Recent Progress in CRISPR/Cas9 Technology

Yue Mei; Yan Wang; Huiqian Chen; Zhong Sheng Sun; Xing-Da Ju

doi:10.1016/j.jgg.2016.01.001

Volume 43 Issue 2

Feb. 2016

Turn off MathJax

Article Contents

Article Navigation > Journal of Genetics and Genomics > 2016 > 43(2): 63-75

PDF( 523 KB)

Recent Progress in CRISPR/Cas9 Technology

doi: 10.1016/j.jgg.2016.01.001

a
Beijing Institutes of Life Science, Chinese Academy of Sciences, Beijing 100101, China
b
University of Chinese Academy of Science, Beijing 100049, China
c
Institute of Genomic Medicine, Wenzhou Medical University, Wenzhou 325000, China
d
Department of Psychology, Northeast Normal University, Changchun 130021, China

More Information

Corresponding author: E-mail address: sunzs@mail.biols.ac.cn (Zhong Sheng Sun); E-mail address: juxd513@nenu.edu.cn (Xing-Da Ju)
Received Date: 2015-08-23
Revised Date: 2015-12-30
Accepted Date: 2016-01-08

Available Online: 2016-01-18

Publish Date: 2016-02-20

Abstract

Abstract

The clustered regularly interspaced short palindromic repeats (CRISPR)/Cas9 system, a simple and efficient tool for genome editing, has experienced rapid progress in its technology and applicability in the past two years. Here, we review the recent advances in CRISPR/Cas9 technology and the ways that have been adopted to expand our capacity for precise genome manipulation. First, we introduce the mechanism of CRISPR/Cas9, including its biochemical and structural implications. Second, we highlight the latest improvements in the CRISPR/Cas9 system, especially Cas9 protein modifications for customization. Third, we review its current applications, in which the versatile CRISPR/Cas9 system was employed to edit the genome, epigenome, or RNA of various organisms. Although CRISPR/Cas9 allows convenient genome editing accompanied by many benefits, we should not ignore the significant ethical and biosafety concerns that it raises. Finally, we discuss the prospective applications and challenges of several promising techniques adapted from CRISPR/Cas9.
- CRISPR/Cas9,
- Genome editing,
- Epigenome editing,
- RNA editing

FullText(HTML)

References(90)

