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Next-generation characterization of the Cancer Cell Line Encyclopedia
Open accessAbstract
Large panels of comprehensively characterized human cancer models, including the Cancer Cell Line Encyclopedia (CCLE), have provided a rigorous framework with which to study genetic variants, candidate targets, and small-molecule and biological therapeutics and to identify new marker-driven cancer dependencies. To improve our understanding of the molecular features that contribute to cancer phenotypes, including drug responses, here we have expanded the characterizations of cancer cell lines to include genetic, RNA splicing, DNA methylation, histone H3 modification, microRNA expression and reverse-phase protein array data for 1,072 cell lines from individuals of various lineages and ethnicities. Integration of these data with functional characterizations such as drug-sensitivity, short hairpin RNA knockdown and CRISPR–Cas9 knockout data reveals potential targets for cancer drugs and associated biomarkers. Together, this dataset and an accompanying public data portal provide a resource for the acceleration of cancer research using model cancer cell lines. The original Cancer Cell Line Encyclopedia (CCLE) is expanded with deeper characterization of over 1,000 cell lines, including genomic, transcriptomic, and proteomic data, and integration with drug-sensitivity and gene-dependency data.
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“Through systematic mining of databases for correlations between the cytotoxicity of 4,518 clinical and pre-clinical small molecules and E3 ligase expression levels across hundreds of human cancer cell lines,3–5 we identified CR8, a cyclin-dependent kinase (CDK) inhibitor,6 as a compound that acts as a molecular glue degrader.”
From The CDK inhibitor CR8 acts as a molecular glue degrader that depletes cyclin K (2020) · cites this paper as [5]
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“Analysis of publicly available transcriptomics data (Ghandi et al, 2019) indicated that the HT1080 cells used for this experiment only mildly express the transporter SLC1A3 as compared to cell lines with detectable aspartate import activity described by Garcia-Bermudez et al. Therefore, exogenous…”
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“org/ccle) mRNA expression data was used to identify distinctively upregulated PLAU in pancreatic cancer cell lines (44, 45).”
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“We also calculated mtCN in 173 human cancer cell lines across 20 lineages from the Cancer Cell Line Encyclopedia (CCLE) using whole - genome sequencing coverage (5) of the mitochondrial versus nuclear genome (Fig.”
xCT Inhibition Increases Sensitivity to Vorinostat in a ROS-Dependent Manner
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“For 558 cell lines, mRNA expression data (CCLE project, (75)) and drug sensitivity data (PRISM Repurposing Primary Screen, (76)) were downloaded from the DepMap portal.”
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Kurzawa, N., Leo, I. R., Stahl, M. M. S., Kunold, E., Becher, I., Audrey, A., Mermelekas, G., Huber, W. K., Mateus, A., Savitski, M. M., et al. (2023) · Nature Chemical Biology · doi:10.1038/s41589-023-01284-8 · Cited by 49
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“Human cancer cell lines serve as one of the main and most powerful in vitro tools in cancer research 68 .”
BackgroundGenoSurf: metadata driven semantic search system for integrated genomic datasets
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Systematic functional identification of cancer multi-drug resistance genes
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“A bioinformatic analysis of protein as well as signaling markers was conducted using the CCLE RPPA database (18).”
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“We then examined the expression profile of MrgprF in various types of human cancer using GEPIA and CCLE (the cancer cell line encyclopedia) datasets.(27,28) Consistent with our previous result,(15) MrgprF was found to be unanimously downregulated in multiple human cancerous tissues and cell lines, including cutaneous…”
MethodYu, C., Lei, X., Chen, F., Mao, S., Lv, L., Liu, H., Hu, X., Wang, R., Shen, L., Zhang, N., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-31197-4 · Cited by 51
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“We utilized two distinct methods to quantify our lncRNA genes expression across CCLE cell lines: (1) A first ‘sensitive/permissive’ approach (STAR 88 ) in combination with featureCounts 91 ), which served as the basis for selection of lncRNA genes for CRISPR library design.”
