[en] The clustered, regularly interspaced, short palindromic repeat (CRISPR) and CRISPR associated protein 9 (Cas9) system discovered as an adaptive immunity mechanism in prokaryotes has emerged as the most popular tool for the precise alterations of the genomes of diverse species. CRISPR/Cas9 system has taken the world of genome editing by storm in recent years. Its popularity as a tool for altering genomes is due to the ability of Cas9 protein to cause double-stranded breaks in DNA after binding with short guide RNA molecules, which can be produced with dramatically less effort and expense than required for production of transcription-activator like effector nucleases (TALEN) and zinc-finger nucleases (ZFN). This system has been exploited in many species from prokaryotes to higher animals including human cells as evidenced by the literature showing increasing sophistication and ease of CRISPR/Cas9 as well as increasing species variety where it is applicable. This technology is poised to solve several complex molecular biology problems faced in life science research including cancer research. In this review, we highlight the recent advancements in CRISPR/Cas9 system in editing genomes of prokaryotes, fungi, plants and animals and provide details on software tools available for convenient design of CRISPR/Cas9 targeting plasmids. We also discuss the future prospects of this advanced molecular technology.
Disciplines :
Biotechnology
Author, co-author :
Stanislaus, Antony Ceasar ; Université de Liège - ULiège > Département des sciences de la vie > Génomique fonctionnelle et imagerie moléculaire végétale
Rajan, Vinothkumar
Prykhozhij, Sergy
Berman, Jason N
Ignacimuthu, S
Language :
English
Title :
Insert, remove or replace: A highly advanced genome editing system using CRISPR/Cas9
Publication date :
June 2016
Journal title :
BBA Molecular Cell Research
ISSN :
0167-4889
Publisher :
Elsevier, Netherlands
Volume :
1863
Pages :
2333-2344
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
Times of India-Loyola College grant (No: 7LCTOI14ERI001). Vinothkumar Rajan is funded through Cancer Research Trainee Program of the Beatrice Hunter Cancer Institute, Nova Scotia in partnership with the Canadian Imperial Bank of Commerce and New Brunswick Health Research Foundation.
Grissa, I., Vergnaud, G., Pourcel, C., The CRISPRdb database and tools to display CRISPRs and to generate dictionaries of spacers and repeats (2007) BMC Bioinf., 8, p. 172
Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J.A., Charpentier, E., A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity (2012) Science, 337, pp. 816-821
Doudna, J.A., Charpentier, E., Genome editing. The new frontier of genome engineering with CRISPR-Cas9 (2014) Science, 346, p. 1258096
Townsend, J.A., Wright, D.A., Winfrey, R.J., Fu, F., Maeder, M.L., Joung, J.K., Voytas, D.F., High-frequency modification of plant genes using engineered zinc-finger nucleases (2009) Nature, 459, pp. 442-445
Wood, A.J., Lo, T.W., Zeitler, B., Pickle, C.S., Ralston, E.J., Lee, A.H., Amora, R., Meyer, B.J., Targeted genome editing across species using ZFNs and TALENs (2011) Science, 333, p. 307
Moscou, M.J., Bogdanove, A.J., A simple cipher governs DNA recognition by TAL effectors (2009) Science, 326, p. 1501
Boch, J., Scholze, H., Schornack, S., Landgraf, A., Hahn, S., Kay, S., Lahaye, T., Bonas, U., Breaking the code of DNA binding specificity of TAL-type III effectors (2009) Science, 326, pp. 1509-1512
Harrison, M.M., Jenkins, B.V., O'Connor-Giles, K.M., Wildonger, J., A CRISPR view of development (2014) Genes Dev., 28, pp. 1859-1872
Cradick, T.J., Fine, E.J., Antico, C.J., Bao, G., CRISPR/Cas9 systems targeting β-globin and CCR5 genes have substantial off-target activity (2013) Nucleic Acids Res., , (gkt714)
Fu, Y., Foden, J.A., Khayter, C., Maeder, M.L., Reyon, D., Joung, J.K., Sander, J.D., High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells (2013) Nat. Biotechnol., 31, pp. 822-826
Hsu, P.D., Lander, E.S., Zhang, F., Development and applications of CRISPR-Cas9 for genome engineering (2014) Cell, 157, pp. 1262-1278
Sander, J.D., Joung, J.K., CRISPR-Cas systems for editing, regulating and targeting genomes (2014) Nat. Biotechnol., 32, pp. 347-355
Rollins, M.F., Schuman, J.T., Paulus, K., Bukhari, H.S., Wiedenheft, B., Mechanism of foreign DNA recognition by a CRISPR RNA-guided surveillance complex from Pseudomonas aeruginosa (2015) Nucleic Acids Res.
