CRISPR-Cas system: A powerful tool for genome engineering

Plant Molecular Biology

Volumn 85, Issue 3, 2014, Pages 209-218

  Liu, Liang ^a,b   Fan, Xiu Duo ^a,b  

^a National Center for Molecular Crop Design   (China)

^b Frontier Laboratories of Systems Crop Design Co Ltd   (China)

Author keywords

Cas9; CRISPR Cas; Genome editing; Immunity; Off target

Indexed keywords

CRISPR CAS SYSTEM; GENE EXPRESSION REGULATION; GENETIC ENGINEERING; GENETICS; GENOMICS; METHODOLOGY; PHYSIOLOGY; PLANT GENOME; REVIEW;

CRISPR-CAS SYSTEMS; GENE EXPRESSION REGULATION, PLANT; GENETIC ENGINEERING; GENOME, PLANT; GENOMICS;

EID: 84900852939     PISSN: 01674412     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11103-014-0188-7     Document Type: Review

References (113)

1. Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, Moineau S, Romero DA, Horvath P (2007) CRISPR provides acquired resistance against viruses in prokaryotes. Science 315(5819): 1709-1712.
2. Beloglazova N, Petit P, Flick R, Brown G, Savchenko A, Yakunin AF (2011) Structure and activity of the Cas3 HD nuclease MJ0384, an effector enzyme of the CRISPR interference. EMBO J 30(22): 4616-4627.
3. Berns K, Hijmans EM, Mullenders J, Brummelkamp TR, Velds A, Heimerikx M, Kerkhoven RM, Madiredjo M, Nijkamp W, Weigelt B (2004) A large-scale RNAi screen in human cells identifies new components of the p53 pathway. Nature 428(6981): 431-437.
4. Bhaya D, Davison M, Barrangou R (2011) CRISPR-Cas systems in bacteria and archaea: versatile small RNAs for adaptive defense and regulation. Annu Rev Genet 45: 273-297. doi: 10. 1146/annurev-genet-110410-132430.
5. Bikard D, Jiang W, Samai P, Hochschild A, Zhang F, Marraffini LA (2013) Programmable repression and activation of bacterial gene expression using an engineered CRISPR-Cas system. Nucleic Acids Res 41(15): 7429-7437. doi: 10. 1093/nar/gkt520.
6. Bogdanove AJ, Voytas DF (2011) TAL effectors: customizable proteins for DNA targeting. Science 333(6051): 1843-1846.
7. Bolotin A, Quinquis B, Sorokin A, Ehrlich SD (2005) Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. Microbiology 151(8): 2551-2561.
8. Boutros M, Kiger AA, Armknecht S, Kerr K, Hild M, Koch B, Haas SA, Paro R, Perrimon N (2004) Genome-wide RNAi analysis of growth and viability in Drosophila cells. Science 303(5659): 832-835.
9. Brouns SJ, Jore MM, Lundgren M, Westra ER, Slijkhuis RJ, Snijders AP, Dickman MJ, Makarova KS, Koonin EV, van Der Oost J (2008) Small CRISPR RNAs guide antiviral defense in prokaryotes. Science 321(5891): 960-964.
10. Cady KC, Bondy-Denomy J, Heussler GE, Davidson AR, O'Toole GA (2012) The CRISPR/Cas adaptive immune system of Pseudomonas aeruginosa mediates resistance to naturally occurring and engineered phages. J Bacteriol 194(21): 5728-5738.
11. Carroll D (2012) A CRISPR approach to gene targeting. Mol Ther 20(9): 1658-1660.
12. Carroll D (2013) Staying on target with CRISPR-Cas. Nat Biotechnol 31(9): 807-809.
13. Carte J, Wang R, Li H, Terns RM, Terns MP (2008) Cas6 is an endoribonuclease that generates guide RNAs for invader defense in prokaryotes. Genes Dev 22(24): 3489-3496.
14. Carte J, Pfister NT, Compton MM, Terns RM, Terns MP (2010) Binding and cleavage of CRISPR RNA by Cas6. RNA 16(11): 2181-2188.
15. Chang N, Sun C, Gao L, Zhu D, Xu X, Zhu X, Xiong JW, Xi JJ (2013) Genome editing with RNA-guided Cas9 nuclease in zebrafish embryos. Cell Res 23(4): 465-472. doi: 10. 1038/cr. 2013. 45.
16. Charpentier E, Doudna JA (2013) Biotechnology: rewriting a genome. Nature 495(7439): 50-51.
