Defining a Cancer Dependency Map

Cell

Volumn 170, Issue 3, 2017, Pages 564-576.e16

  Tsherniak, Aviad ^a   Vazquez, Francisca ^a,b   Montgomery, Phil G ^a   Weir, Barbara A ^a,b   Kryukov, Gregory ^a,b   Cowley, Glenn S ^a   Gill, Stanley ^a,b   Harrington, William F ^a   Pantel, Sasha ^a   Krill Burger, John M ^a   Meyers, Robin M ^a   Ali, Levi ^a   Goodale, Amy ^a   Lee, Yenarae ^a   Jiang, Guozhi ^a   Hsiao, Jessica ^a   Gerath, William F J ^a   Howell, Sara ^a   Merkel, Erin ^a   Ghandi, Mahmoud ^a   Garraway, Levi A ^a,b,c,d,e   Root, David E ^a   Golub, Todd R ^a,b,d,e   Boehm, Jesse S ^a   Hahn, William C ^a,b,c,d   more..

^a BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^b DANA FARBER CANCER INSTITUTE   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

cancer dependencies; cancer targets; genetic vulnerabilities; genomic biomarkers; precision medicine; predictive modeling; RNAi screens; seed effects; shRNA

Indexed keywords

UBIQUITIN;

ARTICLE; CANCER CELL LINE; CANCER MORTALITY; CELL PROLIFERATION; CELL SUBPOPULATION; CELL VIABILITY; CONTROLLED STUDY; FEMALE; GENE DOSAGE; GENE FUNCTION; GENE LIBRARY; GENE MUTATION; GENE SILENCING; GENOME ANALYSIS; HUMAN; HUMAN CELL; MALE; MALIGNANT NEOPLASM; PRIORITY JOURNAL; RNA INTERFERENCE; GENETICS; NEOPLASM; PATHOLOGY; SOFTWARE; TUMOR CELL LINE;

CELL LINE, TUMOR; HUMANS; NEOPLASMS; RNA INTERFERENCE; SOFTWARE; UBIQUITIN;

EID: 85026422523     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2017.06.010     Document Type: Article

References (57)