Heler, R., Samai, P., Modell, J.W., Weiner, C., Goldberg, G.W., Bikard, D., Marraffini, L.A., Cas9 specifies functional viral targets during CRISPR-Cas adaptation (2015) Nature
Choudhary, E., Thakur, P., Pareek, M., Agarwal, N., Gene silencing by CRISPR interference in mycobacteria (2015) Nat. Commun., 6
Jakočiūnas, T., Bonde, I., Herrgård, M., Harrison, S.J., Kristensen, M., Pedersen, L.E., Jensen, M.K., Keasling, J.D., Multiplex metabolic pathway engineering using CRISPR/Cas9 in Saccharomyces cerevisiae (2015) Metab. Eng., 28, pp. 213-222
Osakabe, Y., Osakabe, K., Genome editing with engineered nucleases in plants (2014) Plant Cell Physiol.
Zhang, F., Maeder, M.L., Unger-Wallace, E., Hoshaw, J.P., Reyon, D., Christian, M., Li, X., Peterson, T., High frequency targeted mutagenesis in Arabidopsis thaliana using zinc finger nucleases (2010) Proc. Natl. Acad. Sci., 107, pp. 12028-12033
Li, J.-F., Norville, J.E., Aach, J., McCormack, M., Zhang, D., Bush, J., Church, G.M., Sheen, J., Multiplex and homologous recombination-mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9 (2013) Nat. Biotechnol., 31, pp. 688-691
Nekrasov, V., Staskawicz, B., Weigel, D., Jones, J.D.G., Kamoun, S., Targeted mutagenesis in the model plant Nicotiana benthamiana using Cas9 RNA-guided endonuclease (2013) Nat. Biotechnol., 31, pp. 691-693
Shan, Q., Wang, Y., Li, J., Zhang, Y., Chen, K., Liang, Z., Zhang, K., Gao, C., Targeted genome modification of crop plants using a CRISPR-Cas system (2013) Nat. Biotechnol., 31, pp. 686-688
Shan, Q., Wang, Y., Li, J., Gao, C., Genome editing in rice and wheat using the CRISPR/Cas system (2014) Nat. Protoc., 9, pp. 2395-2410
Jiang, W., Zhou, H., Bi, H., Fromm, M., Yang, B., Weeks, D.P., Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice (2013) Nucleic Acids Res., 41, p. e188
Johnson, R., Gurevich, V., Filler, S., Samach, A., Levy, A., Comparative assessments of CRISPR-Cas nucleases' cleavage efficiency in planta (2015) Plant Mol. Biol., 87, pp. 143-156
Feng, Z., Mao, Y., Xu, N., Zhang, B., Wei, P., Yang, D.L., Wang, Z., Zhu, J.K., Multigeneration analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas-induced gene modifications in Arabidopsis (2014) Proc. Natl. Acad. Sci. U. S. A., 111, pp. 4632-4637
Sugano, S.S., Shirakawa, M., Takagi, J., Matsuda, Y., Shimada, T., Hara-Nishimura, I., Kohchi, T., CRISPR/Cas9-mediated targeted mutagenesis in the liverwort Marchantia polymorpha L (2014) Plant Cell Physiol., 55, pp. 475-481
Woo, J.W., Kim, J., Kwon, S.I., Corvalán, C., Cho, S.W., Kim, H., Kim, S.-G., Kim, J.-S., DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins (2015) Nat. Biotechnol.