17. Cho SW, Kim S, Kim JM, Kim J-S (2013) Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease. Nat Biotechnol 31: 230-232.
18. Chylinski K, Le Rhun A, Charpentier E (2013) The tracrRNA and Cas9 families of type II CRISPR-Cas immunity systems. RNA Biol 10(5): 726-737. doi: 10. 4161/rna. 24321.
19. Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA, Zhang F (2013) Multiplex genome engineering using CRISPR/Cas systems. Science 339(6121): 819-823.
20. Datsenko KA, Pougach K, Tikhonov A, Wanner BL, Severinov K, Semenova E (2012) Molecular memory of prior infections activates the CRISPR/Cas adaptive bacterial immunity system. Nat Commun 3: 945.
21. Deltcheva E, Chylinski K, Sharma CM, Gonzales K, Chao Y, Pirzada ZA, Eckert MR, Vogel J, Charpentier E (2011) CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature 471(7340): 602-607. doi: 10. 1038/nature09886.
22. Deveau H, Barrangou R, Garneau JE, Labonte J, Fremaux C, Boyaval P, Romero DA, Horvath P, Moineau S (2008) Phage response to CRISPR-encoded resistance in Streptococcus thermophilus. J Bacteriol 190(4): 1390-1400. doi: 10. 1128/JB. 01412-07.
23. Deveau H, Garneau JE, Moineau S (2010) CRISPR/Cas system and its role in phage-bacteria interactions. Annu Rev Microbiol 64: 475-493.
24. DiCarlo JE, Norville JE, Mali P, Rios X, Aach J, Church GM (2013) Genome engineering in Saccharomyces cerevisiae using CRISPR-Cas systems. Nucleic Acids Res 41(7): 4336-4343. doi: 10. 1093/nar/gkt135.
25. Dickinson DJ, Ward JD, Reiner DJ, Goldstein B (2013) Engineering the Caenorhabditis elegans genome using Cas9-triggered homologous recombination. Nat Methods 10(10): 1028-1034.
26. Echeverri CJ, Beachy PA, Baum B, Boutros M, Buchholz F, Chanda SK, Downward J, Ellenberg J, Fraser AG, Hacohen N (2006) Minimizing the risk of reporting false positives in large-scale RNAi screens. Nat Methods 3(10): 777-779.
27. Feng Z, Zhang B, Ding W, Liu X, Yang DL, Wei P, Cao F, Zhu S, Zhang F, Mao Y, Zhu JK (2013) Efficient genome editing in plants using a CRISPR/Cas system. Cell Res 23(10): 1229-1232.
28. Feng Z, Mao Y, Xu N, Zhang B, Wei P, Yang DL, Wang Z, Zhang Z, Zheng R, Yang L, Zeng L, Liu X, Zhu JK (2014) Multigeneration analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas-induced gene modifications in Arabidopsis. Proc Natl Acad Sci USA. doi: 10. 1073/pnas. 1400822111.
29. Fonfara I, Le Rhun A, Chylinski K, Makarova KS, Lecrivain AL, Bzdrenga J, Koonin EV, Charpentier E (2013) Phylogeny of Cas9 determines functional exchangeability of dual-RNA and Cas9 among orthologous type II CRISPR-Cas systems. Nucleic Acids Res. doi: 10. 1093/nar/gkt1074.
30. Friedland AE, Tzur YB, Esvelt KM, Colaiácovo MP, Church GM, Calarco JA (2013) Heritable genome editing in C. elegans via a CRISPR-Cas9 system. Nat Methods 10(8): 741-743.
31. Fu Y, Foden JA, Khayter C, Maeder ML, Reyon D, Joung JK, Sander JD (2013) High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat Biotechnol 31(9): 822-826. doi: 10. 1038/nbt. 2623.
32. Gaj T, Gersbach CA, Barbas CF 3rd (2013) ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol 31(7): 397-405. doi: 10. 1016/j. tibtech. 2013. 04. 004.
33. Garneau JE, Dupuis ME, Villion M, Romero DA, Barrangou R, Boyaval P, Fremaux C, Horvath P, Magadan AH, Moineau S (2010) The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature 468(7320): 67-71. doi: 10. 1038/nature09523.
34. Garside EL, Schellenberg MJ, Gesner EM, Bonanno JB, Sauder JM, Burley SK, Almo SC, Mehta G, MacMillan AM (2012) Cas5d processes pre-crRNA and is a member of a larger family of CRISPR RNA endonucleases. RNA 18(11): 2020-2028.
