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Recent advances of genome editing and related technologies in China

Gene Therapy volume 27, pages 312–320 (2020)Cite this article

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Abstract

Genome editing is a powerful tool, enabling scientists to alter DNA sequence at virtually any genome locus in any species. Different technologies have been developed employing programmable nucleases including meganuclease, zinc-finger nucleases, transcription activator-like effector nucleases, and most recently CRISPR-Cas systems. Chinese research groups are making important contributions at an increasing speed in genome editing field in recent years. In this review, we summarize recent progress made by Chinese scientists on the technological development of genome editing and beyond, focusing on the optimization and expanded application of existing genome editing tools, as well as the exploration of novel proteins as potential genome editing tools.

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References

  1. Danna K, Nathans D. Specific cleavage of simian virus 40 DNA by restriction endonuclease of Haemophilus influenzae. Proc Natl Acad Sci USA. 1971;68:2913–7.

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Kelly TJ, Smith HO. A restriction enzyme from Haemophilus influenzae: II. Base sequence of the recognition site. J Mol Biol. 1970;51:393–409.

    CAS  PubMed  Google Scholar 

  3. Smith HO, Wilcox KW. A restriction enzyme from Haemophilus influenzae. I. Purification and general properties. J Mol Biol. 1970;51:379–91.

    CAS  PubMed  Google Scholar 

  4. Stoddard BL. Homing endonuclease structure and function. Q Rev Biophys. 2005;38:49–95.

    CAS  PubMed  Google Scholar 

  5. Silva G, Poirot L, Galetto R, Smith J, Montoya G, Duchateau P, et al. Meganucleases and other tools for targeted genome engineering: perspectives and challenges for gene therapy. Curr Gene Ther. 2011;11:11–27.

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Stoddard BL. Homing endonucleases from mobile group I introns: discovery to genome engineering. Mobile DNA. 2014;5:7.

    PubMed  PubMed Central  Google Scholar 

  7. Kim YG, Cha J, Chandrasegaran S. Hybrid restriction enzymes: zinc finger fusions to Fok I cleavage domain. Proc Natl Acad Sci USA. 1996;93:1156–60.

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Cathomen T, Joung JK. Zinc-finger nucleases: the next generation emerges. Mol Ther. 2008;16:1200–7.

    CAS  PubMed  Google Scholar 

  9. Carroll D. Genome engineering with zinc-finger nucleases. Genetics. 2011;188:773–82.

    CAS  PubMed  PubMed Central  Google Scholar 

  10. 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;186:757–61.

    CAS  PubMed  PubMed Central  Google Scholar 

  11. 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;326:1509–12.

    CAS  PubMed  Google Scholar 

  12. Moscou MJ, Bogdanove AJ. A simple cipher governs DNA recognition by TAL effectors. Science. 2009;326:1501.

    CAS  PubMed  Google Scholar 

  13. 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;337:816–21.

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Koonin EV, Makarova KS. Origins and evolution of CRISPR-Cas systems. Philos Trans R Soc Lond B Biol Sci. 2019;374:20180087.

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Ishino Y, Krupovic M, Forterre P. History of CRISPR-Cas from encounter with a mysterious repeated sequence to genome editing technology. J Bacteriol. 2018;200:e00580–17.

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Lo A, Qi L. Genetic and epigenetic control of gene expression by CRISPR-Cas systems. F1000Res. 2017;6:1–16.

    Google Scholar 

  17. Pulecio J, Verma N, Mejia-Ramirez E, Huangfu D, Raya A. CRISPR/Cas9-based engineering of the epigenome. Cell Stem Cell. 2017;21:431–47.

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Xu X, Qi LS. A CRISPR-dCas toolbox for genetic engineering and synthetic biology. J Mol Biol. 2019;431:34–47.

    CAS  PubMed  Google Scholar 

  19. Brezgin S, Kostyusheva A, Kostyushev D, Chulanov V. Dead Cas systems: types, principles, and applications. Int J Mol Sci. 2019;20:6041.

    CAS  PubMed Central  Google Scholar 

  20. Martin-Laffon J, Kuntz M, Ricroch AE. Worldwide CRISPR patent landscape shows strong geographical biases. Nat Biotechnol. 2019;37:613–20.

    CAS  PubMed  Google Scholar 

  21. Huang Y, Porter A, Zhang Y, Barrangou R. Collaborative networks in gene editing. Nat Biotechnol. 2019;37:1107–9.

    CAS  PubMed  Google Scholar 

  22. Zhang SY, Chen HT, Wang JK. Generate TALE/TALEN as easily and rapidly as generating CRISPR. Mol Ther. 2019;13:310–20.

