Combinatorial CRISPR–Cas9 screens for de novo mapping of genetic interactions
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We developed a systematic approach to map human genetic networks by combinatorial CRISPR-Cas9 perturbations coupled to robust analysis of growth kinetics. We targeted all pairs of 73 cancer genes with dual guide RNAs in three cell lines, comprising 141,912 tests of interaction. Numerous therapeutically relevant interactions were identified, and these patterns replicated with combinatorial drugs at 75% precision. From these results, we anticipate that cellular context will be critical to synthetic-lethal therapies.
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Direct capture of sgRNA molecules lets ECCITE-seq avoid the barcode-swapping problems reported for Perturb-seq.
“ECCITE-seq is readily applicable to any sgRNA library with the Cas9 S. pyogenes scaffold sequence and, by allowing direct capture of sgRNA molecules, overcomes documented problems of barcode swapping events observed with Perturb-seq that have the potential to confound single cell perturbation screens17–20.”
From Multiplexed detection of proteins, transcriptomes, clonotypes and CRISPR perturbations in single cells (2019) · cites this paper as [18]
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“[162] targeted all pairs of 73 cancer genes with dual-gRNAs in HeLa, A549 and 293 T cell lines, altogether comprising 141,912 tests of interaction.”
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Combinatorial CRISPR screen identifies fitness effects of gene paralogues
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“In cancer, CRISPR screens have been performed to identify genes involved in a wide variety of processes [23], including regulators of drug resistance [24–28], synergistic and synthetic lethal interactions [29,30], regulators of PD-L1 expression [31], and essential genes [32–34] (Figure 1).”
BackgroundDiscovery of synthetic lethal and tumor suppressor paralog pairs in the human genome
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“Additionally, a recent CRISPR screen for genetic interactions identified potential SL interactions between DNA-PKcs (PRKDC) and: AKT1, CDK4, CDK9, CHK1, IGFR1, mTOR, VHL, and RRM2 [25]; whether these SL interactions can be replicated with small-molecule DNAPK inhibitors remains to be seen.”
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CRISPR screens in plants: approaches, guidelines, and future prospects
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Self-citationFunctional Genomics via CRISPR–Cas
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“The dual-gRNA library was generated as previously described (Figure S1A) (Shen et al., 2017).”
InfluentialSelf-citationCRISPR screens for functional interrogation of immunity
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De novo generation of multi-target compounds using deep generative chemistry
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“4a) 31 – 33 .”
Self-citationA network of human functional gene interactions from knockout fitness screens in cancer cells
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“…CRISPR, to fi nd cancer genotype-speci fi c synthetic le-thals for drug targeting (Wong et al, 2016; Du et al, 2017; Han et al, 2017; le Sage et al, 2017; Shen et al, 2017; Najm et al, 2018) and to identify genetic interactions that enhance or suppress phenotypes related to drug and toxin resistance…”
CRISPR-Cas9 library screening approach for anti-cancer drug discovery: overview and perspectives
Chan, Y.-T., Lu, Y., Wu, J., Zhang, C., Tan, H., Bian, Z., Wang, N., & Feng, Y. (2022) · Theranostics · doi:10.7150/thno.71144 · Cited by 91 · see citing works
“Dual-gRNA library Multiplex CRISPRko Cas9 Mapping cancer genetic networks by combinatorial screens HeLa, 293T, A549 cell line Numerous therapeutically relevant interactions were identified Cell growth 2017 [136]”
MethodRevolutionizing DNA repair research and cancer therapy with CRISPR–Cas screens
Awwad, S. W., Serrano-Benítez, A., Thomas, J. C., Gupta, V., & Jackson, S. P. (2023) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-022-00571-x · Cited by 87 · see citing works
Synthetic Lethality and Cancer – Penetrance as the Major Barrier
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Encoded Library Technologies as Integrated Lead Finding Platforms for Drug Discovery
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“Advances in disease characterization and target identification [1,2] constantly move the drug discovery portfolio into unchartered territory.”
