BMB Reports

생화학분자생물학회 (Korean Society for Biochemistry and Molecular Biology)
권호 표지
DOI QR코드

DOI QR Code

Evolution of CRISPR towards accurate and efficient mammal genome engineering

  • Ryu, Seuk-Min (Molecular Recognition Research Center, Korea Institute of Science and Technology) ;
  • Hur, Junseok W (Department of Neurosurgery, Korea University College of Medicine) ;
  • Kim, Kyoungmi (Department of Biomedical Sciences and Department of Physiology, Korea University College of Medicine)
  • 투고 : 2019.05.14
  • 발행 : 2019.08.31
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

The evolution of genome editing technology based on CRISPR (clustered regularly interspaced short palindromic repeats) system has led to a paradigm shift in biological research. CRISPR/Cas9-guide RNA complexes enable rapid and efficient genome editing in mammalian cells. This system induces double-stranded DNA breaks (DSBs) at target sites and most DNA breakages induce mutations as small insertions or deletions (indels) by non-homologous end joining (NHEJ) repair pathway. However, for more precise correction as knock-in or replacement of DNA base pairs, using the homology-directed repair (HDR) pathway is essential. Until now, many trials have greatly enhanced knock-in or substitution efficiency by increasing HDR efficiency, or newly developed methods such as Base Editors (BEs). However, accuracy remains unsatisfactory. In this review, we summarize studies to overcome the limitations of HDR using the CRISPR system and discuss future direction.