Holt, N., Wang, J., Kim, K., Friedman, G., Wang, X., Taupin, V., Crooks, G.M., Holmes, M.C., Zinc finger nuclease-mediated CCR5 knockout hematopoietic stem cell transplantation controls HIV-1 in vivo (2010) Nat. Biotechnol., 28, p. 839
Perez, E.E., Wang, J., Miller, J.C., Jouvenot, Y., Kim, K.A., Liu, O., Wang, N., Lee, Y.-L., Establishment of HIV-1 resistance in CD4 + T cells by genome editing using zinc-finger nucleases (2008) Nat. Biotechnol., 26, pp. 808-816
Cong, L., Ran, F.A., Cox, D., Lin, S., Barretto, R., Habib, N., Hsu, P.D., Marraffini, L.A., Multiplex genome engineering using CRISPR/Cas systems (2013) Science, 339, pp. 819-823
Mali, P., Yang, L., Esvelt, K.M., Aach, J., Guell, M., DiCarlo, J.E., Norville, J.E., Church, G.M., RNA-guided human genome engineering via Cas9 (2013) Science, 339, pp. 823-826
Hou, Z., Zhang, Y., Propson, N.E., Howden, S.E., Chu, L.-F., Sontheimer, E.J., Thomson, J.A., Efficient genome engineering in human pluripotent stem cells using Cas9 from Neisseria meningitidis (2013) Proc. Natl. Acad. Sci., 110, pp. 15644-15649
Kleinstiver, B.P., Pattanayak, V., Prew, M.S., Tsai, S.Q., Nguyen, N.T., Zheng, Z., Keith Joung, J., High-fidelity CRISPR–Cas9 nucleases with no detectable genome-wide off-target effects (2016) Nature, 529, pp. 490-495
Pinder, J., Salsman, J., Dellaire, G., Nuclear domain ‘knock-in’ screen for the evaluation and identification of small molecule enhancers of CRISPR-based genome editing (2015) Nucleic Acids Res., 43, pp. 9379-9392
Song, J., Yang, D., Xu, J., Zhu, T., Chen, Y.E., Zhang, J., RS-1 enhances CRISPR/Cas9- and TALEN-mediated knock-in efficiency (2016) Nat. Commun., 7, p. 10548
Schwank, G., Koo, B.-K., Sasselli, V., Dekkers, J.F., Heo, I., Demircan, T., Sasaki, N., van der Ent, C.K., Functional repair of CFTR by CRISPR/Cas9 in intestinal stem cell organoids of cystic fibrosis patients (2013) Cell Stem Cell, 13, pp. 653-658
Hilton, I.B., D'Ippolito, A.M., Vockley, C.M., Thakore, P.I., Crawford, G.E., Reddy, T.E., Gersbach, C.A., Epigenome editing by a CRISPR-Cas9-based acetyltransferase activates genes from promoters and enhancers (2015) Nat. Biotechnol., 33, pp. 510-517
Gilbert, L.A., Larson, M.H., Morsut, L., Liu, Z., Brar, G.A., Torres, S.E., Stern-Ginossar, N., Doudna, J.A., CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes (2013) Cell, 154, pp. 442-451
Qi, L.S., Larson, M.H., Gilbert, L.A., Doudna, J.A., Weissman, J.S., Arkin, A.P., Lim, W.A., Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression (2013) Cell, 152, pp. 1173-1183
Mandegar, M.A., Huebsch, N., Frolov, E.B., Shin, E., Truong, A., Olvera, M.P., Chan, A.H., Conklin, B.R., CRISPR interference efficiently induces specific and reversible gene silencing in human iPSCs (2016) Cell Stem Cell, 18, pp. 541-553