BackgroundSingle-Cell Multi-omics: An Engine for New Quantitative Models of Gene Regulation
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A Versatile Nonviral Delivery System for Multiplex Gene‐Editing in the Liver
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“To discover SL gene pairs as a gold mine of cancer drug targets, researchers have applied various techniques, including chemical screening (8), RNA interference (RNAi) screening (9, 10, 11, 12, 13), Clustered Regularly Interspaced Short Palindromic Repeats (CRISPR) screening (14, 15) and bioinformatics methods (16, 17…”
BackgroundA census of pathway maps in cancer systems biology
Kuenzi, B. M., & Ideker, T. (2020) · Nature reviews. Cancer · doi:10.1038/s41568-020-0240-7 · Cited by 79 · see citing works
Self-citationThe emerging role of systems biology for engineering protein production in CHO cells
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Self-citationToward an integrated map of genetic interactions in cancer cells
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“…engineered mouse models that are often limited by the number of cells that can be transfected or pairwise perturbation experiments as they are now conducted in human cells using CRISPR/Cas9 (Du et al , 2017; Shen et al , 2017), which are limited, by the number of possible gene combinations.”
CRISPR–Cas9 a boon or bane: the bumpy road ahead to cancer therapeutics
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“, 2009), CRISPRbased gRNA libraries are more easily designed and scaled and are more amenable to testing combinatorial gene interactions and interrogating the non-coding genome (Klann et al., 2018; Montalbano et al., 2017; Shen et al., 2017).”
Mapping the multiscale structure of biological systems
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Self-citationSynthetic lethal strategies for the development of cancer therapeutics
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Functional Genomics for Cancer Drug Target Discovery
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High-Throughput Approaches to Pinpoint Function within the Noncoding Genome
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“Other gene-targeting strategies have included paired gRNAs to target two genes in a single cell (Han et al., 2017; Shen et al., 2017; Wong et al., 2016), mutagenesis to identify gain-of-function mutations resulting from inframe NHEJ repair (Donovan et al., 2017), base editing to introduce stop…”
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“By iterating CRISPR adaptation, we created a 2S library (Figure 6) whose diversity is comparable with costly array-synthesized gRNA libraries of recent studies (Han et al., 2017; Shen et al., 2017).”
Gene editing and its applications in biomedicine
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“With improved dual-gene knockout gRNA vectors (Wong et al., 2016), CRISPR/Cas9-based screens might have been performed in synthetic-lethal studies (Han et al., 2017; Shen et al., 2017).”
BackgroundIt’s Getting Complicated—A Fresh Look at p53-MDM2-ARF Triangle in Tumorigenesis and Cancer Therapy
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Genome-wide CRISPR-Cas9 screening in mammalian cells
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A Highly Characterized Synthetic Landing Pad System for Precise Multicopy Gene Integration in Yeast
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In Vivo Imaging with Genetically Encoded Redox Biosensors
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“Particularly, the application of so called combinatorial CRISPR/Cas9 screening [375] where phenotypes of pairwise gene-knockouts are evaluated has allowed for the identification of gene interactions essential to carbohydrate metabolism in several cancer cell lines [376].”
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In vivo profiling of metastatic double knockouts through CRISPR–Cpf1 screens
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High‐resolution mapping of cancer cell networks using co‐functional interactions
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“…hypothesized genetic interactions, technological constraints have limited individual combinatorial sgRNA studies to measuring interactions for only a small fraction of all pairs of human genes (Ogasawara et al , 2015; Wong et al , 2016; Han et al , 2017; Shen et al , 2017; Horlbeck et al , 2018).”
Minimized combinatorial CRISPR screens identify genetic interactions in autophagy
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“24 Although these studies have made promising progress on identifying synthetic lethality, the mechanism of synthetic lethal interactions remains to be fully elucidated because of condition dependencies and difficulties in mutant recovery and detection of these rare events.”
BackgroundInfluentialSynthetic lethality between VPS4A and VPS4B triggers an inflammatory response in colorectal cancer
Szymańska, E., Nowak, P., Kolmus, K., Cybulska, M., Goryca, K., Derezińska‐Wołek, E., Szumera‐Ciećkiewicz, A., Brewińska‐Olchowik, M., Grochowska, A., Piwocka, K., et al. (2020) · EMBO Molecular Medicine · doi:10.15252/emmm.201910812 · Cited by 56 · see citing works
“…identified synthetic lethal interactions demonstrate incomplete penetrance, they are valid only for a fraction of tumor cells with a specific genetic background and are abrogated by other mutations that may appear in a heterologous population of tumor cells (Shen et al, 2017; Ryan et al, 2018).”
