Genome modification by CRISPR/Cas9

FEBS Journal

Volumn 281, Issue 23, 2014, Pages 5186-5193

  Ma, Yuanwu ^a   Zhang, Lianfeng ^a   Huang, Xingxu ^b  

^a INSTITUTE OF LABORATORY ANIMAL SCIENCE   (China)

^b NANJING UNIVERSITY   (China)

Author keywords

Cas9; CRISPR; Gene targeting; Genome editing; SgRNA

Indexed keywords

CRISPR ASSOCIATED PROTEIN; CRISPR ASSOCIATED PROTEIN 9; UNCLASSIFIED DRUG;

ANIMAL BEHAVIOR; CRISPR CAS SYSTEM; DNA END JOINING REPAIR; DNA MODIFICATION; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE LOCUS; GENE MUTATION; GENE REPRESSION; GENETIC ANALYSIS; GENETIC ENGINEERING; HUMAN; NONHUMAN; PROTEIN DOMAIN; REVIEW; RNA EDITING; SEQUENCE ANALYSIS; ANIMAL; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; PHYSIOLOGY;

ANIMALS; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; CRISPR-ASSOCIATED PROTEINS; GENETIC ENGINEERING; HUMANS; RNA EDITING;

EID: 84915745361     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.13110     Document Type: Review

References (63)

