Application of CRISPR/Cas9 for biomedical discoveries

Cell and Bioscience

Volumn 5, Issue 1, 2015, Pages

  Riordan, Sean M ^a   Heruth, Daniel P ^a   Zhang, Li Q ^a   Ye, Shui Qing ^a,b  

^a CHILDREN S MERCY HOSPITAL   (United States)

^b UNIVERSITY OF MISSOURI KANSAS CITY SCHOOL OF MEDICINE   (United States)

Author keywords

Animal model; Cas9; CRISPR; Genome editing

Indexed keywords

ANIMALIA;

EID: 84938998615     PISSN: None     EISSN: 20453701     Source Type: Journal    
DOI: 10.1186/s13578-015-0027-9     Document Type: Review

References (110)

1. Bibikova M, Carroll D, Segal DJ, Trautman JK, Smith J, Kim YG, et al. Stimulation of homologous recombination through targeted cleavage by chimeric nucleases. Mol Cell Biol. 2001;21(1):289-97. doi: 10.1128/mcb.21.1.289-297.2001.
2. Urnov FD, Miller JC, Lee YL, Beausejour CM, Rock JM, Augustus S, et al. Highly efficient endogenous human gene correction using designed zinc-finger nucleases. Nature. 2005;435(7042):646-51. doi: 10.1038/nature03556.
3. Durai S, Mani M, Kandavelou K, Wu J, Porteus MH, Chandrasegaran S. Zinc finger nucleases: custom-designed molecular scissors for genome engineering of plant and mammalian cells. Nucleic Acids Res. 2005;33(18):5978-90. doi: 10.1093/nar/gki912.
4. Kim YG, Cha J, Chandrasegaran S. Hybrid restriction enzymes: zinc finger fusions to Fok I cleavage domain. Proc Natl Acad Sci. 1996;93(3):1156-60.
5. Rouet P, Smih F, Jasin M. Introduction of double-strand breaks into the genome of mouse cells by expression of a rare-cutting endonuclease. Mol Cell Biol. 1994;14(12):8096-106.
6. Pâques F, Duchateau P. Meganucleases and DNA double-strand break-induced recombination: perspectives for gene therapy. Curr Gene Ther. 2007;7(1):49-66.
7. Boch J, Scholze H, Schornack S, Landgraf A, Hahn S, Kay S, et al. Breaking the code of DNA binding specificity of TAL-type III effectors. Science. 2009;326(5959):1509-12. doi: 10.1126/science.1178811.
8. Christian M, Cermak T, Doyle EL, Schmidt C, Zhang F, Hummel A, et al. Targeting DNA Double-Strand Breaks with TAL Effector Nucleases. Genetics. 2010;186(2):757-61. doi: 10.1534/genetics.110.120717.
9. Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, Moineau S, et al. CRISPR provides acquired resistance against viruses in prokaryotes. Science. 2007;315(5819):1709-12. doi: 10.1126/science.1138140.
10. Capecchi MR. Altering the genome by homologous recombination. Science. 1989;244(4910):1288-92.
11. Shalem O, Sanjana NE, Hartenian E, Shi X, Scott DA, Mikkelsen TS, et al. Genome-scale CRISPR-Cas9 knockout screening in human cells. Science. 2014;343(6166):84-7. doi: 10.1126/science.1247005.
12. Wang T, Wei JJ, Sabatini DM, Lander ES. Genetic screens in human cells using the CRISPR-Cas9 system. Science. 2014;343(6166):80-4. doi: 10.1126/science.1246981.
13. Ishino Y, Shinagawa H, Makino K, Amemura M, Nakata A. Nucleotide sequence of the iap gene, responsible for alkaline phosphatase isozyme conversion in Escherichia coli, and identification of the gene product. J Bacteriol. 1987;169(12):5429-33.
14. Jansen R, Embden JDA, Gaastra W, Schouls LM. Identification of genes that are associated with DNA repeats in prokaryotes. Mol Microbiol. 2002;43(6):1565-75.
15. Heler R, Samai P, Modell JW, Weiner C, Goldberg GW, Bikard D, et al. Cas9 specifies functional viral targets during CRISPR-Cas adaptation. Nature. 2015;519(7542):199-202. doi: 10.1038/nature14245.
