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Recent Progress in CRISPR/Cas9 Technology

Mei, Yue, Wang, Yan, Chen, Huiqian, Sun, Zhong Sheng, Ju, Xing-Da·2016·Journal of Genetics and Genomics

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.

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Crossref · 10.1016/j.jgg.2016.01.001

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  • tracrRNA is a long stretch of loops that serve as a binding scaffold for Cas-9 nuclease.

    “whereas tracrRNA is a long stretch of loops that serve as a binding scaffold for Cas-9 nuclease.”
  • HNH domain cleaves the complementary strand, while the RuvC domain cleaves the non-complementary strand of target DNA to produce predominantly blunt-ended DSBs.

    “HNH domain cleaves the complementary strand, while the RuvC domain cleaves the non-complementary strand of target DNA to produce predominantly blunt-ended DSBs.”
  • In prokaryotes, guide RNA targets viral DNA; in gene-editing, it can be synthetically designed by combining crRNA and tracrRNA to form sgRNA to target almost any gene sequence.

    “In prokaryotes, the guide RNA is used to target viral DNA, but in the gene-editing tool, it can be synthetically designed by combining crRNA and tracrRNA to form a single guide RNA (sgRNA) in order to target almost any gene sequence supposed to be edited.11”
  • Guide RNA is made up of two parts: CRISPR RNA (crRNA) and trans-activating CRISPR RNA (tracrRNA).

    “Guide RNA is made up of two parts, CRISPR RNA (crRNA) and trans-activating CRISPR RNA (tracrRNA).”
  • The designed sgRNA recognizes the target sequence in the gene of interest through complementary base pairing.

    “The designed sgRNA recognizes the target sequence in the gene of interest through a complementary base pair.”

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Research works printed but not linked: 74

