The genome editing revolution: A CRISPR-Cas TALE off-target story

BioEssays

Volumn 38, Issue , 2016, Pages S4-S13

  Stella, Stefano ^a   Montoya, Guillermo ^a  

^a University of Copenhagen   (Denmark)

Author keywords

CRISPR Cas9; engineered nucleases; genome editing; specificity; TALE

Indexed keywords

CRISPR ASSOCIATED PROTEIN; DNA; RIBONUCLEOPROTEIN; RNA; TRANSCRIPTION ACTIVATOR LIKE EFFECTOR NUCLEASE; ZINC FINGER PROTEIN;

BACTERIAL STRAIN; BACTERIUM; CRISPR CAS SYSTEM; DNA BINDING; DNA REPAIR; DNA SEQUENCE; GENE THERAPY; GENOME; HUMAN; LIVESTOCK; NONHUMAN; PLANT; REVIEW; YEAST;

EID: 84978827308     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201670903     Document Type: Review

References (92)

1. Carroll D. 2014. Genome engineering with targetable nucleases. Annu Rev Biochem 83: 409–39.
2. Wyman C, Kanaar R. 2006. DNA double-strand break repair: all's well that ends well. Annu Rev Genet 40: 363–83.
3. Lieber MR. 2010. The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu Rev Biochem 79: 181–211.
4. Mimitou EP, Symington LS. 2009. Nucleases and helicases take center stage in homologous recombination. Trends Biochem Sci 34: 264–72.
5. Moore JK, Haber JE. 1996. Cell cycle and genetic requirements of two pathways of nonhomologous end-joining repair of double-strand breaks in Saccharomyces cerevisiae. Mol Cell Biol 16: 2164–73.
6. Boulton SJ, Jackson SP. 1996. Saccharomyces cerevisiae Ku70 potentiates illegitimate DNA double-strand break repair and serves as a barrier to error-prone DNA repair pathways. EMBO J 15: 5093–103.
7. Bétermier M, Bertrand P, Lopez BS. 2014. Is non-homologous end-joining really an inherently error-prone process? PLoS Genet 10: e1004086.
8. Urnov FD, Miller JC, Lee Y-LL, Beausejour CM, et al. 2005. Highly efficient endogenous human gene correction using designed zinc-finger nucleases. Nature 435: 646–51.
9. Bibikova M, Beumer K, Trautman JK, Carroll D. 2003. Enhancing gene targeting with designed zinc finger nucleases. Science 300: 764.
10. Redondo P, Prieto J, Muñoz IGG, Alibés A, et al. 2008. Molecular basis of xeroderma pigmentosum group C DNA recognition by engineered meganucleases. Nature 456: 107–11.
11. Muñoz IGG, Prieto J, Subramanian S, Coloma J, et al. 2011. Molecular basis of engineered meganuclease targeting of the endogenous human RAG1 locus. Nucleic Acids Res 39: 729–43.
12. Stoddard BL. 2011. Homing endonucleases: from microbial genetic invaders to reagents for targeted DNA modification. Structure 19: 7–15.
13. Pabo CO, Peisach E, Grant RA. 2001. Design and selection of novel Cys2His2 zinc finger proteins. Annu Rev Biochem 70: 313–40.
14. Wolfe SA, Nekludova L, Pabo CO. 2000. DNA recognition by Cys2His2 zinc finger proteins. Annu Rev Biophys Biomol Struct 29: 183–212.
15. Arnould S, Perez C, Cabaniols J-PP, Smith J, et al. 2007. Engineered I-CreI derivatives cleaving sequences from the human XPC gene can induce highly efficient gene correction in mammalian cells. J Mol Biol 371: 49–65.
16. Liang P, Xu Y, Zhang X, Ding C, et al. 2015. CRISPR/Cas9-mediated gene editing in human tripronuclear zygotes. Protein Cell 6: 363–72.
17. Cyranoski D, Reardon S. 2015. Embryo editing sparks epic debate. Nature 520: 593–4.
18. Lanphier E, Urnov F, Haecker SE, Werner M, et al. 2015. Don't edit the human germ line. Nature 519: 410–1.
19. Baltimore D, Berg P, Botchan M, Carroll D, et al. 2015. Biotechnology. A prudent path forward for genomic engineering and germline gene modification. Science 348: 36–8.
20. Ledford H. 2015. CRISPR, the disruptor. Nature 522: 20–4.
21. Boch J, Bonas U. 2010. Xanthomonas AvrBs3 family-type III effectors: discovery and function. Annu Rev Phytopathol 48: 419–36.
22. Mak AN, Bradley P, Cernadas RA, Bogdanove AJ, et al. 2012. The crystal structure of TAL effector PthXo1 bound to its DNA target. Science 335: 716–9.