References

[1]	Aida, T., Chiyo, K., Usami, T. et al. Cloning-free CRISPR/Cas system facilitates functional cassette knock-in in mice Genome Biol., 16 (2015),p. 87
[2]	Baltimore, D., Berg, P., Botchan, M. et al. Biotechnology. A prudent path forward for genomic engineering and germline gene modification Science, 348 (2015),pp. 36-38
[3]	Bassett, A.R., Kong, L., Liu, J.L. J. Genet. Genomics, 42 (2015),pp. 301-309
[4]	Bassett, A.R., Tibbit, C., Ponting, C.P. et al. Cell Rep., 4 (2013),pp. 220-228
[5]	Bedell, V.M., Wang, Y., Campbell, J.M. et al. Nature, 491 (2012),pp. 114-118
[6]	Bohannon, J. Biotechnology. Biologists devise invasion plan for mutations Science, 347 (2015)
[7]	Chang, N., Sun, C., Gao, L. et al. Genome editing with RNA-guided Cas9 nuclease in zebrafish embryos Cell Res., 23 (2013),pp. 465-472
[8]	Cho, S.W., Kim, S., Kim, Y. et al. Analysis of off-target effects of CRISPR/Cas-derived RNA-guided endonucleases and nickases Genome Res., 24 (2014),pp. 132-141
[9]	Cong, L., Ran, F.A., Cox, D. et al. Multiplex genome engineering using CRISPR/Cas systems Science, 339 (2013),pp. 819-823
[10]	Datsenko, K.A., Pougach, K., Tikhonov, A. et al. Molecular memory of prior infections activates the CRISPR/Cas adaptive bacterial immunity system Nat. Commun., 3 (2012),p. 945
[11]	Dickinson, D.J., Ward, J.D., Reiner, D.J. et al. Nat. Methods, 10 (2013),pp. 1028-1034
[12]	Dong, C., Qu, L., Wang, H. et al. Targeting hepatitis B virus cccDNA by CRISPR/Cas9 nuclease efficiently inhibits viral replication Antiviral Res., 118 (2015),pp. 110-117
[13]	Friedland, A.E., Tzur, Y.B., Esvelt, K.M. et al. Nat. Methods, 10 (2013),pp. 741-743
[14]	Fu, Y., Sander, J.D., Reyon, D. et al. Improving CRISPR-Cas nuclease specificity using truncated guide RNAs Nat. Biotechnol., 32 (2014),pp. 279-284
[15]	Fujii, W., Onuma, A., Sugiura, K. et al. Biochem. Biophys. Res. Commun., 445 (2014),pp. 791-794
[16]	Fujii, W., Onuma, A., Sugiura, K. et al. One-step generation of phenotype-expressing triple-knockout mice with heritable mutated alleles by the CRISPR/Cas9 system J. Reprod. Dev., 60 (2014),pp. 324-327
[17]	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., 439 (2013),pp. 132-136
[18]	Gantz, V.M., Bier, E. The mutagenic chain reaction: a method for converting heterozygous to homozygous mutations Science, 348 (2015),pp. 442-444
[19]	Gilbert, L.A., Larson, M.H., Morsut, L. et al. CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes Cell, 154 (2013),pp. 442-451
[20]	Gratz, S.J., Cummings, A.M., Nguyen, J.N. et al. Genetics, 194 (2013),pp. 1029-1035
[21]	Han, J., Zhang, J., Chen, L. et al. RNA Biol., 11 (2014),pp. 829-835
[22]	Heintze, J., Luft, C., Ketteler, R. A CRISPR CASe for high-throughput silencing Front. Genet., 4 (2013),p. 193
[23]	Hemphill, J., Borchardt, E.K., Brown, K. et al. Optical control of CRISPR/Cas9 gene editing J. Am. Chem. Soc., 137 (2015),pp. 5642-5645
[24]	Hilton, I.B., D'Ippolito, A.M., Vockley, C.M. et al. Epigenome editing by a CRISPR-Cas9-based acetyltransferase activates genes from promoters and enhancers Nat. Biotechnol., 33 (2015),pp. 510-517
[25]	Hsu, P.D., Lander, E.S., Zhang, F. Development and applications of CRISPR-Cas9 for genome engineering Cell, 157 (2014),pp. 1262-1278
[26]	Hwang, W.Y., Fu, Y., Reyon, D. et al. Efficient genome editing in zebrafish using a CRISPR-Cas system Nat. Biotechnol., 31 (2013),pp. 227-229
[27]	Hyun, Y., Kim, J., Cho, S. et al. Planta, 241 (2015),pp. 271-284
[28]	Jao, L.E., Wente, S.R., Chen, W. Efficient multiplex biallelic zebrafish genome editing using a CRISPR nuclease system Proc. Natl. Acad. Sci. USA, 110 (2013),pp. 13904-13909
[29]	Jinek, M., Chylinski, K., Fonfara, I. et al. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity Science, 337 (2012),pp. 816-821
[30]	Kim, D., Bae, S., Park, J. et al. Digenome-seq: genome-wide profiling of CRISPR-Cas9 off-target effects in human cells Nat. Methods, 12 (2015),pp. 237-243
[31]	Kleinstiver, B.P., Prew, M.S., Tsai, S.Q. et al. Engineered CRISPR-Cas9 nucleases with altered PAM specificities Nature, 523 (2015),pp. 481-485
[32]	Larson, M.H., Gilbert, L.A., Wang, X. et al. CRISPR interference (CRISPRi) for sequence-specific control of gene expression Nat. Protoc., 8 (2013),pp. 2180-2196