1. Aguirre, A.J., Meyers, R.M., Weir, B.A., Vazquez, F., Zhang, C.Z., Ben-David, U., Cook, A., Ha, G., Harrington, W.F., Doshi, M.B., et al. Genomic copy number dictates a gene-independent cell response to CRISPR/Cas9 targeting. Cancer Discov. 6 (2016), 914–929.
2. Aksoy, B.A., Demir, E., Babur, Ö., Wang, W., Jing, X., Schultz, N., Sander, C., Prediction of individualized therapeutic vulnerabilities in cancer from genomic profiles. Bioinformatics 30 (2014), 2051–2059.
3. Ashton, J.M., Balys, M., Neering, S.J., Hassane, D.C., Cowley, G., Root, D.E., Miller, P.G., Ebert, B.L., McMurray, H.R., Land, H., Jordan, C.T., Gene sets identified with oncogene cooperativity analysis regulate in vivo growth and survival of leukemia stem cells. Cell Stem Cell 11 (2012), 359–372.
4. Barbie, D.A., Tamayo, P., Boehm, J.S., Kim, S.Y., Moody, S.E., Dunn, I.F., Schinzel, A.C., Sandy, P., Meylan, E., Scholl, C., et al. Systematic RNA interference reveals that oncogenic KRAS-driven cancers require TBK1. Nature 462 (2009), 108–112.
5. Barretina, J., Caponigro, G., Stransky, N., Venkatesan, K., Margolin, A.A., Kim, S., Wilson, C.J., Lehár, J., Kryukov, G.V., Sonkin, D., et al. The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature 483 (2012), 603–607.
6. Birmingham, A., Anderson, E.M., Reynolds, A., Ilsley-Tyree, D., Leake, D., Fedorov, Y., Baskerville, S., Maksimova, E., Robinson, K., Karpilow, J., et al. 3′ UTR seed matches, but not overall identity, are associated with RNAi off-targets. Nat. Methods 3 (2006), 199–204.
7. Brenner, J.C., Ateeq, B., Li, Y., Yocum, A.K., Cao, Q., Asangani, I.A., Patel, S., Wang, X., Liang, H., Yu, J., et al. Mechanistic rationale for inhibition of poly(ADP-ribose) polymerase in ETS gene fusion-positive prostate cancer. Cancer Cell 19 (2011), 664–678.
8. Buchwalter, G., Hickey, M.M., Cromer, A., Selfors, L.M., Gunawardane, R.N., Frishman, J., Jeselsohn, R., Lim, E., Chi, D., Fu, X., et al. PDEF promotes luminal differentiation and acts as a survival factor for ER-positive breast cancer cells. Cancer Cell 23 (2013), 753–767.
9. Buehler, E., Chen, Y.C., Martin, S., C911: A bench-level control for sequence specific siRNA off-target effects. PLoS ONE, 7, 2012, e51942.
10. Buehler, E., Khan, A.A., Marine, S., Rajaram, M., Bahl, A., Burchard, J., Ferrer, M., siRNA off-target effects in genome-wide screens identify signaling pathway members. Sci. Rep., 2, 2012, 428.
11. Cheung, H.W., Cowley, G.S., Weir, B.A., Boehm, J.S., Rusin, S., Scott, J.A., East, A., Ali, L.D., Lizotte, P.H., Wong, T.C., et al. Systematic investigation of genetic vulnerabilities across cancer cell lines reveals lineage-specific dependencies in ovarian cancer. Proc. Natl. Acad. Sci. USA 108 (2011), 12372–12377.
12. Cibulskis, K., Lawrence, M.S., Carter, S.L., Sivachenko, A., Jaffe, D., Sougnez, C., Gabriel, S., Meyerson, M., Lander, E.S., Getz, G., Sensitive detection of somatic point mutations in impure and heterogeneous cancer samples. Nat. Biotechnol. 31 (2013), 213–219.
13. Cowley, G.S., Weir, B.A., Vazquez, F., Tamayo, P., Scott, J.A., Rusin, S., East-Seletsky, A., Ali, L.D., Gerath, W.F., Pantel, S.E., et al. Parallel genome-scale loss of function screens in 216 cancer cell lines for the identification of context-specific genetic dependencies. Sci. Data, 1, 2014, 140035.
