A Next Generation Connectivity Map: L1000 Platform and the First 1,000,000 Profiles

Cell

Volumn 171, Issue 6, 2017, Pages 1437-1452.e17

  Subramanian, Aravind ^a   Narayan, Rajiv ^a   Corsello, Steven M ^a,b,c   Peck, David D ^a   Natoli, Ted E ^a   Lu, Xiaodong ^a   Gould, Joshua ^a   Davis, John F ^a   Tubelli, Andrew A ^a   Asiedu, Jacob K ^a   Lahr, David L ^a   Hirschman, Jodi E ^a   Liu, Zihan ^a   Donahue, Melanie ^a   Julian, Bina ^a   Khan, Mariya ^a   Wadden, David ^a   Smith, Ian C ^a   Lam, Daniel ^a   Liberzon, Arthur ^a   Toder, Courtney ^a   Bagul, Mukta ^a   Orzechowski, Marek ^a   Enache, Oana M ^a   Piccioni, Federica ^a   Johnson, Sarah A ^a   Lyons, Nicholas J ^a   Berger, Alice H ^a,b,c,g   Shamji, Alykhan F ^a   Brooks, Angela N ^a,b,c,h   Vrcic, Anita ^a   Flynn, Corey ^a   Rosains, Jacqueline ^a,i   Takeda, David Y ^a,b,c   Hu, Roger ^a   Davison, Desiree ^a   Lamb, Justin ^a,j   Ardlie, Kristin ^a   Hogstrom, Larson ^a   Greenside, Peyton ^a,l   Gray, Nathanael S ^a,b,c   Clemons, Paul A ^a   Silver, Serena ^a   Wu, Xiaoyun ^a   Zhao, Wen Ning ^a,c,d   Read Button, Willis ^a   Wu, Xiaohua ^a   Haggarty, Stephen J ^a,c,d   Ronco, Lucienne V ^a,k   Boehm, Jesse S ^a   Schreiber, Stuart L ^a,e,f   Doench, John G ^a   Bittker, Joshua A ^a   Root, David E ^a   Wong, Bang ^a   Golub, Todd R ^a,b,c,f   more..

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

^b DANA FARBER CANCER INSTITUTE   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

^e HARVARD UNIVERSITY   (United States)

^f HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^g UNIVERSITY OF WASHINGTON   (United States)

^h UNIVERSITY OF CALIFORNIA   (United States)

ⁱ Seven Bridges Genomics   (United States)

^j Genometry Inc   (United States)

^k Fulcrum Therapeutics   (United States)

^l STANFORD UNIVERSITY   (United States)

more..

Author keywords

chemical biology; Functional genomics; gene expression profiling

Indexed keywords

CASEIN KINASE IALPHA; SHORT HAIRPIN RNA; DRUG;

ARTICLE; CELL CULTURE; CONTROLLED STUDY; COST BENEFIT ANALYSIS; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE TARGETING; GENETIC ANALYSIS; GENETIC REGULATION; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; GENOME-WIDE ASSOCIATION STUDY; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; HUMAN TISSUE; INTERMETHOD COMPARISON; LIBRARY SCIENCE; MALE; MOLECULAR GENETICS; MOLECULAR LIBRARY; PRIORITY JOURNAL; REPRODUCIBILITY; RNA SEQUENCE; TRANSCRIPTOMICS; ANTIBODY SPECIFICITY; DRUG RESISTANCE; ECONOMICS; METABOLISM; NEOPLASM; PROCEDURES; SEQUENCE ANALYSIS; TUMOR CELL LINE;

CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION PROFILING; HUMANS; NEOPLASMS; ORGAN SPECIFICITY; PHARMACEUTICAL PREPARATIONS; SEQUENCE ANALYSIS, RNA; SMALL MOLECULE LIBRARIES;

EID: 85036572148     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2017.10.049     Document Type: Article

References (55)