    CAS  Google Scholar 

  23. Zhao JL, Sun WY, Liang J, Jiang J, Wu Z. A one-step system for convenient and flexible assembly of transcription activator-like effector nucleases (TALENs). Mol Cells. 2016;39:687–91.

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Yang J, Yuan P, Wen D, Sheng Y, Zhu S, Yu Y, et al. ULtiMATE system for rapid assembly of customized TAL effectors. PloS ONE. 2013;8:e75649.

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Zhang ZQ, Li D, Xu HR, Xin Y, Zhang TT, Ma LX, et al. A simple and efficient method for assembling TALE protein based on plasmid library. PloS ONE. 2013;8:e66459.

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Yang J, Zhang Y, Yuan P, Zhou Y, Cai C, Ren Q, et al. Complete decoding of TAL effectors for DNA recognition. Cell Res. 2014;24:628–31.

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Zhao CZ, Zheng XG, Qu WB, Li GL, Li XY, Miao YL, et al. CRISPR-offinder: a CRISPR guide RNA design and off-target searching tool for user-defined protospacer adjacent motif. Int J Biol Sci. 2017;13:1470–8.

    PubMed  PubMed Central  Google Scholar 

  28. Yan JF, Chuai GH, Zhou C, Zhu CY, Yang J, Zhang C, et al. Benchmarking CRISPR on-target sgRNA design. Brief Bioinform. 2018;19:721–4.

    CAS  PubMed  Google Scholar 

  29. Sun JM, Liu H, Liu JX, Cheng SK, Peng Y, Zhang QH, et al. CRISPR-local: a local single-guide RNA (sgRNA) design tool for non-reference plant genomes. Bioinformatics. 2019;35:2501–3.

    CAS  PubMed  Google Scholar 

  30. Chuai GH, Ma HH, Yan JF, Chen M, Hong NF, Xue DY, et al. DeepCRISPR: optimized CRISPR guide RNA design by deep learning. Genome Biol. 2018;19:80.

    PubMed  PubMed Central  Google Scholar 

  31. Guo JH, Wang TM, Guan CG, Liu B, Luo C, Xie Z, et al. Improved sgRNA design in bacteria via genome-wide activity profiling. Nucleic Acids Res. 2018;46:7052–69.

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Xue L, Tang B, Chen W, Luo JS. Prediction of CRISPR sgRNA activity using a deep convolutional neural network. J Chem Inf Model. 2019;59:615–24.

    CAS  PubMed  Google Scholar 

  33. Xie SS, Shen B, Zhang CB, Huang XX, Zhang YL. sgRNAcas9: a software package for designing CRISPR sgRNA and evaluating potential off-target cleavage sites. PloS ONE. 2014;9:e100448.

    PubMed  PubMed Central  Google Scholar 

  34. Wang L, Zhang JH. Prediction of sgRNA on-target activity in bacteria by deep learning. Bmc Bioinform. 2019;20:517.

    Google Scholar 

  35. Xiong YY, Xie XW, Wang YZ, Ma WB, Liang PP, Zhou SY, et al. pgRNAFinder: a web-based tool to design distance independent paired-gRNA. Bioinformatics. 2017;33:3642–4.

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Zhang HW, Zhang XX, Fan CX, Xie Q, Xu CX, Zhao Q, et al. A novel sgRNA selection system for CRISPR-Cas9 in mammalian cells. Biochem Biophys Res Commun. 2016;471:528–32.

    CAS  PubMed  Google Scholar 

  37. Liang G, Zhang HM, Lou DJ, Yu DQ. Selection of highly efficient sgRNAs for CRISPR/Cas9-based plant genome editing. Sci Rep. 2016;6:21451.

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Chen W, Zhang GQ, Li J, Zhang X, Huang SL, Xiang SL, et al. CRISPRlnc: a manually curated database of validated sgRNAs for lncRNAs. Nucleic Acids Res. 2019;47:D63–8.

    CAS  PubMed  Google Scholar 

  39. Zhou JK, Wang JY, Shen B, Chen L, Su Y, Yang J, et al. Dual sgRNAs facilitate CRISPR/Cas9-mediated mouse genome targeting. FEBS J. 2014;281:1717–25.

    CAS  PubMed  Google Scholar 

  40. Wu JJ, Tang Y, Zhang CL. Targeting N-terminal huntingtin with a dual-sgRNA strategy by CRISPR/Cas9. Biomed Res Int. 2019;2019:1039623.