InfluentialGe, W., Wang, Y., Quan, M., Mao, T., Bischof, E. Y., Xu, H., Zhang, X., Li, S., Yue, M., Ma, J., et al. (2024) · Molecular Cancer · doi:10.1186/s12943-024-01965-5 · Cited by 45
“Expression profile data of human cancer cell lines (CCLs) were obtained from the Broad Institute Cancer Cell Line Encyclopedia (CCLE) project (https:// porta ls. broad insti tute. org/ ccle/) [24].”
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Connexin 43 confers chemoresistance through activating PI3K
Pridham, K. J., Shah, F., Hutchings, K. R., Sheng, K. L., Guo, S., Liu, M., Kanabur, P., Lamouille, S., Lewis, G., Morales, M., et al. (2022) · Oncogenesis · doi:10.1038/s41389-022-00378-7 · Cited by 43
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Oliemuller, E., Newman, R., Tsang, S. M., Foo, S., Muirhead, G., Noor, F., Haider, S. A., Aurrekoetxea-Rodríguez, I., Vivanco, M. D., & Howard, B. A. (2020) · eLife · doi:10.7554/elife.58374 · Cited by 44
Barrows, D., Feng, L., Carroll, T. S., & Allis, C. D. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2008017117 · Cited by 44
Deciphering the signaling network of breast cancer improves drug sensitivity prediction
Tognetti, M., Gábor, A., Yang, M., Cappelletti, V., Windhager, J., Rueda, O. M., Charmpi, K., Esmaeilishirazifard, E., Bruna, A., de Souza, N., et al. (2021) · Cell Systems · doi:10.1016/j.cels.2021.04.002 · Cited by 42
Seier, J. A., Reinhardt, J., Saraf, K., Ng, S. S., Layer, J. P., Corvino, D., Althoff, K., Giordano, F. A., Schramm, A. R., Fischer, M., et al. (2021) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2020-001335 · Cited by 46
Evidence of pioneer factor activity of an oncogenic fusion transcription factor
Sunkel, B. D., Wang, M., LaHaye, S., Kelly, B., Fitch, J., Barr, F. G., White, P., & Stanton, B. Z. (2021) · iScience · doi:10.1016/j.isci.2021.102867 · Cited by 43
Reardon, B. M., Moore, N. D., Moore, N., Kofman, E. R., AlDubayan, S. H., Cheung, A. T. M., Conway, J. R., Elmarakeby, H., Imamović, A., Kamran, S. C., et al. (2021) · Nature Cancer · doi:10.1038/s43018-021-00243-3 · Cited by 43
Co-existing TP53 and ARID1A mutations promote aggressive endometrial tumorigenesis
Reske, J. J., Wilson, M. R., Holladay, J., Siwicki, R. A., Skalski, H. J., Harkins, S. K., Adams, M., Risinger, J. I., Hostetter, G. H., Lin, K. Y., et al. (2021) · PLoS Genetics · doi:10.1371/journal.pgen.1009986 · Cited by 45
Farrell, M. L., Fairfield, H. E., Karam, M., D’Amico, A., Murphy, C. S., Falank, C. R., Sklavenitis‐Pistofidis, R., Cao, A., Marinac, C. R., Dragon, J. A., et al. (2023) · eLife · doi:10.7554/elife.81184 · Cited by 44
“…consistently showed the expression in haematopoetic/lymphoid lineage lines within the Cancer Cell Line Encyclopedia (CCLE) at the gene level ( Figure 1—figure supplement 1B ) and protein level ( Figure 1—figure supplement 1C , “ DepMap 22Q2, 2022 ; Ghandi et al., 2019 ; Nusinow et al., 2020 ).”