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. Berger, A.H., Brooks, A.N., Wu, X., Shrestha, Y., Chouinard, C., Piccioni, F., Bagul, M., Kamburov, A., Imielinski, M., Hogstrom, L., et al. High-throughput Phenotyping of Lung Cancer Somatic Mutations. Cancer Cell 30 (2016), 214–228.
3. Brum, A.M., van de Peppel, J., van der Leije, C.S., Schreuders-Koedam, M., Eijken, M., van der Eerden, B.C.J., van Leeuwen, J.P.T.M., Connectivity Map-based discovery of parbendazole reveals targetable human osteogenic pathway. Proc. Natl. Acad. Sci. USA 112 (2015), 12711–12716.
4. Carlino, M.S., Gowrishankar, K., Saunders, C.A.B., Pupo, G.M., Snoyman, S., Zhang, X.D., Saw, R., Becker, T.M., Kefford, R.F., Long, G.V., Rizos, H., Antiproliferative effects of continued mitogen-activated protein kinase pathway inhibition following acquired resistance to BRAF and/or MEK inhibition in melanoma. Mol. Cancer Ther. 12 (2013), 1332–1342.
5. Churchman, M.L., Low, J., Qu, C., Paietta, E.M., Kasper, L.H., Chang, Y., Payne-Turner, D., Althoff, M.J., Song, G., Chen, S.-C., et al. Efficacy of Retinoids in IKZF1-Mutated BCR-ABL1 Acute Lymphoblastic Leukemia. Cancer Cell 28 (2015), 343–356.
6. Corsello, S.M., Bittker, J.A., Liu, Z., Gould, J., McCarren, P., Hirschman, J.E., Johnston, S.E., Vrcic, A., Wong, B., Khan, M., et al. The Drug Repurposing Hub: a next-generation drug library and information resource. Nat. Med. 23 (2017), 405–408.
7. Davis, M.I., Hunt, J.P., Herrgard, S., Ciceri, P., Wodicka, L.M., Pallares, G., Hocker, M., Treiber, D.K., Zarrinkar, P.P., Comprehensive analysis of kinase inhibitor selectivity. Nat. Biotechnol. 29 (2011), 1046–1051.
8. Dinwiddie, M.T., Terry, P.D., Chen, J., Recent evidence regarding triclosan and cancer risk. Int. J. Environ. Res. Public Health 11 (2014), 2209–2217.
9. Dixit, A., Parnas, O., Li, B., Chen, J., Fulco, C.P., Jerby-Arnon, L., Marjanovic, N.D., Dionne, D., Burks, T., Raychowdhury, R., et al. Perturb-Seq: Dissecting Molecular Circuits with Scalable Single-Cell RNA Profiling of Pooled Genetic Screens. Cell 167 (2016), 1853–1866.
10. Donner, Y., Feng, T., Benoist, C., Koller, D., Imputing gene expression from selectively reduced probe sets. Nat. Methods 9 (2012), 1120–1125.
11. Dudley, J.T., Sirota, M., Shenoy, M., Pai, R.K., Roedder, S., Chiang, A.P., Morgan, A.A., Sarwal, M.M., Pasricha, P.J., Butte, A.J., Computational Repositioning of the anticonvulsant topiramate for inflammatory bowel disease. Sci. Transl. Med., 3, 2011 96ra76.
12. Dyle, M.C., Ebert, S.M., Cook, D.P., Kunkel, S.D., Fox, D.K., Bongers, K.S., Bullard, S.A., Dierdorff, J.M., Adams, C.M., Systems-based discovery of tomatidine as a natural small molecule inhibitor of skeletal muscle atrophy. J. Biol. Chem. 289 (2014), 14913–14924.
13. Edgar, R., Domrachev, M., Lash, A.E., Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30 (2002), 207–210.
14. Farooq, F., Balabanian, S., Liu, X., Holcik, M., MacKenzie, A., p38 Mitogen-activated protein kinase stabilizes SMN mRNA through RNA binding protein HuR. Hum. Mol. Genet. 18 (2009), 4035–4045.