  1. Aida, 2015, Cloning-free CRISPR/Cas system facilitates functional cassette knock-in in mice, Genome Biol., 16, 87, 10.1186/s13059-015-0653-x · DOI
  2. Bassett, 2015, A genome-wide CRISPR library for high-throughput genetic screening in Drosophila cells, J. Genet. Genomics, 42, 301, 10.1016/j.jgg.2015.03.011 · DOI
  3. Bassett, 2013, Highly efficient targeted mutagenesis of Drosophila with the CRISPR/Cas9 system, Cell Rep., 4, 220, 10.1016/j.celrep.2013.06.020 · DOI
  4. Bedell, 2012, In vivo genome editing using a high-efficiency TALEN system, Nature, 491, 114, 10.1038/nature11537 · DOI
  5. Bohannon, 2015, Biotechnology. Biologists devise invasion plan for mutations, Science, 347, 10.1126/science.347.6228.1300 · DOI
  6. Chang, 2013, Genome editing with RNA-guided Cas9 nuclease in zebrafish embryos, Cell Res., 23, 465, 10.1038/cr.2013.45 · DOI
  7. Cho, 2014, Analysis of off-target effects of CRISPR/Cas-derived RNA-guided endonucleases and nickases, Genome Res., 24, 132, 10.1101/gr.162339.113 · DOI · Paper page
  8. Cong, 2013, Multiplex genome engineering using CRISPR/Cas systems, Science, 339, 819, 10.1126/science.1231143 · DOI · Paper page
  9. Datsenko, 2012, Molecular memory of prior infections activates the CRISPR/Cas adaptive bacterial immunity system, Nat. Commun., 3, 945, 10.1038/ncomms1937 · DOI · Paper page
  10. Dickinson, 2013, Engineering the C. elegans genome using Cas9-triggered homologous recombination, Nat. Methods, 10, 1028, 10.1038/nmeth.2641 · DOI
  11. Dong, 2015, Targeting hepatitis B virus cccDNA by CRISPR/Cas9 nuclease efficiently inhibits viral replication, Antiviral Res., 118, 110, 10.1016/j.antiviral.2015.03.015 · DOI
  12. Fujii, 2014, Efficient generation of genome-modified mice via offset-nicking by CRISPR/Cas system, Biochem. Biophys. Res. Commun., 445, 791, 10.1016/j.bbrc.2014.01.141 · DOI
  13. Fujii, 2014, One-step generation of phenotype-expressing triple-knockout mice with heritable mutated alleles by the CRISPR/Cas9 system, J. Reprod. Dev., 60, 324, 10.1262/jrd.2013-139 · DOI
  14. Fujita, 2013, 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, 132, 10.1016/j.bbrc.2013.08.013 · DOI
  15. Gantz, 2015, The mutagenic chain reaction: a method for converting heterozygous to homozygous mutations, Science, 348, 442, 10.1126/science.aaa5945 · DOI
  16. Gratz, 2013, Genome engineering of Drosophila with the CRISPR RNA-guided Cas9 nuclease, Genetics, 194, 1029, 10.1534/genetics.113.152710 · DOI
  17. Han, 2014, Efficient in vivo deletion of a large imprinted lncRNA by CRISPR/Cas9, RNA Biol., 11, 829, 10.4161/rna.29624 · DOI
  18. Heintze, 2013, A CRISPR CASe for high-throughput silencing, Front. Genet., 4, 193, 10.3389/fgene.2013.00193 · DOI
  19. Hemphill, 2015, Optical control of CRISPR/Cas9 gene editing, J. Am. Chem. Soc., 137, 5642, 10.1021/ja512664v · DOI
  20. Hilton, 2015, Epigenome editing by a CRISPR-Cas9-based acetyltransferase activates genes from promoters and enhancers, Nat. Biotechnol., 33, 510, 10.1038/nbt.3199 · DOI
  21. Hsu, 2014, Development and applications of CRISPR-Cas9 for genome engineering, Cell, 157, 1262, 10.1016/j.cell.2014.05.010 · DOI · Paper page
  22. Hyun, 2015, Site-directed mutagenesis in Arabidopsis thaliana using dividing tissue-targeted RGEN of the CRISPR/Cas system to generate heritable null alleles, Planta, 241, 271, 10.1007/s00425-014-2180-5 · DOI
  23. Jao, 2013, Efficient multiplex biallelic zebrafish genome editing using a CRISPR nuclease system, Proc. Natl. Acad. Sci. USA, 110, 13904, 10.1073/pnas.1308335110 · DOI · Paper page
  24. Jinek, 2012, A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity, Science, 337, 816, 10.1126/science.1225829 · DOI · Paper page
  25. Kim, 2015, Digenome-seq: genome-wide profiling of CRISPR-Cas9 off-target effects in human cells, Nat. Methods, 12, 237, 10.1038/nmeth.3284 · DOI · Paper page
  26. Larson, 2013, CRISPR interference (CRISPRi) for sequence-specific control of gene expression, Nat. Protoc., 8, 2180, 10.1038/nprot.2013.132 · DOI