A thiol-bound drug reservoir enhances APR-246-induced mutant p53 tumor cell death
Ceder, S., Eriksson, S. E., Cheteh, E. H., Dawar, S., Corrales Benitez, M., Bykov, V. J. N., Fujihara, K. M., Grandin, M., Li, X., Ramm, S., et al. (2021) · EMBO Molecular Medicine · doi:10.15252/emmm.201910852 · Cited by 41
Drug-adapted cancer cell lines as preclinical models of acquired resistance
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PTENα functions as an immune suppressor and promotes immune resistance in PTEN-mutant cancer
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Liang, H.-C., Costanza, M., Prutsch, N., Zimmerman, M. W., Gurnhofer, E., Montes-Mojarro, I. A., Abraham, B. J., Prokoph, N., Stoiber, S., Tangermann, S., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-25379-9 · Cited by 43
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“…databases (http://gepia.cancer-pku.cn/) (Tang et al., 2017) to analyze the expression of UBE2C in pan-cancer, the Cancer Cell Line Encyclopedia (CCLE) tool (https://portals. broadinstitute.org/ccle/) (Ghandi et al., 2019) was employed to examine the expression of UBE2C in diverse cancer cell lines.”
Rational drug combinations with CDK4/6 inhibitors in acute lymphoblastic leukemia
Bride, K. L., Hu, H., Tikhonova, A. N., Fuller, T. J., Vincent, T. L., Shraim, R., Li, M. M., Carroll, W. L., Raetz, E. A., Aifantis, I., et al. (2021) · Haematologica · doi:10.3324/haematol.2021.279410 · Cited by 43
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IFITM proteins assist cellular uptake of diverse linked chemotypes
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Upregulation of FGF9 in Lung Adenocarcinoma Transdifferentiation to Small Cell Lung Cancer
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Integrative Characterization of the Role of IL27 In Melanoma Using Bioinformatics Analysis
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Insulin-like growth factor binding protein 5: Diverse roles in cancer
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“To assess the complexity of IGFBP expression in cancer-derived cell lines, we analyzed the previously published Cancer Cell Line Encyclopedia (CCLE) via cBioportal (60, 61).”
MethodRicarte‐Filho, J. C., Casado‐Medrano, V., Reichenberger, E. R., Spangler, Z., Scheerer, M., Isaza, A. R., Baran, J. A., Patel, T., MacFarland, S. P., Brodeur, G. M., et al. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1083382 · Cited by 42
“To our knowledge, there are no commercially available cancer cell lines with spontaneous hotspot mutation in the RNase IIIb domain of DICER1 (50).”
BackgroundGlobal impact of somatic structural variation on the cancer proteome
Chen, F., Zhang, Y., Chandrashekar, D. S., Varambally, S., & Creighton, C. J. (2023) · Nature Communications · doi:10.1038/s41467-023-41374-8 · Cited by 46
Most large structural variants in cancer genomes can be detected without long reads
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“We integrated genomics 2,63 , transcriptomics 26 , methylomics 25 , proteomics 11 , metabolomics 27 , drug response 25,28,29 , and CRISPR-Cas9 gene essentiality 4,64 .”
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The Challenges and Opportunities of LncRNAs in Ovarian Cancer Research and Clinical Use
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Long Noncoding RNAs at the Crossroads of Cell Cycle and Genome Integrity
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“HCC827 lung adenocarcinoma cells exhibited the lowest SAMHD1 expression among CCLE-annotated solid tumor cells (Supplemental Figure 2, A and B) and were highly susceptible and Supplemental Figure 1F) (19).”
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Background
Metadata
- Authors
- Ghandi, M., Huang, F. W., Jané-Valbuena, J., Kryukov, G. V., Lo, C. C., McDonald, E. R., Barretina, J., Gelfand, E. T., Bielski, C. M., Li, H., Hu, K., Andreev-Drakhlin, A. Y., Kim, J., Hess, J. M., Haas, B. J., Aguet, F., Weir, B. A., Rothberg, M. V., Paolella, B. R., Lawrence, M. S., Akbani, R., Lu, Y., Tiv, H. L., Gokhale, P. C., de Weck, A., Mansour, A. A., Oh, C., Shih, J., Hadi, K., Rosen, Y., Bistline, J., Venkatesan, K., Reddy, A., Sonkin, D., Liu, M., Lehar, J., Korn, J. M., Porter, D. A., Jones, M. D., Golji, J., Caponigro, G., Taylor, J. E., Dunning, C. M., Creech, A. L., Warren, A. C., McFarland, J. M., Zamanighomi, M., Kauffmann, A., Stransky, N., Imielinski, M., Maruvka, Y. E., Cherniack, A. D., Tsherniak, A., Vazquez, F., Jaffe, J. D., Lane, A. A., Weinstock, D. M., Johannessen, C. M., Morrissey, M. P., Stegmeier, F., Schlegel, R., Hahn, W. C., Getz, G., Mills, G. B., Boehm, J. S., Golub, T. R., Garraway, L. A., & Sellers, W. R.
