TALEN-mediated genome editing: Prospects and perspectives

Biochemical Journal

Volumn 462, Issue 1, 2014, Pages 15-24

  Wright, David A ^a   Li, Ting ^a   Yang, Bing ^a   Spalding, Martin H ^a  

^a IOWA STATE UNIVERSITY   (United States)

Author keywords

Genetic engineering; Genome editing; Homologous recombination (HR); Meganuclease; NHEJ (non homologous end joining); Transcription activator like effector nuclease (TALEN); Zinc finger nuclease

Indexed keywords

DNA BASE; EXONUCLEASE; HETERODIMER; HOMODIMER; MICRORNA; NUCLEASE; PROTEIN; PROTEIN FOKI; TRANSCRIPTION ACTIVATOR LIKE EFFECTOR NUCLEASE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; ZINC FINGER NUCLEASE;

CRYSTAL STRUCTURE; DNA BINDING; DNA CLEAVAGE; DNA END JOINING REPAIR; DOUBLE STRANDED DNA BREAK; GENE FUNCTION; GENE MUTATION; GENETIC ENGINEERING; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; REVIEW;

ANIMALS; DNA END-JOINING REPAIR; DNA REPAIR; ENDONUCLEASES; GENETIC ENGINEERING; GENOME; HUMANS; PLANTS; RECOMBINATION, GENETIC; RECOMBINATIONAL DNA REPAIR; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION;

EID: 84904615174     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20140295     Document Type: Review

References (98)