16. Garneau JE, Dupuis M-E, Villion M, Romero DA, Barrangou R, Boyaval P, et al. The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature. 2010;468(7320):67-71. doi: 10.1038/nature09523.
17. Haft DH, Selengut J, Mongodin EF, Nelson KE. A guild of 45 CRISPR-associated (Cas) protein families and multiple CRISPR/Cas subtypes exist in prokaryotic genomes. PLoS Comput Biol. 2005;1(6):e60. doi: 10.1371/journal.pcbi.0010060.
18. Makarova KS, Haft DH, Barrangou R, Brouns SJJ, Charpentier E, Horvath P, et al. Evolution and classification of the CRISPR-Cas systems. Nat Rev Microbiol. 2011;9(6):467-77. doi: 10.1038/nrmicro2577.
19. Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science. 2012;337(6096):816-21. doi: 10.1126/science.1225829.
20. Nishimasu H, Ran FA, Hsu PD, Konermann S, Shehata SI, Dohmae N, et al. Crystal structure of Cas9 in complex with guide RNA and target DNA. Cell. 2014;156(5):935-49. doi: 10.1016/j.cell.2014.02.001.
21. Ran FA, Hsu PD, Lin CY, Gootenberg JS, Konermann S, Trevino AE, et al. Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell. 2013;154(6):1380-9. doi: 10.1016/j.cell.2013.08.021.
22. Bikard D, Jiang W, Samai P, Hochschild A, Zhang F, Marraffini LA. Programmable repression and activation of bacterial gene expression using an engineered CRISPR-Cas system. Nucleic Acids Res. 2013;41(15):7429-37. doi: 10.1093/nar/gkt520.
23. Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, et al. Multiplex genome engineering using CRISPR/Cas systems. Science. 2013;339(6121):819-23. doi: 10.1126/science.1231143.
24. Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, et al. RNA-guided human genome engineering via Cas9. Science. 2013;339(6121):823-6. doi: 10.1126/science.1232033.
25. Makarova K, Grishin N, Shabalina S, Wolf Y, Koonin E. 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. 2006;1(1):7.
26. Kunin V, Sorek R, Hugenholtz P. Evolutionary conservation of sequence and secondary structures in CRISPR repeats. Genome Biol. 2007;8(4):R61.
27. Hochstrasser ML, Doudna JA. Cutting it close: CRISPR-associated endoribonuclease structure and function. Trends Biochem Sci. 2015;40(1):58-66. doi: 10.1016/j.tibs.2014.10.007.
28. Chylinski K, Makarova KS, Charpentier E, Koonin EV. Classification and evolution of type II CRISPR-Cas systems. Nucleic Acids Res. 2014;42(10):6091-105. doi: 10.1093/nar/gku241.
29. Rousseau C, Gonnet M, Le Romancer M, Nicolas J. CRISPI: a CRISPR interactive database. Bioinformatics. 2009;25(24):3317-8. doi: 10.1093/bioinformatics/btp586.
30. Deltcheva E, Chylinski K, Sharma CM, Gonzales K, Chao Y, Pirzada ZA, et al. CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature. 2011;471(7340):602-7. doi: 10.1038/nature09886.
31. Jiang W, Bikard D, Cox D, Zhang F, Marraffini LA. CRISPR-assisted editing of bacterial genomes. Nat Biotechnol. 2013;31(3):233-9. doi: 10.1038/nbt.2508.
32. Hou Z, Zhang Y, Propson NE, Howden SE, Chu L-F, Sontheimer EJ, et al. Efficient genome engineering in human pluripotent stem cells using Cas9 from Neisseria meningitidis. Proc Natl Acad Sci U S A. 2013;110(39):15644-9. doi: 10.1073/pnas.1313587110.
33. Ran FA, Cong L, Yan WX, Scott DA, Gootenberg JS, Kriz AJ, et al. In vivo genome editing using Staphylococcus aureus Cas9. Nature. 2015;520(7546):186-91. doi: 10.1038/nature14299.
34. Gasiunas G, Barrangou R, Horvath P, Siksnys V. Cas9-crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. Proc Natl Acad Sci. 2012;109(39):E2579-86. doi: 10.1073/pnas.1208507109.
