Design, execution, and analysis of pooled in vitro CRISPR/Cas9 screens

FEBS Journal

Volumn , Issue , 2016, Pages 3170-3180

  Miles, Linde A ^a   Garippa, Ralph J ^b   Poirier, John T ^b,c  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

CRISPR; Libraries; Screening; sgRNA

Indexed keywords

CRISPR ASSOCIATED PROTEIN; RNA;

CELL LINE; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; DNA MODIFICATION; GENE EXPRESSION; GENE LIBRARY; GENE SILENCING; GENETIC MANIPULATION; GENETIC SCREENING; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN ANALYSIS; QUALITY CONTROL; REVIEW; SEQUENCE ANALYSIS; STATISTICAL ANALYSIS; TECHNOLOGY;

EID: 84986208237     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.13770     Document Type: Review

References (42)

1. 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.
2. Paddison PJ, Silva JM, Conklin DS, Schlabach M, Li M, Aruleba S, Balija V, O'Shaughnessy A, Gnoj L, Scobie K et al. (2004) A resource for large-scale RNA-interference-based screens in mammals. Nature 428, 427–431.
3. Deans RM, Morgens DW, Okesli A, Pillay S, Horlbeck MA, Kampmann M, Gilbert LA, Li A, Mateo R, Smith M et al. (2016) Parallel shRNA and CRISPR-Cas9 screens enable antiviral drug target identification. Nat Chem Biol 12, 361–366.
4. Morgens DW, Deans RM, Li A & Bassik MC (2016) Systematic comparison of CRISPR/Cas9 and RNAi screens for essential genes. Nat Biotechnol 34, 634–636.
5. Evers B, Jastrzebski K, Heijmans JPM, Grernrum W, Beijersbergen RL & Bernards R (2016) CRISPR knockout screening outperforms shRNA and CRISPRi in identifying essential genes. Nat Biotechnol 34, 631–633.
6. Carette JE, Guimaraes CP, Wuethrich I, Blomen VA, Varadarajan M, Sun C, Bell G, Yuan B, Muellner MK, Nijman SM et al. (2011) Global gene disruption in human cells to assign genes to phenotypes by deep sequencing. Nat Biotechnol 29, 542–546.
7. Carette JE, Raaben M, Wong AC, Herbert AS, Obernosterer G, Mulherkar N, Kuehne AI, Kranzusch PJ, Griffin AM, Ruthel G et al. (2011) Ebola virus entry requires the cholesterol transporter Niemann-Pick C1. Nature 477, 340–343.
8. Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA et al. (2013) Multiplex genome engineering using CRISPR/Cas systems. Science 339, 819–823.
9. Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, Norville JE & Church GM (2013) RNA-guided human genome engineering via Cas9. Science 339, 823–826.
10. Shalem O, Sanjana NE, Hartenian E, Shi X, Scott DA, Mikkelsen TS, Heckl D, Ebert BL, Root DE, Doench JG et al. (2014) Genome-scale CRISPR-Cas9 knockout screening in human cells. Science 343, 84–87.
11. Wang T, Wei JJ, Sabatini DM & Lander ES (2014) Genetic screens in human cells using the CRISPR-Cas9 system. Science 343, 80–84.
12. Wang T, Birsoy K, Hughes NW, Krupczak KM, Post Y, Wei JJ, Lander ES & Sabatini DM (2015) Identification and characterization of essential genes in the human genome. Science 350, 1096–1101.
13. Sanjana NE, Shalem O & Zhang F (2014) Improved vectors and genome-wide libraries for CRISPR screening. Nat Methods 11, 783–784.
14. Hart T, Chandrashekhar M, Aregger M, Steinhart Z, Brown KR, MacLeod G, Mis M, Zimmermann M, Fradet-Turcotte A, Sun S et al. (2015) High-resolution CRISPR screens reveal fitness genes and genotype-specific cancer liabilities. Cell 163, 1515–1526.
15. Doench JG, Fusi N, Sullender M, Hegde M, Vaimberg EW, Donovan KF, Smith I, Tothova Z, Wilen C, Orchard R et al. (2016) Optimized sgRNA design to maximize activity and minimize off-target effects of CRISPR-Cas9. Nat Biotechnol 34, 184–191.
16. Shi J, Wang E, Milazzo JP, Wang Z, Kinney JB & Vakoc CR (2015) Discovery of cancer drug targets by CRISPR-Cas9 screening of protein domains. Nat Biotechnol 33, 661–667.
17. Koike-Yusa H, Li Y, Tan EP, Velasco-Herrera Mdel C & Yusa K (2014) Genome-wide recessive genetic screening in mammalian cells with a lentiviral CRISPR-guide RNA library. Nat Biotechnol 32, 267–273.