  27. Lawhorn, 2014, Evaluation of sgRNA target sites for CRISPR-mediated repression of TP53, PLoS One, 9, e113232, 10.1371/journal.pone.0113232 · DOI
  28. Levy, 2015, CRISPR adaptation biases explain preference for acquisition of foreign DNA, Nature, 520, 505, 10.1038/nature14302 · DOI
  29. Li, 2013, Heritable gene targeting in the mouse and rat using a CRISPR-Cas system, Nat. Biotechnol., 31, 681, 10.1038/nbt.2661 · DOI
  30. Li, 2014, Efficient genetic manipulation of the NOD-Rag1-/-IL2RgammaC-null mouse by combining in vitro fertilization and CRISPR/Cas9 technology, Sci. Rep., 4, 5290, 10.1038/srep05290 · DOI
  31. Li, 2015, Efficient inversions and duplications of mammalian regulatory DNA elements and gene clusters by CRISPR/Cas9, J. Mol. Cell Biol., 7, 284, 10.1093/jmcb/mjv016 · DOI
  32. Li, 2013, Simultaneous generation and germline transmission of multiple gene mutations in rat using CRISPR-Cas systems, Nat. Biotechnol., 31, 684, 10.1038/nbt.2652 · DOI
  33. Liang, 2015, CRISPR/Cas9-mediated gene editing in human tripronuclear zygotes, Protein Cell, 6, 363, 10.1007/s13238-015-0153-5 · DOI · Paper page
  34. Liao, 2015, Use of the CRISPR/Cas9 system as an intracellular defense against HIV-1 infection in human cells, Nat. Commun., 6, 6413, 10.1038/ncomms7413 · DOI
  35. Liao, 2015, Targeted disruption of DNMT1, DNMT3A and DNMT3B in human embryonic stem cells, Nat. Genet., 47, 469, 10.1038/ng.3258 · DOI
  36. Lin, 2014, Enhanced homology-directed human genome engineering by controlled timing of CRISPR/Cas9 delivery, eLife, 3, e04766, 10.7554/eLife.04766 · DOI · Paper page
  37. Ma, 2014, CRISPR/Cas9 mediated multiplex genome editing and heritable mutagenesis of BmKu70 in Bombyx mori, Sci. Rep., 4, 4489, 10.1038/srep04489 · DOI
  38. Mashiko, 2014, Feasibility for a large scale mouse mutagenesis by injecting CRISPR/Cas plasmid into zygotes, Dev. Growth Differ., 56, 122, 10.1111/dgd.12113 · DOI
  39. Matsunaga, 2014, Single-step generation of gene knockout-rescue system in pluripotent stem cells by promoter insertion with CRISPR/Cas9, Biochem. Biophys. Res. Commun., 444, 158, 10.1016/j.bbrc.2014.01.037 · DOI
  40. Nihongaki, 2015, CRISPR-Cas9-based photoactivatable transcription system, Chem. Biol., 22, 169, 10.1016/j.chembiol.2014.12.011 · DOI
  41. O'Connell, 2014, Programmable RNA recognition and cleavage by CRISPR/Cas9, Nature, 516, 263, 10.1038/nature13769 · DOI
  42. Ota, 2014, Multiple genome modifications by the CRISPR/Cas9 system in zebrafish, Genes Cells, 19, 555, 10.1111/gtc.12154 · DOI
  43. Parikh, 2015, Detailed phenotypic and molecular analyses of genetically modified mice generated by CRISPR-Cas9-mediated editing, PLoS One, 10, e0116484, 10.1371/journal.pone.0116484 · DOI
  44. Pefanis, 2015, RNA exosome-regulated long non-coding RNA transcription controls super-enhancer activity, Cell, 161, 774, 10.1016/j.cell.2015.04.034 · DOI · Paper page
  45. Platt, 2014, CRISPR-Cas9 knockin mice for genome editing and cancer modeling, Cell, 159, 440, 10.1016/j.cell.2014.09.014 · DOI · Paper page
  46. Polstein, 2015, A light-inducible CRISPR-Cas9 system for control of endogenous gene activation, Nat. Chem. Biol., 11, 198, 10.1038/nchembio.1753 · DOI
  47. Qin, 2015, Efficient CRISPR/Cas9-mediated genome editing in mice by zygote electroporation of nuclease, Genetics, 200, 423, 10.1534/genetics.115.176594 · DOI
  48. Qin, 2014, One-step generation of mice carrying gene-edited alleles by the CRISPR/Cas-mediated genome engineering with high efficiency, Transgenic Res., 23
  49. Ran, 2013, Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity, Cell, 154, 1380, 10.1016/j.cell.2013.08.021 · DOI · Paper page
  50. Ratz, 2015, CRISPR/Cas9-mediated endogenous protein tagging for RESOLFT super-resolution microscopy of living human cells, Sci. Rep., 5, 9592, 10.1038/srep09592 · DOI
  51. Rodriguez, 2014, AAV-CRISPR: a new therapeutic approach to nucleotide repeat diseases, Mol. Ther., 22
  52. Rojas-Fernandez, 2015, Rapid generation of endogenously driven transcriptional reporters in cells through CRISPR/Cas9, Sci. Rep., 5, 9811, 10.1038/srep09811 · DOI