Shalem, O., Sanjana, N.E., Hartenian, E., Shi, X., Scott, D.A., Mikkelsen, T.S., Heckl, D., Doench, J.G., Genome-scale CRISPR-Cas9 knockout screening in human cells (2014) Science, 343, pp. 84-87
Wang, T., Wei, J.J., Sabatini, D.M., Lander, E.S., Genetic screens in human cells using the CRISPR-Cas9 system (2014) Science, 343, pp. 80-84
Tzelepis, K., Koike-Yusa, H., De Braekeleer, E., Li, Y., Metzakopian, E., Dovey, O.M., Mupo, A., Gozdecka, M., A crispr/Cas9 drop-out screen identifies genome-wide genetic valnerubilities in acute myeloid leukaemia (2015) Blood, 126, p. 554
Port, F., Muschalik, N., Bullock, S.L., Systematic evaluation of Drosophila CRISPR tools reveals safe and robust alternatives to autonomous gene drives in basic research (2015) G3 (Bethesda), 5, pp. 1493-1502
Xu, J., Ren, X., Sun, J., Wang, X., Qiao, H.-H., Xu, B.-W., Liu, L.-P., Ni, J.-Q., A toolkit of CRISPR-based genome editing systems in Drosophila (2015) J. Genet. Genomics, 42, pp. 141-149
Ward, J.D., Rendering the intractable more tractable: tools from Caenorhabditis elegans ripe for import into parasitic nematodes (2015) Genetics, 201, pp. 1279-1294
Xu, S., The application of CRISPR-Cas9 genome editing in Caenorhabditis elegans (2015) J. Genet. Genomics, 42, pp. 413-421
Pelletier, S., Gingras, S., Green, D.R., Mouse genome engineering via CRISPR-Cas9 for study of immune function (2015) Immunity, 42, pp. 18-27
Duncker, D.J., Bakkers, J., Brundel, B.J., Robbins, J., Tardiff, J.C., Carrier, L., Animal and in silico models for the study of sarcomeric cardiomyopathies (2015) Cardiovasc. Res., 105, pp. 439-448
Horii, T., Hatada, I., Genome editing using mammalian haploid cells (2015) Int. J. Mol. Sci., 16, pp. 23604-23614
Skarnes, W.C., Is mouse embryonic stem cell technology obsolete? (2015) Genome Biol., 16, p. 109
Nakade, S., Tsubota, T., Sakane, Y., Kume, S., Sakamoto, N., Obara, M., Daimon, T., Suzuki, K.T., Microhomology-mediated end-joining-dependent integration of donor DNA in cells and animals using TALENs and CRISPR/Cas9 (2014) Nat. Commun., 5, p. 5560
Nakayama, T., Fish, M.B., Fisher, M., Oomen-Hajagos, J., Thomsen, G.H., Grainger, R.M., Simple and efficient CRISPR/Cas9-mediated targeted mutagenesis in Xenopus tropicalis (2013) Genesis, 51, pp. 835-843
Wang, F., Shi, Z., Cui, Y., Guo, X., Shi, Y.-B., Chen, Y., Targeted gene disruption in Xenopus laevis using CRISPR/Cas9 (2015) Cell Biosci., 5, pp. 1-5
Ansai, S., Kinoshita, M., Targeted mutagenesis using CRISPR/Cas system in medaka (2014) Biology Open, 3, pp. 362-371
Stemmer, M., Thumberger, T., del Sol Keyer, M., Wittbrodt, J., Mateo, J.L., CCTop: an intuitive, flexible and reliable CRISPR/Cas9 target prediction tool (2015) PLoS One, 10. , e0124633