1. Kim H & Kim JS (2014) A guide to genome engineering with programmable nucleases. Nat Rev Genet 15, 321-334.
2. 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, 816-821.
3. Mali P, Aach J, Stranges PB, Esvelt KM, Moosburner M, Kosuri S, Yang L & Church GM (2013) CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering. Nat Biotechnol 31, 833-838.
4. Jinek M, Jiang F, Taylor DW, Sternberg SH, Kaya E, Ma E, Anders C, Hauer M, Zhou K, Lin S et al. (2014) Structures of Cas9 endonucleases reveal RNA-mediated conformational activation. Science 343, 1247997.
5. Nishimasu H, Ran FA, Hsu PD, Konermann S, Shehata SI, Dohmae N, Ishitani R, Zhang F & Nureki O (2014) Crystal structure of Cas9 in complex with guide RNA and target DNA. Cell 156, 935-949.
6. Jinek M, East A, Cheng A, Lin S, Ma E & Doudna J (2013) RNA-programmed genome editing in human cells. Elife 2, e00471.
7. Shen B, Zhang J, Wu H, Wang J, Ma K, Li Z, Zhang X, Zhang P & Huang X (2013) Generation of genemodified mice via Cas9/RNA-mediated gene targeting. Cell Res 23, 720-723.
8. Li D, Qiu Z, Shao Y, Chen Y, Guan Y, Liu M, Li Y, Gao N, Wang L, Lu X et al. (2013) Heritable gene targeting in the mouse and rat using a CRISPR-Cas system. Nat Biotechnol 31, 681-683.
9. Jiang W, Bikard D, Cox D, Zhang F & Marraffini LA (2013) RNA-guided editing of bacterial genomes using CRISPR-Cas systems. Nat Biotechnol 31, 233-239.
10. 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, 4336-4343.
11. Li JF, Norville JE, Aach J, McCormack M, Zhang D, Bush J, Church GM & Sheen J (2013) Multiplex and homologous recombination-mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nat Biotechnol 31, 688-691.
12. 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, 691-693.
13. Shan Q, Wang Y, Li J, Zhang Y, Chen K, Liang Z, Zhang K, Liu J, Xi JJ, Qiu JL et al. (2013) Targeted genome modification of crop plants using a CRISPRCas system. Nat Biotechnol 31, 686-688.
14. Friedland AE, Tzur YB, Esvelt KM, Colaiacovo MP, Church GM & Calarco JA (2013) Heritable genome editing in C. elegans via a CRISPR-Cas9 system. Nat Methods 10, 741-743.
15. Wang Y, Li Z, Xu J, Zeng B, Ling L, You L, Chen Y, Huang Y & Tan A (2013) The CRISPR/Cas System mediates efficient genome engineering in Bombyx mori. Cell Res 23, 1414-1416.
16. Bassett AR, Tibbit C, Ponting CP & Liu JL (2013) Highly efficient targeted mutagenesis of Drosophila with the CRISPR/Cas9 system. Cell Rep 4, 220-228.
17. Hwang WY, Fu Y, Reyon D, Maeder ML, Tsai SQ, Sander JD, Peterson RT, Yeh JR & Joung JK (2013) Efficient genome editing in zebrafish using a CRISPRCas system. Nat Biotechnol 31, 227-229.
18. Nakayama T, Fish MB, Fisher M, Oomen-Hajagos J, Thomsen GH & Grainger RM (2013) Simple and efficient CRISPR/Cas9-mediated targeted mutagenesis in Xenopus tropicalis. Genesis 51, 835-843.
19. Yang D, Xu J, Zhu T, Fan J, Lai L, Zhang J & Chen YE (2014) Effective gene targeting in rabbits using RNA-guided Cas9 nucleases. J Mol Cell Biol 6, 97-99.
20. Wang H, Yang H, Shivalila CS, Dawlaty MM, Cheng AW, Zhang F & Jaenisch R (2013) One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell 153, 910-918.
21. Li W, Teng F, Li T & Zhou Q (2013) Simultaneous generation and germline transmission of multiple gene mutations in rat using CRISPR-Cas systems. Nat Biotechnol 31, 684-686.
22. Hai T, Teng F, Guo R, Li W & Zhou Q (2014) Onestep generation of knockout pigs by zygote injection of CRISPR/Cas system. Cell Res 24, 372-375.
23. Niu Y, Shen B, Cui Y, Chen Y, Wang J, Wang L, Kang Y, Zhao X, Si W, Li W et al. (2014) Generation of gene-modified cynomolgus monkey via Cas9/RNAmediated gene targeting in one-cell embryos. Cell 156, 836-843.
24. 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.
25. 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.
26. Cho SW, Kim S, Kim JM & Kim JS (2013) Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease. Nat Biotechnol 31, 230-232.
27. Ma Y, Shen B, Zhang X, Lu Y, Chen W, Ma J, Huang X & Zhang L (2014) Heritable multiplex genetic engineering in rats using CRISPR/Cas9. PLoS One 9, e89413.
28. Zhou J, Shen B, Zhang W, Wang J, Yang J, Chen L, Zhang N, Zhu K, Xu J, Hu B et al. (2014) One-step generation of different immunodeficient mice with multiple gene modifications by CRISPR/Cas9 mediated genome engineering. Int J Biochem Cell Biol 46, 49-55.
29. Jao LE, Wente SR & Chen W (2013) Efficient multiplex biallelic zebrafish genome editing using a CRISPR nuclease system. Proc Natl Acad Sci U S A 110, 13904-13909.
30. Xiao A, Wang Z, Hu Y, Wu Y, Luo Z, Yang Z, Zu Y, Li W, Huang P, Tong X et al. (2013) Chromosomal deletions and inversions mediated by TALENs and CRISPR/Cas in zebrafish. Nucleic Acids Res 41, e141.
31. 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/Casmediated genome engineering. Cell 154, 1370-1379.
32. Ma Y, Zhang X, Shen B, Lu Y, Chen W, Ma J, Bai L, Huang X & Zhang L (2014) Generating rats with conditional alleles using CRISPR/Cas9. Cell Res 24, 122-125.
33. Ma Y, Ma J, Zhang X, Chen W, Yu L, Lu Y, Bai L, Shen B, Huang X & Zhang L (2014) Generation of eGFP and Cre knockin rats by CRISPR/Cas9. FEBS J 281, 3779-3790.