35. Gasiunas G, Barrangou R, Horvath P, Siksnys V (2012) Cas9-crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. Proc Natl Acad Sci 109(39): E2579-E2586.
36. Gesner EM, Schellenberg MJ, Garside EL, George MM, MacMillan AM (2011) Recognition and maturation of effector RNAs in a CRISPR interference pathway. Nat Struct Mol Biol 18(6): 688-692.
37. Gilbert LA, Larson MH, Morsut L, Liu Z, Brar GA, Torres SE, Stern-Ginossar N, Brandman O, Whitehead EH, Doudna JA, Lim WA, Weissman JS, Qi LS (2013) CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell 154(2): 442-451. doi: 10. 1016/j. cell. 2013. 06. 044.
38. Hale CR, Zhao P, Olson S, Duff MO, Graveley BR, Wells L, Terns RM, Terns MP (2009) RNA-guided RNA cleavage by a CRISPR RNA-Cas protein complex. Cell 139(5): 945-956. doi: 10. 1016/j. cell. 2009. 07. 040.
39. Hannon GJ (2002) RNA interference. Nature 418(6894): 244-251.
40. Hatoum-Aslan A, Maniv I, Marraffini LA (2011) Mature clustered, regularly interspaced, short palindromic repeats RNA (crRNA) length is measured by a ruler mechanism anchored at the precursor processing site. Proc Natl Acad Sci 108(52): 21218-21222.
41. Haurwitz RE, Jinek M, Wiedenheft B, Zhou K, Doudna JA (2010) Sequence- and structure-specific RNA processing by a CRISPR endonuclease. Science 329(5997): 1355-1358. doi: 10. 1126/science. 1192272.
42. Hockemeyer D, Wang H, Kiani S, Lai CS, Gao Q, Cassady JP, Cost GJ, Zhang L, Santiago Y, Miller JC (2011) Genetic engineering of human pluripotent cells using TALE nucleases. Nat Biotechnol 29(8): 731-734.
43. Horvath P, Barrangou R (2010) CRISPR/Cas, the immune system of bacteria and archaea. Science 327(5962): 167-170.
44. Hruscha A, Krawitz P, Rechenberg A, Heinrich V, Hecht J, Haass C, Schmid B (2013) Efficient CRISPR/Cas9 genome editing with low off-target effects in zebrafish. Development 140(24): 4982-4987.
45. Hsu PD, Scott DA, Weinstein JA, Ran FA, Konermann S, Agarwala V, Li Y, Fine EJ, Wu X, Shalem O, Cradick TJ, Marraffini LA, Bao G, Zhang F (2013) DNA targeting specificity of RNA-guided Cas9 nucleases. Nat Biotechnol 31(9): 827-832. doi: 10. 1038/nbt. 2647.
46. Hwang WY, Fu Y, Reyon D, Maeder ML, Tsai SQ, Sander JD, Peterson RT, Yeh JJ, Joung JK (2013) Efficient genome editing in zebrafish using a CRISPR-Cas system. Nat Biotechnol 31(3): 227-229.
47. Ishino Y, Shinagawa H, Makino K, Amemura M, Nakata A (1987) Nucleotide sequence of the iap gene, responsible for alkaline phosphatase isozyme conversion in Escherichia coli, and identification of the gene product. J Bacteriol 169(12): 5429-5433.
48. Jao L-E, Wente SR, Chen W (2013) Efficient multiplex biallelic zebrafish genome editing using a CRISPR nuclease system. Proc Natl Acad Sci 110(34): 13904-13909.
49. Jiang W, Bikard D, Cox D, Zhang F, Marraffini LA (2013a) RNA-guided editing of bacterial genomes using CRISPR-Cas systems. Nat Biotechnol 31(3): 233-239. doi: 10. 1038/nbt. 2508.
50. Jiang W, Zhou H, Bi H, Fromm M, Yang B, Weeks DP (2013b) Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice. Nucleic Acids Res 41(20): e188. doi: 10. 1093/nar/gkt780.
51. Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337(6096): 816-821.
52. Jinek M, East A, Cheng A, Lin S, Ma E, Doudna J (2013) RNA-programmed genome editing in human cells. Elife 2: e00471.
53. Jinek M, Jiang F, Taylor DW, Sternberg SH, Kaya E, Ma E, Anders C, Hauer M, Zhou K, Lin S, Kaplan M, Iavarone AT, Charpentier E, Nogales E, Doudna JA (2014) Structures of Cas9 endonucleases reveal RNA-mediated conformational activation. Science (New York, NY).