23. Deng D, Yan C, Pan X, Mahfouz M, et al. 2012. Structural basis for sequence-specific recognition of DNA by TAL effectors. Science 335: 720–3.
24. Stella S, Molina R, Yefimenko I, Prieto J, et al. 2013. Structure of the AvrBs3-DNA complex provides new insights into the initial thymine-recognition mechanism. Acta Crystallogr D Biol Crystallogr 69: 1707–16.
25. Boch J, Scholze H, Schornack S, Landgraf A, et al. 2009. Breaking the code of DNA binding specificity of TAL-type III effectors. Science 326: 1509–12.
26. Moscou MJ, Bogdanove AJ. 2009. A simple cipher governs DNA recognition by TAL effectors. Science 326: 1501.
27. Briggs AW, Rios X, Chari R, Yang L, et al. 2012. Iterative capped assembly: rapid and scalable synthesis of repeat-module DNA such as TAL effectors from individual monomers. Nucleic Acids Res 40: e117.
28. Cermak T, Doyle EL, Christian M, Wang L, et al. 2011. Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res 39: e82.
29. Schmid-Burgk JL, Schmidt T, Kaiser V, Höning K, et al. 2013. A ligation-independent cloning technique for high-throughput assembly of transcription activator–like effector genes. Nat Biotechnol 31: 76–81.
30. Reyon D, Tsai SQ, Khayter C, Foden JA, et al. 2012. FLASH assembly of TALENs for high-throughput genome editing. Nat Biotechnol 30: 460–5.
31. Yang L, Guell M, Byrne S, Yang JL. 2013. Optimization of scarless human stem cell genome editing. Nucleic Acids Res 41: 9049–61.
32. Holkers M, Maggio I, Liu J, Janssen JM, et al. 2013. Differential integrity of TALE nuclease genes following adenoviral and lentiviral vector gene transfer into human cells. Nucleic Acids Res 41: e63.
33. Juillerat A, Bertonati C, Dubois G, Guyot V, et al. 2014. BurrH: a new modular DNA binding protein for genome engineering. Sci Rep 4: srep03831.
34. Doyle EL, Hummel AW, Demorest ZL, Starker CG, et al. 2013. TAL effector specificity for base 0 of the DNA target is altered in a complex, effector- and assay-dependent manner by substitutions for the tryptophan in cryptic repeat −1. PLoS One 8: e82120.
35. Christian ML, Demorest ZL, Starker CG, Osborn MJ, et al. 2012. Targeting G with TAL effectors: a comparison of activities of TALENs constructed with NN and NK repeat variable di-residues. PLoS One 7: e45383.
36. Stella S, Molina R, López-Méndez B, Juillerat A, et al. 2014. BuD, a helix-loop-helix DNA-binding domain for genome modification. Acta Crystallogr D Biol Crystallogr 70: 2042–52.
37. Li T, Huang S, Jiang WZ, Wright D, et al. 2011. TAL nucleases (TALNs): hybrid proteins composed of TAL effectors and FokI DNA-cleavage domain. Nucleic Acids Res 39: 359–72.
38. Christian M, Cermak T, Doyle EL, Schmidt C, et al. 2010. Targeting DNA double-strand breaks with TAL effector nucleases. Genetics 186: 757–61.
39. Beurdeley M, Bietz F, Li J, Thomas S, et al. 2013. Compact designer TALENs for efficient genome engineering. Nat Commun 4: 1762.
40. Lin J, Chen H, Luo L, Lai Y, et al. 2015. Creating a monomeric endonuclease TALE-I-SceI with high specificity and low genotoxicity in human cells. Nucleic Acids Res 43: 1112–22.
41. Kleinstiver BP, Wang L, Wolfs JM, Kolaczyk T, et al. 2014. The I-TevI nuclease and linker domains contribute to the specificity of monomeric TALENs. G3 (Bethesda) 4: 1155–65.
42. Miller JC, Tan S, Qiao G, Barlow KA, et al. 2011. A TALE nuclease architecture for efficient genome editing. Nat Biotechnol 29: 143–8.
43. Mercer AC, Gaj T, Fuller RP, Barbas CF. 2012. Chimeric TALE recombinases with programmable DNA sequence specificity. Nucleic Acids Res 40: 11163–72.
44. Mojica FJ, Díez-Villaseñor C, García-Martínez J, Soria E. 2005. Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. J Mol Evol 60: 174–82.