    PubMed  PubMed Central  Google Scholar 

  41. Tang YD, Guo JC, Wang TY, Zhao K, Liu JT, Gao JC, et al. CRISPR/Cas9-mediated 2-sgRNA cleavage facilitates pseudorabies virus editing. FASEB J. 2018;32:4293–301.

    CAS  PubMed  Google Scholar 

  42. Chen XY, Xu F, Zhu CM, Ji JJ, Zhou XF, Feng XZ, et al. Dual sgRNA-directed gene knockout using CRISPR/Cas9 technology in Caenorhabditis elegans. Sci Rep. 2014;4:7581.

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Zuo E, Cai YJ, Li K, Wei Y, Wang BA, Sun Y, et al. One-step generation of complete gene knockout mice and monkeys by CRISPR/Cas9-mediated gene editing with multiple sgRNAs. Cell Res. 2017;27:933–45.

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Zhang JP, Li XL, Neises A, Chen WQ, Hu LP, Ji GZ, et al. Different effects of sgRNA length on CRISPR-mediated gene knockout efficiency. Sci Rep. 2016;6:28566.

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Xu JY, Lian W, Jia YN, Li LY, Huang Z. Optimized guide RNA structure for genome editing via Cas9. Oncotarget. 2017;8:94166–71.

    PubMed  PubMed Central  Google Scholar 

  46. Long L, Guo DD, Gao W, Yang WW, Hou LP, Ma XN, et al. Optimization of CRISPR/Cas9 genome editing in cotton by improved sgRNA expression. Plant Methods. 2018;14:85.

    PubMed  PubMed Central  Google Scholar 

  47. Liu WQ, Li SF, Zhang YB, Li JS, Li YP. Efficient CRISPR-based genome editing using tandem guide RNAs and editable surrogate reporters. FEBS Open Bio. 2018;8:1167–75.

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Zhang DB, Zhang HW, Li TD, Chen KL, Qiu JL, Gao CX. Perfectly matched 20-nucleotide guide RNA sequences enable robust genome editing using high-fidelity SpCas9 nucleases. Genome Biol. 2017;18:191.

    PubMed  PubMed Central  Google Scholar 

  49. Mu W, Zhang Y, Xue X, Liu L, Wei X, Wang H. 5’ capped and 3’ polyA-tailed sgRNAs enhance the efficiency of CRISPR-Cas9 system. Protein Cell. 2019;10:223–8.

    CAS  PubMed  Google Scholar 

  50. Mu W, Tang N, Cheng C, Sun W, Wei X, Wang H. In vitro transcribed sgRNA causes cell death by inducing interferon release. Protein Cell. 2019;10:461–5.

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Ren XJ, Yang ZH, Xu J, Sun J, Mao DC, Hu YH, et al. Enhanced specificity and efficiency of the CRISPR/Cas9 system with optimized sgRNA parameters in Drosophila. Cell Rep. 2014;9:1151–62.

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Choi GCG, Zhou P, Yuen CTL, Chan BKC, Xu F, Bao S, et al. Combinatorial mutagenesis en masse optimizes the genome editing activities of SpCas9. Nat Methods. 2019;16:722–30.

    CAS  PubMed  Google Scholar 

  53. Ma DC, Xu ZM, Zhang ZY, Chen X, Zeng XZ, Zhang YY, et al. Engineer chimeric Cas9 to expand PAM recognition based on evolutionary information. Nat Commun. 2019;10:560.

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Zetsche B, Gootenberg JS, Abudayyeh OO, Slaymaker IM, Makarova KS, Essletzbichler P, et al. Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell. 2015;163:759–71.

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Tu M, Lin L, Cheng Y, He X, Sun H, Xie H, et al. A ‘new lease of life’: FnCpf1 possesses DNA cleavage activity for genome editing in human cells. Nucleic Acids Res. 2017;45:11295–304.

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Teng F, Li J, Cui TT, Xu K, Guo L, Gao QQ, et al. Enhanced mammalian genome editing by new Cas12a orthologs with optimized crRNA scaffolds. Genome Biol. 2019;20:15.

    PubMed  PubMed Central  Google Scholar 

  57. Wu H, Liu QS, Shi H, Xie JK, Zhang QJ, Ouyang Z, et al. Engineering CRISPR/Cpf1 with tRNA promotes genome editing capability in mammalian systems. Cell Mol Life Sci. 2018;75:3593–607.

    CAS  PubMed  Google Scholar 

  58. Zhao C, Zhao YZ, Zhang JF, Lu J, Chen L, Zhang Y, et al. HIT-Cas9: a CRISPR/Cas9 genome-editing device under tight and effective drug control. Mol Ther Nucleic Acids. 2018;13:208–19.

