: transcriptional regulation in identified doomed neurons of the Drosophila CNS. Dev Biol 190:206–213
Jiang CG, Baerhecke EH, Thummel CS (1997) Steroid regulated programmed cell deatn during Drosophila metamorphosis. Development 124:4673–4683
Link N, Kurtz P, O’Neal M, Garcia-Hughes G, Abrams JM (2013) A p53 enhancer region regulates target genes through chromatin conformations in cis and in trans. Genes Dev 27:2433–2438
Lohmann I (2003) Dissecting the regulation of the Drosophila cell death activator reaper. Gene Expr Patterns 3:159–163
Tan Y, Yamada-Mabuchi M, Arya R, St Pierre S, Tang W, Tosa M et al (2011) Coordinated expression of cell death genes regulates neuroblast apoptosis. Development 138:2197–2206
Brodsky MH, Nordstrom W, Tsang G, Kwan E, Rubin GM, Abrams JM (2000) Drosophila p53 binds a damage response element at the reaper locus. Cell 101:103–113
Chen P, Ho SI, Shi Z, Abrams JM (2004) Bifunctional killing activity encoded by conserved reaper proteins. Cell Death Differ 11:704–713
Chen P, Lee P, Otto L, Abrams J (1996) Apoptotic activity of REAPER is distinct from signaling by the tumor necrosis factor receptor 1 death domain. J Biol Chem 271:25735–25737
Claveria C, Albar JP, Serrano A, Buesa JM, Barbero JL, Martinez AC et al (1998) Drosophila grim induces apoptosis in mammalian cells. EMBO J 17:7199–7208
Claveria C, Caminero E, Martinez AC, Campuzano S, Torres M (2002) GH3, a novel proapoptotic domain in Drosophila Grim, promotes a mitochondrial death pathway. EMBO J 21:3327–3336
Claveria C, Martinez AC, Torres M (2004) A Bax/Bak-independent mitochondrial death pathway triggered by Drosophila Grim GH3 domain in mammalian cells. J Biol Chem 279:1368–1375
Tait SW, Werner AB, de Vries E, Borst J (2004) Mechanism of action of Drosophila reaper in mammalian cells: reaper globally inhibits protein synthesis and induces apoptosis independent of mitochondrial permeability. Cell Death Differ 11:800–811
Thress K, Evans EK, Kornbluth S (1999) Reaper-induced dissociation of a Scythe-sequestered cytochrome c-releasing activity. EMBO J 18:5486–5493
Olson MR, Holley CL, Gan EC, Colon-Ramos DA, Kaplan B, Kornbluth S (2003) A GH3-like domain in reaper is required for mitochondrial localization and induction of IAP degradation. J Biol Chem 278:44758–44768
Zhou L (2005) The ‘unique key’ feature of the Iap-binding motifs in RHG proteins. Cell Death Differ 12:1148–1151
Freel CD, Richardson DA, Thomenius MJ, Gan EC, Horn SR, Olson MR et al (2008) Mitochondrial localization of Reaper to promote inhibitors of apoptosis protein degradation conferred by GH3 domain-lipid interactions. J Biol Chem 283:367–379
Sandu C, Ryoo HD, Steller H (2010) Drosophila IAP antagonists form multimeric complexes to promote cell death. J Cell Biol 190:1039–1052
Thomenius M, Freel CD, Horn S, Krieser R, Abdelwahid E, Cannon R et al (2011) Mitochondrial fusion is regulated by Reaper to modulate Drosophila programmed cell death. Cell Death Differ 18:1640–1650
Morishita J, Kang MJ, Fidelin K, Ryoo HD (2013) CDK7 regulates the mitochondrial localization of a tail-anchored proapoptotic protein, Hid. Cell reports 5:1481–1488
Evans EK, Kuwana T, Strum SL, Smith JJ, Newmeyer DD, Kornbluth S (1997) Reaper-induced apoptosis in a vertebrate system. EMBO J 16:7372–7381