54. Jore MM, Lundgren M, van Duijn E, Bultema JB, Westra ER, Waghmare SP, Wiedenheft B, Pul Ü, Wurm R, Wagner R (2011) Structural basis for CRISPR RNA-guided DNA recognition by Cascade. Nat Struct Mol Biol 18(5): 529-536.
55. Joung JK, Sander JD (2012) TALENs: a widely applicable technology for targeted genome editing. Nat Rev Mol Cell Biol 14(1): 49-55.
56. Kaelin WG (2012) Use and abuse of RNAi to study mammalian gene function. Science 337(6093): 421-422.
57. Klug A (2010) The discovery of zinc fingers and their applications in gene regulation and genome manipulation. Annu Rev Biochem 79: 213-231.
58. Koonin EV, Makarova KS (2009) CRISPR-Cas: an adaptive immunity system in prokaryotes. F1000 biology reports 1: 95.
59. Larson MH, Gilbert LA, Wang X, Lim WA, Weissman JS, Qi LS (2013) CRISPR interference (CRISPRi) for sequence-specific control of gene expression. Nat Protoc 8(11): 2180-2196. doi: 10. 1038/nprot. 2013. 132.
60. Li T, Liu B, Spalding MH, Weeks DP, Yang B (2012) High-efficiency TALEN-based gene editing produces disease-resistant rice. Nat Biotechnol 30(5): 390-392.
61. Li D, Qiu Z, Shao Y, Chen Y, Guan Y, Liu M, Li Y, Gao N, Wang L, Lu X (2013a) Heritable gene targeting in the mouse and rat using a CRISPR-Cas system. Nat Biotechnol 31(8): 681-683.
62. Li JF, Norville JE, Aach J, McCormack M, Zhang D, Bush J, Church GM, Sheen J (2013b) Multiplex and homologous recombination-mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nat Biotechnol 31: 688-691. doi: 10. 1038/nbt. 265010. 1038/nbt. 2623.
63. Li W, Teng F, Li T, Zhou Q (2013c) Simultaneous generation and germline transmission of multiple gene mutations in rat using CRISPR-Cas systems. Nat Biotechnol 31(8): 684-686.
64. Lopez-Sanchez MJ, Sauvage E, Da Cunha V, Clermont D, Ratsima Hariniaina E, Gonzalez-Zorn B, Poyart C, Rosinski-Chupin I, Glaser P (2012) The highly dynamic CRISPR1 system of Streptococcus agalactiae controls the diversity of its mobilome. Mol Microbiol 85(6): 1057-1071.
65. Makarova KS, Grishin NV, Shabalina SA, Wolf YI, Koonin EV (2006) A putative RNA-interference-based immune system in prokaryotes: computational analysis of the predicted enzymatic machinery, functional analogies with eukaryotic RNAi, and hypothetical mechanisms of action. Biol Direct 1(1): 7.
66. Makarova KS, Haft DH, Barrangou R, Brouns SJ, Charpentier E, Horvath P, Moineau S, Mojica FJ, Wolf YI, Yakunin AF (2011) Evolution and classification of the CRISPR-Cas systems. Nat Rev Microbiol 9(6): 467-477. doi: 10. 1038/nrmicro2577.
67. Mali P, Aach J, Stranges PB, Esvelt KM, Moosburner M, Kosuri S, Yang L, Church GM (2013a) CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering. Nat Biotechnol 31(9): 833-838. doi: 10. 1038/nbt. 2675.
68. Mali P, Esvelt KM, Church GM (2013b) Cas9 as a versatile tool for engineering biology. Nat Methods 10(10): 957-963. doi: 10. 1038/nmeth. 2649.
69. Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, Norville JE, Church GM (2013c) RNA-guided human genome engineering via Cas9. Science 339(6121): 823-826.
70. Marraffini LA, Sontheimer EJ (2008) CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science 322(5909): 1843-1845.
71. Marraffini LA, Sontheimer EJ (2010a) CRISPR interference: RNA-directed adaptive immunity in bacteria and archaea. Nat Rev Genet 11(3): 181-190. doi: 10. 1038/nrg2749.
72. Marraffini LA, Sontheimer EJ (2010b) Self versus non-self discrimination during CRISPR RNA-directed immunity. Nature 463(7280): 568-571.