35. Sternberg SH, Redding S, Jinek M, Greene EC, Doudna JA. DNA interrogation by the CRISPR RNA-guided endonuclease Cas9. Nature. 2014;507(7490):62-7. doi: 10.1038/nature13011.
36. Bétermier M, Bertrand P, Lopez BS. Is non-homologous end-joining really an inherently error-prone process? PLoS Genet. 2014;10(1):e1004086. doi: 10.1371/journal.pgen.1004086.
37. Sharan SK, Thomason LC, Kuznetsov SG, Court DL. Recombineering: A Homologous Recombination-Based Method of Genetic Engineering. Nat Protoc. 2009;4(2):206-23. doi: 10.1038/nprot.2008.227.
38. Vasquez KM, Marburger K, Intody Z, Wilson JH. Manipulating the mammalian genome by homologous recombination. Proc Natl Acad Sci. 2001;98(15):8403-10. doi: 10.1073/pnas.111009698.
39. Chu VT, Weber T, Wefers B, Wurst W, Sander S, Rajewsky K, et al. Increasing the efficiency of homology-directed repair for CRISPR-Cas9-induced precise gene editing in mammalian cells. Nature biotechnology. 2015;33(5):543-8. doi: 10.1038/nbt.3198.
40. Heyer W-D, Ehmsen KT, Liu J. Regulation of homologous recombination in eukaryotes. Annu Rev Genet. 2010;44:113-39. doi: 10.1146/annurev-genet-051710-150955.
41. Sakuma T, Nishikawa A, Kume S, Chayama K, Yamamoto T. Multiplex genome engineering in human cells using all-in-one CRISPR/Cas9 vector system. Sci Rep. 2014;4:5400. doi: 10.1038/srep05400.
42. Guo L, Xu K, Liu Z, Zhang C, Xin Y, Zhang Z. Assembling the Streptococcus thermophilus CRISPR array for multiplex DNA targeting. Anal Biochem. 2015;478:131-3. doi: 10.1016/j.ab.2015.02.028.
43. Ma Y, Shen B, Zhang X, Lu Y, Chen W, Ma J, et al. Heritable multiplex genetic engineering in rats using CRISPR/Cas9. PLoS One. 2014;9(3):e89413. doi: 10.1371/journal.pone.0089413.
44. Cobb RE, Wang Y, Zhao H. High-Efficiency Multiplex Genome Editing of Streptomyces Species Using an Engineered CRISPR/Cas System. ACS synthetic biology. 2014. doi: 10.1021/sb500351f.
45. Xing HL, Dong L, Wang ZP, Zhang HY, Han CY, Liu B, et al. A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biol. 2014;14:327. doi: 10.1186/s12870-014-0327-y.
46. Ryan OW, Skerker JM, Maurer MJ, Li X, Tsai JC, Poddar S et al. Selection of chromosomal DNA libraries using a multiplex CRISPR system. eLife. 2014;3. doi: 10.7554/eLife.03703.
47. Li P, Estrada JL, Burlak C, Montgomery J, Butler JR, Santos RM, et al. Efficient generation of genetically distinct pigs in a single pregnancy using multiplexed single-guide RNA and carbohydrate selection. Xenotransplantation. 2015;22(1):20-31. doi: 10.1111/xen.12131.
48. Guo X, Zhang T, Hu Z, Zhang Y, Shi Z, Wang Q, et al. Efficient RNA/Cas9-mediated genome editing in Xenopus tropicalis. Development. 2014;141(3):707-14. doi: 10.1242/dev.099853.
49. Yin L, Maddison LA, Li M, Kara N, LaFave MC, Varshney GK et al. Multiplex Conditional Mutagenesis Using Transgenic Expression of Cas9 and sgRNAs. Genetics. 2015. doi: 10.1534/genetics.115.176917.
50. Jao LE, Wente SR, Chen W. Efficient multiplex biallelic zebrafish genome editing using a CRISPR nuclease system. Proc Natl Acad Sci U S A. 2013;110(34):13904-9. doi: 10.1073/pnas.1308335110.
51. Ousterout DG, Kabadi AM, Thakore PI, Majoros WH, Reddy TE, Gersbach CA. Multiplex CRISPR/Cas9-based genome editing for correction of dystrophin mutations that cause Duchenne muscular dystrophy. Nat Commun. 2015;6:6244. doi: 10.1038/ncomms7244.