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Zhao C, Zhang Y, Zhao YZ, Ying Y, Ai RN, Zhang JF, et al. Multiple chemical inducible Tal effectors for genome editing and transcription activation. ACS Chem Biol. 2018;13:609–17.

    CAS  PubMed  Google Scholar 

  60. Lin B, An Y, Meng L, Zhang H, Song J, Zhu Z, et al. Control of CRISPR-Cas9 with small molecule-activated allosteric aptamer regulating sgRNAs. Chem Commun. 2019;55:12223–6.

    CAS  Google Scholar 

  61. Nishida K, Arazoe T, Yachie N, Banno S, Kakimoto M, Tabata M, et al. Targeted nucleotide editing using hybrid prokaryotic and vertebrate adaptive immune systems. Science. 2016;353:aaf8729.

    PubMed  Google Scholar 

  62. Komor AC, Kim YB, Packer MS, Zuris JA, Liu DR. Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage. Nature. 2016;533:420–4.

    CAS  PubMed  PubMed Central  Google Scholar 

  63. Gaudelli NM, Komor AC, Rees HA, Packer MS, Badran AH, Bryson DI, et al. Programmable base editing of A*T to G*C in genomic DNA without DNA cleavage. Nature. 2017;551:464–71.

    CAS  PubMed  PubMed Central  Google Scholar 

  64. Li X, Wang Y, Liu Y, Yang B, Wang X, Wei J, et al. Base editing with a Cpf1-cytidine deaminase fusion. Nat Biotechnol. 2018;36:324–7.

    CAS  PubMed  Google Scholar 

  65. Zhang YH, Qin W, Lu XC, Xu JS, Huang HG, Bai HP, et al. Programmable base editing of zebrafish genome using a modified CRISPR-Cas9 system. Nat Commun. 2017;8:118.

    CAS  PubMed  PubMed Central  Google Scholar 

  66. Wu Y, Xu W, Wang FP, Zhao S, Feng F, Song JL, et al. Increasing cytosine base editing scope and efficiency with engineered Cas9-PmCDA1 fusions and the modified sgRNA in rice. Front Genet. 2019;10:379.

    PubMed  PubMed Central  Google Scholar 

  67. Qin R, Li J, Li H, Zhang Y, Liu X, Miao Y, et al. Developing a highly efficient and wildly adaptive CRISPR-SaCas9 toolset for plant genome editing. Plant Biotechnol J. 2019;17:706–8.

    PubMed  PubMed Central  Google Scholar 

  68. Liu XY, Li GL, Zhou XL, Qiao YB, Wang RX, Tang SH, et al. Improving editing efficiency for the sequences with NGH PAM using xCas9-derived base editors. Mol Ther Nucleic Acids. 2019;17:626–35.

    PubMed  PubMed Central  Google Scholar 

  69. Hua K, Tao XP, Zhu JK. Expanding the base editing scope in rice by using Cas9 variants. Plant Biotechnol J. 2019;17:499–504.

    PubMed  Google Scholar 

  70. Zeng D, Li X, Huang J, Li Y, Cai S, Yu W, et al. Engineered Cas9 variant tools expand targeting scope of genome and base editing in rice. Plant Biotechnol J. 2019;18:1348–50.

    PubMed  PubMed Central  Google Scholar 

  71. Yang L, Zhang X, Wang L, Yin S, Zhu B, Xie L, et al. Increasing targeting scope of adenosine base editors in mouse and rat embryos through fusion of TadA deaminase with Cas9 variants. Protein Cell. 2018;9:814–9.

    PubMed  PubMed Central  Google Scholar 

  72. Cheng TL, Li S, Yuan B, Wang XL, Zhou WH, Qiu ZL. Expanding C-T base editing toolkit with diversified cytidine deaminases. Nat Commun. 2019;10:3612.

    PubMed  PubMed Central  Google Scholar 

  73. Jiang W, Feng S, Huang S, Yu W, Li G, Yang G, et al. BE-PLUS: a new base editing tool with broadened editing window and enhanced fidelity. Cell Res. 2018;28:855–61.

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Liu Y, Li G, Yang G, Gu H, Huang S, Yu W, et al. Increasing the targeting scope and efficiency of base editing with Proxy-BE strategy. FEBS Lett. 2019;594:1319–28.

    PubMed  Google Scholar 

  75. Wang X, Li J, Wang Y, Yang B, Wei J, Wu J, et al. Efficient base editing in methylated regions with a human APOBEC3A-Cas9 fusion. Nat Biotechnol. 2018;36:946–9.

