ATARiS: Computational quantification of gene suppression phenotypes from multisample RNAi screens

Genome Research

Volumn 23, Issue 4, 2013, Pages 665-678

  Shao, Diane D ^a,b   Tsherniak, Aviad ^a   Gopal, Shuba ^a   Weir, Barbara A ^a   Tamayo, Pablo ^a   Stransky, Nicolas ^a,e   Schumacher, Steven E ^a,b   Zack, Travis I ^a,b,c   Beroukhim, Rameen ^a,b,d   Garraway, Levi A ^a,b,d   Margolin, Adam A ^a,f   Root, David E ^a   Hahn, William C ^a,b,d   Mesirov, Jill P ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b DANA FARBER CANCER INSTITUTE   (United States)

^c HARVARD UNIVERSITY   (United States)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

^e Blueprint Medicines   (United States)

^f SAGE BIONETWORKS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B RAF KINASE; HEPATOCYTE NUCLEAR FACTOR 1BETA; MESSENGER RNA; REAGENT; SHORT HAIRPIN RNA;

ANALYTIC TECHNIQUE FOR ASSESSMENT OF RNAI BY SIMILARITY; ARTICLE; CANCER CELL; CELL CYCLE G1 PHASE; CELL IMMORTALIZATION; CELL SURVIVAL; GENE; GENE AMPLIFICATION; GENE REPRESSION; GENETIC ANALYSIS; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; IN VIVO STUDY; MOLECULAR PHYLOGENY; MUTATION; PHENOTYPE; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RNA ANALYSIS; RNA INTERFERENCE;

ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; COMPUTATIONAL BIOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENOMICS; HEPATOCYTE NUCLEAR FACTOR 1-BETA; HUMANS; INTERNET; MICE; NEOPLASMS; PHENOTYPE; REPRODUCIBILITY OF RESULTS; RNA INTERFERENCE; RNA, SMALL INTERFERING; SOFTWARE;

EID: 84875978905     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.143586.112     Document Type: Article

References (58)