52. Mojica FJM, Díez-Villaseñor C, García-Martínez J, Almendros C. Short motif sequences determine the targets of the prokaryotic CRISPR defence system. Microbiology. 2009;155(Pt 3):733-40. doi: 10.1099/mic.0.023960-0.
53. DiCarlo JE, Norville JE, Mali P, Rios X, Aach J, Church GM. Genome engineering in Saccharomyces cerevisiae using CRISPR-Cas systems. Nucleic Acids Res. 2013;41(7):4336-43. doi: 10.1093/nar/gkt135.
54. Guilinger JP, Thompson DB, Liu DR. Fusion of catalytically inactive Cas9 to FokI nuclease improves the specificity of genome modification. Nat Biotechnol. 2014;32(6):577-82. doi: 10.1038/nbt.2909.
55. Tsai SQ, Wyvekens N, Khayter C, Foden JA, Thapar V, Reyon D, et al. Dimeric CRISPR RNA-guided FokI nucleases for highly specific genome editing. Nat Biotechnol. 2014;32(6):569-76. doi: 10.1038/nbt.2908.
56. Qi LS, Larson MH, Gilbert LA, Doudna JA, Weissman JS, Arkin AP, et al. Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell. 2013;152(5):1173-83. doi: 10.1016/j.cell.2013.02.022.
57. Maeder ML, Linder SJ, Cascio VM, Fu Y, Ho QH, Joung JK. CRISPR RNA-guided activation of endogenous human genes. Nat Methods. 2013;10(10):977-9. doi: 10.1038/nmeth.2598.
58. Konermann S, Brigham MD, Trevino AE, Joung J, Abudayyeh OO, Barcena C, et al. Genome-scale transcriptional activation by an engineered CRISPR-Cas9 complex. Nature. 2015;517(7536):583-8. doi: 10.1038/nature14136.
59. Gilbert LA, Larson MH, Morsut L, Liu Z, Brar GA, Torres SE, et al. CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell. 2013;154(2):442-51. doi: 10.1016/j.cell.2013.06.044.
60. Zhao Y, Dai Z, Liang Y, Yin M, Ma K, He M, et al. Sequence-specific inhibition of microRNA via CRISPR/CRISPRi system. Sci Rep. 2014;4:3943. doi: 10.1038/srep03943.
61. Gilbert LA, Horlbeck MA, Adamson B, Villalta JE, Chen Y, Whitehead EH, et al. Genome-Scale CRISPR-Mediated Control of Gene Repression and Activation. Cell. 2014;159(3):647-61. doi: 10.1016/j.cell.2014.09.029.
62. Mizuno S, Dinh TT, Kato K, Mizuno-Iijima S, Tanimoto Y, Daitoku Y, et al. Simple generation of albino C57BL/6 J mice with G291T mutation in the tyrosinase gene by the CRISPR/Cas9 system. Mamm Genome. 2014;25(7-8):327-34. doi: 10.1007/s00335-014-9524-0.
63. Shen B, Zhang J, Wu H, Wang J, Ma K, Li Z, et al. Generation of gene-modified mice via Cas9/RNA-mediated gene targeting. Cell Res. 2013;23(5):720-3. doi: 10.1038/cr.2013.46.
64. Wang H, Yang H, Shivalila Chikdu S, Dawlaty Meelad M, Cheng Albert W, Zhang F, et al. One-Step Generation of Mice Carrying Mutations in Multiple Genes by CRISPR/Cas-Mediated Genome Engineering. Cell. 2013;153(4):910-8. http://dx.doi.org/10.1016/j.cell.2013.04.025.
65. Wu Y, Liang D, Wang Y, Bai M, Tang W, Bao S, et al. Correction of a Genetic Disease in Mouse via Use of CRISPR-Cas9. Cell Stem Cell. 2013;13(6):659-62. http://dx.doi.org/10.1016/j.stem.2013.10.016.
66. Fujii W, Kawasaki K, Sugiura K, Naito K. Efficient generation of large-scale genome-modified mice using gRNA and CAS9 endonuclease. Nucleic Acids Res. 2013;41(20):e187. doi: 10.1093/nar/gkt772.
