Genome-wide recessive genetic screening in mammalian cells with a lentiviral CRISPR-guide RNA library

Nature Biotechnology

Volumn 32, Issue 3, 2014, Pages 267-273

  Koike Yusa, Hiroko ^a   Li, Yilong ^a   Tan, E Pien ^a   Velasco Herrera, Martin Del Castillo ^a   Yusa, Kosuke ^a  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALS; RNA;

GENETIC SCREENING; HIGH THROUGHPUT; LENTIVIRAL VECTOR; MOUSE EMBRYONIC STEM CELLS; MUTANT LIBRARIES; PARTIAL DEPLETION; PROTEIN-CODING GENES; RNA INTERFERENCE;

GENES;

CLOSTRIDIUM TOXIN; GUIDE RNA; HOST FACTOR; LENTIVIRUS VECTOR; TIOGUANINE;

ANIMAL CELL; ARTICLE; CLOSTRIDIUM SEPTICUM; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; CONTROLLED STUDY; DEPLETION; DIPLOIDY; EMBRYONIC STEM CELL; GENE ACTIVITY; GENE EXPRESSION; GENE MUTATION; GENE TARGETING; GENETIC ASSOCIATION; GENETIC SCREENING; GENOME; MAMMAL CELL; MOUSE; MOUSE MUTANT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROVIRUS; RNA INTERFERENCE; RNA LIBRARY; RNA STRUCTURE; SCREENING; TRANSGENE; VIRAL GENE THERAPY; ANIMAL; BIOTECHNOLOGY; CELL CULTURE; CRISPR CAS SYSTEM; GENE LIBRARY; GENETICS; GENOMICS; LENTIVIRINAE; PROCEDURES; REPRODUCIBILITY;

ANIMALS; BIOTECHNOLOGY; CELLS, CULTURED; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; CRISPR-CAS SYSTEMS; EMBRYONIC STEM CELLS; GENE LIBRARY; GENOME; GENOMICS; LENTIVIRUS; MICE; REPRODUCIBILITY OF RESULTS; RNA INTERFERENCE; RNA, GUIDE;

EID: 84898665052     PISSN: 10870156     EISSN: 15461696     Source Type: Journal    
DOI: 10.1038/nbt.2800     Document Type: Article

References (46)