키워드

참고문헌

  1. Wang H, Yang H, Shivalila CS et al (2013) One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell 153, 910-918 https://doi.org/10.1016/j.cell.2013.04.025
  2. Yang H, Wang H, Shivalila CS, Cheng AW, Shi L and Jaenisch R (2013) One-step generation of mice carrying reporter and conditional alleles by CRISPR/Cas-mediated genome engineering. Cell 154, 1370-1379 https://doi.org/10.1016/j.cell.2013.08.022
  3. Barrangou R, Fremaux C, Deveau H et al (2007) CRISPR provides acquired resistance against viruses in prokaryotes. Science 315, 1709-1712 https://doi.org/10.1126/science.1138140
  4. Horvath P and Barrangou R (2010) CRISPR/Cas, the immune system of bacteria and archaea. Science 327, 167-170 https://doi.org/10.1126/science.1179555
  5. Terns MP and Terns RM (2011) CRISPR-based adaptive immune systems. Curr Opin Microbiol 14, 321-327 https://doi.org/10.1016/j.mib.2011.03.005
  6. Bhaya D, Davison M and Barrangou R (2011) CRISPR-Cas systems in bacteria and archaea: versatile small RNAs for adaptive defense and regulation. Annu Rev Genet 45, 273-297 https://doi.org/10.1146/annurev-genet-110410-132430
  7. Cho SW, Kim S, Kim JM and Kim JS (2013) Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease. Nat Biotechnol 31, 230-232 https://doi.org/10.1038/nbt.2507
  8. Cong L, Ran FA, Cox D et al (2013) Multiplex genome engineering using CRISPR/Cas systems. Science 339, 819-823 https://doi.org/10.1126/science.1231143
  9. Jiang W, Bikard D, Cox D, Zhang F and Marraffini LA (2013) RNA-guided editing of bacterial genomes using CRISPR-Cas systems. Nat Biotechnol 31, 233-239 https://doi.org/10.1038/nbt.2508
  10. Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA and Charpentier E (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337, 816-821 https://doi.org/10.1126/science.1225829
  11. Mali P, Yang L, Esvelt KM et al (2013) RNA-guided human genome engineering via Cas9. Science 339, 823-826 https://doi.org/10.1126/science.1232033
  12. Hsu PD, Lander ES and Zhang F (2014) Development and applications of CRISPR-Cas9 for genome engineering. Cell 157, 1262-1278 https://doi.org/10.1016/j.cell.2014.05.010
  13. Woo JW, Kim J, Kwon SI et al (2015) DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins. Nat Biotechnol 33, 1162-1164 https://doi.org/10.1038/nbt.3389
  14. Amoasii L, Hildyard JCW, Li H et al (2018) Gene editing restores dystrophin expression in a canine model of Duchenne muscular dystrophy. Science 362, 86-91 https://doi.org/10.1126/science.aau1549
  15. Niu D, Wei HJ, Lin L et al (2017) Inactivation of porcine endogenous retrovirus in pigs using CRISPR-Cas9. Science 357, 1303-1307 https://doi.org/10.1126/science.aan4187
  16. Liang F, Han M, Romanienko PJ and Jasin M (1998) Homology-directed repair is a major double-strand break repair pathway in mammalian cells. Proc Natl Acad Sci U S A 95, 5172-5177 https://doi.org/10.1073/pnas.95.9.5172
  17. Kakarougkas A and Jeggo PA (2014) DNA DSB repair pathway choice: an orchestrated handover mechanism. Br J Radiol 87, 20130685 https://doi.org/10.1259/bjr.20130685
  18. Lindahl T (1982) DNA repair enzymes. Annu Rev Biochem 51, 61-87 https://doi.org/10.1146/annurev.bi.51.070182.000425
  19. Steentoft C, Vakhrushev SY, Vester-Christensen MB et al (2011) Mining the O-glycoproteome using zinc-finger nuclease-glycoengineered SimpleCell lines. Nat Methods 8, 977-982 https://doi.org/10.1038/nmeth.1731
  20. Kim Y, Kweon J, Kim A et al (2013) A library of TAL effector nucleases spanning the human genome. Nat Biotechnol 31, 251-258 https://doi.org/10.1038/nbt.2517
  21. Lehner K, Mudrak SV, Minesinger BK and Jinks-Robertson S (2012) Frameshift mutagenesis: the roles of primertemplate misalignment and the nonhomologous end-joining pathway in Saccharomyces cerevisiae. Genetics 190, 501-510 https://doi.org/10.1534/genetics.111.134890
  22. Smithies O, Gregg RG, Boggs SS, Koralewski MA and Kucherlapati RS (1985) Insertion of DNA sequences into the human chromosomal beta-globin locus by homologous recombination. Nature 317, 230-234 https://doi.org/10.1038/317230a0
  23. Zelensky AN, Schimmel J, Kool H, Kanaar R and Tijsterman M (2017) Inactivation of Pol theta and C-NHEJ eliminates off-target integration of exogenous DNA. Nat Commun 8, 66 https://doi.org/10.1038/s41467-017-00124-3
  24. Schimmel J, Kool H, van Schendel R and Tijsterman M (2017) Mutational signatures of non-homologous and polymerase theta-mediated end-joining in embryonic stem cells. EMBO J 36, 3634-3649 https://doi.org/10.15252/embj.201796948