67. Fujii W, Onuma A, Sugiura K, Naito K. Efficient generation of genome-modified mice via offset-nicking by CRISPR/Cas system. Biochem Biophys Res Commun. 2014;445(4):791-4. doi: 10.1016/j.bbrc.2014.01.141.
68. Gantz VM, Bier E. Genome editing. The mutagenic chain reaction: a method for converting heterozygous to homozygous mutations. Science. 2015;348(6233):442-4. doi: 10.1126/science.aaa5945.
69. González F, Zhu Z, Shi Z-D, Lelli K, Verma N, Li QV, et al. An iCRISPR platform for rapid, multiplexable, and inducible genome editing in human pluripotent stem cells. Cell Stem Cell. 2014;15(2):215-26. doi: 10.1016/j.stem.2014.05.018.
70. Konermann S, Brigham MD, Trevino AE, Hsu PD, Heidenreich M, Cong L, et al. Optical control of mammalian endogenous transcription and epigenetic states. Nature. 2013;500(7463):472-6. doi: 10.1038/nature12466.
71. Polstein LR, Gersbach CA. A light-inducible CRISPR-Cas9 system for control of endogenous gene activation. Nat Chem Biol. 2015;11(3):198-200. doi: 10.1038/nchembio.1753.
72. Inui M, Miyado M, Igarashi M, Tamano M, Kubo A, Yamashita S, et al. Rapid generation of mouse models with defined point mutations by the CRISPR/Cas9 system. Sci Rep. 2014;4:5396. doi: 10.1038/srep05396.
73. Yu Z, Ren M, Wang Z, Zhang B, Rong YS, Jiao R, et al. Highly efficient genome modifications mediated by CRISPR/Cas9 in Drosophila. Genetics. 2013;195(1):289-91. doi: 10.1534/genetics.113.153825.
74. Lin S-C, Chang Y-Y, Chan C-C. Strategies for gene disruption in Drosophila. Cell Biosci. 2014;4(1):63. doi: 10.1186/2045-3701-4-63.
75. Dickinson DJ, Ward JD, Reiner DJ, Goldstein B. Engineering the Caenorhabditis elegans genome using Cas9-triggered homologous recombination. Nat Methods. 2013;10(10):1028-34. doi: 10.1038/nmeth.2641.
76. Friedland AE, Tzur YB, Esvelt KM, Colaiacovo MP, Church GM, Calarco JA. Heritable genome editing in C. elegans via a CRISPR-Cas9 system. Nat Methods. 2013;10(8):741-3. doi: 10.1038/nmeth.2532.
77. Mans R, van Rossum HM, Wijsman M, Backx A, Kuijpers NG, van den Broek M et al. CRISPR/Cas9: a molecular Swiss army knife for simultaneous introduction of multiple genetic modifications in Saccharomyces cerevisiae. FEMS Yeast Res. 2015;15(2). doi:10.1093/femsyr/fov004
78. Chang N, Sun C, Gao L, Zhu D, Xu X, Zhu X, et al. Genome editing with RNA-guided Cas9 nuclease in zebrafish embryos. Cell Res. 2013;23(4):465-72. doi: 10.1038/cr.2013.45.
79. Hwang WY, Fu Y, Reyon D, Maeder ML, Kaini P, Sander JD, et al. Heritable and precise zebrafish genome editing using a CRISPR-Cas system. PLoS One. 2013;8(7):e68708. doi: 10.1371/journal.pone.0068708.
80. Shao Y, Guan Y, Wang L, Qiu Z, Liu M, Chen Y, et al. CRISPR/Cas-mediated genome editing in the rat via direct injection of one-cell embryos. Nat Protoc. 2014;9(10):2493-512. doi: 10.1038/nprot.2014.171.
81. Hu X, Chang N, Wang X, Zhou F, Zhou X, Zhu X, et al. Heritable gene-targeting with gRNA/Cas9 in rats. Cell Res. 2013;23(11):1322-5. doi: 10.1038/cr.2013.141.
82. Ma Y, Zhang X, Shen B, Lu Y, Chen W, Ma J, et al. Generating rats with conditional alleles using CRISPR/Cas9. Cell Res. 2014;24(1):122-5. doi: 10.1038/cr.2013.157.