Goyal G, Fell B, Sarin A, Youle RJ, Sriram V (2007) Role of mitochondrial remodeling in programmed cell death in Drosophila melanogaster. Dev Cell 12:807–816
Thress K, Henzel W, Shillinglaw W, Kornbluth S (1998) Scythe: a novel reaper-binding apoptotic regulator. EMBO J 17:6135–6143
Brun S, Rincheval V, Gaumer S, Mignotte B, Guenal I (2002) reaper and bax initiate two different apoptotic pathways affecting mitochondria and antagonized by bcl-2 in Drosophila. Oncogene 21:6458–6470
Aouacheria A, Combet C, Tompa P, Hardwick JM (2015) Redefining the BH3 Death Domain as a 'Short Linear Motif'. Trends Biochem Sci 40:736–748
Martinou JC, Youle RJ (2011) Mitochondria in apoptosis: bcl-2 family members and mitochondrial dynamics. Dev Cell 21:92–101
Brachmann CB, Jassim OW, Wachsmuth BD, Cagan RL (2000) The Drosophila bcl-2 family member dBorg-1 functions in the apoptotic response to UV-irradiation. Curr Biol 10:547–550
Colussi PA, Quinn LM, Huang DC, Coombe M, Read SH, Richardson H et al (2000) Debcl, a proapoptotic Bcl-2 homologue, is a component of the Drosophila melanogaster cell death machinery. J Cell Biol 148:703–714
Igaki T, Kanuka H, Inohara N, Sawamoto K, Nunez G, Okano H et al (2000) Drob-1, a Drosophila member of the bcl-2/CED-9 family that promotes cell death. Proc Natl Acad Sci USA 97:662–667
Quinn L, Coombe KM, Tasman D, Colussi P, Kumar S, Richardson H (2003) Buffy, a Drosophila Bcl-2 protein, has anti-apoptotic and cell cycle inhibitory functions. EMBO J 22:3568–3579
Zhang H, Huang Q, Ke N, Matsuyama S, Hammock B, Godzik A et al (2000) Drosophila pro-apoptotic Bcl-2/Bax homologue reveals evolutionary conservation of cell death mechanisms. J Biol Chem 275:27303–27306
Doumanis J, Dorstyn L, Kumar S (2007) Molecular determinants of the subcellular localization of the Drosophila Bcl-2 homologues DEBCL and BUFFY. Cell Death Differ 14:907–915
Igaki T, Miura M (2004) Role of Bcl-2 family members in invertebrates. Biochim Biophys Acta 1644:73–81
Ly LL, Suyari O, Yoshioka Y, Tue NT, Yoshida H, Yamaguchi M (2013) dNF-YB plays dual roles in cell death and cell differentiation during Drosophila eye development. Gene 520:106–118
Colin J, Garibal J, Clavier A, Rincheval-Arnold A, Gaumer S, Mignotte B et al (2014) The drosophila Bcl-2 family protein Debcl is targeted to the proteasome by the beta-TrCP homologue slimb. Apoptosis 19:1444–1456
Clavier A, Baillet A, Rincheval-Arnold A, Coleno-Costes A, Lasbleiz C, Mignotte B et al (2014) The pro-apoptotic activity of Drosophila Rbf1 involves dE2F2-dependent downregulation of diap1 and buffy mRNA. Cell Death Dis 5:e1405
Clavier A, Ruby V, Rincheval-Arnold A, Mignotte B, Guenal I (2015) The Drosophila retinoblastoma protein, Rbf1, induces a debcl and drp1-dependent mitochondrial apoptosis. J Cell Sci 128:3239–3249
Colin J, Garibal J, Clavier A, Szuplewski S, Risler Y, Milet C et al (2015) Screening of suppressors of bax-induced cell death identifies glycerophosphate oxidase-1 as a mediator of debcl-induced apoptosis in Drosophila. Genes Cancer 6:241–253
Park J, Kim Y, Choi S, Koh H, Lee SH, Kim JM et al (2010) Drosophila Porin/VDAC affects mitochondrial morphology. PLoS One 5:e13151
Kanda H, Igaki T, Okano H, Miura M (2011) Conserved metabolic energy production pathways govern Eiger/TNF-induced nonapoptotic cell death. Proc Natl Acad Sci USA 108:18977–18982