    CAS  PubMed  Google Scholar 

  76. Cox DBT, Gootenberg JS, Abudayyeh OO, Franklin B, Kellner MJ, Joung J, et al. RNA editing with CRISPR-Cas13. Science. 2017;358:1019–27.

    CAS  PubMed  PubMed Central  Google Scholar 

  77. Chew WL, Tabebordbar M, Cheng JK, Mali P, Wu EY, Ng AH, et al. A multifunctional AAV-CRISPR-Cas9 and its host response. Nat Methods. 2016;13:868–74.

    CAS  PubMed  PubMed Central  Google Scholar 

  78. Teoh PJ, An O, Chung TH, Chooi JY, Toh SHM, Fan S, et al. Aberrant hyperediting of the myeloma transcriptome by ADAR1 confers oncogenicity and is a marker of poor prognosis. Blood. 2018;132:1304–17.

    CAS  PubMed  Google Scholar 

  79. Qu L, Yi Z, Zhu S, Wang C, Cao Z, Zhou Z, et al. Programmable RNA editing by recruiting endogenous ADAR using engineered RNAs. Nat Biotechnol. 2019;37:1380.

    CAS  PubMed  Google Scholar 

  80. Liang P, Xie X, Zhi S, Sun H, Zhang X, Chen Y, et al. Genome-wide profiling of adenine base editor specificity by EndoV-seq. Nat Commun. 2019;10:67.

    CAS  PubMed  PubMed Central  Google Scholar 

  81. Liu Z, Lu Z, Yang G, Huang S, Li G, Feng S, et al. Efficient generation of mouse models of human diseases via ABE- and BE-mediated base editing. Nat Commun. 2018;9:2338.

    PubMed  PubMed Central  Google Scholar 

  82. Zuo E, Sun Y, Wei W, Yuan T, Ying W, Sun H, et al. Cytosine base editor generates substantial off-target single-nucleotide variants in mouse embryos. Science. 2019;364:289–92.

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Jin S, Zong Y, Gao Q, Zhu Z, Wang Y, Qin P, et al. Cytosine, but not adenine, base editors induce genome-wide off-target mutations in rice. Science. 2019;364:292–5.

    CAS  PubMed  Google Scholar 

  84. Zhou C, Sun Y, Yan R, Liu Y, Zuo E, Gu C, et al. Off-target RNA mutation induced by DNA base editing and its elimination by mutagenesis. Nature. 2019;571:275–8.

    CAS  PubMed  Google Scholar 

  85. Cheng AW, Jillette N, Lee P, Plaskon D, Fujiwara Y, Wang W, et al. Casilio: a versatile CRISPR-Cas9-Pumilio hybrid for gene regulation and genomic labeling. Cell Res. 2016;26:254–7.

    CAS  PubMed  PubMed Central  Google Scholar 

  86. Xu XH, Gao JL, Dai W, Wang DY, Wu J, Wang JK. Gene activation by a CRISPR-assisted trans enhancer. Elife. 2019;8:e45973.

    PubMed  PubMed Central  Google Scholar 

  87. Zhan HJ, Zhou Q, Gao QJ, Li JF, Huang WR, Liu YC. Multiplexed promoterless gene expression with CRISPReader. Genome Biol. 2019;20:113.

    PubMed  PubMed Central  Google Scholar 

  88. Zhang XC, Wang JM, Cheng QX, Zheng X, Zhao GP, Wang J. Multiplex gene regulation by CRISPR-ddCpf1. Cell Discov. 2017;3:17018.

    CAS  PubMed  PubMed Central  Google Scholar 

  89. Ma DC, Peng SG, Huang WR, Cai ZM, Xie Z. Rational design of mini-Cas9 for transcriptional activation. ACS Synth Biol. 2018;7:978–85.

    CAS  PubMed  Google Scholar 

  90. Ma D, Peng S, Xie Z. Integration and exchange of split dCas9 domains for transcriptional controls in mammalian cells. Nat Commun. 2016;7:13056.

    CAS  PubMed  PubMed Central  Google Scholar 

  91. Zhou H, Liu J, Zhou C, Gao N, Rao Z, Li H, et al. In vivo simultaneous transcriptional activation of multiple genes in the brain using CRISPR-dCas9-activator transgenic mice. Nat Neurosci. 2018;21:440–6.

    CAS  PubMed  Google Scholar 

  92. Consortium EP. An integrated encyclopedia of DNA elements in the human genome. Nature. 2012;489:57–74.

    Google Scholar 

  93. Davis CA, Hitz BC, Sloan CA, Chan ET, Davidson JM, Gabdank I, et al. The encyclopedia of DNA elements (ENCODE): data portal update. Nucleic Acids Res. 2018;46:D794–801.

