Home LiteratureArticle Details
PMID: 19483676 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Genome-wide silencing in Drosophila captures conserved apoptotic effectors.

Nature ·Vol. 460 ·No. 7251 ·2009-07-02 ·Pages 123-7

Chew SK, Chen P, Link N, Galindo KA, Pogue K, Abrams JM

Abstract

Apoptosis is a conserved form of programmed cell death firmly established in the aetiology, pathogenesis and treatment of many human diseases. Central to the core machinery of apoptosis are the caspases and their proximal regulators. Current models for caspase control involve a balance of opposing elements, with variable contributions from positive and negative regulators among different cell types and species. To advance a comprehensive view of components that support caspase-dependent cell death, we conducted a genome-wide silencing screen in the Drosophila model. Our strategy used a library of double-stranded RNAs together with a chemical antagonist of Inhibitor of apoptosis proteins (IAPs) that simulates the action of native regulators in the Reaper and Smac (also known as Diablo) families. Here we present a highly validated set of targets that is necessary for death provoked by several stimuli. Among these, Tango7 is identified as a new effector. Cells depleted for this gene resisted apoptosis at a step before the induction of effector caspase activity, and the directed silencing of Tango7 in Drosophila prevented caspase-dependent programmed cell death. Unlike known apoptosis regulators in this model system, Tango7 activity did not influence stimulus-dependent loss of Drosophila DIAP1 (also known as th and IAP1), but instead regulated levels of the apical caspase Dronc (Nc). Similarly, the human Tango7 counterpart, PCID1 (also known as EIF3M), impinged on caspase 9, revealing a new regulatory axis affecting the apoptosome.