Carroll, D., Charo, R.A., The societal opportunities and challenges of genome editing (2015) Genome Biol., 16, p. 242
Wang, Z., Genome engineering in cattle: recent technological advancements (2015) Chromosom. Res., 23, pp. 17-29
Grobet, L., Royo Martin, L.J., Poncelet, D., Pirottin, D., Brouwers, B., Riquet, J., Schoeberlein, A., Georges, M., A deletion in the bovine myostatin gene causes the double-muscled phenotype in cattle (1997) Nat. Genet., 17, pp. 71-74
Proudfoot, C., Carlson, D.F., Huddart, R., Long, C.R., Pryor, J.H., King, T.J., Lillico, S.G., Fahrenkrug, S.C., Genome edited sheep and cattle (2015) Transgenic Res., 24, pp. 147-153
Heo, Y.T., Quan, X., Xu, Y.N., Baek, S., Choi, H., Kim, N.-H., Kim, J., CRISPR/Cas9 nuclease-mediated gene knock-in in bovine-induced pluripotent cells (2015) Stem Cells Dev., 24, pp. 393-402
Ni, W., Qiao, J., Hu, S., Zhao, X., Regouski, M., Yang, M., Polejaeva, I.A., Chen, C., Efficient gene knockout in goats using CRISPR/Cas9 system (2014) PLoS One, 9, p. e106718
Wang, X., Yu, H., Lei, A., Zhou, J., Zeng, W., Zhu, H., Dong, Z., Chen, Y., Generation of gene-modified goats targeting MSTN and FGF5 via zygote injection of CRISPR/Cas9 system (2015) Sci. Rep., 5, p. 13878
Hai, T., Teng, F., Guo, R., Li, W., Zhou, Q., One-step generation of knockout pigs by zygote injection of CRISPR/Cas system (2014) Cell Res., 24, pp. 372-375
Zhou, X., Xin, J., Fan, N., Zou, Q., Huang, J., Ouyang, Z., Zhao, Y., Lai, L., Generation of CRISPR/Cas9-mediated gene-targeted pigs via somatic cell nuclear transfer (2014) Cell. Mol. Life Sci., 72, pp. 1175-1184
Peng, J., Wang, Y., Jiang, J., Zhou, X., Song, L., Wang, L., Ding, C., Zhang, P., Production of human albumin in pigs through CRISPR/Cas9-mediated knockin of human cDNA into swine albumin locus in the zygotes (2015) Sci. Rep., 5, p. 16705
Zhou, X., Wang, L., Du, Y., Xie, F., Li, L., Liu, Y., Liu, C., Wei, H., Efficient generation of gene-modified pigs harboring precise orthologous human mutation via CRISPR/Cas9-induced homology-directed repair in zygotes (2015) Hum. Mutat., 37, pp. 110-118
Honda, A., Hirose, M., Sankai, T., Yasmin, L., Yuzawa, K., Honsho, K., Izu, H., Ogura, A., Single-step generation of rabbits carrying a targeted allele of the tyrosinase gene using CRISPR/Cas9 (2015) Exp. Anim., 64, pp. 31-37
Ikmi, A., Mckinney, S.A., Delventhal, K.M., Gibson, M.C., TALEN and CRISPR/Cas9-mediated genome editing in the early-branching metazoan Nematostella vectensis (2014) Nat. Commun., 5, p. 5486
Witte, H., Moreno, E., Rodelsperger, C., Kim, J., Streit, A., Sommer, R.J., Gene inactivation using the CRISPR/Cas9 system in the nematode Pristionchus pacificus (2014) Dev. Genes Evol.
