A case study of the reproducibility of transcriptional reporter cell-based RNAi screens in Drosophila

Genome Biology

Volumn 8, Issue 9, 2007, Pages

  DasGupta, Ramanuj ^a   Nybakken, Kent ^b   Booker, Matthew ^c   Mathey Prevot, Bernard ^c   Gonsalves, Foster ^a   Changkakoty, Binita ^a   Perrimon, Norbert ^c,d  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BOSTON BIOMEDICAL RESEARCH INSTITUTE   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED RNA; GENOMIC DNA; SONIC HEDGEHOG PROTEIN; WNT PROTEIN; DROSOPHILA PROTEIN; RNA;

ARTICLE; CELL ASSAY; CELL SPECIFICITY; CONTROLLED STUDY; DNA SCREENING; DROSOPHILA; GENE LIBRARY; GENE TARGETING; GENE TECHNOLOGY; GENETIC IDENTIFICATION; GENETIC REGULATION; GENETIC TRANSCRIPTION; HIGH THROUGHPUT SCREENING; NONHUMAN; PROMOTER REGION; REPORTER GENE; REPRODUCIBILITY; RNA INTERFERENCE; RNA TRANSCRIPTION; ANIMAL; BIOLOGICAL MODEL; GENE; GENE EXPRESSION REGULATION; GENETIC PROCEDURES; GENETICS; GENOME; METABOLISM; SENSITIVITY AND SPECIFICITY;

ERINACEIDAE;

ANIMALS; DROSOPHILA; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION; GENE LIBRARY; GENES, INSECT; GENETIC TECHNIQUES; GENOME; MODELS, GENETIC; RNA; RNA INTERFERENCE; RNA, DOUBLE-STRANDED; SENSITIVITY AND SPECIFICITY; TRANSCRIPTION, GENETIC;

EID: 44049098353     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2007-8-9-r203     Document Type: Article

References (43)