    CAS  PubMed  Google Scholar 

  94. Bernstein BE, Stamatoyannopoulos JA, Costello JF, Ren B, Milosavljevic A, Meissner A, et al. The NIH roadmap epigenomics mapping consortium. Nat Biotechnol. 2010;28:1045–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  95. Xu XX, Tao YH, Gao XB, Zhang L, Li XF, Zou WG, et al. A CRISPR-based approach for targeted DNA demethylation. Cell Discov. 2016;2:16009.

    CAS  PubMed  PubMed Central  Google Scholar 

  96. Liu X-M, Zhou J, Mao Y, Ji Q, Qian S-B. Programmable RNA N6-methyladenosine editing by CRISPR-Cas9 conjugates. Nat Chem Biol. 2019;15:865–71.

    CAS  PubMed  PubMed Central  Google Scholar 

  97. Lin L, Liu Y, Xu FP, Huang JR, Daugaard TF, Petersen TS, et al. Genome-wide determination of on-target and off-target characteristics for RNA-guided DNA methylation by dCas9 methyltransferases. Gigascience. 2018;7:1–19.

    PubMed  Google Scholar 

  98. Zhang Y, Liu LL, Guo SJ, Song JH, Zhu CX, Yue ZW, et al. Deciphering TAL effectors for 5-methylcytosine and 5-hydroxymethylcytosine recognition. Nat Commun. 2017;8:901.

    PubMed  PubMed Central  Google Scholar 

  99. Dixon JR, Selvaraj S, Yue F, Kim A, Li Y, Shen Y, et al. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature. 2012;485:376–80.

    CAS  PubMed  PubMed Central  Google Scholar 

  100. Bickmore WA. The spatial organization of the human genome. Annu Rev Genom Hum Genet. 2013;14:67–84.

    CAS  Google Scholar 

  101. Ren R, Deng L, Xue Y, Suzuki K, Zhang W, Yu Y, et al. Visualization of aging-associated chromatin alterations with an engineered TALE system. Cell Res. 2017;27:483–504.

    PubMed  PubMed Central  Google Scholar 

  102. Shao SP, Zhang WW, Hu H, Xue BX, Qin JS, Sun CY, et al. Long-term dual-color tracking of genomic loci by modified sgRNAs of the CRISPR/Cas9 system. Nucleic Acids Res. 2016;44:e86.

    PubMed  PubMed Central  Google Scholar 

  103. Chen BH, Zou W, Xu HY, Liang Y, Huang B. Efficient labeling and imaging of protein-coding genes in living cells using CRISPR-Tag. Nat Commun. 2018;9:5065.

    PubMed  PubMed Central  Google Scholar 

  104. Ma H, Tu LC, Naseri A, Chung YC, Grunwald D, Zhang S, et al. CRISPR-Sirius: RNA scaffolds for signal amplification in genome imaging. Nat Methods. 2018;15:928–31.

    CAS  PubMed  PubMed Central  Google Scholar 

  105. Wu XT, Mao SQ, Yang YT, Rushdi MN, Krueger CJ, Chen AK. A CRISPR/molecular beacon hybrid system for live-cell genomic imaging. Nucleic Acids Res. 2018;46:e80.

    PubMed  PubMed Central  Google Scholar 

  106. Mao SQ, Ying YC, Wu XT, Krueger CJ, Chen AK. CRISPR/dual-FRET molecular beacon for sensitive live-cell imaging of non-repetitive genomic loci. Nucleic Acids Res. 2019;47:e131.

    CAS  PubMed  PubMed Central  Google Scholar 

  107. 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;509:487–91.

    CAS  PubMed  Google Scholar 

  108. Zhu S, Li W, Liu J, Chen CH, Liao Q, Xu P, et al. Genome-scale deletion screening of human long non-coding RNAs using a paired-guide RNA CRISPR-Cas9 library. Nat Biotechnol. 2016;34:1279–86.

    CAS  PubMed  PubMed Central  Google Scholar 

  109. Zhu SY, Cao ZZ, Liu ZH, He Y, Wang YA, Yuan PF, et al. Guide RNAs with embedded barcodes boost CRISPR-pooled screens. Genome Biol. 2019;20:20.

    PubMed  PubMed Central  Google Scholar 

  110. Zhong CQ, Yin Q, Xie ZF, Bai MZ, Dong R, Tang W, et al. CRISPR-Cas9-mediated genetic screening in mice with haploid embryonic stem cells carrying a guide RNA library. Cell Stem Cell. 2015;17:221–32.