Perry, K.J., Henry, J.Q., CRISPR/Cas9-mediated genome modification in the mollusc, Crepidula fornicata (2015) Genesis, 53, pp. 237-244
Nakanishi, T., Kato, Y., Matsuura, T., Watanabe, H., CRISPR/Cas-mediated targeted mutagenesis in Daphnia magna (2014) PLoS One, 9
Martin, A., Serano, J.M., Jarvis, E., Bruce, H.S., Wang, J., Ray, S., Barker, C.A., Patel, N.H., CRISPR/Cas9 mutagenesis reveals versatile roles of Hox genes in crustacean limb specification and evolution (2015) Curr. Biol., 26, pp. 14-26
Wei, W., Xin, H., Roy, B., Dai, J., Miao, Y., Gao, G., Heritable genome editing with CRISPR/Cas9 in the silkworm, Bombyx mori (2014) PLoS One, 9, p. e101210
Li, X., Fan, D., Zhang, W., Liu, G., Zhang, L., Zhao, L., Fang, X., Wang, W., Outbred genome sequencing and CRISPR/Cas9 gene editing in butterflies (2015) Nat. Commun., 6, p. 8212
Gilles, A.F., Schinko, J.B., Averof, M., Efficient CRISPR-mediated gene targeting and transgene replacement in the beetle Tribolium castaneum (2015) Development, 142, pp. 2832-2839
Kistler, K.E., Vosshall, L.B., Matthews, B.J., Genome engineering with CRISPR-Cas9 in the mosquito Aedes aegypti (2015) Cell Rep., 11, pp. 51-60
Gantz, V.M., Jasinskiene, N., Tatarenkova, O., Fazekas, A., Macias, V.M., Bier, E., James, A.A., Highly efficient Cas9-mediated gene drive for population modification of the malaria vector mosquito Anopheles stephensi (2015) Proc. Natl. Acad. Sci., 112, pp. E6736-E6743
Hammond, A., Galizi, R., Kyrou, K., Simoni, A., Siniscalchi, C., Katsanos, D., Gribble, M., Nolan, T., A CRISPR-Cas9 gene drive system targeting female reproduction in the malaria mosquito vector Anopheles gambiae (2015) Nat. Biotechnol., 34, pp. 1-8
Che-Yi Lin, Y.-H.S., Genome editing in sea urchin embryos by using a CRISPR/Cas9 system (2015) Dev. Biol., 409, pp. 1-9
Stolfi, A., Gandhi, S., Salek, F., Christiaen, L., Tissue-specific genome editing in Ciona embryos by CRISPR/Cas9 (2014) Development, 141, pp. 4115-4120
Square, T., Romasek, M., Jandzik, D., Cattell, M.V., Klymkowsky, M., Medeiros, D.M., CRISPR/Cas9-mediated mutagenesis in the sea lamprey, Petromyzon marinus: a powerful tool for understanding ancestral gene functions in vertebrates (2015) Development, 142, pp. 4180-4187
Aluru, N., Karchner, S.I., Franks, D.G., Nacci, D., Champlin, D., Hahn, M.E., Targeted mutagenesis of aryl hydrocarbon receptor 2a and 2b genes in Atlantic killifish (Fundulus heteroclitus) (2015) Aquat. Toxicol., 158, pp. 192-201
Harel, I., Benayoun, B.A., Machado, B., Singh, P.P., Hu, C.K., Pech, M.F., Valenzano, D.R., Brunet, A., A platform for rapid exploration of aging and diseases in a naturally short-lived vertebrate (2015) Cell, 160, pp. 1013-1026
Flowers, G.P., Timberlake, A.T., McLean, K.C., Monaghan, J.R., Crews, C.M., Highly efficient targeted mutagenesis in axolotl using Cas9 RNA-guided nuclease (2014) Development, 141, pp. 2165-2171
Hwang, W.Y., Fu, Y., Reyon, D., Maeder, M.L., Kaini, P., Sander, J.D., Joung, J.K., Yeh, J., Heritable and precise zebrafish genome editing using a CRISPR-Cas system (2013) PLoS One, 8, p. e68708
Hwang, W.Y., Fu, Y., Reyon, D., Maeder, M.L., Tsai, S.Q., Sander, J.D., Peterson, R.T., Joung, J.K., Efficient genome editing in zebrafish using a CRISPR-Cas system (2013) Nat. Biotechnol., 31, pp. 227-229
Chang, N., Sun, C., Gao, L., Zhu, D., Xu, X., Zhu, X., Xiong, J.-W., Xi, J.J., Genome editing with RNA-guided Cas9 nuclease in zebrafish embryos (2013) Cell Res., 23, pp. 465-472
Jao, L.-E., Wente, S.R., Chen, W., Efficient multiplex biallelic zebrafish genome editing using a CRISPR nuclease system (2013) Proc. Natl. Acad. Sci., 110, pp. 13904-13909
Hruscha, A., Krawitz, P., Rechenberg, A., Heinrich, V., Hecht, J., Haass, C., Schmid, B., Efficient CRISPR/Cas9 genome editing with low off-target effects in zebrafish (2013) Development, 140, pp. 4982-4987
Irion, U., Krauss, J., Nüsslein-Volhard, C., Precise and efficient genome editing in zebrafish using the CRISPR/Cas9 system (2014) Development, 141, pp. 4827-4830
Xiao, A., Wang, Z., Hu, Y., Wu, Y., Luo, Z., Yang, Z., Zu, Y., Zhang, B., Chromosomal deletions and inversions mediated by TALENs and CRISPR/Cas in zebrafish (2013) Nucleic Acids Res.