83. Sato M, Miyoshi K, Nagao Y, Nishi Y, Ohtsuka M, Nakamura S, et al. The combinational use of CRISPR/Cas9-based gene editing and targeted toxin technology enables efficient biallelic knockout of the alpha-1,3-galactosyltransferase gene in porcine embryonic fibroblasts. Xenotransplantation. 2014;21(3):291-300. doi: 10.1111/xen.12089.
84. Tan W, Carlson DF, Lancto CA, Garbe JR, Webster DA, Hackett PB, et al. Efficient nonmeiotic allele introgression in livestock using custom endonucleases. Proc Natl Acad Sci U S A. 2013;110(41):16526-31. doi: 10.1073/pnas.1310478110.
85. Whitworth KM, Lee K, Benne JA, Beaton BP, Spate LD, Murphy SL, et al. Use of the CRISPR/Cas9 system to produce genetically engineered pigs from in vitro-derived oocytes and embryos. Biol Reprod. 2014;91(3):78. doi: 10.1095/biolreprod.114.121723.
86. Zhou X, Xin J, Fan N, Zou Q, Huang J, Ouyang Z, et al. Generation of CRISPR/Cas9-mediated gene-targeted pigs via somatic cell nuclear transfer. CMLS. 2015;72(6):1175-84. doi: 10.1007/s00018-014-1744-7.
87. Ni W, Qiao J, Hu S, Zhao X, Regouski M, Yang M, et al. Efficient gene knockout in goats using CRISPR/Cas9 system. PLoS One. 2014;9(9):e106718. doi: 10.1371/journal.pone.0106718.
88. Feng W, Dai Y, Mou L, Cooper DKC, Shi D, Cai Z. The Potential of the Combination of CRISPR/Cas9 and Pluripotent Stem Cells to Provide Human Organs from Chimaeric Pigs. Int J Mol Sci. 2015;16(3):6545-56. doi: 10.3390/ijms16036545.
89. Niu Y, Shen B, Cui Y, Chen Y, Wang J, Wang L, et al. Generation of gene-modified cynomolgus monkey via Cas9/RNA-mediated gene targeting in one-cell embryos. Cell. 2014;156(4):836-43. doi: 10.1016/j.cell.2014.01.027.
90. Chen Y, Zheng Y, Kang Y, Yang W, Niu Y, Guo X, et al. Functional disruption of the dystrophin gene in Rhesus Monkey Using CRISPR/Cas9. Human molecular genetics. 2015;24(13):3764-74. doi: 10.1093/hmg/ddv120.
91. Genade T, Benedetti M, Terzibasi E, Roncaglia P, Valenzano DR, Cattaneo A, et al. Annual fishes of the genus Nothobranchius as a model system for aging research. Aging Cell. 2005;4(5):223-33. doi: 10.1111/j.1474-9726.2005.00165.x.
92. Harel I, Benayoun BA, Machado B, Singh PP, Hu CK, Pech MF, et al. A platform for rapid exploration of aging and diseases in a naturally short-lived vertebrate. Cell. 2015;160(5):1013-26. doi: 10.1016/j.cell.2015.01.038.
93. Zhou Y, Zhu S, Cai C, Yuan P, Li C, Huang Y, et al. High-throughput screening of a CRISPR/Cas9 library for functional genomics in human cells. Nature. 2014;509(7501):487-91. doi: 10.1038/nature13166.
94. Koike-Yusa H, Li Y, Tan EP, Velasco-Herrera Mdel C, Yusa K. Genome-wide recessive genetic screening in mammalian cells with a lentiviral CRISPR-guide RNA library. Nat Biotechnol. 2014;32(3):267-73. doi: 10.1038/nbt.2800.
95. Ren Q, Li C, Yuan P, Cai C, Zhang L, Luo GG, et al. A Dual-Reporter System for Real-Time Monitoring and High-throughput CRISPR/Cas9 Library Screening of the Hepatitis C Virus. Sci Rep. 2015;5:8865. doi: 10.1038/srep08865.
96. Chen S, Sanjana NE, Zheng K, Shalem O, Lee K, Shi X, et al. Genome-wide CRISPR Screen in a Mouse Model of Tumor Growth and Metastasis. Cell. 2015;160(6):1246-60. doi: 10.1016/j.cell.2015.02.038.