MeSH Terms
Animals Apoptosis/genetics,physiology Apoptosomes/metabolism Aryl Hydrocarbon Receptor Nuclear Translocator/genetics,metabolism Caspase 9/metabolism Caspases/metabolism Conserved Sequence Drosophila Proteins/deficiency,genetics,metabolism Drosophila melanogaster/genetics Eukaryotic Initiation Factor-3 Eukaryotic Initiation Factors/metabolism Gene Silencing Genes, Insect/genetics Genome, Insect/genetics Humans Inhibitor of Apoptosis Proteins/antagonists & inhibitors,genetics,metabolism Mitochondrial Proteins Molecular Mimicry RNA Interference RNA, Double-Stranded/genetics Reproducibility of Results Xenopus Proteins
Chemicals
Apoptosomes DIABLO protein, Xenopus DIAP1 protein, Drosophila Drosophila Proteins EIF3M protein, human Eukaryotic Initiation Factor-3 Eukaryotic Initiation Factors Inhibitor of Apoptosis Proteins Mitochondrial Proteins RNA, Double-Stranded Xenopus Proteins eIF3m protein, Drosophila Aryl Hydrocarbon Receptor Nuclear Translocator Caspase 9 Caspases dronc protein, Drosophila
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Chew Su Kit
Department of Cell Biology, University of Texas Southwestern Medical Center, Dallas, Texas 75390, USA.
Chen Po
Link Nichole
Galindo Kathleen A
Pogue Kristi
Abrams John M
References (32)
32 references, click to expand
  1. Herpes simplex virus entry mediator associates in infected cells in a complex with viral proteins gD and at least gH.
    J Virol. 2005 Apr;79(7):4540-4 PMID: 15767456
  2. A non-apoptotic role for caspase-9 in muscle differentiation.
    J Cell Sci. 2008 Nov 15;121(Pt 22):3786-93 PMID: 18957517
  3. The role of ARK in stress-induced apoptosis in Drosophila cells.
    J Cell Biol. 2002 Mar 18;156(6):1077-87 PMID: 11901172
  4. Requirement of cytochrome c for apoptosis in human cells.
    Cell Death Differ. 2006 Dec;13(12):2062-7 PMID: 16729029
  5. GAPDH and autophagy preserve survival after apoptotic cytochrome c release in the absence of caspase activation.
    Cell. 2007 Jun 1;129(5):983-97 PMID: 17540177
  6. Cytochrome c-d regulates developmental apoptosis in the Drosophila retina.
    EMBO Rep. 2006 Sep;7(9):933-9 PMID: 16906130
  7. Caspase-independent cell death.
    Nat Med. 2005 Jul;11(7):725-30 PMID: 16015365
  8. Caspase-dependent cell death in Drosophila.
    Annu Rev Cell Dev Biol. 2006;22:623-50 PMID: 16842034
  9. Caspase activation, inhibition, and reactivation: a mechanistic view.
    Protein Sci. 2004 Aug;13(8):1979-87 PMID: 15273300
  10. Genome-wide RNAi analysis of growth and viability in Drosophila cells.
    Science. 2004 Feb 6;303(5659):832-5 PMID: 14764878
  11. Use of double-stranded RNA interference in Drosophila cell lines to dissect signal transduction pathways.
    Proc Natl Acad Sci U S A. 2000 Jun 6;97(12):6499-503 PMID: 10823906
  12. A new class of receptor for herpes simplex virus has heptad repeat motifs that are common to membrane fusion proteins.
    J Virol. 2005 Jun;79(12):7419-30 PMID: 15919898
  13. A collective form of cell death requires homeodomain interacting protein kinase.
    J Cell Biol. 2007 Aug 13;178(4):567-74 PMID: 17682052
  14. A Simple Statistical Parameter for Use in Evaluation and Validation of High Throughput Screening Assays.
    J Biomol Screen. 1999;4(2):67-73 PMID: 10838414
  15. The Drosophila DIAP1 protein is required to prevent accumulation of a continuously generated, processed form of the apical caspase DRONC.
    J Biol Chem. 2002 Dec 20;277(51):49644-50 PMID: 12397080
  16. Prevalence of off-target effects in Drosophila RNA interference screens.
    Nature. 2006 Sep 21;443(7109):359-63 PMID: 16964239
  17. Autophagy occurs upstream or parallel to the apoptosome during histolytic cell death.
    Development. 2006 Apr;133(8):1457-65 PMID: 16540507
  18. Cell death in normal and rough eye mutants of Drosophila.
    Development. 1991 Nov;113(3):825-39 PMID: 1821853
  19. Cell death regulation by the mammalian IAP antagonist Diablo/Smac.
    Apoptosis. 2002 Apr;7(2):163-6 PMID: 11865200
  20. A novel p53 rescue compound induces p53-dependent growth arrest and sensitises glioma cells to Apo2L/TRAIL-induced apoptosis.
    Cell Death Differ. 2008 Apr;15(4):718-29 PMID: 18202704
  21. Caspase activation - stepping on the gas or releasing the brakes? Lessons from humans and flies.
    Oncogene. 2004 Apr 12;23(16):2774-84 PMID: 15077141
  22. The Drosophila caspase Ice is important for many apoptotic cell deaths and for spermatid individualization, a nonapoptotic process.
    Development. 2006 Sep;133(17):3305-15 PMID: 16887831
  23. Dark is a Drosophila homologue of Apaf-1/CED-4 and functions in an evolutionarily conserved death pathway.
    Nat Cell Biol. 1999 Sep;1(5):272-9 PMID: 10559939
  24. Functional genomics reveals genes involved in protein secretion and Golgi organization.
    Nature. 2006 Feb 2;439(7076):604-7 PMID: 16452979
  25. A small molecule Smac mimic potentiates TRAIL- and TNFalpha-mediated cell death.
    Science. 2004 Sep 3;305(5689):1471-4 PMID: 15353805
  26. The apical caspase dronc governs programmed and unprogrammed cell death in Drosophila.
    Dev Cell. 2004 Dec;7(6):897-907 PMID: 15572131
  27. Activation of the cAMP/PKA signaling pathway is required for post-ecdysial cell death in wing epidermal cells of Drosophila melanogaster.
    Development. 2004 Apr;131(7):1597-606 PMID: 14998927
  28. Evidence of off-target effects associated with long dsRNAs in Drosophila melanogaster cell-based assays.
    Nat Methods. 2006 Oct;3(10):833-8 PMID: 16964256
  29. Degradation of DIAP1 by the N-end rule pathway is essential for regulating apoptosis.
    Nat Cell Biol. 2003 May;5(5):467-73 PMID: 12692559
  30. The CARD-carrying caspase Dronc is essential for most, but not all, developmental cell death in Drosophila.
    Development. 2005 May;132(9):2125-34 PMID: 15800001
  31. Statistical practice in high-throughput screening data analysis.
    Nat Biotechnol. 2006 Feb;24(2):167-75 PMID: 16465162
  32. Core signaling pathways in human pancreatic cancers revealed by global genomic analyses.
    Science. 2008 Sep 26;321(5897):1801-6 PMID: 18772397
Article Info
Journal
Nature
Abbr.
Nature
ISSN
1476-4687
Published
2009-07-02
Epub
2009-00-31
Pages
123-7
Language
English
Region
England
NLM ID
0410462
PMCID
PMC2777527
Subset
IM
Grants
NIAAA NIH HHS · R01 AA017328-01 · United States
NIGMS NIH HHS · R01 GM072124-13 · United States
NIGMS NIH HHS · R01 GM072124 · United States
NIAAA NIH HHS · R01 AA017328 · United States
NIGMS NIH HHS · R01 GM072124-11 · United States
NIGMS NIH HHS · R01 GM072124-12 · United States
NIAAA NIH HHS · R01 AA017328-02 · United States
NIGMS NIH HHS · R01 GM072124-14A1 · United States
NIGMS NIH HHS · R56 GM072124 · United States
NIGMS NIH HHS · R01 GM072124-10 · United States
NIGMS NIH HHS · R56 GM072124-14 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com