14. D'Antonio, M., Guerra, R.F., Cereda, M., Marchesi, S., Montani, F., Nicassio, F., Di Fiore, P.P., Ciccarelli, F.D., Recessive cancer genes engage in negative genetic interactions with their functional paralogs. Cell Rep. 5 (2013), 1519–1526.
15. DeLuca, D.S., Levin, J.Z., Sivachenko, A., Fennell, T., Nazaire, M.D., Williams, C., Reich, M., Winckler, W., Getz, G., RNA-SeQC: RNA-seq metrics for quality control and process optimization. Bioinformatics 28 (2012), 1530–1532.
16. Dobin, A., Davis, C.A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Batut, P., Chaisson, M., Gingeras, T.R., STAR: Ultrafast universal RNA-seq aligner. Bioinformatics 29 (2013), 15–21.
17. Helming, K.C., Wang, X., Wilson, B.G., Vazquez, F., Haswell, J.R., Manchester, H.E., Kim, Y., Kryukov, G.V., Ghandi, M., Aguirre, A.J., et al. ARID1B is a specific vulnerability in ARID1A-mutant cancers. Nat. Med. 20 (2014), 251–254.
18. Hothorn, T., Hornik, K., Zeileis, A., Unbiased recursive partitioning: A conditional inference framework. J. Comput. Graph. Stat. 15 (2006), 651–674.
19. Jackson, A.L., Linsley, P.S., Noise amidst the silence: Off-target effects of siRNAs?. Trends Genet. 20 (2004), 521–524.
20. Jackson, A.L., Burchard, J., Schelter, J., Chau, B.N., Cleary, M., Lim, L., Linsley, P.S., Widespread siRNA “off-target” transcript silencing mediated by seed region sequence complementarity. RNA 12 (2006), 1179–1187.
21. Kampmann, M., Bassik, M.C., Weissman, J.S., Integrated platform for genome-wide screening and construction of high-density genetic interaction maps in mammalian cells. Proc. Natl. Acad. Sci. USA 110 (2013), E2317–E2326.
22. Kampmann, M., Horlbeck, M.A., Chen, Y., Tsai, J.C., Bassik, M.C., Gilbert, L.A., Villalta, J.E., Kwon, S.C., Chang, H., Kim, V.N., Weissman, J.S., Next-generation libraries for robust RNA interference-based genome-wide screens. Proc. Natl. Acad. Sci. USA 112 (2015), E3384–E3391.
23. König, R., Chiang, C.Y., Tu, B.P., Yan, S.F., DeJesus, P.D., Romero, A., Bergauer, T., Orth, A., Krueger, U., Zhou, Y., Chanda, S.K., A probability-based approach for the analysis of large-scale RNAi screens. Nat. Methods 4 (2007), 847–849.
24. Krönke, J., Hurst, S.N., Ebert, B.L., Lenalidomide induces degradation of IKZF1 and IKZF3. OncoImmunology, 3, 2014, e941742.
25. Lage, K., Karlberg, E.O., Størling, Z.M., Olason, P.I., Pedersen, A.G., Rigina, O., Hinsby, A.M., Tümer, Z., Pociot, F., Tommerup, N., et al. A human phenome-interactome network of protein complexes implicated in genetic disorders. Nat. Biotechnol. 25 (2007), 309–316.
26. Lage, K., Hansen, N.T., Karlberg, E.O., Eklund, A.C., Roque, F.S., Donahoe, P.K., Szallasi, Z., Jensen, T.S., Brunak, S., A large-scale analysis of tissue-specific pathology and gene expression of human disease genes and complexes. Proc. Natl. Acad. Sci. USA 105 (2008), 20870–20875.
27. Laury, A.R., Perets, R., Piao, H., Krane, J.F., Barletta, J.A., French, C., Chirieac, L.R., Lis, R., Loda, M., Hornick, J.L., et al. A comprehensive analysis of PAX8 expression in human epithelial tumors. Am. J. Surg. Pathol. 35 (2011), 816–826.
28. Liu, Y., Zhang, X., Han, C., Wan, G., Huang, X., Ivan, C., Jiang, D., Rodriguez-Aguayo, C., Lopez-Berestein, G., Rao, P.H., et al. TP53 loss creates therapeutic vulnerability in colorectal cancer. Nature 520 (2015), 697–701.
29. Lu, G., Middleton, R.E., Sun, H., Naniong, M., Ott, C.J., Mitsiades, C.S., Wong, K.K., Bradner, J.E., Kaelin, W.G. Jr., The myeloma drug lenalidomide promotes the cereblon-dependent destruction of Ikaros proteins. Science 343 (2014), 305–309.