1. Mladenov, E. and Iliakis, G. (2011) Induction and repair of DNA double strand breaks: the increasing spectrum of non-homologous end joining pathways. Mut. Res. 711, 61-72 CrossRef
2. San Filippo, J., Sung, P. and Klein, H. (2008) Mechanism of eukaryotic homologous recombination. Annu. Rev. Biochem. 77, 229-257 CrossRef
3. Puchta, H., Dujon, B. and Hohn, B. (1993) Homologous recombination in plant cells is enhanced by in vivo induction of double strand breaks into DNA by a site-specific endonuclease. Nucleic Acids Res. 21, 5034-5040 CrossRef PubMed (Pubitemid 23342510)
4. Rouet, P., Smih, F. and Jasin, M. (1994) Expression of a site-specific endonuclease stimulates homologous recombination in mammalian cells. Proc. Natl. Acad. Sci. U.S.A. 91, 6064-6068 CrossRef PubMed (Pubitemid 24188283)
5. Segal, D. J. and Carroll, D. (1995) Endonuclease-induced, targeted homologous extrachromosomal recombination in Xenopus oocytes. Proc. Natl. Acad. Sci. U.S.A. 92, 806-810 CrossRef PubMed
6. Arnould, S., Chames, P., Perez, C., Lacroix, E., Duclert, A., Epinat, J. C., Stricher, F., Petit, A. S., Patin, A., Guillier, S. et al. (2006) Engineering of large numbers of highly specific homing endonucleases that induce recombination on novel DNA targets. J. Mol. Biol. 355, 443-458 CrossRef PubMed (Pubitemid 41785749)
7. Ashworth, J., Taylor, G. K., Havranek, J. J., Quadri, S. A., Stoddard, B. L. and Baker, D. (2010) Computational reprogramming of homing endonuclease specificity at multiple adjacent base pairs. Nucleic Acids Res. 38, 5601-5608 CrossRef PubMed
8. Smith, J., Grizot, S., Arnould, S., Duclert, A., Epinat, J. C., Chames, P., Prieto, J., Redondo, P., Blanco, F. J., Bravo, J. et al. (2006) A combinatorial approach to create artificial homing endonucleases cleaving chosen sequences. Nucleic Acids Res. 34, e149 CrossRef PubMed
9. Sussman, D., Chadsey, M., Fauce, S., Engel, A., Bruett, A., Monnat, Jr, R., Stoddard, B. L. and Seligman, L. M. (2004) Isolation and characterization of new homing endonuclease specificities at individual target site positions. J. Mol. Biol. 342, 31-41 CrossRef PubMed (Pubitemid 39094503)
10. Smith, J., Bibikova, M., Whitby, F. G., Reddy, A. R., Chandrasegaran, S. and Carroll, D. (2000) Requirements for double-strand cleavage by chimeric restriction enzymes with zinc finger DNA-recognition domains. Nucleic Acids Res. 28, 3361-3369 CrossRef PubMed (Pubitemid 30662302)
11. Bibikova, M., Beumer, K., Trautman, J. K. and Carroll, D. (2003) Enhancing gene targeting with designed zinc finger nucleases. Science 300, 764 CrossRef PubMed (Pubitemid 36532104)
12. Bibikova, M., Carroll, D., Segal, D. J., Trautman, J. K., Smith, J., Kim, Y. G. and Chandrasegaran, S. (2001) Stimulation of homologous recombination through targeted cleavage by chimeric nucleases. Mol. Cell. Biol. 21, 289-297 CrossRef PubMed
13. Bibikova, M., Golic, M., Golic, K. G. and Carroll, D. (2002) Targeted chromosomal cleavage and mutagenesis in Drosophila using zinc-finger nucleases. Genetics 161, 1169-1175 PubMed (Pubitemid 34831440)
14. Porteus, M. H. and Baltimore, D. (2003) Chimeric nucleases stimulate gene targeting in human cells. Science 300, 763 CrossRef PubMed (Pubitemid 36532103)
15. Lloyd, A., Plaisier, C. L., Carroll, D. and Drews, G. N. (2005) Targeted mutagenesis using zinc-finger nucleases in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 102, 2232-2237 CrossRef PubMed (Pubitemid 40262041)