- Affiliations
- Broad Institute (US)
- The University of Texas MD Anderson Cancer Center (US)
- Cornell University (US)
- National Cancer Institute (US)
- Novartis Institutes for BioMedical Research (CH)
- Dana-Farber Cancer Institute (US)
- Corresponding author
- Sellers, William R.
- ORCID
- Ghandi, Mahmoud
- Huang, Franklin W.
- Kryukov, Gregory V.
- McDonald, E. Robert
- Barretina, Jordi
- Li, Haoxin
- Hu, Kevin
- Andreev-Drakhlin, Alexander Y.
- Kim, Jaegil
- Hess, Julian M.
- Haas, Brian J.
- Aguet, François
- Rothberg, Michael V.
- Paolella, Brenton R.
- Lawrence, Michael S.
- Akbani, Rehan
- Lu, Yiling
- Tiv, Hong L.
- Gokhale, Prafulla C.
- Oh, Coyin
- Shih, Juliann
- Hadi, Kevin
- Rosen, Yanay
- Venkatesan, Kavitha
- Reddy, Anupama
- Sonkin, Dmitriy
- Liu, Manway
- Korn, Joshua M.
- Jones, Michael D.
- Taylor, Jordan E.
- Creech, Amanda L.
- McFarland, James M.
- Zamanighomi, Mahdi
- Kauffmann, Audrey
- Stransky, Nicolas
- Imielinski, Marcin
- Maruvka, Yosef E.
- Cherniack, Andrew D.
- Tsherniak, Aviad
- Jaffe, Jacob D.
- Lane, Andrew A.
- Weinstock, David M.
- Johannessen, Cory M.
- Stegmeier, Frank
- Hahn, William C.
- Getz, Gad
- Mills, Gordon B.
- Boehm, Jesse S.
- Golub, Todd R.
- Garraway, Levi A.
- Sellers, William R.
- Venue
- Nature
- Published
- 2019-05
- Volume
- 569
- Issue
- 7757
- Pages
- 503-508
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC6697103
- OpenAlex
- W2944727022
- Semantic Scholar
- b3631d8d2656c0c72ad92f3b0a77af2afde649a5
- Cited by
- 3,394
- References
- 67
- Citations by year
- 2026: 297 · 2025: 472 · 2024: 560 · 2023: 551 · 2022: 550 · 2021: 594 · 2020: 306 · 2019: 59
- FWCI
- 121.99
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- European Hematology Association (TRTH56)
- National Institutes of Health (5r21da025720-02)
- National Institute on Drug Abuse (R21-DA025720)
- National Cancer Institute (R50CA221675, P50CA217685, R01CA219943, P50CA098258, U24CA180922, U54CA224068, U24CA210949, U24CA210950, R50CA211461, R37CA225191, U01CA217842, U01CA176058, P30CA016672)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer Genomics and Diagnostics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gene expression and cancer classification
- Keywords
- Cancer Cell Line Encyclopedia, cancer cell lines, drug sensitivity, gene dependency, RNA splicing, DNA methylation, histone H3 modifications, microRNA expression, reverse phase protein array, CRISPR/Cas9 knockout, shRNA knockdown, therapeutic target, biomarkers, multi-omics integration, public data portals
- MeSH terms
- Gene Editing, Antineoplastic Agents, Ethnicity, Histones, Humans, Neoplasms, RNA Splicing, Biomarkers, Tumor, Drug Resistance, Neoplasm, DNA Methylation, MicroRNAs, Protein Array Analysis, Cell Line, Tumor, Molecular Targeted Therapy
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