30. Luo, B., Cheung, H.W., Subramanian, A., Sharifnia, T., Okamoto, M., Yang, X., Hinkle, G., Boehm, J.S., Beroukhim, R., Weir, B.A., et al. Highly parallel identification of essential genes in cancer cells. Proc. Natl. Acad. Sci. USA 105 (2008), 20380–20385.
31. Marcotte, R., Brown, K.R., Suarez, F., Sayad, A., Karamboulas, K., Krzyzanowski, P.M., Sircoulomb, F., Medrano, M., Fedyshyn, Y., Koh, J.L., et al. Essential gene profiles in breast, pancreatic, and ovarian cancer cells. Cancer Discov. 2 (2012), 172–189.
32. Marcotte, R., Sayad, A., Brown, K.R., Sanchez-Garcia, F., Reimand, J., Haider, M., Virtanen, C., Bradner, J.E., Bader, G.D., Mills, G.B., et al. Functional genomic landscape of human breast cancer drivers, vulnerabilities, and resistance. Cell 164 (2016), 293–309.
33. Mi, H., Poudel, S., Muruganujan, A., Casagrande, J.T., Thomas, P.D., PANTHER version 10: Expanded protein families and functions, and analysis tools. Nucleic Acids Res. 44:D1 (2016), D336–D342.
34. Morin, R.D., Mungall, K., Pleasance, E., Mungall, A.J., Goya, R., Huff, R.D., Scott, D.W., Ding, J., Roth, A., Chiu, R., et al. Mutational and structural analysis of diffuse large B-cell lymphoma using whole-genome sequencing. Blood 122 (2013), 1256–1265.
35. Muller, F.L., Colla, S., Aquilanti, E., Manzo, V.E., Genovese, G., Lee, J., Eisenson, D., Narurkar, R., Deng, P., Nezi, L., et al. Passenger deletions generate therapeutic vulnerabilities in cancer. Nature 488 (2012), 337–342.
36. Munoz, D.M., Cassiani, P.J., Li, L., Billy, E., Korn, J.M., Jones, M.D., Golji, J., Ruddy, D.A., Yu, K., McAllister, G., et al. CRISPR screens provide a comprehensive assessment of cancer vulnerabilities but generate false-positive hits for highly amplified genomic regions. Cancer Discov. 6 (2016), 900–913.
37. Nijhawan, D., Zack, T.I., Ren, Y., Strickland, M.R., Lamothe, R., Schumacher, S.E., Tsherniak, A., Besche, H.C., Rosenbluh, J., Shehata, S., et al. Cancer vulnerabilities unveiled by genomic loss. Cell 150 (2012), 842–854.
38. Pomerantz, M.M., Li, F., Takeda, D.Y., Lenci, R., Chonkar, A., Chabot, M., Cejas, P., Vazquez, F., Cook, J., Shivdasani, R.A., et al. The androgen receptor cistrome is extensively reprogrammed in human prostate tumorigenesis. Nat. Genet. 47 (2015), 1346–1351.
39. Ramos, A.H., Lichtenstein, L., Gupta, M., Lawrence, M.S., Pugh, T.J., Saksena, G., Meyerson, M., Getz, G., Oncotator: Cancer variant annotation tool. Hum. Mutat. 36 (2015), E2423–E2429.
40. Rosenbluh, J., Mercer, J., Shrestha, Y., Oliver, R., Tamayo, P., Doench, J.G., Tirosh, I., Piccioni, F., Hartenian, E., Horn, H., et al. Genetic and proteomic interrogation of lower confidence candidate genes reveals signaling networks in beta-catenin-active cancers. Cell Syst. 3 (2016), 302–316.
41. Ruepp, A., Waegele, B., Lechner, M., Brauner, B., Dunger-Kaltenbach, I., Fobo, G., Frishman, G., Montrone, C., Mewes, H.W., CORUM: The comprehensive resource of mammalian protein complexes–2009. Nucleic Acids Res. 38 (2010), D497–D501.
42. Saunders, C.T., Wong, W.S., Swamy, S., Becq, J., Murray, L.J., Cheetham, R.K., Strelka: Accurate somatic small-variant calling from sequenced tumor-normal sample pairs. Bioinformatics 28 (2012), 1811–1817.
43. Schmich, F., Szczurek, E., Kreibich, S., Dilling, S., Andritschke, D., Casanova, A., Low, S.H., Eicher, S., Muntwiler, S., Emmenlauer, M., et al. gespeR: A statistical model for deconvoluting off-target-confounded RNA interference screens. Genome Biol., 16, 2015, 220.