73. Marx J (2007) New bacterial defense against phage invaders identified. Science 315(5819): 1650-1651.
74. Miao J, Guo D, Zhang J, Huang Q, Qin G, Zhang X, Wan J, Gu H, Qu LJ (2013) Targeted mutagenesis in rice using CRISPR-Cas system. Cell Res 23(10): 1233-1236. doi: 10. 1038/cr. 2013. 123.
75. Mojica FJ, García-Martínez J, Soria E (2005) Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. J Mol Evol 60(2): 174-182.
76. Moscou MJ, Bogdanove AJ (2009) A simple cipher governs DNA recognition by TAL effectors. Science 326(5959): 1501.
77. Mulepati S, Bailey S (2011) Structural and biochemical analysis of nuclease domain of clustered regularly interspaced short palindromic repeat (CRISPR)-associated protein 3 (Cas3). J Biol Chem 286(36): 31896-31903.
78. Mussolino C, Cathomen T (2013) RNA guides genome engineering. Nat Biotechnol 31(3): 208-209.
79. Nekrasov V, Staskawicz B, Weigel D, Jones JD, Kamoun S (2013) Targeted mutagenesis in the model plant Nicotiana benthamiana using Cas9 RNA-guided endonuclease. Nat Biotechnol 31(8): 691-693.
80. Pattanayak V, Lin S, Guilinger JP, Ma E, Doudna JA, Liu DR (2013) High-throughput profiling of off-target DNA cleavage reveals RNA-programmed Cas9 nuclease specificity. Nat Biotechnol 31(9): 839-843. doi: 10. 1038/nbt. 2673.
81. Pennisi E (2013) The CRISPR craze. Science 341: 833-836.
82. Pourcel C, Salvignol G, Vergnaud G (2005) CRISPR elements in Yersinia pestis acquire new repeats by preferential uptake of bacteriophage DNA, and provide additional tools for evolutionary studies. Microbiology 151(3): 653-663.
83. 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(5): 1173-1183. doi: 10. 1016/j. cell. 2013. 02. 022.
84. Ran FA, Hsu PD, Lin CY, Gootenberg JS, Konermann S, Trevino AE, Scott DA, Inoue A, Matoba S, Zhang Y, Zhang F (2013a) Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154(6): 1380-1389. doi: 10. 1016/j. cell. 2013. 08. 021.
85. Ran FA, Hsu PD, Wright J, Agarwala V, Scott DA, Zhang F (2013b) Genome engineering using the CRISPR-Cas9 system. Nat Protoc 8(11): 2281-2308. doi: 10. 1038/nprot. 2013. 143.
86. Rusk N (2014) CRISPRs and epigenome editing. Nat Methods 11(1): 28.
87. Sapranauskas R, Gasiunas G, Fremaux C, Barrangou R, Horvath P, Siksnys V (2011) The Streptococcus thermophilus CRISPR/Cas system provides immunity in Escherichia coli. Nucleic Acids Res 39(21): 9275-9282.
88. Sashital DG, Jinek M, Doudna JA (2011) An RNA-induced conformational change required for CRISPR RNA cleavage by the endoribonuclease Cse3. Nat Struct Mol Biol 18(6): 680-687.
89. Shalem O, Sanjana NE, Hartenian E, Shi X, Scott DA, Mikkelson T, Heckl D, Ebert BL, Root DE, Doench JG, Zhang F (2013) Genome-scale CRISPR-Cas9 knockout screening in human cells. Science 303: 84-87.
90. Shan Q, Wang Y, Chen K, Liang Z, Li J, Zhang Y, Zhang K, Liu J, Voytas DF, Zheng X (2013a) Rapid and efficient gene modification in rice and Brachypodium using TALENs. Molecular plant 6(4): 1365-1368.
91. Shan Q, Wang Y, Li J, Zhang Y, Chen K, Liang Z, Zhang K, Liu J, Xi JJ, Qiu J-L (2013b) Targeted genome modification of crop plants using a CRISPR-Cas system. Nat Biotechnol 31(8): 686-688.
92. Shen B, Zhang J, Wu H, Wang J, Ma K, Li Z, Zhang X, Zhang P, Huang X (2013) Generation of gene-modified mice via Cas9/RNA-mediated gene targeting. Cell Res 23: 720-723.
93. Sinkunas T, Gasiunas G, Fremaux C, Barrangou R, Horvath P, Siksnys V (2011) Cas3 is a single-stranded DNA nuclease and ATP-dependent helicase in the CRISPR/Cas immune system. EMBO J 30(7): 1335-1342.