45. Grissa I, Vergnaud G, Pourcel C. 2007. The CRISPRdb database and tools to display CRISPRs and to generate dictionaries of spacers and repeats. BMC Bioinformatics 8: 172.
46. Jinek M, Chylinski K, Fonfara I, Hauer M, et al. 2012. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337: 816–21.
47. Gasiunas G, Barrangou R, Horvath P, Siksnys V. 2012. Cas9-crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. Proc Natl Acad Sci U S A 109: E2579–86.
48. Sapranauskas R, Gasiunas G, Fremaux C, Barrangou R, et al. 2011. The Streptococcus thermophilus CRISPR/Cas system provides immunity in Escherichia coli. Nucleic Acids Res 39: 9275–82.
49. Semenova E, Jore MM, Datsenko KA, Semenova A, et al. 2011. Interference by clustered regularly interspaced short palindromic repeat (CRISPR) RNA is governed by a seed sequence. Proc Natl Acad Sci U S A 108: 10098–103.
50. Cong L, Ran FA, Cox D, Lin S, et al. 2013. Multiplex genome engineering using CRISPR/Cas systems. Science 339: 819–23.
51. Jiang W, Bikard D, Cox D, Zhang F, et al. 2013. RNA-guided editing of bacterial genomes using CRISPR-Cas systems. Nat Biotechnol 31: 233–9.
52. Ran FA, Hsu PD, Lin C-YY, Gootenberg JS, et al. 2013. Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154: 1380–9.
53. Maeder ML, Linder SJ, Cascio VM, Fu Y, et al. 2013. CRISPR RNA-guided activation of endogenous human genes. Nat Methods 10: 977–9.
54. Gilbert LA, Larson MH, Morsut L, Liu Z, et al. 2013. CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell 154: 442–51.
55. Qi LS, Larson MH, Gilbert LA, Doudna JA, et al. 2013. Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell 152: 1173–83.
56. Perez-Pinera P, Kocak DD, Vockley CM, Adler AF, et al. 2013. RNA-guided gene activation by CRISPR-Cas9-based transcription factors. Nat Methods 10: 973–6.
57. Chen B, Gilbert LA, Cimini BA, Schnitzbauer J. 2013. Dynamic imaging of genomic loci in living human cells by an optimized CRISPR/Cas system. Cell 155: 1479–91.
58. Tsai SQ, Wyvekens N, Khayter C, Foden JA, et al. 2014. Dimeric CRISPR RNA-guided FokI nucleases for highly specific genome editing. Nat Biotechnol 32: 569–76.
59. Sternberg SH, Doudna JA. 2015. Expanding the Biologist's Toolkit with CRISPR-Cas9. Mol Cell 58: 568–74.
60. Mussolino C, Morbitzer R, Lütge F, Dannemann N, et al. 2011. A novel TALE nuclease scaffold enables high genome editing activity in combination with low toxicity. Nucleic Acids Res 39: 9283–93.
61. Corrigan-Curay J, O'Reilly M, Kohn DB, Cannon PM, et al. 2015. Genome editing technologies: defining a path to clinic. Mol Ther 23: 796–806.
62. Hsu PD, Scott DA, Weinstein JA, Ran FA, et al. 2013. DNA targeting specificity of RNA-guided Cas9 nucleases. Nat Biotechnol 31: 827–32.
63. Doyle EL, Booher NJ, Standage DS, Voytas DF, et al. 2012. TAL Effector-Nucleotide Targeter (TALE-NT) 2.0: tools for TAL effector design and target prediction. Nucleic Acids Res 40: W117–22.
64. Fu Y, Foden JA, Khayter C, Maeder ML, et al. 2013. High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat Biotechnol 31: 822–6.
65. Kim Y, Kweon J, Kim A, Chon JK, et al. 2013. A library of TAL effector nucleases spanning the human genome. Nat Biotechnol 31: 251–8.
66. Guilinger JP, Pattanayak V, Reyon D, Tsai SQ, et al. 2014. Broad specificity profiling of TALENs results in engineered nucleases with improved DNA-cleavage specificity. Nat Methods 11: 429–35.
67. Pattanayak V, Ramirez CL, Joung JK, Liu DR. 2011. Revealing off-target cleavage specificities of zinc-finger nucleases by in vitro selection. Nat Methods 8: 765–70.
68. Pattanayak V, Lin S, Guilinger JP, Ma E, et al. 2013. High-throughput profiling of off-target DNA cleavage reveals RNA-programmed Cas9 nuclease specificity. Nat Biotechnol 31: 839–43.
69. Gabriel R, Lombardo A, Arens A, Miller JC, et al. 2011. An unbiased genome-wide analysis of zinc-finger nuclease specificity. Nat Biotechnol 29: 816–23.