1. Amit I, Garber M, Chevrier N, Leite AP, Donner Y, Eisenhaure T, Guttman M, Grenier JK, Li W, Zuk O, et al. 2009. Unbiased reconstruction of a mammalian transcriptional network mediating pathogen responses. Science 326: 257-263.
2. Barbacci E, Reber M, Ott MO, Breillat C, Huetz F, Cereghini S. 1999. Variant hepatocyte nuclear factor 1 is required for visceral endoderm specification. Development 126: 4795-4805.
3. Barbie D, Tamayo P, Boehm J, Kim S, Moody S, Dunn I, Schinzel A, Sandy P, Meylan E, Scholl C, et al. 2009. Systematic RNA interference reveals that oncogenic KRAS-driven cancers require TBK1. Nature 462: 108-112.
4. Bard F, Casano L, Mallabiabarrena A, Wallace E, Saito K, Kitayama H, Guizzunti G, Hu Y, Wendler F, Dasgupta R, et al. 2006. Functional genomics reveals genes involved in protein secretion and Golgi organization. Nature 439: 604-607.
5. Barretina J, Caponigro G, Stransky N, Venkatesan K, Margolin AA, Kim S, Wilson CJ, Lehár J, Kryukov GV, Sonkin D, et al. 2012. The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature 483: 603-607.
6. Bellanne-Chantelot C, Clauin S, Chauveau D, Collin P, Daumont M, Douillard C, Dubois-Laforgue D, Dusselier L, Gautier JF, Jadoul M, et al. 2005. Large genomic rearrangements in the hepatocyte nuclear factor-1 (TCF2) gene are the most frequent cause of maturity-onset diabetes of the young type 5. Diabetes 54: 3126-3132.
7. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol 57: 289-300.
8. Beroukhim R, Getz G, Nghiemphu L, Barretina J, Hsueh T, Linhart D, Vivanco I, Lee JC, Huang JH, Alexander S, et al. 2007. Assessing the significance of chromosomal aberrations in cancer: Methodology and application to glioma. Proc Natl Acad Sci 104: 20007-20012.
9. Beroukhim R, Mermel CH, Porter D, Wei G, Raychaudhuri S, Donovan J, Barretina J, Boehm JS, Dobson J, Urashima M, et al. 2010. The landscape of somatic copy-number alteration across human cancers. Nature 463: 899-905.
10. Birmingham A, Anderson EM, Reynolds A, Ilsley-Tyree D, Leake D, Fedorov Y, Baskerville S, Maksimova E, Robinson K, Karpilow J, et al. 2006. 39 UTR seed matches, but not overall identity, are associated with RNAi off-targets. Nat Methods 3: 199-204.
11. Boehm J, Zhao J, Yao J, Kim S. 2007. Integrative genomic approaches identify IKBKE as a breast cancer oncogene. Cell 129: 1065-1079.
12. Brough R, Frankum JR, Sims D, Mackay A, Mendes-Pereira AM, Bajrami I, Costa-Cabral S, Rafiq R, Ahmad AS, Cerone MA, et al. 2011. Functional viability profiles of breast cancer. Cancer Discov 1: 260-273.
13. Bussey KJ, Chin K, Lababidi S, Reimers M, Reinhold WC, KuoW-L, Gwadry F, Ajay, Kouros-Mehr H, Fridlyand J, et al. 2006. Integrating data on DNA copy number with gene expression levels and drug sensitivities in the NCI-60 cell line panel. Mol Cancer Ther 5: 853-867.
14. Cheung HW, Cowley GS, Weir BA, Boehm JS, Rusin S, Scott JA, East A, Ali LD, Lizotte PH, Wong TC, et al. 2011. Systematic investigation of genetic vulnerabilities across cancer cell lines reveals lineagespecific dependencies in ovarian cancer. Proc Natl Acad Sci 108: 12372-12377.
15. Chung N, Zhang XD, Kreamer A, Locco L, Kuan P-F, Bartz S, Linsley PS, Ferrer M, Strulovici B. 2008. Median absolute deviation to improve hit selection for genome-scale RNAi screens. J Biomol Screen 13: 149-158.
16. Collinet C, Stöter M, Bradshaw CR, Samusik N, Rink JC, Kenski D, Habermann B, Buchholz F, Henschel R, Mueller MS, et al. 2010. Systems survey of endocytosis by multiparametric image analysis. Nature 464: 243-249.
17. Csiszar I, Tusnady G. 1984. Information geometry and alternating minimization procedures. Statist Decisions (Supplement) 1984: 205-237. http://www.mit.edu/;6.454/www-fall-2002/shaas/Csiszar.pdf. http://research. microsoft.com/apps/pubs/default.aspx?id=64832.