  53. Sapranauskas, 2011, The Streptococcus thermophilus CRISPR/Cas system provides immunity in E. coli, Nucleic Acids Res., 39, 9275, 10.1093/nar/gkr606 · DOI
  54. Senis, 2014, An AAV vector toolbox for CRISPR/Cas9-mediated genome engineering, Hum. Gene Ther., 25, A24
  55. Seruggia, 2015, Functional validation of mouse tyrosinase non-coding regulatory DNA elements by CRISPR-Cas9-mediated mutagenesis, Nucleic Acids Res., 43, 4855, 10.1093/nar/gkv375 · DOI
  56. Shen, 2013, Generation of gene-modified mice via Cas9/RNA-mediated gene targeting, Cell Res., 23, 720, 10.1038/cr.2013.46 · DOI · Paper page
  57. Shen, 2014, Efficient genome modification by CRISPR-Cas9 nickase with minimal off-target effects, Nat. Methods, 11, 399, 10.1038/nmeth.2857 · DOI · Paper page
  58. Singh, 2015, A mouse geneticist's practical guide to CRISPR applications, Genetics, 199, 1, 10.1534/genetics.114.169771 · DOI
  59. Tanenbaum, 2014, A protein-tagging system for signal amplification in gene expression and fluorescence imaging, Cell, 159, 635, 10.1016/j.cell.2014.09.039 · DOI
  60. Urnov, 2005, Highly efficient endogenous human gene correction using designed zinc-finger nucleases, Nature, 435, 646, 10.1038/nature03556 · DOI
  61. Wang, 2015, CRISPR/Cas9 nuclease cleavage combined with Gibson assembly for seamless cloning, BioTechniques, 58, 161, 10.2144/000114261 · DOI
  62. Wang, 2015, Egg cell-specific promoter-controlled CRISPR/Cas9 efficiently generates homozygous mutants for multiple target genes in Arabidopsis in a single generation, Genome Biol., 16, 144, 10.1186/s13059-015-0715-0 · DOI
  63. Westra, 2013, Type I-E CRISPR-Cas systems discriminate target from non-target DNA through base pairing-independent PAM recognition, PLoS Genet., 9, e1003742, 10.1371/journal.pgen.1003742 · DOI
  64. Xu, 2015, A toolkit of CRISPR-based genome editing systems in Drosophila, J. Genet. Genomics, 42, 141, 10.1016/j.jgg.2015.02.007 · DOI
  65. Xue, 2014, CRISPR-mediated direct mutation of cancer genes in the mouse liver, Nature, 514, 380, 10.1038/nature13589 · DOI · Paper page
  66. Yang, 2013, One-step generation of mice carrying reporter and conditional alleles by CRISPR/Cas-mediated genome engineering, Cell, 154, 1370, 10.1016/j.cell.2013.08.022 · DOI · Paper page
  67. Yin, 2014, Genome editing with Cas9 in adult mice corrects a disease mutation and phenotype, Nat. Biotechnol., 32, 551, 10.1038/nbt.2884 · DOI · Paper page
  68. Yu, 2013, Highly efficient genome modifications mediated by CRISPR/Cas9 in Drosophila, Genetics, 195, 289, 10.1534/genetics.113.153825 · DOI
  69. Zhang, 2015, Large genomic fragment deletions and insertions in mouse using CRISPR/Cas9, PLoS One, 10, e0120396, 10.1371/journal.pone.0120396 · DOI
  70. Zhang, 2015, Urgency to rein in the gene-editing technology, Protein Cell, 6, 10.1007/s13238-015-0161-5 · DOI
  71. Zhang, 2015, An efficient method for multiple site-directed mutagenesis using type IIs restriction enzymes, Anal. Biochem., 476, 26, 10.1016/j.ab.2015.01.010 · DOI
  72. Zhong, 2015, CRISPR-engineered mosaicism rapidly reveals that loss of Kcnj13 function in mice mimics human disease phenotypes, Sci. Rep., 5, 8366, 10.1038/srep08366 · DOI
  73. Zhou, 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, 10.1016/j.biocel.2013.10.010 · DOI
  74. Zhu, 2014, An efficient genotyping method for genome-modified animals and human cells generated with CRISPR/Cas9 system, Sci. Rep., 4, 6420, 10.1038/srep06420 · DOI

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Metadata

Authors
Mei, Y., Wang, Y., Chen, H., Sun, Z. S., & Ju, X.-D.
Venue
Journal of Genetics and Genomics
Publisher
Elsevier BV
Published
2016-02
Volume
43
Issue
2
Pages
63-75
ISSN
1673-8527
Cited by
148
References
16
Language
en
Funders
  • Major State Basic Research Development Program of China (2012CB517902, 2012CB517904)
  • Fundamental Research Funds for the Central Universities, (14QNJJ042)
  • National Health and Family Planning Commission of China (201302002)

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