16. Wright, D. A., Townsend, J. A., Winfrey, Jr, R. J., Irwin, P. A., Rajagopal, J., Lonosky, P. M., Hall, B. D., Jondle, M. D. and Voytas, D. F. (2005) High-frequency homologous recombination in plants mediated by zinc-finger nucleases. Plant J. 44, 693-705 CrossRef PubMed
17. Heuer, H., Yin, Y. N., Xue, Q. Y., Smalla, K. and Guo, J. H. (2007) Repeat domain diversity of avrBs3-like genes in Ralstonia solanacearum strains and association with host preferences in the field. Appl. Environ. Microbiol. 73, 4379-4384 CrossRef PubMed (Pubitemid 47068184)
18. Li, L., Atef, A., Piatek, A., Ali, Z., Piatek, M., Aouida, M., Sharakuu, A., Mahjoub, A., Wang, G., Khan, S. et al. (2013) Characterization and DNA-binding specificities of Ralstonia TAL-like effectors. Mol. Plant 6, 1318-1330 CrossRef PubMed
19. Boch, J. and Bonas, U. (2010) Xanthomonas AvrBs3 family-type III effectors: discovery and function. Annu. Rev. Phytopathol. 48, 419-436 CrossRef
20. Moscou, M. J. and Bogdanove, A. J. (2009) A simple cipher governs DNA recognition by TAL effectors. Science 326, 1501 CrossRef PubMed
21. Romer, P., Hahn, S., Jordan, T., Strauss, T., Bonas, U. and Lahaye, T. (2007) Plant pathogen recognition mediated by promoter activation of the pepper Bs3 resistance gene. Science 318, 645-648 CrossRef PubMed (Pubitemid 350014838)
22. Schornack, S., Minsavage, G. V., Stall, R. E., Jones, J. B. and Lahaye, T. (2008) Characterization of AvrHah1, a novel AvrBs3-like effector from Xanthomonas gardneri with virulence and avirulence activity. New Phytol. 179, 546-556 CrossRef PubMed (Pubitemid 351991429)
23. Yang, B., Zhu, W., Johnson, L. B. and White, F. F. (2000) The virulence factor AvrXa7 of Xanthomonas oryzae pv. oryzae is a type III secretion pathway-dependent nuclear-localized double-stranded DNA-binding protein. Proc. Natl. Acad. Sci. U.S.A. 97, 9807-9812 CrossRef PubMed (Pubitemid 30650857)
24. Boch, J., Scholze, H., Schornack, S., Landgraf, A., Hahn, S., Kay, S., Lahaye, T., Nickstadt, A. and Bonas, U. (2009) Breaking the code of DNA binding specificity of TAL-type III effectors. Science 326, 1509-1512 CrossRef PubMed
25. Meckler, J. F., Bhakta, M. S., Kim, M. S., Ovadia, R., Habrian, C. H., Zykovich, A., Yu, A., Lockwood, S. H., Morbitzer, R., Elsaesser, J. et al. (2013) Quantitative analysis of TALE-DNA interactions suggests polarity effects. Nucleic Acids Res. 41, 4118-4128 CrossRef PubMed
26. Deng, D., Yan, C., Pan, X., Mahfouz, M., Wang, J., Zhu, J. K., Shi, Y. and Yan, N. (2012) Structural basis for sequence-specific recognition of DNA by TAL effectors. Science 335, 720-723 CrossRef PubMed
27. Mak, A. N., Bradley, P., Cernadas, R. A., Bogdanove, A. J. and Stoddard, B. L. (2012) The crystal structure of TAL effector PthXo1 bound to its DNA target. Science 335, 716-719 CrossRef PubMed
28. Mussolino, C., Morbitzer, R., Lutge, F., Dannemann, N., Lahaye, T. and Cathomen, T. (2011) A novel TALE nuclease scaffold enables high genome editing activity in combination with low toxicity. Nucleic Acids Res. 39, 9283-9293 CrossRef PubMed
29. Doyon, Y., Vo, T. D., Mendel, M. C., Greenberg, S. G., Wang, J., Xia, D. F., Miller, J. C., Urnov, F. D., Gregory, P. D. and Holmes, M. C. (2011) Enhancing zinc-finger-nuclease activity with improved obligate heterodimeric architectures. Nat. Methods 8, 74-79 CrossRef PubMed