Grusche FA, Degoutin JL, Richardson HE, Harvey KF (2011) The Salvador/Warts/Hippo pathway controls regenerative tissue growth in Drosophila melanogaster. Dev Biol 350:255–266
Copeland JM, Bosdet I, Freeman JD, Guo M, Gorski SM, Hay BA (2007) Echinus, required for interommatidial cell sorting and cell death in the Drosophila pupal retina, encodes a protein with homology to ubiquitin-specific proteases. BMC Dev Biol 7:82
Senoo-Matsuda N, Igaki T, Miura M (2005) Bax-like protein Drob-1 protects neurons from expanded polyglutamine-induced toxicity in Drosophila. EMBO J 24:2700–2713
Cheng WC, Berman SB, Ivanovska I, Jonas EA, Lee SJ, Chen Y et al (2006) Mitochondrial factors with dual roles in death and survival. Oncogene 25:4697–4705
Sevrioukov EA, Burr J, Huang EW, Assi HH, Monserrate JP, Purves DC et al (2007) Drosophila Bcl-2 proteins participate in stress-induced apoptosis, but are not required for normal development. Genesis 45:184–193
Tanner EA, Blute TA, Brachmann CB, McCall K (2011) Bcl-2 proteins and autophagy regulate mitochondrial dynamics during programmed cell death in the Drosophila ovary. Development 138:327–338
Tanner EA, McCall K (2011) Mitochondrial regulation of cell death in the Drosophila ovary. Autophagy 7:793–794
Wu JN, Nguyen N, Aghazarian M, Tan Y, Sevrioukov EA, Mabuchi M et al (2010) Grim promotes programmed cell death of Drosophila microchaete glial cells. Mech Dev 127:407–417
Galindo KA, Lu WJ, Park JH, Abrams JM (2009) The Bax/Bak ortholog in Drosophila, Debcl, exerts limited control over programmed cell death. Development 136:275–283
Hou YC, Chittaranjan S, Barbosa SG, McCall K, Gorski SM (2008) Effector caspase Dcp-1 and IAP protein Bruce regulate starvation-induced autophagy during Drosophila melanogaster oogenesis. J Cell Biol 182:1127–1139
Monserrate JP, Chen MY, Brachmann CB (2012) Drosophila larvae lacking the bcl-2 gene, buffy, are sensitive to nutrient stress, maintain increased basal target of rapamycin (Tor) signaling and exhibit characteristics of altered basal energy metabolism. BMC Biol 10:63
Tsubouchi A, Tsuyama T, Fujioka M, Kohda H, Okamoto-Furuta K, Aigaki T et al (2009) Mitochondrial protein Preli-like is required for development of dendritic arbors and prevents their regression in the Drosophila sensory nervous system. Development 136:3757–3766
Frank S, Gaume B, Bergmann-Leitner ES, Leitner WW, Robert EG, Catez F et al (2001) The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Dev Cell 1:515–525
Lee YJ, Jeong SY, Karbowski M, Smith CL, Youle RJ (2004) Roles of the mammalian mitochondrial fission and fusion mediators Fis1, Drp1, and Opa1 in apoptosis. Mol Biol Cell 15:5001–5011
Cassidy-Stone A, Chipuk JE, Ingerman E, Song C, Yoo C, Kuwana T et al (2008) Chemical inhibition of the mitochondrial division dynamin reveals its role in Bax/Bak-dependent mitochondrial outer membrane permeabilization. Dev Cell 14:193–204
Ishihara N, Nomura M, Jofuku A, Kato H, Suzuki SO, Masuda K et al (2009) Mitochondrial fission factor Drp1 is essential for embryonic development and synapse formation in mice. Nat Cell Biol 11:958–966
Wakabayashi J, Zhang Z, Wakabayashi N, Tamura Y, Fukaya M, Kensler TW et al (2009) The dynamin-related GTPase Drp1 is required for embryonic and brain development in mice. J Cell Biol 186:805–816