94. Sontheimer EJ, Marraffini LA (2010) Microbiology: slicer for DNA. Nature 468(7320): 45-46.
95. Sorek R, Kunin V, Hugenholtz P (2008) CRISPR-a widespread system that provides acquired resistance against phages in bacteria and archaea. Nat Rev Microbiol 6(3): 181-186.
96. Streubel J, Blücher C, Landgraf A, Boch J (2012) TAL effector RVD specificities and efficiencies. Nat Biotechnol 30(7): 593-595.
97. Swarts DC, Mosterd C, van Passel MW, Brouns SJ (2012) CRISPR interference directs strand specific spacer acquisition. PLoS One 7(4): e35888.
98. Terns MP, Terns RM (2011) CRISPR-based adaptive immune systems. Curr Opin Microbiol 14(3): 321-327.
99. van der Oost J, Jore MM, Westra ER, Lundgren M, Brouns SJ (2009) CRISPR-based adaptive and heritable immunity in prokaryotes. Trends Biochem Sci 34(8): 401-407.
100. Wang H, Yang H, Shivalila CS, Dawlaty MM, Cheng AW, Zhang F, Jaenisch R (2013a) One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell 153(4): 910-918. doi: 10. 1016/j. cell. 2013. 04. 025.
101. Wang T, Wei JJ, Sabatini DM, Lander ES (2013b) Genetic screens in human cells using the CRISPR/Cas9 system. Science 303: 80-84.
102. Waters LS, Storz G (2009) Regulatory RNAs in bacteria. Cell 136(4): 615-628.
103. Weinthal D, Tovkach A, Zeevi V, Tzfira T (2010) Genome editing in plant cells by zinc finger nucleases. Trends Plant Sci 15(6): 308-321.
104. Wiedenheft B, Lander GC, Zhou K, Jore MM, Brouns SJ, van der Oost J, Doudna JA, Nogales E (2011a) Structures of the RNA-guided surveillance complex from a bacterial immune system. Nature 477(7365): 486-489.
105. Wiedenheft B, van Duijn E, Bultema JB, Waghmare SP, Zhou K, Barendregt A, Westphal W, Heck AJ, Boekema EJ, Dickman MJ (2011b) RNA-guided complex from a bacterial immune system enhances target recognition through seed sequence interactions. Proc Natl Acad Sci 108(25): 10092-10097.
106. Wiedenheft B, Sternberg SH, Doudna JA (2012) RNA-guided genetic silencing systems in bacteria and archaea. Nature 482(7385): 331-338. doi: 10. 1038/nature10886.
107. Wu Y, Liang D, Wang Y, Bai M, Tang W, Bao S, Yan Z, Li D, Li J (2013) Correction of a genetic disease in mouse via use of CRISPR-Cas9. Cell Stem Cell 13(6): 659-662. doi: 10. 1016/j. stem. 2013. 10. 016.
108. Yang H, Wang H, Shivalila CS, Cheng AW, Shi L, Jaenisch R (2013) One-step generation of mice carrying reporter and conditional alleles by CRISPR/Cas-mediated genome engineering. Cell 154(6): 1370-1379. doi: 10. 1016/j. cell. 2013. 08. 022.
109. Yosef I, Goren MG, Qimron U (2012) Proteins and DNA elements essential for the CRISPR adaptation process in Escherichia coli. Nucleic Acids Res 40(12): 5569-5576.
110. Yu Z, Ren M, Wang Z, Zhang B, Rong YS, Jiao R, Gao G (2013) Highly efficient genome modifications mediated by CRISPR/Cas9 in Drosophila. Genetics 195(1): 289-291.
111. Zhang F, Maeder ML, Unger-Wallace E, Hoshaw JP, Reyon D, Christian M, Li X, Pierick CJ, Dobbs D, Peterson T (2010) High frequency targeted mutagenesis in Arabidopsis thaliana using zinc finger nucleases. Proc Natl Acad Sci 107(26): 12028-12033.
112. Zhang Y, Heidrich N, Ampattu BJ, Gunderson CW, Seifert HS, Schoen C, Vogel J, Sontheimer EJ (2013a) Processing-independent CRISPR RNAs limit natural transformation in Neisseria meningitidis. Mol Cell 50(4): 488-503.
113. Zhang Y, Zhang F, Li X, Baller JA, Qi Y, Starker CG, Bogdanove AJ, Voytas DF (2013b) Transcription activator-like effector nucleases enable efficient plant genome engineering. Plant Physiol 161(1): 20-27.