30. Guo, J., Gaj, T. and Barbas, III, C. F. (2010) Directed evolution of an enhanced and highly efficient FokI cleavage domain for zinc finger nucleases. J. Mol. Biol. 400, 96-107 CrossRef PubMed
31. Miller, J. C., Holmes, M. C., Wang, J., Guschin, D. Y., Lee, Y. L., Rupniewski, I., Beausejour, C. M., Waite, A. J., Wang, N. S., Kim, K. A. et al. (2007) An improved zinc-finger nuclease architecture for highly specific genome editing. Nat. Biotechnol. 25, 778-785 CrossRef PubMed (Pubitemid 47052191)
32. Sizova, I., Greiner, A., Awasthi, M., Kateriya, S. and Hegemann, P. (2013) Nuclear gene targeting in Chlamydomonas using engineered zinc-finger nucleases. Plant J. 73, 873-882 CrossRef PubMed
33. Szczepek, M., Brondani, V., Buchel, J., Serrano, L., Segal, D. J. and Cathomen, T. (2007) Structure-based redesign of the dimerization interface reduces the toxicity of zinc-finger nucleases. Nat. Biotechnol. 25, 786-793 CrossRef PubMed (Pubitemid 47052189)
34. Briggs, A. W., Rios, X., Chari, R., Yang, L., Zhang, F., Mali, P. and Church, G. M. (2012) Iterative capped assembly: rapid and scalable synthesis of repeat-module DNA such as TAL effectors from individual monomers. Nucleic Acids Res. 40, e117 CrossRef PubMed
35. Cermak, T., Doyle, E. L., Christian, M., Wang, L., Zhang, Y., Schmidt, C., Baller, J. A., Somia, N. V., Bogdanove, A. J. and Voytas, D. F. (2011) Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res. 39, e82 CrossRef PubMed
36. Kim, Y., Kweon, J., Kim, A., Chon, J. K., Yoo, J. Y., Kim, H. J., Kim, S., Lee, C., Jeong, E., Chung, E. et al. (2013) A library of TAL effector nucleases spanning the human genome. Nat. Biotechnol. 31, 251-258 CrossRef PubMed
37. Li, T., Huang, S., Zhao, X., Wright, D. A., Carpenter, S., Spalding, M. H., Weeks, D. P. and Yang, B. (2011) Modularly assembled designer TAL effector nucleases for targeted gene knockout and gene replacement in eukaryotes. Nucleic Acids Res. 39, 6315-6325 CrossRef PubMed
38. Liang, J., Chao, R., Abil, Z., Bao, Z. and Zhao, H. (2013) FairyTALE: A High-Throughput TAL Effector Synthesis Platform. ACS Synth. Biol. 3, 67-73 CrossRef
39. Reyon, D., Tsai, S. Q., Khayter, C., Foden, J. A., Sander, J. D. and Joung, J. K. (2012) FLASH assembly of TALENs for high-throughput genome editing. Nat. Biotechnol. 30, 460-465 CrossRef PubMed
40. Schmid-Burgk, J. L., Schmidt, T., Kaiser, V., Honing, K. and Hornung, V. (2013) A ligation-independent cloning technique for high-throughput assembly of transcription activator-like effector genes. Nat. Biotechnol. 31, 76-81 CrossRef PubMed
41. Yang, J., Yuan, P., Wen, D., Sheng, Y., Zhu, S., Yu, Y., Gao, X. and Wei, W. (2013) ULtiMATE system for rapid assembly of customized TAL effectors. PloS ONE 8, e75649 CrossRef PubMed
42. Zhang, Z., Li, D., Xu, H., Xin, Y., Zhang, T., Ma, L., Wang, X., Chen, Z. and Zhang, Z. (2013) A simple and efficient method for assembling TALE protein based on plasmid library. PLoS ONE 8, e66459 CrossRef PubMed
43. Miller, J. C., Tan, S., Qiao, G., Barlow, K. A., Wang, J., Xia, D. F., Meng, X., Paschon, D. E., Leung, E., Hinkley, S. J. et al. (2011) A TALE nuclease architecture for efficient genome editing. Nat. Biotechnol. 29, 143-148 CrossRef PubMed