[33]	Lawhorn, I.E., Ferreira, J.P., Wang, C.L. PLoS One, 9 (2014),p. e113232
[34]	Levy, A., Goren, M.G., Yosef, I. et al. CRISPR adaptation biases explain preference for acquisition of foreign DNA Nature, 520 (2015),pp. 505-510
[35]	Li, D., Qiu, Z., Shao, Y. et al. Heritable gene targeting in the mouse and rat using a CRISPR-Cas system Nat. Biotechnol., 31 (2013),pp. 681-683
[36]	Li, F., Cowley, D.O., Banner, D. et al. Sci. Rep., 4 (2014),p. 5290
[37]	Li, J., Shou, J., Guo, Y. et al. Efficient inversions and duplications of mammalian regulatory DNA elements and gene clusters by CRISPR/Cas9 J. Mol. Cell Biol., 7 (2015),pp. 284-298
[38]	Li, W., Teng, F., Li, T. et al. Simultaneous generation and germline transmission of multiple gene mutations in rat using CRISPR-Cas systems Nat. Biotechnol., 31 (2013),pp. 684-686
[39]	Liang, P.P., Xu, Y.W., Zhang, X.Y. et al. CRISPR/Cas9-mediated gene editing in human tripronuclear zygotes Protein Cell, 6 (2015),pp. 363-372
[40]	Liao, H.K., Gu, Y., Diaz, A. et al. Use of the CRISPR/Cas9 system as an intracellular defense against HIV-1 infection in human cells Nat. Commun., 6 (2015),p. 6413
[41]	Liao, J., Karnik, R., Gu, H. et al. Nat. Genet., 47 (2015),pp. 469-478
[42]	Lin, S., Staahl, B.T., Alla, R.K. et al. Enhanced homology-directed human genome engineering by controlled timing of CRISPR/Cas9 delivery eLife, 3 (2014),p. e04766
[43]	Ma, S., Chang, J., Wang, X. et al. Sci. Rep., 4 (2014),p. 4489
[44]	Maddalo, D., Manchado, E., Concepcion, C.P. et al. Nature, 516 (2014),pp. 423-427
[45]	Mali, P., Yang, L.H., Esvelt, K.M. et al. Science, 339 (2013),pp. 823-826
[46]	Maruyama, T., Dougan, S.K., Truttmann, M.C. et al. Increasing the efficiency of precise genome editing with CRISPR-Cas9 by inhibition of nonhomologous end joining Nat. Biotechnol., 33 (2015),pp. 538-542
[47]	Mashiko, D., Young, S.A., Muto, M. et al. Feasibility for a large scale mouse mutagenesis by injecting CRISPR/Cas plasmid into zygotes Dev. Growth Differ., 56 (2014),pp. 122-129
[48]	Matsunaga, T., Yamashita, J.K. Single-step generation of gene knockout-rescue system in pluripotent stem cells by promoter insertion with CRISPR/Cas9 Biochem. Biophys. Res. Commun., 444 (2014),pp. 158-163
[49]	Nihongaki, Y., Yamamoto, S., Kawano, F. et al. CRISPR-Cas9-based photoactivatable transcription system Chem. Biol., 22 (2015),pp. 169-174
[50]	Nishimasu, H., Ran, F.A., Hsu, P.D. et al. Crystal structure of Cas9 in complex with guide RNA and target DNA Cell, 156 (2014),pp. 935-949
[51]	O'Connell, M.R., Oakes, B.L., Sternberg, S.H. et al. Programmable RNA recognition and cleavage by CRISPR/Cas9 Nature, 516 (2014),pp. 263-266
[52]	Ota, S., Hisano, Y., Ikawa, Y. et al. Multiple genome modifications by the CRISPR/Cas9 system in zebrafish Genes Cells, 19 (2014),pp. 555-564
[53]	Parikh, B.A., Beckman, D.L., Patel, S.J. et al. Detailed phenotypic and molecular analyses of genetically modified mice generated by CRISPR-Cas9-mediated editing PLoS One, 10 (2015),p. e0116484
[54]	Pefanis, E., Wang, J.G., Rothschild, G. et al. RNA exosome-regulated long non-coding RNA transcription controls super-enhancer activity Cell, 161 (2015),pp. 774-789
[55]	Platt, R.J., Chen, S.D., Zhou, Y. et al. CRISPR-Cas9 knockin mice for genome editing and cancer modeling Cell, 159 (2014),pp. 440-455
[56]	Polstein, L.R., Gersbach, C.A. A light-inducible CRISPR-Cas9 system for control of endogenous gene activation Nat. Chem. Biol., 11 (2015),pp. 198-200
[57]	Qin, W., Dion, S.L., Kutny, P.M. et al. Efficient CRISPR/Cas9-mediated genome editing in mice by zygote electroporation of nuclease Genetics, 200 (2015),pp. 423-430
[58]	Qin, W.N., Kutny, P., Dion, S. et al. One-step generation of mice carrying gene-edited alleles by the CRISPR/Cas-mediated genome engineering with high efficiency Transgenic Res., 23 (2014)
[59]	Ran, F.A., Cong, L., Yan, W.X. et al. Nature, 520 (2015),pp. 186-191
[60]	Ran, F.A., Hsu, P.D., Lin, C.Y. et al. Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity Cell, 154 (2013),pp. 1380-1389
[61]	Ran, F.A., Hsu, P.D., Wright, J. et al. Genome engineering using the CRISPR-Cas9 system Nat. Protoc., 8 (2013),pp. 2281-2308