Ablain, J., Durand, E.M., Yang, S., Zhou, Y., Zon, L.I., A CRISPR/Cas9 vector system for tissue-specific gene disruption in zebrafish (2015) Dev. Cell, 32, pp. 756-764
Yin, L., Maddison, L.A., Li, M., Kara, N., LaFave, M.C., Varshney, G.K., Burgess, S.M., Chen, W., Multiplex conditional mutagenesis using transgenic expression of Cas9 and sgRNAs (2015) Genetics, 200, pp. 431-441
Shah, A.N., Davey, C.F., Whitebirch, A.C., Miller, A.C., Moens, C.B., Rapid reverse genetic screening using CRISPR in zebrafish (2015) Nat. Methods, 12, pp. 535-540
Varshney, G.K., Pei, W., LaFave, M.C., Idol, J., Xu, L., Gallardo, V., Carrington, B., Burgess, S.M., High-throughput gene targeting and phenotyping in zebrafish using CRISPR/Cas9 (2015) Genome Res., 25, pp. 1030-1042
Long, L., Guo, H., Yao, D., Xiong, K., Li, Y., Liu, P., Zhu, Z., Liu, D., Regulation of transcriptionally active genes via the catalytically inactive Cas9 in C. elegans and D. rerio (2015) Cell Res., 25, pp. 638-641
Auer, T.O., Duroure, K., De Cian, A., Concordet, J.-P., Del Bene, F., Highly efficient CRISPR/Cas9-mediated knock-in in zebrafish by homology-independent DNA repair (2014) Genome Res., 24, pp. 142-153
Kimura, Y., Hisano, Y., Kawahara, A., Higashijima, S., Efficient generation of knock-in transgenic zebrafish carrying reporter/driver genes by CRISPR/Cas9-mediated genome engineering (2014) Sci. Rep., 4, p. 6545
Li, J., Zhang, B.-B., Ren, Y.-G., Gu, S.-Y., Xiang, Y.-H., Huang, C., Du, J.-L., Intron targeting-mediated and endogenous gene integrity-maintaining knockin in zebrafish using the CRISPR/Cas9 system (2015) Cell Res., 25, pp. 634-637
Hisano, Y., Sakuma, T., Nakade, S., Ohga, R., Ota, S., Okamoto, H., Yamamoto, T., Kawahara, A., Precise in-frame integration of exogenous DNA mediated by CRISPR/Cas9 system in zebrafish (2015) Sci. Rep., 5, p. 8841
Hoshijima, K., Jurynec, M.J., Grunwald, D.J., Precise editing of the zebrafish genome made simple and efficient (2016) Dev. Cell, 36, pp. 654-667
Prykhozhij, S.V., Rajan, V., Gaston, D., Berman, J.N., CRISPR MultiTargeter: a web tool to find common and unique CRISPR single guide RNA targets in a set of similar sequences (2015) PLoS One, 10. , e0119372
Prykhozhij, S.V., Rajan, V., Berman, J.N., A guide to computational tools and design strategies for genome editing experiments in zebrafish using CRISPR/Cas9 (2016) Zebrafish, 13, pp. 70-73
Doench, J.G., Hartenian, E., Graham, D.B., Tothova, Z., Hegde, M., Smith, I., Sullender, M., Root, D.E., Rational design of highly active sgRNAs for CRISPR-Cas9-mediated gene inactivation (2014) Nat. Biotechnol., 32, pp. 1262-1267
Doench, J.G., Fusi, N., Sullender, M., Hegde, M., Vaimberg, E.W., Donovan, K.F., Smith, I., Root, D.E., Optimized sgRNA design to maximize activity and minimize off-target effects of CRISPR-Cas9 (2016) Nat. Biotechnol., 34, pp. 184-191
Xu, H., Xiao, T., Chen, C.-H., Li, W., Meyer, C., Wu, Q., Wu, D., Liu, S.X., Sequence determinants of improved CRISPR sgRNA design (2015) Genome Res.