44. Christian, M., Cermak, T., Doyle, E. L., Schmidt, C., Zhang, F., Hummel, A., Bogdanove, A. J. and Voytas, D. F. (2010) Targeting DNA double-strand breaks with TAL effector nucleases. Genetics 186, 757-761 CrossRef PubMed
45. Christian, M. L., Demorest, Z. L., Starker, C. G., Osborn, M. J., Nyquist, M. D., Zhang, Y., Carlson, D. F., Bradley, P., Bogdanove, A. J. and Voytas, D. F. (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 CrossRef PubMed
46. Ma, S., Zhang, S., Wang, F., Liu, Y., Liu, Y., Xu, H., Liu, C., Lin, Y., Zhao, P. and Xia, Q. (2012) Highly efficient and specific genome editing in silkworm using custom TALENs. PloS ONE 7, e45035 CrossRef PubMed
47. Bedell, V. M., Wang, Y., Campbell, J. M., Poshusta, T. L., Starker, C. G., Krug, II, R. G., Tan, W., Penheiter, S. G., Ma, A. C., Leung, A. Y. et al. (2012) In vivo genome editing using a high-efficiency TALEN system. Nature 491, 114-118 CrossRef PubMed
48. Wood, A. J., Lo, T. W., Zeitler, B., Pickle, C. S., Ralston, E. J., Lee, A. H., Amora, R., Miller, J. C., Leung, E., Meng, X. et al. (2011) Targeted genome editing across species using ZFNs and TALENs. Science 333, 307 CrossRef PubMed
49. Huang, P., Xiao, A., Zhou, M., Zhu, Z., Lin, S. and Zhang, B. (2011) Heritable gene targeting in zebrafish using customized TALENs. Nat. Biotechnol. 29, 699-700 CrossRef PubMed
50. Wang, H., Hu, Y. C., Markoulaki, S., Welstead, G. G., Cheng, A. W., Shivalila, C. S., Pyntikova, T., Dadon, D. B., Voytas, D. F., Bogdanove, A. J. et al. (2013) TALEN-mediated editing of the mouse Y chromosome. Nat. Biotechnol. 31, 530-532 CrossRef PubMed
51. Carlson, D. F., Tan, W., Lillico, S. G., Stverakova, D., Proudfoot, C., Christian, M., Voytas, D. F., Long, C. R., Whitelaw, C. B. and Fahrenkrug, S. C. (2012) Efficient TALEN-mediated gene knockout in livestock. Proc. Natl. Acad. Sci. U.S.A. 109, 17382-17387 CrossRef PubMed
52. Christian, M., Qi, Y., Zhang, Y. and Voytas, D. F. (2013) Targeted mutagenesis of Arabidopsis thaliana using engineered TAL effector nucleases. G3 3, 1697-1705 CrossRef PubMed
53. Liang, Z., Zhang, K., Chen, K. and Gao, C. (2013) Targeted mutagenesis in Zea mays using TALENs and the CRISPR/Cas system. J. Genet. Genom. 41, 63-68 CrossRef
54. Shan, Q., Wang, Y., Chen, K., Liang, Z., Li, J., Zhang, Y., Zhang, K., Liu, J., Voytas, D. F., Zheng, X. et al. (2013) Rapid and efficient gene modification in rice and Brachypodium using TALENs. Mol. Plant 6, 1365-1368 CrossRef PubMed
55. Wendt, T., Holm, P. B., Starker, C. G., Christian, M., Voytas, D. F., Brinch-Pedersen, H. and Holme, I. B. (2013) TAL effector nucleases induce mutations at a pre-selected location in the genome of primary barley transformants. Plant Mol. Biol. 83, 279-285 CrossRef PubMed
56. Zhang, Y., Zhang, F., Li, X., Baller, J. A., Qi, Y., Starker, C. G., Bogdanove, A. J. and Voytas, D. F. (2013) Transcription activator-like effector nucleases enable efficient plant genome engineering. Plant Physiol. 161, 20-27 CrossRef PubMed
57. Li, T., Liu, B., Spalding, M. H., Weeks, D. P. and Yang, B. (2012) High-efficiency TALEN-based gene editing produces disease-resistant rice. Nat. Biotechnol. 30, 390-392 CrossRef PubMed
58. Stroud, D. A., Formosa, L. E., Wijeyeratne, X. W., Nguyen, T. N. and Ryan, M. T. (2013) Gene knockout using transcription activator-like effector nucleases (TALENs) reveals that human NDUFA9 protein is essential for stabilizing the junction between membrane and matrix arms of complex I. J. Biol. Chem. 288, 1685-1690 CrossRef PubMed