18. Cullen BR. 2006. Enhancing and confirming the specificity of RNAi experiments. Nat Methods 3: 677-681.
19. Dyson N. 1998. The regulation of E2F by pRB-family proteins. Genes Dev 12: 2245-2262.
20. Echeverri C, Beachy P, Baum B, Boutros M. 2006. Minimizing the risk of reporting false positives in large-scale RNAi screens. Nat Methods 3: 777-779.
21. Elbashir SM, Harborth J, Lendeckel W, Yalcin A, Weber K, Tuschl T. 2001. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411: 494-498.
22. Garraway L, Widlund H, Rubin M, Getz G. 2005. Integrative genomic analyses identify MITF as a lineage survival oncogene amplified in malignant melanoma. Nature 436: 117-122.
23. Hahn WC, Counter CM, Lundberg AS, Beijersbergen RL, Brooks MW, Weinberg RA. 1999. Creation of human tumour cells with defined genetic elements. Nature 400: 464-468.
24. Hirsch AJ. 2010. The use of RNAi-based screens to identify host proteins involved in viral replication. Future Microbiol 5: 303-311.
25. Horn T, Sandmann T, Fischer B, Axelsson E. 2011. Mapping of signaling networks through synthetic genetic interaction analysis by RNAi. Nat Methods 8: 341-346.
26. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP. 2003. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 31: e15.
27. Jackson AL, Bartz SR, Schelter J, Kobayashi SV, Burchard J, Mao M, Li B, Cavet G, Linsley PS. 2003. Expression profiling reveals off-target gene regulation by RNAi. Nat Biotechnol 21: 635-637.
28. Jackson AL, Burchard J, Schelter J, Chau BN, Cleary M, Lim L, Linsley PS. 2006. Widespread siRNA "off-target" transcript silencing mediated by seed region sequence complementarity. RNA 12: 1179-1187.
29. Kittler R, Pelletier L. 2008. Systems biology of mammalian cell division. Cell Cycle 7: 2123-2128.
30. Koh JL, Brown KR, Sayad A, Kasimer D, Ketela T, Moffat J. 2012. COLTCancer: Functional genetic screening resource for essential genes in human cancer cell lines. Nucleic Acids Res 40: D957-D963.
31. König R, Chiang C-Y, Tu BP, Yan SF, Dejesus PD, Romero A, Bergauer T, Orth A, Krueger U, Zhou Y, et al. 2007. A probability-based approach for the analysis of large-scale RNAi screens. Nat Methods 4: 847-849.
32. Leone G, Sears R, Huang E, Rempel R, Nuckolls F, Park CH, Giangrande P,Wu L, Saavedra HI, Field SJ, et al. 2001. Myc requires distinct E2F activities to induce S phase and apoptosis. Mol Cell 8: 105-113.
33. Li C, Hung Wong W. 2001. Model-based analysis of oligonucleotide arrays: Model validation, design issues and standard error application. Genome Biol 2: RESEARCH0032.
34. Li CG, Nyman JE, Braithwaite AW, Eccles MR. 2011. PAX8 promotes tumor cell growth by transcriptionally regulating E2F1 and stabilizing RB protein. Oncogene 30: 4824-4834.
35. Liu JJ, Chao JR, Jiang MC, Ng SY, Yen JJ, Yang-Yen HF. 1995. Ras transformation results in an elevated level of cyclin D1 and acceleration of G1 progression in NIH 3T3 cells. Mol Cell Biol 15: 3654-3663.
36. Luo B, Cheung HW, Subramanian A, Sharifnia T, Okamoto M, Yang X, Hinkle G, Boehm JS, Beroukhim R, Weir BA, et al. 2008. Highly parallel identification of essential genes in cancer cells. Proc Natl Acad Sci 105: 20380-20385.
37. Marcotte R, Brown KR, Suarez F, Sayad A, Karamboulas K, Krzyzanowski PM, Sircoulomb F, Medrano M, Fedyshyn Y, Koh JLY. 2012. Essential gene profiles in breast, pancreatic, and ovarian cancer cells. Cancer Discov 2: 172-189.
38. Marine S, Bahl A, Ferrer M, Buehler E. 2012. Common seed analysis to identify off-target effects in siRNA screens. J Biomol Screen 17: 370-378.
39. Mason SJ, Graham NE. 2002. Areas beneath the relative operating characteristics (ROC) and relative operating levels (ROL) curves: Statistical significance and interpretation. Q J R Meteorol Soc 128: 2145-2166.