15. Fortney, K., Griesman, J., Kotlyar, M., Pastrello, C., Angeli, M., Sound-Tsao, M., Jurisica, I., Prioritizing therapeutics for lung cancer: an integrative meta-analysis of cancer gene signatures and chemogenomic data. PLoS Comput. Biol., 11, 2015, e1004068.
16. GTEx Consortium. Human genomics. The Genotype-Tissue Expression (GTEx) pilot analysis: multitissue gene regulation in humans. Science 348 (2015), 648–660.
17. Hao, B., Oehlmann, S., Sowa, M.E., Harper, J.W., Pavletich, N.P., Structure of a Fbw7-Skp1-cyclin E complex: multisite-phosphorylated substrate recognition by SCF ubiquitin ligases. Mol. Cell 26 (2007), 131–143.
18. Hast, B.E., Cloer, E.W., Goldfarb, D., Li, H., Siesser, P.F., Yan, F., Walter, V., Zheng, N., Hayes, D.N., Major, M.B., Cancer-derived mutations in KEAP1 impair NRF2 degradation but not ubiquitination. Cancer Res. 74 (2014), 808–817.
19. Hughes, T.R., Marton, M.J., Jones, A.R., Roberts, C.J., Stoughton, R., Armour, C.D., Bennett, H.A., Coffey, E., Dai, H., He, Y.D., et al. Functional discovery via a compendium of expression profiles. Cell 102 (2000), 109–126.
20. Illumina Inc. (2007). BeadStudio Normalization Algorithms for Gene Expression Data (Illumina Technical Bulletin Pub. No.470-2007-005).
21. Jackson, A.L., Bartz, S.R., Schelter, J., Kobayashi, S.V., Burchard, J., Mao, M., Li, B., Cavet, G., Linsley, P.S., Expression profiling reveals off-target gene regulation by RNAi. Nat. Biotechnol. 21 (2003), 635–637.
22. Järås, M., Miller, P.G., Chu, L.P., Puram, R.V., Fink, E.C., Schneider, R.K., Al-Shahrour, F., Peña, P., Breyfogle, L.J., Hartwell, K.A., et al. Csnk1a1 inhibition has p53-dependent therapeutic efficacy in acute myeloid leukemia. J. Exp. Med. 211 (2014), 605–612.
23. Johnson, W.E., Li, C., Rabinovic, A., Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics 8 (2007), 118–127.
24. Kent, W.J., BLAT–the BLAST-like alignment tool. Genome Res. 12 (2002), 656–664.
25. Krönke, J., Fink, E.C., Hollenbach, P.W., MacBeth, K.J., Hurst, S.N., Udeshi, N.D., Chamberlain, P.P., Mani, D.R., Man, H.W., Gandhi, A.K., et al. Lenalidomide induces ubiquitination and degradation of CK1α in del(5q) MDS. Nature 523 (2015), 183–188.
26. Lamb, J., Crawford, E.D., Peck, D., Modell, J.W., Blat, I.C., Wrobel, M.J., Lerner, J., Brunet, J.-P., Subramanian, A., Ross, K.N., et al. The Connectivity Map: using gene-expression signatures to connect small molecules, genes, and disease. Science 313 (2006), 1929–1935.
27. Lantermann, A.B., Chen, D., McCutcheon, K., Hoffman, G., Frias, E., Ruddy, D., Rakiec, D., Korn, J., McAllister, G., Stegmeier, F., et al. Inhibition of Casein Kinase 1 Alpha Prevents Acquired Drug Resistance to Erlotinib in EGFR-Mutant Non-Small Cell Lung Cancer. Cancer Res. 75 (2015), 4937–4948.
28. Litichevskiy, L., Peckner, R., Abelin, J.G., Asiedu, J.K., Creech, A.L., Davis, J.F., Davison, D., Dunning, C.M., Egertson, J.D., Egri, S., et al. A Library of Phosphoproteomic and Chromatin Signatures for Characterizing Cellular Responses to Drug Perturbations. bioRxiv, 2017, 10.1101/185918.
29. Liu, J., Lee, J., Salazar Hernandez, M.A., Mazitschek, R., Ozcan, U., Treatment of obesity with celastrol. Cell 161 (2015), 999–1011.