59. Hu, R., Wallace, J., Dahlem, T. J., Grunwald, D. J. and O'Connell, R. M. (2013) Targeting human microRNA genes using engineered Tal-effector nucleases (TALENs). PloS ONE 8, e63074 CrossRef PubMed
60. Kim, Y. K., Wee, G., Park, J., Kim, J., Baek, D., Kim, J. S. and Kim, V. N. (2013) TALEN-based knockout library for human microRNAs. Nat. Struct. Mol. Biol. 20, 1458-1464 CrossRef PubMed
61. Takada, S., Sato, T., Ito, Y., Yamashita, S., Kato, T., Kawasumi, M., Kanai-Azuma, M., Igarashi, A., Kato, T., Tamano, M. and Asahara, H. (2013) Targeted gene deletion of miRNAs in mice by TALEN system. PloS ONE 8, e76004 CrossRef PubMed
62. Cheng, Z., Yi, P., Wang, X., Chai, Y., Feng, G., Yang, Y., Liang, X., Zhu, Z., Li, W. and Ou, G. (2013) Conditional targeted genome editing using somatically expressed TALENs in C. elegans. Nat. Biotechnol. 31, 934-937 CrossRef PubMed
63. Treen, N., Yoshida, K., Sakuma, T., Sasaki, H., Kawai, N., Yamamoto, T. and Sasakura, Y. (2014) Tissue-specific and ubiquitous gene knockouts by TALEN electroporation provide new approaches to investigating gene function in Ciona. Development 141, 481-487 CrossRef PubMed
64. Gupta, A., Hall, V. L., Kok, F. O., Shin, M., McNulty, J. C., Lawson, N. D. and Wolfe, S. A. (2013) Targeted chromosomal deletions and inversions in zebrafish. Genome Res. 23, 1008-1017 CrossRef PubMed
65. Nyquist, M. D., Li, Y., Hwang, T. H., Manlove, L. S., Vessella, R. L., Silverstein, K. A., Voytas, D. F. and Dehm, S. M. (2013) TALEN-engineered AR gene rearrangements reveal endocrine uncoupling of androgen receptor in prostate cancer. Proc. Natl. Acad. Sci. U.S.A. 110, 17492-17497 CrossRef PubMed
66. Piganeau, M., Ghezraoui, H., De Cian, A., Guittat, L., Tomishima, M., Perrouault, L., Rene, O., Katibah, G. E., Zhang, L., Holmes et al. (2013) Cancer translocations in human cells induced by zinc finger and TALE nucleases. Genome Res. 23, 1182-1193 CrossRef PubMed
67. Elliott, B., Richardson, C., Winderbaum, J., Nickoloff, J. A. and Jasin, M. (1998) Gene conversion tracts from double-strand break repair in mammalian cells. Mol. Cell. Biol. 18, 93-101 PubMed (Pubitemid 28021021)
68. Lee, C. M., Flynn, R., Hollywood, J. A., Scallan, M. F. and Harrison, P. T. (2012) Correction of the deltaF508 mutation in the cystic fibrosis transmembrane conductance regulator gene by zinc-finger nuclease homology-directed repair. Biores. Open Access 1, 99-108 CrossRef PubMed
69. Porteus, M. H. (2006) Mammalian gene targeting with designed zinc finger nucleases. Mol. Ther. 13, 438-446 CrossRef PubMed
70. Townsend, J. A., Wright, D. A., Winfrey, R. J., Fu, F., Maeder, M. L., Joung, J. K. and Voytas, D. F. (2009) High-frequency modification of plant genes using engineered zinc-finger nucleases. Nature 459, 442-445 CrossRef PubMed
71. Urnov, F. D., Miller, J. C., Lee, Y. L., Beausejour, C. M., Rock, J. M., Augustus, S., Jamieson, A. C., Porteus, M. H., Gregory, P. D. and Holmes, M. C. (2005) Highly efficient endogenous human gene correction using designed zinc-finger nucleases. Nature 435, 646-651 CrossRef PubMed (Pubitemid 40825505)