    CAS  PubMed  Google Scholar 

  111. Duan B, Zhou C, Zhu CY, Yu YF, Li GY, Zhang SH, et al. Model-based understanding of single-cell CRISPR screening. Nat Commun. 2019;10:2233.

    PubMed  PubMed Central  Google Scholar 

  112. Ma Y, Zhang J, Yin W, Zhang Z, Song Y, Chang X. Targeted AID-mediated mutagenesis (TAM) enables efficient genomic diversification in mammalian cells. Nat Methods. 2016;13:1029–35.

    CAS  PubMed  Google Scholar 

  113. Ren B, Yan F, Kuang YJ, Li N, Zhang DW, Zhou XP, et al. Improved base editor for efficiently inducing genetic variations in rice with CRISPR/Cas9-guided hyperactive hAID mutant. Mol Plant. 2018;11:623–6.

    CAS  PubMed  Google Scholar 

  114. Li C, Zhang R, Meng X, Chen S, Zong Y, Lu C, et al. Targeted, random mutagenesis of plant genes with dual cytosine and adenine base editors. Nat Biotechnol. 2020;38:875–82.

    CAS  PubMed  Google Scholar 

  115. Sun Y, Zhang B, Luo L, Shi DL, Wang H, Cui Z, et al. Systematic genome editing of the genes on zebrafish Chromosome 1 by CRISPR/Cas9. Genome Res. 2019;30:118–26.

    Google Scholar 

  116. Jiang J, Yan M, Li D, Li J. Genome tagging project: tag every protein in mice through ‘artificial spermatids’. Natl Sci Rev. 2018;6:394–6.

    PubMed  PubMed Central  Google Scholar 

  117. Li SY, Cheng QX, Liu JK, Nie XQ, Zhao GP, Wang J. CRISPR-Cas12a has both cis- and trans-cleavage activities on single-stranded DNA. Cell Res. 2018;28:491–3.

    CAS  PubMed  PubMed Central  Google Scholar 

  118. Chen JS, Ma E, Harrington LB, Da Costa M, Tian X, Palefsky JM, et al. CRISPR-Cas12a target binding unleashes indiscriminate single-stranded DNase activity. Science. 2018;360:436–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  119. Li SY, Cheng QX, Wang JM, Li XY, Zhang ZL, Gao S, et al. CRISPR-Cas12a-assisted nucleic acid detection. Cell Discov. 2018;4:20.

    PubMed  PubMed Central  Google Scholar 

  120. Bai J, Lin HS, Li HJ, Zhou Y, Liu JS, Zhong GR, et al. Cas12a-based on-site and rapid nucleic acid detection of African swine fever. Front Microbiol. 2019;10:2830.

    PubMed  PubMed Central  Google Scholar 

  121. Li LX, Li SY, Wu N, Wu JC, Wang G, Zhao GP, et al. HOLMESv2: a CRISPR-Cas12b-assisted platform for nucleic acid detection and DNA methylation quantitation. ACS Synth Biol. 2019;8:2228–37.

    CAS  PubMed  Google Scholar 

  122. Teng F, Guo L, Cui TT, Wang XG, Xu K, Gao QQ, et al. CDetection: CRISPR-Cas12b-based DNA detection with sub-attomolar sensitivity and single-base specificity. Genome Biol. 2019;20:132.

    PubMed  PubMed Central  Google Scholar 

  123. Wang B, Wang R, Wang DQ, Wu J, Li JX, Wang J, et al. Cas12aVDet: a CRISPR/Cas12a-based platform for rapid and visual nucleic acid detection. Anal Chem. 2019;91:12156–61.

    CAS  PubMed  Google Scholar 

  124. Zhao X, Zhang W, Qiu X, Mei Q, Luo Y, Fu W. Rapid and sensitive exosome detection with CRISPR/Cas12a. Anal Bioanal Chem. 2020;412:601–9.

    CAS  PubMed  Google Scholar 

  125. Hu JY, Jiang M, Liu R, Lv Y. Label-Free CRISPR/Cas9 assay for site-specific nucleic acid detection. Anal Chem. 2019;91:10870–8.

    CAS  PubMed  Google Scholar 

  126. Qiu XY, Zhu LY, Zhu CS, Ma JX, Hou T, Wu XM, et al. Highly effective and low-cost microRNA detection with CRISPR-Cas9. ACS Synth Biol. 2018;7:807–13.