1. Forsburg, S.L. The art and design of genetic screens: yeast. Nat. Rev. Genet. 2, 659-668 (2001).
2. Jorgensen, E.M. & Mango, S.E. The art and design of genetic screens: Caenohabditis elegans. Nat. Rev. Genet. 3, 356-369 (2002).
3. Boutros, M. & Ahringer, J. The art and design of genetic screens: RNA interference. Nat. Rev. Genet. 9, 554-566 (2008).
4. Moffat, J. et al. A lentiviral RNAi library for human and mouse genes applied to an arrayed viral high-content screen. Cell 124, 1283-1298 (2006).
5. Iorns, E., Lord, C.J., Turner, N. & Ashworth, A. Utilizing RNA interference to enhance cancer drug discovery. Nat. Rev. Drug Discov. 6, 556-568 (2007).
6. Carette, J.E. et al. Haploid genetic screens in human cells identify host factors used by pathogens. Science 326, 1231-1235 (2009).
7. Carette, J.E. et al. Global gene disruption in human cells to assign genes to phenotypes by deep sequencing. Nat. Biotechnol. 29, 542-546 (2011).
8. Carette, J.E. et al. Ebola virus entry requires the cholesterol transporter Niemann-Pick C1. Nature 477, 340-343 (2011).
9. L eeb, M. & Wutz, A. Derivation of haploid embryonic stem cells from mouse embryos. Nature 479, 131-134 (2011).
10. Yang, H. et al. Generation of genetically modified mice by oocyte injection of androgenetic haploid embryonic stem cells. Cell 149, 605-617 (2012).
11. Elling, U. et al. Forward and reverse genetics through derivation of haploid mouse embryonic stem cells. Cell Stem Cell 9, 563-574 (2011).
12. Yang, H. et al. Generation of haploid embryonic stem cells from Macaca fascicularis monkey parthenotes. Cell Res. 23, 1187-1200 (2013).
13. Urnov, F.D., Rebar, E.J., Holmes, M.C., Zhang, H.S. & Gregory, P.D. Genome editing with engineered zinc finger nucleases. Nat. Rev. Genet. 11, 636-646 (2010).
14. Joung, J.K. & Sander, J.D. TALENs: a widely applicable technology for targeted genome editing. Nat. Rev. Mol. Cell Biol. 14, 49-55 (2013).
15. Cho, S.W., Kim, S., Kim, J.M. & Kim, J.S. Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease. Nat. Biotechnol. 31, 230-232 (2013).
16. Cong, L. et al. Multiplex genome engineering using CRISPR/Cas systems. Science 339, 819-823 (2013).
17. Mali, P. et al. RNA-guided human genome engineering via Cas9. Science 339, 823-826 (2013).
18. Wang, H. et al. One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell 153, 910-918 (2013).
19. Takeda, J. et al. Deficiency of the GPI anchor caused by a somatic mutation of the PIG-A gene in paroxysmal nocturnal hemoglobinuria. Cell 73, 703-711 (1993).
20. Kinoshita, T., Fujita, M. & Maeda, Y. Biosynthesis, remodelling and functions of mammalian GPI-anchored proteins: recent progress. J. Biochem. 144, 287-294 (2008).
21. Gordon, V.M. et al. Clostridium septicum alpha toxin uses glycosylphosphatidylinositolanchored protein receptors. J. Biol. Chem. 274, 27274-27280 (1999).
22. Fu, Y. et al. High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat. Biotechnol. 31, 822-826 (2013).
23. Hsu, P.D. et al. DNA targeting specificity of RNA-guided Cas9 nucleases. Nat. Biotechnol. 31, 827-832 (2013).
24. E llis, J. Silencing and variegation of gammaretrovirus and lentivirus vectors. Hum. Gene Ther. 16, 1241-1246 (2005).
25. Bennardo, N., Cheng, A., Huang, N. & Stark, J.M. Alternative-NHEJ is a mechanistically distinct pathway of mammalian chromosome break repair. PLoS Genet. 4, e1000110 (2008).
26. Nichols, J. et al. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 95, 379-391 (1998).
27. Mitsui, K. et al. The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 113, 631-642 (2003).
28. Hakem, R. et al. The tumor suppressor gene Brca1 is required for embryonic cellular proliferation in the mouse. Cell 85, 1009-1023 (1996).
29. Tsuzuki, T. et al. Targeted disruption of the Rad51 gene leads to lethality in embryonic mice. Proc. Natl. Acad. Sci. USA 93, 6236-6240 (1996).
30. Luo, J. et al. A genome-wide RNAi screen identifies multiple synthetic lethal interactions with the Ras oncogene. Cell 137, 835-848 (2009).
31. Agaisse, H. et al. Genome-wide RNAi screen for host factors required for intracellular bacterial infection. Science 309, 1248-1251 (2005).
32. Karlas, A. et al. Genome-wide RNAi screen identifies human host factors crucial for influenza virus replication. Nature 463, 818-822 (2010).
33. Ran, F.A. et al. Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154, 1380-1389 (2013).
34. Mali, P. et al. CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering. Nat. Biotechnol. 31, 833-838 (2013).
35. Pattanayak, V. et al. High-throughput profiling of off-target DNA cleavage reveals RNA-programmed Cas9 nuclease specificity. Nat. Biotechnol. 31, 839-843 (2013).
36. Cadinanos, J. & Bradley, A. Generation of an inducible and optimized piggyBac transposon system. Nucleic Acids Res. 35, e87 (2007).
37. Yusa, K., Rad, R., Takeda, J. & Bradley, A. Generation of transgene-free induced pluripotent mouse stem cells by the piggyBac transposon. Nat. Methods 6, 363-369 (2009).
38. Carey, B.W. et al. Reprogramming of murine and human somatic cells using a single polycistronic vector. Proc. Natl. Acad. Sci. USA 106, 157-162 (2009).
39. Subach, O.M. et al. Conversion of red fluorescent protein into a bright blue probe. Chem. Biol. 15, 1116-1124 (2008).
40. Quinlan, A.R. & Hall, I.M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841-842 (2010).
41. Pettitt, S.J. et al. Agouti C57BL/6N embryonic stem cells for mouse genetic resources. Nat. Methods 6, 493-495 (2009).
42. Wang, W., Bradley, A. & Huang, Y. A piggyBac transposon-based genome-wide library of insertionally mutated Blm-deficient murine ES cells. Genome Res. 19, 667-673 (2009).
43. A buin, A., Zhang, H. & Bradley, A. Genetic analysis of mouse embryonic stem cells bearing Msh3 and Msh2 single and compound mutations. Mol. Cell. Biol. 20, 149-157 (2000).
44. L i, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760 (2009).
45. Quail, M.A. et al. Optimal enzymes for amplifying sequencing libraries. Nat. Methods 9, 10-11 (2012).
46. Huang, da W. et al. DAVID gene ID conversion tool. Bioinformation 2, 428-430 (2008).