34. 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, 465-472.
35. 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.
36. 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 CRISPRguide RNA library. Nat Biotechnol 32, 267-273.
37. Wang T, Wei JJ, Sabatini DM & Lander ES (2014) Genetic screens in human cells using the CRISPR-Cas9 system. Science 343, 80-84.
38. Gilbert LA, Larson MH, Morsut L, Liu Z, Brar GA, Torres SE, Stern-Ginossar N, Brandman O, Whitehead EH, Doudna JA et al. (2013) CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell 154, 442-451.
39. Konermann S, Brigham MD, Trevino AE, Hsu PD, Heidenreich M, Cong L, Platt RJ, Scott DA, Church GM & Zhang F (2013) Optical control of mammalian endogenous transcription and epigenetic states. Nature 500, 472-476.
40. 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, 659-662.
41. Schwank G, Koo BK, Sasselli V, Dekkers JF, Heo I, Demircan T, Sasaki N, Boymans S, Cuppen E, van der Ent CK et al. (2013) Functional repair of CFTR by CRISPR/Cas9 in intestinal stem cell organoids of cystic fibrosis patients. Cell Stem Cell 13, 653-658.
42. Yin H, Xue W, Chen S, Bogorad RL, Benedetti E, Grompe M, Koteliansky V, Sharp PA, Jacks T & Anderson DG (2014) Genome editing with Cas9 in adult mice corrects a disease mutation and phenotype. Nat Biotechnol 32, 551-553.
43. Sung YH, Kim JM, Kim HT, Lee J, Jeon J, Jin Y, Choi JH, Ban YH, Ha SJ, Kim CH et al. (2014) Highly efficient gene knockout in mice and zebrafish with RNA-guided endonucleases. Genome Res 24, 125-131.
44. Jiang W, Zhou H, Bi H, Fromm M, Yang B & Weeks DP (2013) Demonstration of CRISPR/Cas9/sgRNAmediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice. Nucleic Acids Res 41, e188.
45. Tsai SQ, Wyvekens N, Khayter C, Foden JA, Thapar V, Reyon D, Goodwin MJ, Aryee MJ & Joung JK (2014) Dimeric CRISPR RNA-guided FokI nucleases for highly specific genome editing. Nat Biotechnol 32, 569-576.
46. Fu Y, Foden JA, Khayter C, Maeder ML, Reyon D, Joung JK & Sander JD (2013) High-frequency offtarget mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat Biotechnol 31, 822-826.
47. Fu Y, Sander JD, Reyon D, Cascio VM & Joung JK (2014) Improving CRISPR-Cas nuclease specificity using truncated guide RNAs. Nat Biotechnol 32, 279-284.
48. Guilinger JP, Thompson DB & Liu DR (2014) Fusion of catalytically inactive Cas9 to FokI nuclease improves the specificity of genome modification. Nat Biotechnol 32, 577-582.
49. Cho SW, Kim S, Kim Y, Kweon J, Kim HS, Bae S & Kim JS (2013) Analysis of off-target effects of CRISPR/Cas-derived RNA-guided endonucleases and nickases. Genome Res 24, 132-141.
50. Shen B, Zhang W, Zhang J, Zhou J, Wang J, Chen L, Wang L, Hodgkins A, Iyer V, Huang X et al. (2014) Efficient genome modification by CRISPR-Cas9 nickase with minimal off-target effects. Nat Methods 11, 399-402.
51. Montague TG, Cruz JM, Gagnon JA, Church GM & Valen E (2014) CHOPCHOP: a CRISPR/Cas9 and TALEN web tool for genome editing. Nucleic Acids Res 42, W401-W407.
52. O'Brien A & Bailey TL (2014) GT-Scan: identifying unique genomic targets. Bioinformatics 30, 2673-2675.
53. Lin Y, Cradick TJ, Brown MT, Deshmukh H, Ranjan P, Sarode N, Wile BM, Vertino PM, Stewart FJ & Bao G (2014) CRISPR/Cas9 systems have off-target activity with insertions or deletions between target DNA and guide RNA sequences. Nucleic Acids Res 42, 7473-7485.
54. Pattanayak V, Lin S, Guilinger JP, Ma E, Doudna JA & Liu DR (2013) High-throughput profiling of offtarget DNA cleavage reveals RNA-programmed Cas9 nuclease specificity. Nat Biotechnol 31, 839-843.
55. Hsu PD, Scott DA, Weinstein JA, Ran FA, Konermann S, Agarwala V, Li Y, Fine EJ, Wu X, Shalem O et al. (2013) DNA targeting specificity of RNA-guided Cas9 nucleases. Nat Biotechnol 31, 827-832.
56. Cho SW, Kim S, Kim Y, Kweon J, Kim HS, Bae S & Kim JS (2014) Analysis of off-target effects of CRISPR/Cas-derived RNA-guided endonucleases and nickases. Genome Res 24, 132-141.
57. Ran FA, Hsu PD, Lin CY, Gootenberg JS, Konermann S, Trevino AE, Scott DA, Inoue A, Matoba S, Zhang Y et al. (2013) Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154, 1380-1389.
58. Sander JD & Joung JK (2014) CRISPR-Cas systems for editing, regulating and targeting genomes. Nat Biotechnol 32, 347-355.
59. 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.
60. 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.
61. Cheng AW, Wang H, Yang H, Shi L, Katz Y, Theunissen TW, Rangarajan S, Shivalila CS, Dadon DB & Jaenisch R (2013) Multiplexed activation of endogenous genes by CRISPR-on, an RNA-guided transcriptional activator system. Cell Res 23, 1163-1171.
62. Mendenhall EM, Williamson KE, Reyon D, Zou JY, Ram O, Joung JK & Bernstein BE (2013) Locusspecific editing of histone modifications at endogenous enhancers. Nat Biotechnol 31, 1133-1136.
63. Chen B, Gilbert LA, Cimini BA, Schnitzbauer J, Zhang W, Li GW, Park J, Blackburn EH, Weissman JS, Qi LS et al. (2013) Dynamic imaging of genomic loci in living human cells by an optimized CRISPR/Cas system. Cell 155, 1479-1491.