40. Müller P, Kuttenkeuler D, Gesellchen V, Zeidler MP, Boutros M. 2005. Identification of JAK/STATsignalling components by genome-wide RNA interference. Nature 436: 871-875.
41. Musgrove EA, Caldon CE, Barraclough J, Stone A, Sutherland RL. 2011. Cyclin D as a therapeutic target in cancer. Nat Rev Cancer 11: 558-572.
42. OeggerliM, Schraml P, Ruiz C, Bloch M, Novotny H, Mirlacher M, Sauter G, Simon R. 2006. E2F3 is the main target gene of the 6p22 amplicon with high specificity for human bladder cancer. Oncogene 25: 6538-6543.
43. Ramsay RG, Gonda TJ. 2008. MYB function in normal and cancer cells. Nat Rev Cancer 8: 523-534.
44. Reich M, Liefeld T, Gould J, Lerner J, Tamayo P, Mesirov JP. 2006. GenePattern 2.0. Nat Genet 38: 500-501.
45. Root DE, Hacohen N, Hahn WC, Lander ES, Sabatini DM. 2006. Genomescale loss-of-function screening with a lentiviral RNAi library. Nat Methods 3: 715-719.
46. Ryffel GU. 2001. Mutations in the human genes encoding the transcription factors of the hepatocyte nuclear factor (HNF)1 and HNF4 families: Functional and pathological consequences. J Mol Endocrinol 27: 11-29.
47. Schumacher FR, Berndt SI, Siddiq A, Jacobs KB, Wang Z, Lindstrom S, Stevens VL, Chen C, Mondul AM, Travis RC, et al. 2011. Genome-wide association study identifies new prostate cancer susceptibility loci. Hum Mol Genet 20: 3867-3875.
48. Sigoillot FD, Lyman S, Huckins JF, Adamson B. 2012. A bioinformatics method identifies prominent off-targeted transcripts in RNAi screens. Nat Methods 9: 363-366.
49. Spurdle AB, Thompson DJ, Ahmed S, Ferguson K, Healey CS, O'Mara T, Walker LC, Montgomery SB, Dermitzakis ET, Fahey P, et al. 2011. Genome-wide association study identifies a common variant associated with risk of endometrial cancer. Nat Genet 43: 451-454.
50. Stouffer SA, Suchman EA, DeVinney LC, Star SA, Williams RMJ. 1949. The American soldier, Vol. 1: Adjustment during army life, 1st ed. Princeton University Press, Princeton.
51. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, et al. 2005. Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. 102: 15545-15550.
52. Terasawa K, Toyota M, Sagae S, Ogi K, Suzuki H, Sonoda T, Akino K, Maruyama R, Nishikawa N, Imai K, et al. 2006. Epigenetic inactivation of TCF2 in ovarian cancer and various cancer cell lines. Br J Cancer 94: 914-921.
53. Tsuchiya A, Sakamoto M, Yasuda J, Chuma M, Ohta T, Ohki M, Yasugi T, Taketani Y, Hirohashi S. 2003. Expression profiling in ovarian clear cell carcinoma: Identification of hepatocyte nuclear factor-1b as a molecular marker and a possible molecular target for therapy of ovarian clear cell carcinoma. Am J Pathol 163: 2503-2512.
54. Verdeguer F, Le Corre S, Fischer E, Callens C, Garbay S, Doyen A, Igarashi P, Terzi F, Pontoglio M. 2009. Amitotic transcriptional switch in polycystic kidney disease. Nat Med 16: 106-110.
55. Whitlock MC. 2005. Combining probability from independent tests: The weighted Z-method is superior to Fisher's approach. J Evol Biol 18: 1368-1373.
56. Zender L, Spector MS, XueW, Flemming P, Cordon-Cardo C, Silke J, Fan S-T, Luk JM,Wigler M, Hannon GJ, et al. 2006. Identification and validation of oncogenes in liver cancer using an integrative oncogenomic approach. Cell 125: 1253-1267.
57. Zhang XD, Ferrer M, Espeseth AS, Marine SD, Stec EM, Crackower MA, Holder DJ, Heyse JF, Strulovici B. 2007. The use of strictly standardized mean difference for hit selection in primary RNA interference highthroughput screening experiments. J Biomol Screen 12: 497-509.
58. Zhang XD, Santini F, Lacson R, Marine SD, Wu Q, Benetti L, Yang R, McCampbell A, Berger JP, Toolan DM, et al. 2011. cSSMD: Assessing collective activity for addressing off-target effects in genome-scale RNA interference screens. Bioinformatics 27: 2775-2781.