70. Pattanayak V, Guilinger JP, Liu DR. 2014. Determining the specificities of TALENs, Cas9, and other genome-editing enzymes. Meth Enzymol 546: 47–78.
71. Wang X, Wang Y, Wu X, Wang J, et al. 2015. Unbiased detection of off-target cleavage by CRISPR-Cas9 and TALENs using integrase-defective lentiviral vectors. Nat Biotechnol 33: 175–8.
72. Lin Y, Cradick TJ, Brown MT, Deshmukh H, et al. 2014. CRISPR/Cas9 systems have off-target activity with insertions or deletions between target DNA and guide RNA sequences. Nucleic Acids Res 42: 7473–85.
73. Richter A, Streubel J, Blücher C, Szurek B, et al. 2014. A TAL effector repeat architecture for frameshift binding. Nat Commun 5: 3447.
74. Smith C, Gore A, Yan W, Abalde-Atristain L, et al. 2014. Whole-genome sequencing analysis reveals high specificity of CRISPR/Cas9 and TALEN-based genome editing in human iPSCs. Cell Stem Cell 15: 12–3.
75. Yao X, Yuan T, Goebl A, Tang S, et al. 2014. Targeted gene correction minimally impacts whole-genome mutational load in human-disease-specific induced pluripotent stem cell clones. Cell Stem Cell 3: 31–6.
76. Veres A, Gosis BS, Ding Q, Collins R, et al. 2014. Low incidence of off-target mutations in individual CRISPR-Cas9 and TALEN targeted human stem cell clones detected by whole-genome sequencing. Cell Stem Cell 15: 27–30.
77. Tsai SQ, Joung JK. 2014. What's changed with genome editing? Cell Stem Cell 15: 3–4.
78. Chapman JR, Taylor MR, Boulton SJ. 2012. Playing the end game: DNA double-strand break repair pathway choice. Mol Cell 47: 497–510.
79. Delacôte F, Perez C, Guyot V, Duhamel M, et al. 2013. High frequency targeted mutagenesis using engineered endonucleases and DNA-end processing enzymes. PLoS One 8: e53217.
80. Cencic R, Miura H, Malina A, Robert F, et al. 2014. Protospacer adjacent motif (PAM)-distal sequences engage CRISPR Cas9 DNA target cleavage. PLoS One 9: e109213.
81. Kuscu C, Arslan S, Singh R, Thorpe J, et al. 2014. Genome-wide analysis reveals characteristics of off-target sites bound by the Cas9 endonuclease. Nat Biotechnol 32: 677–83.
82. Wu X, Scott D, Kriz A, Chiu A, et al. 2014. Genome-wide binding of the CRISPR endonuclease Cas9 in mammalian cells. Nat Biotechnol 32: 670–6.
83. Mendenhall EM, Williamson KE, Reyon D, Zou JY, et al. 2013. Locus-specific editing of histone modifications at endogenous enhancers. Nat Biotechnol 31: 1133–6.
84. Tsai SQ, Zheng Z, Nguyen NT, Liebers M, et al. 2015. GUIDE-seq enables genome-wide profiling of off-target cleavage by CRISPR-Cas nucleases. Nat Biotechnol 33: 187–97.
85. Frock RL, Hu J, Meyers RM, Ho Y-JJ, et al. 2015. Genome-wide detection of DNA double-stranded breaks induced by engineered nucleases. Nat Biotechnol 33: 179–86.
86. Kim D, Bae S, Park J, Kim E, et al. 2015. Digenome-seq: genome-wide profiling of CRISPR-Cas9 off-target effects in human cells. Nat Methods 12: 237–43.
87. Chiarle R, Zhang Y, Frock RL, Lewis SM, et al. 2011. Genome-wide translocation sequencing reveals mechanisms of chromosome breaks and rearrangements in B cells. Cell 147: 107–19.
88. Schmidt M, Schwarzwaelder K, Bartholomae C, Zaoui K, et al. 2007. High-resolution insertion-site analysis by linear amplification-mediated PCR (LAM-PCR). Nat Methods 4: 1051–7.
89. Gabriel R, von Kalle C, Schmidt M. 2015. Mapping the precision of genome editing. Nat Biotechnol 33: 150–2.
90. Osborn MJ, Starker CG, McElroy AN, Webber BR, et al. 2013. TALEN-based gene correction for epidermolysis bullosa. Mol Ther 21: 1151–9.
91. Maggio I, Gonçalves MA. 2015. Genome editing at the crossroads of delivery, specificity, and fidelity. Trends Biotechnol 33: 280–91.
92. Anders C, Niewoehner O, Duerst A, Jinek M. 2014. Structural basis of PAM-dependent target DNA recognition by the Cas9 endonuclease. Nature 513: 569–73.