1. Baeg GH Zhou R Perrimon N Genome-wide RNAi analysis of JAK/STAT signaling components in Drosophila. Genes Dev 2005, 19:1861-1870. 1186186 16055650 10.1101/gad.1320705
2. Boutros M Kiger AA Armknecht S Kerr K Hild M Koch B Haas SA Consortium HF Paro R Perrimon N Genome-wide RNAi analysis of growth and viability in Drosophila cells. Science 2004, 303:832-835. 10.1126/science.1091266 14764878
3. DasGupta R Kaykas A Moon RT Perrimon N Functional genomic analysis of the Wnt-wingless signaling pathway. Science 2005, 308:826-833. 10.1126/ science.1109374 15817814
4. Friedman A Perrimon N A functional RNAi screen for regulators of receptor tyrosine kinase and ERK signalling. Nature 2006, 444:230-234. 10.1038/nature05280 17086199
5. Kiger AA Baum B Jones S Jones MR Coulson A Echeverri C Perrimon N A functional genomic analysis of cell morphology using RNA interference. J Biol 2003, 2:27. 333409 14527345 10.1186/1475-4924-2-27
6. Nybakken K Vokes SA Lin TY McMahon AP Perrimon N A genome-wide RNA interference screen in Drosophila melanogaster cells for new components of the Hh signaling pathway. Nat Genet 2005, 37:1323-1332 10.1038/ng1682 16311596
7. Lum L Yao S Mozer B Rovescalli A Von Kessler D Nirenberg M Beachy PA Identification of Hedgehog pathway components by RNAi in Drosophila cultured cells. Science 2003, 299:2039-2045 10.1126/science.1081403 12663920
8. Feske S Gwack Y Prakriya M Srikanth S Puppel SH Tanasa B Hogan PG Lewis RS Daly M Rao A A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature 2006, 441:179-185 10.1038/ nature04702 16582901
9. Gwack Y Sharma S Nardone J Tanasa B Iuga A Srikanth S Okamura H Bolton D Feske S Hogan PG A genome-wide Drosophila RNAi screen identifies DYRK-family kinases as regulators of NFAT. Nature 2006, 441:646-650 10.1038/nature04631 16511445
10. Zamore PD Haley B Ribo-gnome: The big world of small RNAs. Science 2005, 309:1519-1524. 10.1126/science.1111444 16141061
11. Clemens JC Worby CA Simonson-Leff N Muda M Maehama T Hemmings BA Dixon JE Use of double-stranded RNA interference in Drosophila cell lines to dissect signal transduction pathways. Proc Natl Acad Sci USA 2000, 97:6499-6503. 18635 10823906 10.1073/pnas.110149597
12. Bridge AJ Pebernard S Ducraux A Nicoulaz AL Iggo R Induction of an interferon response by RNAi vectors in mammalian cells. Nat Genet 2003, 34:263-264 10.1038/ng1173 12796781
13. Scacheri PC Rozenblatt-Rosen O Caplen NJ Wolfsberg TG Umayam L Lee JC Hughes CM Shanmugam KS Bhattacharjee A Meyerson M Short interfering RNAs can induce unexpected and divergent changes in the levels of untargeted proteins in mammalian cells. Proc Natl Acad Sci USA 2004, 101:1892-1897. 357023 14769924 10.1073/pnas.0308698100
14. Sledz CA Holko M de Veer MJ Silverman RH Williams BR Activation of the interferon system by short-interfering RNAs. Nat Cell Biol 2003, 5:834-839 10.1038/ncb1038 12942087
15. Yang S Tutton S Pierce E Yoon K Specific double-stranded RNA interference in undifferentiated mouse embryonic stem cells. Mol Cell Biol 2001, 21:7807-7816 99950 11604515 10.1128/MCB.21.22.7807-7816.2001
16. Bartel DP MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 2004, 116:281-297. 10.1016/S0092-8674(04)00045-5 14744438
17. Zamore PD Tuschl T Sharp PA Bartel DP RNAi: Double-stranded RNA directs the ATP-dependent cleavage of mRNA at 21 to 23 nucleotide intervals. Cell 2000, 101:25-33. 10.1016/S0092-8674(00)80620-0 10778853
18. Echeverri CJ Beachy PA Baum B Boutros M Buchholz F Chanda SK Downward J Ellenberg J Fraser AG Hacohen N Minimizing the risk of reporting false positives in large-scale RNAi screens. Nat Methods 2006, 3:777-779. 10.1038/nmeth1006-777 16990807
19. Echeverri CJ Perrimon N High-throughput RNAi screening in cultured cells: A user's guide. Nat Rev Genet 2006 7 373 384 10.1038/nrg1836 16607398
20. Saxena S Jonsson ZO Dutta A Small RNAs with imperfect match to endogenous mRNA repress translation. Implications for off-target activity of small inhibitory RNA in mammalian cells. The Journal of biological chemistry 2003, 278:44312-44319 10.1074/jbc.M307089200 12952966
21. Off-Target Effects: Disturbing the Silence of RNA interference (RNAi) [http://www.gelifesciences.co.jp/technologies/sirna/pdf/ap_offtarget.pdf]
22. Birmingham A Anderson EM Reynolds A Ilsley-Tyree D Leake D Fedorov Y Baskerville S Maksimova E Robinson K Karpilow J 3′ UTR seed matches, but not overall identity, are associated with RNAi off-targets. Nat Methods 2006, 3:199-204. 10.1038/nmeth854 16489337