  25. Mateos-Gomez PA, Kent T, Deng SK et al (2017) The helicase domain of Poltheta counteracts RPA to promote alt-NHEJ. Nat Struct Mol Biol 24, 1116-1123 https://doi.org/10.1038/nsmb.3494
  26. Rees HA and Liu DR (2018) Base editing: precision chemistry on the genome and transcriptome of living cells. Nat Rev Genet 19, 770-788 https://doi.org/10.1038/s41576-018-0059-1
  27. Kim JS (2018) Precision genome engineering through adenine and cytosine base editing. Nat Plants 4, 148-151 https://doi.org/10.1038/s41477-018-0115-z
  28. Komor AC, Kim YB, Packer MS, Zuris JA and Liu DR (2016) Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage. Nature 533, 420-424 https://doi.org/10.1038/nature17946
  29. Nishida K, Arazoe T, Yachie N et al (2016) Targeted nucleotide editing using hybrid prokaryotic and vertebrate adaptive immune systems. Science 353, aaf8729 https://doi.org/10.1126/science.aaf8729
  30. Gaudelli NM, Komor AC, Rees HA et al (2017) Programmable base editing of A*T to G*C in genomic DNA without DNA cleavage. Nature 551, 464-471 https://doi.org/10.1038/nature24644
  31. Kim K, Ryu SM, Kim ST et al (2017) Highly efficient RNA-guided base editing in mouse embryos. Nat Biotechnol 35, 435-437 https://doi.org/10.1038/nbt.3816
  32. Ryu SM, Koo T, Kim K et al (2018) Adenine base editing in mouse embryos and an adult mouse model of Duchenne muscular dystrophy. Nat Biotechnol 36, 536-539 https://doi.org/10.1038/nbt.4148
  33. Liang P, Ding C, Sun H et al (2017) Correction of beta-thalassemia mutant by base editor in human embryos. Protein Cell 8, 811-822 https://doi.org/10.1007/s13238-017-0475-6
  34. Liu Z, Chen M, Chen S et al (2018) Highly efficient RNA-guided base editing in rabbit. Nat Commun 9, 2717 https://doi.org/10.1038/s41467-018-05232-2
  35. Yeh WH, Chiang H, Rees HA, Edge ASB and Liu DR (2018) In vivo base editing of post-mitotic sensory cells. Nat Commun 9, 2184 https://doi.org/10.1038/s41467-018-04580-3
  36. Chang HHY, Pannunzio NR, Adachi N and Lieber MR (2017) Non-homologous DNA end joining and alternative pathways to double-strand break repair. Nat Rev Mol Cell Biol 18, 495-506 https://doi.org/10.1038/nrm.2017.48
  37. Lee SH, Kim S and Hur JK (2018) CRISPR and Target-Specific DNA Endonucleases for Efficient DNA Knock-in in Eukaryotic Genomes. Mol Cells 41, 943-952 https://doi.org/10.14348/molcells.2018.0408
  38. Cox DB, Platt RJ and Zhang F (2015) Therapeutic genome editing: prospects and challenges. Nat Med 21, 121-131 https://doi.org/10.1038/nm.3793
  39. Renaud JB, Boix C, Charpentier M et al (2016) Improved Genome Editing Efficiency and Flexibility Using Modified Oligonucleotides with TALEN and CRISPR-Cas9 Nucleases. Cell Rep 14, 2263-2272 https://doi.org/10.1016/j.celrep.2016.02.018
  40. Paquet D, Kwart D, Chen A et al (2016) Efficient introduction of specific homozygous and heterozygous mutations using CRISPR/Cas9. Nature 533, 125-129 https://doi.org/10.1038/nature17664
  41. Quadros RM, Miura H, Harms DW et al (2017) Easi-CRISPR: a robust method for one-step generation of mice carrying conditional and insertion alleles using long ssDNA donors and CRISPR ribonucleoproteins. Genome Biol 18, 92 https://doi.org/10.1186/s13059-017-1220-4
  42. Gu B, Posfai E and Rossant J (2018) Efficient generation of targeted large insertions by microinjection into two-cellstage mouse embryos. Nat Biotechnol 36, 632-637 https://doi.org/10.1038/nbt.4166
  43. Aird EJ, Lovendahl KN, St Martin A, Harris RS and Gordon WR (2018) Increasing Cas9-mediated homology-directed repair efficiency through covalent tethering of DNA repair template. Commun Biol 1, 54 https://doi.org/10.1038/s42003-018-0054-2
  44. Nakade S, Tsubota T, Sakane Y et al (2014) Microhomology-mediated end-joining-dependent integration of donor DNA in cells and animals using TALENs and CRISPR/Cas9. Nat Commun 5, 5560 https://doi.org/10.1038/ncomms6560
  45. Sakuma T, Nakade S, Sakane Y, Suzuki KT and Yamamoto T (2016) MMEJ-assisted gene knock-in using TALENs and CRISPR-Cas9 with the PITCh systems. Nat Protoc 11, 118-133 https://doi.org/10.1038/nprot.2015.140
  46. Yao X, Wang X, Liu J et al (2017) CRISPR/Cas9 - Mediated Precise Targeted Integration In Vivo Using a Double Cut Donor with Short Homology Arms. EBioMedicine 20, 19-26 https://doi.org/10.1016/j.ebiom.2017.05.015
  47. Yao X, Wang X, Hu X et al (2017) Homology-mediated end joining-based targeted integration using CRISPR/Cas9. Cell Res 27, 801-814 https://doi.org/10.1038/cr.2017.76