44. Seashore-Ludlow, B., Rees, M.G., Cheah, J.H., Cokol, M., Price, E.V., Coletti, M.E., Jones, V., Bodycombe, N.E., Soule, C.K., Gould, J., et al. Harnessing Connectivity in a Large-Scale Small-Molecule Sensitivity Dataset. Cancer Discov. 5 (2015), 1210–1223.
45. Shao, D.D., Tsherniak, A., Gopal, S., Weir, B.A., Tamayo, P., Stransky, N., Schumacher, S.E., Zack, T.I., Beroukhim, R., Garraway, L.A., et al. ATARiS: Computational quantification of gene suppression phenotypes from multisample RNAi screens. Genome Res. 23 (2013), 665–678.
46. Southan, C., Sharman, J.L., Benson, H.E., Faccenda, E., Pawson, A.J., Alexander, S.P., Buneman, O.P., Davenport, A.P., McGrath, J.C., Peters, J.A., et al., NC-IUPHAR. The IUPHAR/BPS Guide to PHARMACOLOGY in 2016: Towards curated quantitative interactions between 1300 protein targets and 6000 ligands. Nucleic Acids Res. 44:D1 (2016), D1054–D1068.
47. Stelzer, G., Rosen, N., Plaschkes, I., Zimmerman, S., Twik, M., Fishilevich, S., Stein, T.I., Nudel, R., Lieder, I., Mazor, Y., et al. The GeneCards Suite: From gene data mining to disease genome sequence analyses. Curr. Protoc Bioinformatics 54 (2016), 1.30.1–1.30.33.
48. Stewart, S.A., Dykxhoorn, D.M., Palliser, D., Mizuno, H., Yu, E.Y., An, D.S., Sabatini, D.M., Chen, I.S., Hahn, W.C., Sharp, P.A., et al. Lentivirus-delivered stable gene silencing by RNAi in primary cells. RNA 9 (2003), 493–501.
49. Strobl, C., Boulesteix, A.L., Kneib, T., Augustin, T., Zeileis, A., Conditional variable importance for random forests. BMC Bioinformatics, 9, 2008, 307.
50. Vaquerizas, J.M., Kummerfeld, S.K., Teichmann, S.A., Luscombe, N.M., A census of human transcription factors: Function, expression and evolution. Nat. Rev. Genet. 10 (2009), 252–263.
51. Wagner, A.H., Coffman, A.C., Ainscough, B.J., Spies, N.C., Skidmore, Z.L., Campbell, K.M., Krysiak, K., Pan, D., McMichael, J.F., Eldred, J.M., et al. DGIdb 2.0: Mining clinically relevant drug-gene interactions. Nucleic Acids Res. 44:D1 (2016), D1036–D1044.
52. Wang, K., Li, M., Hakonarson, H., ANNOVAR: Functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res., 38, 2010, e164.
53. Wang, T., Birsoy, K., Hughes, N.W., Krupczak, K.M., Post, Y., Wei, J.J., Lander, E.S., Sabatini, D.M., Identification and characterization of essential genes in the human genome. Science 350 (2015), 1096–1101.
54. Weir, B.A., Woo, M.S., Getz, G., Perner, S., Ding, L., Beroukhim, R., Lin, W.M., Province, M.A., Kraja, A., Johnson, L.A., et al. Characterizing the cancer genome in lung adenocarcinoma. Nature 450 (2007), 893–898.
55. Wilson, B.G., Helming, K.C., Wang, X., Kim, Y., Vazquez, F., Jagani, Z., Hahn, W.C., Roberts, C.W., Residual complexes containing SMARCA2 (BRM) underlie the oncogenic drive of SMARCA4 (BRG1) mutation. Mol. Cell. Biol. 34 (2014), 1136–1144.
56. Yilmazel, B., Hu, Y., Sigoillot, F., Smith, J.A., Shamu, C.E., Perrimon, N., Mohr, S.E., Online GESS: Prediction of miRNA-like off-target effects in large-scale RNAi screen data by seed region analysis. BMC Bioinformatics, 15, 2014, 192.
57. Zhang, X.D., Santini, F., Lacson, R., Marine, S.D., Wu, Q., Benetti, L., Yang, R., McCampbell, A., Berger, J.P., Toolan, D.M., et al. cSSMD: Assessing collective activity for addressing off-target effects in genome-scale RNA interference screens. Bioinformatics 27 (2011), 2775–2781.