30. Locatelli, G., Bosotti, R., Ciomei, M., Brasca, M.G., Calogero, R., Mercurio, C., Fiorentini, F., Bertolotti, M., Scacheri, E., Scaburri, A., et al. Transcriptional analysis of an E2F gene signature as a biomarker of activity of the cyclin-dependent kinase inhibitor PHA-793887 in tumor and skin biopsies from a phase I clinical study. Mol. Cancer Ther. 9 (2010), 1265–1273.
31. Long, G.V., Fung, C., Menzies, A.M., Pupo, G.M., Carlino, M.S., Hyman, J., Shahheydari, H., Tembe, V., Thompson, J.F., Saw, R.P., et al. Increased MAPK reactivation in early resistance to dabrafenib/trametinib combination therapy of BRAF-mutant metastatic melanoma. Nat. Commun., 5, 2014, 5694.
32. Massard, C., Soria, J.-C., Anthoney, D.A., Proctor, A., Scaburri, A., Pacciarini, M.A., Laffranchi, B., Pellizzoni, C., Kroemer, G., Armand, J.-P., et al. A first in man, phase I dose-escalation study of PHA-793887, an inhibitor of multiple cyclin-dependent kinases (CDK2, 1 and 4) reveals unexpected hepatotoxicity in patients with solid tumors. Cell Cycle 10 (2011), 963–970.
33. Muthuswami, M., Ramesh, V., Banerjee, S., Viveka Thangaraj, S., Periasamy, J., Bhaskar Rao, D., Barnabas, G.D., Raghavan, S., Ganesan, K., Breast tumors with elevated expression of 1q candidate genes confer poor clinical outcome and sensitivity to Ras/PI3K inhibition. PLoS ONE, 8, 2013, e77553.
34. O'Boyle, N.M., Banck, M., James, C.A., Morley, C., Vandermeersch, T., Hutchison, G.R., Open Babel: An open chemical toolbox. J. Cheminform., 3, 2011, 33.
35. Peck, D., Crawford, E.D., Ross, K.N., Stegmaier, K., Golub, T.R., Lamb, J., A method for high-throughput gene expression signature analysis. Genome Biol., 7, 2006, R61.
36. Rohban, M.H., Singh, S., Wu, X., Berthet, J.B., Bray, M.-A., Shrestha, Y., Varelas, X., Boehm, J.S., Carpenter, A.E., Systematic morphological profiling of human gene and allele function via Cell Painting. eLife, 6, 2017.
37. Rosenbluth, J.M., Mays, D.J., Pino, M.F., Tang, L.J., Pietenpol, J.A., A gene signature-based approach identifies mTOR as a regulator of p73. Mol. Cell. Biol. 28 (2008), 5951–5964.
38. Rovedo, M.A., Krett, N.L., Rosen, S.T., Inhibition of glycogen synthase kinase-3 increases the cytotoxicity of enzastaurin. J. Invest. Dermatol. 131 (2011), 1442–1449.
39. Saito, S., Furuno, A., Sakurai, J., Sakamoto, A., Park, H.R., Shin-Ya, K., Tsuruo, T., Tomida, A., Chemical genomics identifies the unfolded protein response as a target for selective cancer cell killing during glucose deprivation. Cancer Res. 69 (2009), 4225–4234.
40. Schneider, R.K., Ademà V., Heckl, D., Järås, M., Mallo, M., Lord, A.M., Chu, L.P., McConkey, M.E., Kramann, R., Mullally, A., et al. Role of casein kinase 1A1 in the biology and targeted therapy of del(5q) MDS. Cancer Cell 26 (2014), 509–520.
41. Schnell, S.A., Ambesi-Impiombato, A., Sanchez-Martin, M., Belver, L., Xu, L., Qin, Y., Kageyama, R., Ferrando, A.A., Therapeutic targeting of HES1 transcriptional programs in T-ALL. Blood 125 (2015), 2806–2814.
42. Seiler, K.P., George, G.A., Happ, M.P., Bodycombe, N.E., Carrinski, H.A., Norton, S., Brudz, S., Sullivan, J.P., Muhlich, J., Serrano, M., et al. ChemBank: a small-molecule screening and cheminformatics resource database. Nucleic Acids Res. 36 (2008), D351–D359.