97. Shalem O, Sanjana NE, Zhang F. High-throughput functional genomics using CRISPR-Cas9. Nat Rev Genet. 2015;16(5):299-311. doi: 10.1038/nrg3899.
98. Pichavant C, Aartsma-Rus A, Clemens PR, Davies KE, Dickson G, Takeda S, et al. Current status of pharmaceutical and genetic therapeutic approaches to treat DMD. Mol Ther. 2011;19(5):830-40. doi: 10.1038/mt.2011.59.
99. Li Hongmei L, Fujimoto N, Sasakawa N, Shirai S, Ohkame T, Sakuma T, et al. Precise Correction of the Dystrophin Gene in Duchenne Muscular Dystrophy Patient Induced Pluripotent Stem Cells by TALEN and CRISPR-Cas9. Stem Cell Rep. 2015;4(1):143-54. doi: 10.1016/j.stemcr.2014.10.013.
100. Long C, McAnally JR, Shelton JM, Mireault AA, Bassel-Duby R, Olson EN. Prevention of muscular dystrophy in mice by CRISPR/Cas9-mediated editing of germline DNA. Science. 2014;345(6201):1184-8. doi: 10.1126/science.1254445.
101. Zhen S, Hua L, Liu YH, Gao LC, Fu J, Wan DY, et al. Harnessing the clustered regularly interspaced short palindromic repeat (CRISPR)/CRISPR-associated Cas9 system to disrupt the hepatitis B virus. Gene Therapy. 2015;22(5):404-12. doi: 10.1038/gt.2015.2.
102. Hu W, Kaminski R, Yang F, Zhang Y, Cosentino L, Li F, et al. RNA-directed gene editing specifically eradicates latent and prevents new HIV-1 infection. Proc Natl Acad Sci U S A. 2014;111(31):11461-6. doi: 10.1073/pnas.1405186111.
103. Yin H, Xue W, Chen S, Bogorad RL, Benedetti E, Grompe M, et al. Genome editing with Cas9 in adult mice corrects a disease mutation and phenotype. Nat Biotechnol. 2014;32(6):551-3. doi: 10.1038/nbt.2884.
104. Blasco RB, Karaca E, Ambrogio C, Cheong TC, Karayol E, Minero VG, et al. Simple and rapid in vivo generation of chromosomal rearrangements using CRISPR/Cas9 technology. Cell Rep. 2014;9(4):1219-27. doi: 10.1016/j.celrep.2014.10.051.
105. Jurkowski TP, Ravichandran M, Stepper P. Synthetic epigenetics-towards intelligent control of epigenetic states and cell identity. Clin Epigenetics. 2015;7(1):18. doi: 10.1186/s13148-015-0044-x.
106. Chen B, Gilbert LA, Cimini BA, Schnitzbauer J, Zhang W, Li GW, et al. Dynamic imaging of genomic loci in living human cells by an optimized CRISPR/Cas system. Cell. 2013;155(7):1479-91. doi: 10.1016/j.cell.2013.12.001.
107. Ma H, Naseri A, Reyes-Gutierrez P, Wolfe SA, Zhang S, Pederson T. Multicolor CRISPR labeling of chromosomal loci in human cells. Proc Natl Acad Sci U S A. 2015;112(10):3002-7. doi: 10.1073/pnas.1420024112.
108. Fujita T, Fujii H. Efficient isolation of specific genomic regions and identification of associated proteins by engineered DNA-binding molecule-mediated chromatin immunoprecipitation (enChIP) using CRISPR. Biochem Biophys Res Commun. 2013;439(1):132-6. doi: 10.1016/j.bbrc.2013.08.013.
109. Ablain J, Durand EM, Yang S, Zhou Y, Zon LI. A CRISPR/Cas9 Vector System for Tissue-Specific Gene Disruption in Zebrafish. Dev Cell. 2015;32(6):756-64. doi: 10.1016/j.devcel.2015.01.032.
110. Albers J, Danzer C, Rechsteiner M, Lehmann H, Brandt LP, Hejhal T, et al. A versatile modular vector system for rapid combinatorial mammalian genetics. J Clin Invest. 2015;125(4):1603-19. doi: 10.1172/JCI79743.