23. Boese Q Leake D Reynolds A Read S Scaringe SA Marshall WS Khvorova A Mechanistic insights aid computational short interfering RNA design. Methods in enzymology 2005, 392:73-96 15644176 10.1016/ S0076-6879(04)92005-8
24. Fedorov Y Anderson EM Birmingham A Reynolds A Karpilow J Robinson K Leake D Marshall WS Khvorova A Off-target effects by siRNA can induce toxic phenotype. RNA (New York, NY) 2006, 12:1188-1196.
25. Schwarz DS Hutvagner G Haley B Zamore PD Evidence that siRNAs function as guides, not primers, in the Drosophila and human RNAi pathways. Mol Cell 2002, 10:537-548. 10.1016/S1097-2765(02)00651-2 12408822
26. Kulkarni MM Booker M Silver SJ Friedman A Hong P Perrimon N Mathey-Prevot B Evidence of off-target effects associated with long dsRNAs in Drosophila melanogaster cell-based assays. Nat Methods 2006, 3:833-838. 16964256
27. Ma Y Creanga A Lum L Beachy PA Prevalence of off-target effects in Drosophila RNA interference screens. Nature 2006, 443:359-363 10.1038/ nature05179 16964239
28. Carmell MA Hannon GJ RNase III enzymes and the initiation of gene silencing. Nat Struct Mol Biol 2004, 11:214-218 10.1038/nsmb729 14983173
29. Zhang H Kolb FA Brondani V Billy E Filipowicz W Human Dicer preferentially cleaves dsRNAs at their termini without a requirement for ATP. Embo J 2002, 21:5875-5885 131079 12411505 10.1093/emboj/cdf582
30. Hild M Beckmann B Haas SA Koch B Solovyev V Busold C Fellenberg K Boutros M Vingron M Sauer F An integrated gene annotation and transcriptional profiling approach towards the full gene content of the Drosophila genome. Genome biology 2003, 5:R3. 395735 14709175 10.1186/ gb-2003-5-1-r3
31. Yandell M Bailey AM Misra S Shu S Wiel C Evans-Holm M Celniker SE Rubin GM A computational and experimental approach to validating annotations and gene predictions in the Drosophila melanogaster genome. Proc Natl Acad Sci USA 2005, 102:1566-1571. 545494 15668397 10.1073/pnas.0409421102
32. Tuschl T Zamore PD Lehmann R Bartel DP Sharp PA Targeted mRNA degradation by double-stranded RNA in vitro. Genes Dev 1999, 13:3191-3197. 317199 10617568 10.1101/gad.13.24.3191
33. Armknecht S Boutros M Kiger A Nybakken K Mathey-Prevot B Perrimon N High-throughput RNA interference screens in Drosophila tissue culture cells. Methods in enzymology 2005, 392:55-73 10.1016/ S0076-6879(04)92004-6 15644175
34. Tolwinski NS Wehrli M Rives A Erdeniz N DiNardo S Wieschaus E Wg/Wnt signal can be transmitted through arrow/LRP5,6 and Axin independently of Zw3/Gsk3beta activity. Developmental cell 2003, 4:407-418 10.1016/ S1534-5807(03)00063-7 12636921
35. Yanagawa S Lee JS Ishimoto A Identification and characterization of a novel line of Drosophila Schneider S2 cells that respond to wingless signaling. The Journal of biological chemistry 1998, 273:32353-32359. 10.1074/jbc.273.48.32353 9822716
36. Jho EH Zhang T Domon C Joo CK Freund JN Costantini F Wnt/beta-catenin/ Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol Cell Biol 2002, 22:1172-1183 134648 11809808 10.1128/MCB.22.4.1172-1183.2002
37. Lustig B Jerchow B Sachs M Weiler S Pietsch T Karsten U van de Wetering M Clevers H Schlag PM Birchmeier W Negative feedback loop of Wnt signaling through upregulation of conductin/axin2 in colorectal and liver tumors. Mol Cell Biol 2002, 22:1184-1193 134640 11809809 10.1128/ MCB.22.4.1184-1193.2002
38. Yang L Lin C Liu ZR P68 RNA Helicase Mediates PDGF-Induced Epithelial Mesenchymal Transition by Displacing Axin from beta-Catenin. Cell 2006, 127:139-155 10.1016/j.cell.2006.08.036 17018282
39. Gold DA Baek SH Schork NJ Rose DW Larsen DD Sachs BD Rosenfeld MG Hamilton BA RORalpha coordinates reciprocal signaling in cerebellar development through sonic hedgehog and calcium-dependent pathways. Neuron 2003, 40:1119-1131. 10.1016/S0896-6273(03)00769-4 14687547
40. Kim JH Kim B Cai L Choi HJ Ohgi KA Tran C Chen C Chung CH Huber O Rose DW Transcriptional regulation of a metastasis suppressor gene by Tip60 and beta-catenin complexes. Nature 2005, 434:921-926. 10.1038/ nature03452 15829968
41. Sierra J Yoshida T Joazeiro CA Jones KA The APC tumor suppressor counteracts beta-catenin activation and H3K4 methylation at Wnt target genes. Genes Dev 2006, 20:586-600 1410807 16510874 10.1101/gad.1385806
42. Kent D Bush EW Hooper JE Roadkill attenuates Hedgehog responses through degradation of Cubitus interruptus. Development (Cambridge, England) 2006, 133:2001-2010. 16651542
43. Zhang Q Zhang L Wang B Ou CY Chien CT Jiang J A hedgehog-induced BTB protein modulates hedgehog signaling by degrading Ci/Gli transcription factor. Developmental cell 2006, 10:719-729. 10.1016/ j.devcel.2006.05.004 16740475