Jahani-Asl A, Cheung EC, Neuspiel M, MacLaurin JG, Fortin A, Park DS et al (2007) Mitofusin 2 protects cerebellar granule neurons against injury-induced cell death. J Biol Chem 282:23788–23798
Sugioka R, Shimizu S, Tsujimoto Y (2004) Fzo1, a protein involved in mitochondrial fusion, inhibits apoptosis. J Biol Chem 279:52726–52734
Rolland SG, Conradt B (2010) New role of the BCL2 family of proteins in the regulation of mitochondrial dynamics. Curr Opin Cell Biol 22:852–858
Autret A, Martin SJ (2009) Emerging role for members of the Bcl-2 family in mitochondrial morphogenesis. Mol Cell 36:355–363
Park J, Lee SB, Lee S, Kim Y, Song S, Kim S et al (2006) Mitochondrial dysfunction in Drosophila PINK1 mutants is complemented by parkin. Nature 441:1157–1161
Igaki T (2009) Correcting developmental errors by apoptosis: lessons from Drosophila JNK signaling. Apoptosis 14:1021–1028
Morey M, Corominas M, Serras F (2003) DIAP1 suppresses ROS-induced apoptosis caused by impairment of the selD/sps1 homolog in Drosophila. J Cell Sci 116:4597–4604
Mollereau B, Ma D (2014) The p53 control of apoptosis and proliferation: lessons from Drosophila. Apoptosis 19:1421–1429
Gowda PS, Zhou F, Chadwell LV, McEwen DG (2012) p53 binding prevents phosphatase-mediated inactivation of diphosphorylated c-Jun N-terminal kinase. J Biol Chem 287:17554–17567
Qi Y, Liu H, Daniels MP, Zhang G, Xu H (2015) Loss of Drosophila i-AAA protease, dYME1L, causes abnormal mitochondria and apoptotic degeneration. Cell Death Differ. doi:10.1038/cdd.2015.94
Joza N, Galindo K, Pospisilik JA, Benit P, Rangachari M, Kanitz EE et al (2008) The molecular archaeology of a mitochondrial death effector: AIF in Drosophila. Cell Death Differ 15:1009–1018
Yi CH, Sogah DK, Boyce M, Degterev A, Christofferson DE, Yuan J (2007) A genome-wide RNAi screen reveals multiple regulators of caspase activation. J Cell Biol 179:619–626
Lin R, Angelin A, Da Settimo F, Martini C, Taliani S, Zhu S et al (2014) Genetic analysis of dTSPO, an outer mitochondrial membrane protein, reveals its functions in apoptosis, longevity, and Ab42-induced neurodegeneration. Aging Cell 13:507–518
Estaquier J, Vallette F, Vayssiere JL, Mignotte B (2012) The mitochondrial pathways of apoptosis. Adv Exp Med Biol 942:157–183
Abdelwahid E, Rolland S, Teng X, Conradt B, Hardwick JM, White K (2011) Mitochondrial involvement in cell death of non-mammalian eukaryotes. Biochim Biophys Acta 1813:597–607
Bueler H (2010) Mitochondrial dynamics, cell death and the pathogenesis of Parkinson’s disease. Apoptosis 15:1336–1353
Guo M (2012) Drosophila as a model to study mitochondrial dysfunction in Parkinson’s disease. Cold Spring Harb Perspect Med 2 131. Aouacheria A, Combet C, Tompa P, Hardwick JM. (2015) Redefining the BH3 Death Domain as a 'Short Linear Motif'. Trends Biochem Sci 40:736-748.
Acknowledgments
We are grateful to Tommaso Villa for his critical reading of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Clavier, A., Rincheval-Arnold, A., Colin, J. et al. Apoptosis in Drosophila: which role for mitochondria?. Apoptosis 21, 239–251 (2016). https://doi.org/10.1007/s10495-015-1209-y
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10495-015-1209-y