43. Singh, A.R., Joshi, S., Zulcic, M., Alcaraz, M., Garlich, J.R., Morales, G.A., Cho, Y.J., Bao, L., Levy, M.L., Newbury, R., et al. PI-3K Inhibitors Preferentially Target CD15+ Cancer Stem Cell Population in SHH Driven Medulloblastoma. PLoS ONE, 11, 2016, e0150836.
44. Smith, I., Greenside, P., Wadden, D., Tirosh, I., Natoli, T., Narayan, R., Root, D.E., Golub, T.R., Subramanian, A., Doench, J.G., Evaluation of RNAi and CRISPR technologies by large-scale gene expression profiling in the Connectivity Map. bioRxiv, 2017, 10.1101/147504.
45. Stockwell, S.R., Platt, G., Barrie, S.E., Zoumpoulidou, G., Te Poele, R.H., Aherne, G.W., Wilson, S.C., Sheldrake, P., McDonald, E., Venet, M., et al. Mechanism-based screen for G1/S checkpoint activators identifies a selective activator of EIF2AK3/PERK signalling. PLoS ONE, 7, 2012, e28568.
46. Subramanian, A., Tamayo, P., Mootha, V.K., Mukherjee, S., Ebert, B.L., Gillette, M.A., Paulovich, A., Pomeroy, S.L., Golub, T.R., Lander, E.S., Mesirov, J.P., Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 102 (2005), 15545–15550.
47. Tseng, G.C., Wong, W.H., Tight clustering: a resampling-based approach for identifying stable and tight patterns in data. Biometrics 61 (2005), 10–16.
48. Tsherniak, A., Vazquez, F., Montgomery, P.G., Weir, B.A., Kryukov, G., Cowley, G.S., Gill, S., Harrington, W.F., Pantel, S., Krill-Burger, J.M., et al. Defining a Cancer Dependency Map. Cell 170 (2017), 564–576.
49. van der Maaten, L., Hinton, G., Visualizing Data using t-SNE. J. Mach. Learn. Res. 9 (2008), 2579–2605.
50. Wagle, N., Van Allen, E.M., Treacy, D.J., Frederick, D.T., Cooper, Z.A., Taylor-Weiner, A., Rosenberg, M., Goetz, E.M., Sullivan, R.J., Farlow, D.N., et al. MAP kinase pathway alterations in BRAF-mutant melanoma patients with acquired resistance to combined RAF/MEK inhibition. Cancer Discov. 4 (2014), 61–68.
51. Wang, S.E., Xiang, B., Guix, M., Olivares, M.G., Parker, J., Chung, C.H., Pandiella, A., Arteaga, C.L., Transforming growth factor beta engages TACE and ErbB3 to activate phosphatidylinositol-3 kinase/Akt in ErbB2-overexpressing breast cancer and desensitizes cells to trastuzumab. Mol. Cell. Biol. 28 (2008), 5605–5620.
52. Wang, G., Ye, Y., Yang, X., Liao, H., Zhao, C., Liang, S., Expression-based in silico screening of candidate therapeutic compounds for lung adenocarcinoma. PLoS ONE 6 (2011), e14573–e14577.
53. Wawer, M.J., Li, K., Gustafsdottir, S.M., Ljosa, V., Bodycombe, N.E., Marton, M.A., Sokolnicki, K.L., Bray, M.-A., Kemp, M.M., Winchester, E., et al. Toward performance-diverse small-molecule libraries for cell-based phenotypic screening using multiplexed high-dimensional profiling. Proc. Natl. Acad. Sci. USA 111 (2014), 10911–10916.
54. Yueh, M.-F., Taniguchi, K., Chen, S., Evans, R.M., Hammock, B.D., Karin, M., Tukey, R.H., The commonly used antimicrobial additive triclosan is a liver tumor promoter. Proc. Natl. Acad. Sci. USA 111 (2014), 17200–17205.
55. Zhang, M., Luo, H., Xi, Z., Rogaeva, E., Drug repositioning for diabetes based on ‘omics’ data mining. PLoS ONE, 10, 2015, e0126082.