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Advances in therapeutic targeting of the DNA damage response in cancer
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“None were conserved amongst all three lines, demonstrating the importance tumor type specific treatments [56].”
BackgroundPredicting synthetic lethal interactions using heterogeneous data sources
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Optimal control nodes in disease-perturbed networks as targets for combination therapy
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“…small subsets of genes to: [1] identify GIs among panels of cancer genes revealing potential targets for synthetic lethal-based cancer therapy [13,15]; [2] explore genes encoding known drug targets to identify opportunities for combinatorial therapies [12] and; [3] chromatin regulatory…”
BackgroundTargeting Cell Metabolism as Cancer Therapy
Ngoi, N. Y. L., Eu, J. Q., Hirpara, J. L., Wang, L., Lim, J. S. J., Lee, S. C., Lim, Y., Pervaiz, S., Goh, B. C., & Wong, A. L. A. (2019) · Antioxidants and Redox Signaling · doi:10.1089/ars.2019.7947 · Cited by 51 · see citing works
“Although single-knock out (SKO) CRISPR screening approaches are limited by the plasticity of CCM, several groups have shown how combinatorial gene knock-out (KO) screening effectively studies CCM gene interactions and dispensability (12, 54, 130, 176).”
Computational methods, databases and tools for synthetic lethality prediction
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“study [44] CRISPR screening Combinatorial CRISPR screening Human cell lines HeLa: 52 A549: 57293 T: 59 293 T - http://www.”
- Authors
- Shen, J. P., Zhao, D., Sasik, R., Luebeck, J., Birmingham, A., Bojorquez-Gomez, A., Licon, K., Klepper, K., Pekin, D., Beckett, A. N., Sanchez, K. S., Thomas, A., Kuo, C.-C., Du, D., Roguev, A., Lewis, N. E., Chang, A. N., Kreisberg, J. F., Krogan, N., Qi, L., Ideker, T., & Mali, P.
- Affiliations
- University of California San Diego (US)
- University of California, San Francisco (US)
- Stanford University (US)
- Corresponding author
- Ideker, Trey
- Mali, Prashant
- ORCID
- Venue
- Nature Methods
- Published
- 2017-03-20
- Volume
- 14
- Issue
- 6
- Pages
- 573-576
- ISSN
- 1548-7091 (ISSN-L)
- 1548-7105
- PMC
- PMC5449203
- OpenAlex
- W2601016637
- Cited by
- 359
- References
- 39
- Citations by year
- 2026: 24 · 2025: 30 · 2024: 25 · 2023: 30 · 2022: 33 · 2021: 38 · 2020: 55 · 2019: 53 · 2018: 48 · 2017: 23
- FWCI
- 20.10
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Methods (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- U.S. Department of Veterans Affairs (CDA 16-150)
- Novo Nordisk Fonden (NNF10CC1016517)
- National Institutes of Health (UL1TR001442)
- National Institute on Drug Abuse (R01DA036858)
- National Cancer Institute (U54CA209891, L30 CA171000, R21CA199292)
- National Institute of General Medical Sciences (P50GM082250, P50GM085764, R01GM084279, T32GM008806, R35GM119850)
- National Institute of Environmental Health Sciences (R01ES014811)
- National Center for Advancing Translational Sciences
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › CRISPR and Genetic Engineering
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gene Regulatory Network Analysis
- Keywords
- CRISPR-Cas9 screen, synthetic lethality, cancer genes, genetic interaction networks, growth kinetics, cellular context, drug repurposing
- MeSH terms
- A549 Cells, Chromosome Mapping, Epistasis, Genetic, HeLa Cells, Humans, Neoplasm Proteins, Combinatorial Chemistry Techniques, Cell Line, Tumor, High-Throughput Nucleotide Sequencing, Clustered Regularly Interspaced Short Palindromic Repeats
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