Wong, N., Liu, W., Wang, X., WU-CRISPR: characteristics of functional guide RNAs for the CRISPR/Cas9 system (2015) Genome Biol., 16, p. 218
Chari, R., Mali, P., Moosburner, M., Church, G.M., Unraveling CRISPR-Cas9 genome engineering parameters via a library-on-library approach (2015) Nat. Methods, 12, pp. 1-7
Lin, Y., Cradick, T.J., Brown, M.T., Deshmukh, H., Ranjan, P., Sarode, N., Wile, B.M., Bao, G., CRISPR/Cas9 systems have off-target activity with insertions or deletions between target DNA and guide RNA sequences (2014) Nucleic Acids Res., 42, pp. 7473-7485
Heigwer, F., Kerr, G., Boutros, M., E-CRISP: fast CRISPR target site identification (2014) Nat. Methods, 11, pp. 122-123
Lei, Y., Lu, L., Liu, H.Y., Li, S., Xing, F., Chen, L.L., CRISPR-P: a web tool for synthetic single-guide RNA design of CRISPR-system in plants (2014) Mol. Plant, 7, pp. 1494-1496
Naito, Y., Hino, K., Bono, H., Ui-Tei, K., CRISPRdirect: software for designing CRISPR/Cas guide RNA with reduced off-target sites (2014) Bioinformatics
Hsu, P.D., Scott, D.A., Weinstein, J.A., Ran, F.A., Konermann, S., Agarwala, V., Li, Y., Zhang, F., DNA targeting specificity of RNA-guided Cas9 nucleases (2013) Nat. Biotechnol., 31, pp. 827-832
Montague, T.G., Cruz, J.M., Gagnon, J.A., Church, G.M., Valen, E., CHOPCHOP: a CRISPR/Cas9 and TALEN web tool for genome editing (2014) Nucleic Acids Res.
Guo, D., Li, X., Zhu, P., Feng, Y., Yang, J., Zheng, Z., Online high-throughput mutagenesis designer using scoring matrix of sequence-specific endonucleases (2015) J. Integr. Bioinform., 12, p. 283
Xie, S., Shen, B., Zhang, C., Huang, X., Zhang, Y., sgRNAcas9: a software package for designing CRISPR sgRNA and evaluating potential off-target cleavage sites (2014) PLoS One, 9, p. e100448
Zhu, L.J., Holmes, B.R., Aronin, N., Brodsky, M.H., CRISPRseek: a bioconductor package to identify target-specific guide RNAs for CRISPR-Cas9 genome-editing systems (2014) PLoS One, 9, p. e108424
Bae, S., Park, J., Kim, J.-S., Cas-OFFinder: a fast and versatile algorithm that searches for potential off-target sites of Cas9 RNA-guided endonucleases (2014) Bioinformatics, 30, pp. 1473-1475
Ledford, H., CRISPR, the disruptor (2015) Nature, 522, pp. 20-24
Webber, B.L., Raghu, S., Edwards, O.R., Opinion: is CRISPR-based gene drive a biocontrol silver bullet or global conservation threat? (2015) Proc. Natl. Acad. Sci., 112, pp. 10565-10567
Ma, M., Ye, A.Y., Zheng, W., Kong, L., A guide RNA sequence design platform for the CRISPR/Cas9 system for model organism genomes (2013) BioMed Res. Int., 2013, p. 270805
Liu, H., Wei, Z., Dominguez, A., Li, Y., Wang, X., Qi, L.S., CRISPR-ERA: a comprehensive design tool for CRISPR-mediated gene editing, repression and activation (2015) Bioinformatics, 31, pp. 3676-3678