[62]	Ratz, M., Testa, I., Hell, S.W. et al. CRISPR/Cas9-mediated endogenous protein tagging for RESOLFT super-resolution microscopy of living human cells Sci. Rep., 5 (2015),p. 9592
[63]	Rodriguez, E., Keiser, M., McLoughlin, H. et al. AAV-CRISPR: a new therapeutic approach to nucleotide repeat diseases Mol. Ther., 22 (2014)
[64]	Rojas-Fernandez, A., Herhaus, L., Macartney, T. et al. Rapid generation of endogenously driven transcriptional reporters in cells through CRISPR/Cas9 Sci. Rep., 5 (2015),p. 9811
[65]	Sapranauskas, R., Gasiunas, G., Fremaux, C. et al. Nucleic Acids Res., 39 (2011),pp. 9275-9282
[66]	Senis, E., Fatouros, C., Grosse, S. et al. An AAV vector toolbox for CRISPR/Cas9-mediated genome engineering Hum. Gene Ther., 25 (2014),pp. A24-A25
[67]	Seruggia, D., Fernandez, A., Cantero, M. et al. Functional validation of mouse tyrosinase non-coding regulatory DNA elements by CRISPR-Cas9-mediated mutagenesis Nucleic Acids Res., 43 (2015),pp. 4855-4867
[68]	Shen, B., Zhang, J., Wu, H. et al. Cell Res., 23 (2013),pp. 720-723
[69]	Shen, B., Zhang, W., Zhang, J. et al. Efficient genome modification by CRISPR-Cas9 nickase with minimal off-target effects Nat. Methods, 11 (2014),pp. 399-402
[70]	Singh, P., Schimenti, J.C., Bolcun-Filas, E. A mouse geneticist's practical guide to CRISPR applications Genetics, 199 (2015),pp. 1-15
[71]	Swiech, L., Heidenreich, M., Banerjee, A. et al. Nat. Biotechnol., 33 (2015),pp. 102-106
[72]	Tanenbaum, M.E., Gilbert, L.A., Qi, L.S. et al. A protein-tagging system for signal amplification in gene expression and fluorescence imaging Cell, 159 (2014),pp. 635-646
[73]	Urnov, F.D., Miller, J.C., Lee, Y.L. et al. Highly efficient endogenous human gene correction using designed zinc-finger nucleases Nature, 435 (2005),pp. 646-651
[74]	Wang, H., Yang, H., Shivalila, C.S. et al. One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering Cell, 153 (2013),pp. 910-918
[75]	Wang, J.W., Wang, A., Li, K.Y. et al. CRISPR/Cas9 nuclease cleavage combined with Gibson assembly for seamless cloning BioTechniques, 58 (2015),pp. 161-170
[76]	Wang, Z.P., Xing, H.L., Dong, L. et al. Genome Biol., 16 (2015),p. 144
[77]	Westra, E.R., Semenova, E., Datsenko, K.A. et al. Type I-E CRISPR-Cas systems discriminate target from non-target DNA through base pairing-independent PAM recognition PLoS Genet., 9 (2013),p. e1003742
[78]	Wu, X., Scott, D.A., Kriz, A.J. et al. Genome-wide binding of the CRISPR endonuclease Cas9 in mammalian cells Nat. Biotechnol., 32 (2014),pp. 670-676
[79]	Wu, Y.X., Liang, D., Wang, Y.H. et al. Cell Stem Cell, 13 (2013),pp. 659-662
[80]	Xu, J., Ren, X., Sun, J. et al. J. Genet. Genomics, 42 (2015),pp. 141-149
[81]	Xue, W., Chen, S., Yin, H. et al. CRISPR-mediated direct mutation of cancer genes in the mouse liver Nature, 514 (2014),pp. 380-384
[82]	Yang, H., Wang, H., Shivalila, C.S. et al. One-step generation of mice carrying reporter and conditional alleles by CRISPR/Cas-mediated genome engineering Cell, 154 (2013),pp. 1370-1379
[83]	Yin, H., Xue, W., Chen, S. et al. Genome editing with Cas9 in adult mice corrects a disease mutation and phenotype Nat. Biotechnol., 32 (2014),pp. 551-553
[84]	Yu, Z., Ren, M., Wang, Z. et al. Genetics, 195 (2013),pp. 289-291
[85]	Zhang, L.Q., Jia, R.R., Palange, N.J. et al. Large genomic fragment deletions and insertions in mouse using CRISPR/Cas9 PLoS One, 10 (2015),p. e0120396
[86]	Zhang, X.X. Urgency to rein in the gene-editing technology Protein Cell, 6 (2015)
[87]	Zhang, Z.Q., Xu, K., Xin, Y. et al. An efficient method for multiple site-directed mutagenesis using type IIs restriction enzymes Anal. Biochem., 476 (2015),pp. 26-28
[88]	Zhong, H., Chen, Y.Y., Li, Y.M. et al. Sci. Rep., 5 (2015),p. 8366
[89]	Zhou, J., Shen, B., Zhang, W. et al. One-step generation of different immunodeficient mice with multiple gene modifications by CRISPR/Cas9 mediated genome engineering Int. J. Biochem. Cell Biol., 46 (2014),pp. 49-55
[90]	Zhu, X., Xu, Y., Yu, S. et al. An efficient genotyping method for genome-modified animals and human cells generated with CRISPR/Cas9 system Sci. Rep., 4 (2014),p. 6420