    CAS  PubMed  Google Scholar 

  127. Wang Q, Zhang BB, Xu XH, Long FF, Wang JK. CRISPR-typing PCR (ctPCR), a new Cas9-based DNA detection method. Sci Rep. 2018;8:14126.

    PubMed  PubMed Central  Google Scholar 

  128. Wang Y, Bai JL, Qu XC, Gao YF, Wang J, Li S, et al. High-specificity double-stranded DNA detection with a “humanoid” molecular beacon and TALEs. Nanoscale. 2018;10:18354–61.

    CAS  PubMed  Google Scholar 

  129. Lei C, Li SY, Liu JK, Zheng X, Zhao GP, Wang J. The CCTL (Cpf1-assisted cutting and Taq DNA ligase-assisted Ligation) method for efficient editing of large DNA constructs in vitro. Nucleic Acids Res. 2017;45:e74.

    CAS  PubMed  PubMed Central  Google Scholar 

  130. Li SY, Zhao GP, Wang J. C-Brick: a new standard for assembly of biological parts using Cpf1. ACS Synth Biol. 2016;5:1383–8.

    CAS  PubMed  Google Scholar 

  131. Wang LP, Wang HJ, Liu HY, Zhao QY, Liu B, Wang L, et al. Improved CRISPR-Cas12a-assisted one-pot DNA editing method enables seamless DNA editing. Biotechnol Bioeng. 2019;116:1463–74.

    CAS  PubMed  Google Scholar 

  132. She WW, Ni J, Shui K, Wang F, He RY, Xue JH, et al. Rapid and error-free site-directed mutagenesis by a PCR-free in vitro CRISPR/Cas9-mediated mutagenic system. ACS Synth Biol. 2018;7:2236–44.

    CAS  PubMed  Google Scholar 

  133. Shmakov S, Abudayyeh OO, Makarova KS, Wolf YI, Gootenberg JS, Semenova E, et al. Discovery and functional characterization of diverse class 2 CRISPR-Cas systems. Mol Cell. 2015;60:385–97.

    CAS  PubMed  PubMed Central  Google Scholar 

  134. Teng F, Cui TT, Feng GH, Guo L, Xu K, Gao QQ, et al. Repurposing CRISPR-Cas12b for mammalian genome engineering. Cell Discov. 2018;4:63.

    PubMed  PubMed Central  Google Scholar 

  135. Hegge JW, Swarts DC, van der Oost J. Prokaryotic argonaute proteins: novel genome-editing tools? Nat Rev Microbiol. 2017;16:5–11.

    PubMed  Google Scholar 

  136. Cao Y, Sun W, Wang J, Sheng G, Xiang G, Zhang T, et al. Argonaute proteins from human gastrointestinal bacteria catalyze DNA-guided cleavage of single- and double-stranded DNA at 37 degrees C. Cell Discov. 2019;5:38.

    PubMed  PubMed Central  Google Scholar 

  137. Xu S, Cao SS, Zou BJ, Yue YY, Gu C, Chen X, et al. An alternative novel tool for DNA editing without target sequence limitation: the structure-guided nuclease. Genome Biol. 2016;17:186.

    PubMed  PubMed Central  Google Scholar 

  138. Adli M. The CRISPR tool kit for genome editing and beyond. Nat Commun. 2018;9:1911.

    PubMed  PubMed Central  Google Scholar 

  139. Zhang F. Development of CRISPR-Cas systems for genome editing and beyond. Q Rev Biophys. 2019;52:1–31.

    Google Scholar 

  140. Rees HA, Liu DR. Base editing: precision chemistry on the genome and transcriptome of living cells. Nat Rev Genet. 2018;19:770–788.

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

HW is supported by the National Key Research and Development Program of China (Nos 2018YFA0107703, 2019YFA0110000), Strategic Priority Research Program of the Chinese Academy of Sciences (No. XDA16010503), and National Natural Science Foundation of China (No. 31722036). WS is supported by the National Key Research and Development Program of China (No. 2018YFE0201102).

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Authors and Affiliations

  1. State Key Laboratory of Stem Cell and Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, 100101, Beijing, China

    Wen Sun & Haoyi Wang

  2. Institute for Stem Cell and Regeneration, Chinese Academy of Sciences, 100101, Beijing, China

    Wen Sun & Haoyi Wang

  3. University of the Chinese Academy of Sciences, 100049, Beijing, China

    Haoyi Wang

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  1. Wen Sun
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  2. Haoyi Wang
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Sun, W., Wang, H. Recent advances of genome editing and related technologies in China. Gene Ther 27, 312–320 (2020). https://doi.org/10.1038/s41434-020-0181-5

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