  48. Yao X, Zhang M, Wang X et al (2018) Tild-CRISPR Allows for Efficient and Precise Gene Knockin in Mouse and Human Cells. Dev Cell 45, 526-536 e525 https://doi.org/10.1016/j.devcel.2018.04.021
  49. Shrivastav M, De Haro LP and Nickoloff JA (2008) Regulation of DNA double-strand break repair pathway choice. Cell Res 18, 134-147 https://doi.org/10.1038/cr.2007.111
  50. Allen C, Halbrook J and Nickoloff JA (2003) Interactive competition between homologous recombination and non-homologous end joining. Mol Cancer Res 1, 913-920
  51. Hartlerode AJ and Scully R (2009) Mechanisms of double-strand break repair in somatic mammalian cells. Biochem J 423, 157-168 https://doi.org/10.1042/BJ20090942
  52. Ceccaldi R, Rondinelli B and D'Andrea AD (2016) Repair Pathway Choices and Consequences at the Double-Strand Break. Trends Cell Biol 26, 52-64 https://doi.org/10.1016/j.tcb.2015.07.009
  53. Pannunzio NR, Watanabe G and Lieber MR (2018) Nonhomologous DNA end-joining for repair of DNA double-strand breaks. J Biol Chem 293, 10512-10523 https://doi.org/10.1074/jbc.TM117.000374
  54. Shibata A (2017) Regulation of repair pathway choice at two-ended DNA double-strand breaks. Mutat Res 803-805, 51-55 https://doi.org/10.1016/j.mrfmmm.2017.07.011
  55. Chu VT, Weber T, Wefers B et al (2015) Increasing the efficiency of homology-directed repair for CRISPR-Cas9-induced precise gene editing in mammalian cells. Nat Biotechnol 33, 543-548 https://doi.org/10.1038/nbt.3198
  56. Maruyama T, Dougan SK, Truttmann MC, Bilate AM, Ingram JR and Ploegh HL (2015) Increasing the efficiency of precise genome editing with CRISPR-Cas9 by inhibition of nonhomologous end joining. Nat Biotechnol 33, 538-542 https://doi.org/10.1038/nbt.3190
  57. Yu C, Liu Y, Ma T et al (2015) Small molecules enhance CRISPR genome editing in pluripotent stem cells. Cell Stem Cell 16, 142-147 https://doi.org/10.1016/j.stem.2015.01.003
  58. Riesenberg S and Maricic T (2018) Targeting repair pathways with small molecules increases precise genome editing in pluripotent stem cells. Nat Commun 9, 2164 https://doi.org/10.1038/s41467-018-04609-7
  59. Orthwein A, Fradet-Turcotte A, Noordermeer SM et al (2014) Mitosis inhibits DNA double-strand break repair to guard against telomere fusions. Science 344, 189-193 https://doi.org/10.1126/science.1248024
  60. Heyer WD, Ehmsen KT and Liu J (2010) Regulation of homologous recombination in eukaryotes. Annu Rev Genet 44, 113-139 https://doi.org/10.1146/annurev-genet-051710-150955
  61. Lin S, Staahl BT, Alla RK and Doudna JA (2014) Enhanced homology-directed human genome engineering by controlled timing of CRISPR/Cas9 delivery. Elife 3, e04766 https://doi.org/10.7554/eLife.04766
  62. Li G, Zhang X, Zhong C et al (2017) Small molecules enhance CRISPR/Cas9-mediated homology-directed genome editing in primary cells. Sci Rep 7, 8943 https://doi.org/10.1038/s41598-017-09306-x
  63. Yang D, Scavuzzo MA, Chmielowiec J et al (2016) Enrichment of G2/M cell cycle phase in human pluripotent stem cells enhances HDR-mediated gene repair with customizable endonucleases. Sci Rep 6, 21264 https://doi.org/10.1038/srep21264
  64. Canny MD, Moatti N, Wan LCK et al (2018) Inhibition of 53BP1 favors homology-dependent DNA repair and increases CRISPR-Cas9 genome-editing efficiency. Nat Biotechnol 36, 95-102 https://doi.org/10.1038/nbt.4021
  65. Song J, Yang D, Xu J, Zhu T, Chen YE and Zhang J (2016) RS-1 enhances CRISPR/Cas9- and TALEN-mediated knock-in efficiency. Nat Commun 7, 10548 https://doi.org/10.1038/ncomms10548
  66. Lee HK, Willi M, Miller SM et al (2018) Targeting fidelity of adenine and cytosine base editors in mouse embryos. Nat Commun 9, 4804 https://doi.org/10.1038/s41467-018-07322-7
  67. Liu Z, Lu Z, Yang G et al (2018) Efficient generation of mouse models of human diseases via ABE- and BE-mediated base editing. Nat Commun 9, 2338 https://doi.org/10.1038/s41467-018-04768-7
  68. Kim YB, Komor AC, Levy JM, Packer MS, Zhao KT and Liu DR (2017) Increasing the genome-targeting scope and precision of base editing with engineered Cas9-cytidine deaminase fusions. Nat Biotechnol 35, 371-376 https://doi.org/10.1038/nbt.3803
  69. Banno S, Nishida K, Arazoe T, Mitsunobu H and Kondo A (2018) Deaminase-mediated multiplex genome editing in Escherichia coli. Nat Microbiol 3, 423-429 https://doi.org/10.1038/s41564-017-0102-6
  70. Hu JH, Miller SM, Geurts MH et al (2018) Evolved Cas9 variants with broad PAM compatibility and high DNA specificity. Nature 556, 57-63 https://doi.org/10.1038/nature26155