18. Campeau E & Gobeil S (2011) RNA interference in mammals: behind the screen. Briefings Funct Gen 10, 215–226.
19. Ren Q, Li C, Yuan P, Cai C, Zhang L, Luo GG & Wei W (2015) A Dual-reporter system for real-time monitoring and high-throughput CRISPR/Cas9 library screening of the hepatitis C virus. Sci Rep 5, 8865.
20. Qi LS, Larson MH, Gilbert LA, Doudna JA, Weissman JS, Arkin AP & Lim WA (2013) Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell 152, 1173–1183.
21. Gilbert LA, Horlbeck MA, Adamson B, Villalta JE, Chen Y, Whitehead EH, Guimaraes C, Panning B, Ploegh HL, Bassik MC et al. (2014) Genome-Scale CRISPR-mediated control of gene repression and activation. Cell 159, 647–661.
22. Maeder ML, Linder SJ, Cascio VM, Fu Y, Ho QH & Joung JK (2013) CRISPR RNA-guided activation of endogenous human genes. Nat Methods 10, 977–979.
23. Perez-Pinera P, Kocak DD, Vockley CM, Adler AF, Kabadi AM, Polstein LR, Thakore PI, Glass KA, Ousterout DG, Leong KW et al. (2013) RNA-guided gene activation by CRISPR-Cas9-based transcription factors. Nat Methods 10, 973–976.
24. Tanenbaum ME, Gilbert LA, Qi LS, Weissman JS & Vale RD (2014) A protein-tagging system for signal amplification in gene expression and fluorescence imaging. Cell 159, 635–646.
25. Konermann S, Brigham MD, Trevino AE, Joung J, Abudayyeh OO, Barcena C, Hsu PD, Habib N, Gootenberg JS, Nishimasu H et al. (2015) Genome-scale transcriptional activation by an engineered CRISPR-Cas9 complex. Nature 517, 583–588.
26. Stratton MR, Campbell PJ & Futreal PA (2009) The cancer genome. Nature 458, 719–724.
27. Hsu PD, Lander ES & Zhang F (2014) Development and applications of CRISPR-Cas9 for genome engineering. Cell 157, 1262–1278.
28. Hoeijmakers JH (2001) Genome maintenance mechanisms for preventing cancer. Nature 411, 366–374.
29. Good IJ & Toulmin GH (1956) The number of new species, and the increase in population coverage, when a sample is increased. Biometrika 43, 45–63.
30. Deng C, Daley T & Smith AD (2015) Applications of species accumulation curves in large-scale biological data analysis. Quantit Biol 3, 135–144.
31. Ritchie ME, Phipson B, Wu D, Hu Y, Law CW, Shi W & Smyth GK (2015) limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res 43, e47.
32. Robinson MD, McCarthy DJ & Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139–140.
33. 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 USA 105, 20380–20385.
34. Konig R, Chiang CY, 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.
35. Diaz AA, Qin H, Ramalho-Santos M & Song JS (2015) HiTSelect: a comprehensive tool for high-complexity-pooled screen analysis. Nucleic Acids Res 43, e16.
36. Li W, Xu H, Xiao T, Cong L, Love MI, Zhang F, Irizarry RA, Liu JS, Brown M & Liu XS (2014) MAGeCK enables robust identification of essential genes from genome-scale CRISPR/Cas9 knockout screens. Genome Biol 15, 554.
37. Wu D, Lim E, Vaillant F, Asselin-Labat ML, Visvader JE & Smyth GK (2010) ROAST: rotation gene set tests for complex microarray experiments. Bioinformatics 26, 2176–2182.
38. Wu D & Smyth GK (2012) Camera: a competitive gene set test accounting for inter-gene correlation. Nucleic Acids Res 40, e133.
39. Ran FA, Hsu PD, Wright J, Agarwala V, Scott DA & Zhang F (2013) Genome engineering using the CRISPR-Cas9 system. Nat Protoc 8, 2281–2308.
40. Kim JM, Kim D, Kim S & Kim JS (2014) Genotyping with CRISPR-Cas-derived RNA-guided endonucleases. Nat Commun 5, 3157.
41. Price EP, Smith H, Huygens F & Giffard PM (2007) High-resolution DNA melt curve analysis of the clustered, regularly interspaced short-palindromic-repeat locus of Campylobacter jejuni. Appl Environ Microbiol 73, 3431–3436.
42. Hendel A, Kildebeck EJ, Fine EJ, Clark JT, Punjya N, Sebastiano V, Bao G & Porteus MH (2014) Quantifying genome-editing outcomes at endogenous loci with SMRT sequencing. Cell Rep 7, 293–305.