72. Shukla, V. K., Doyon, Y., Miller, J. C., DeKelver, R. C., Moehle, E. A., Worden, S. E., Mitchell, J. C., Arnold, N. L., Gopalan, S., Meng, X. et al. (2009) Precise genome modification in the crop species Zea mays using zinc-finger nucleases. Nature 459, 437-441 CrossRef PubMed
73. Davies, B., Davies, G., Preece, C., Puliyadi, R., Szumska, D. and Bhattacharya, S. (2013) Site specific mutation of the Zic2 locus by microinjection of TALEN mRNA in mouse CD1, C3H and C57BL/6J oocytes. PLoS ONE 8, e60216 CrossRef PubMed
74. Pruett-Miller, S. M., Reading, D. W., Porter, S. N. and Porteus, M. H. (2009) Attenuation of zinc finger nuclease toxicity by small-molecule regulation of protein levels. PLoS Genet. 5, e1000376 CrossRef PubMed
75. Gaj, T., Guo, J., Kato, Y., Sirk, S. J. and Barbas, III, C. F. (2012) Targeted gene knockout by direct delivery of zinc-finger nuclease proteins. Nat. Methods 9, 805-807 CrossRef PubMed
76. Liu, J., Gaj, T., Patterson, J. T., Sirk, S. J. and Barbas, III, C. F. (2014) Cell-penetrating peptide-mediated delivery of TALEN proteins via bioconjugation for genome engineering. PloS ONE 9, e85755 CrossRef PubMed
77. Ru, R., Yao, Y., Yu, S., Yin, B., Xu, W., Zhao, S., Qin, L. and Chen, X. (2013) Targeted genome engineering in human induced pluripotent stem cells by penetrating TALENs. Cell Regen. 2, 1-8 CrossRef
78. Tesson, L., Usal, C., Menoret, S., Leung, E., Niles, B. J., Remy, S., Santiago, Y., Vincent, A. I., Meng, X., Zhang, L. et al. (2011) Knockout rats generated by embryo microinjection of TALENs. Nat. Biotechnol. 29, 695-696 CrossRef PubMed
79. Holkers, M., Maggio, I., Liu, J., Janssen, J. M., Miselli, F., Mussolino, C., Recchia, A., Cathomen, T. and Goncalves, M. A. (2013) Differential integrity of TALE nuclease genes following adenoviral and lentiviral vector gene transfer into human cells. Nucleic Acids Res. 41, e63 CrossRef PubMed
80. Barampuram, S. and Zhang, Z. J. (2011) Recent advances in plant transformation. Methods Mol. Biol. 701, 1-35 CrossRef PubMed
81. Baltes, N. J., Gil-Humanes, J., Cermak, T., Atkins, P. A. and Voytas, D. F. (2014) DNA replicons for plant genome engineering. Plant Cell 26, 151-163 CrossRef PubMed
82. Kim, H. J., Lee, H. J., Kim, H., Cho, S. W. and Kim, J. S. (2009) Targeted genome editing in human cells with zinc finger nucleases constructed via modular assembly. Genome Res. 19, 1279-1288 CrossRef PubMed
83. Oleykowski, C. A., Bronson Mullins, C. R., Godwin, A. K. and Yeung, A. T. (1998) Mutation detection using a novel plant endonuclease. Nucleic Acids Res. 26, 4597-4602 CrossRef PubMed (Pubitemid 28466605)
84. Dahlem, T. J., Hoshijima, K., Jurynec, M. J., Gunther, D., Starker, C. G., Locke, A. S., Weis, A. M., Voytas, D. F. and Grunwald, D. J. (2012) Simple methods for generating and detecting locus-specific mutations induced with TALENs in the zebrafish genome. PLoS Genet. 8, e1002861 CrossRef PubMed
85. Ansai, S., Inohaya, K., Yoshiura, Y., Schartl, M., Uemura, N., Takahashi, R. and Kinoshita, M. (2014) Design, evaluation, and screening methods for efficient targeted mutagenesis with transcription activator-like effector nucleases in medaka. Dev. Growth Differ. 56, 98-107 CrossRef PubMed
86. Wei, C., Liu, J., Yu, Z., Zhang, B., Gao, G. and Jiao, R. (2013) TALEN or Cas9 - rapid, efficient and specific choices for genome modifications. J. Genet. Genom. 40, 281-289 CrossRef
87. Mashimo, T., Kaneko, T., Sakuma, T., Kobayashi, J., Kunihiro, Y., Voigt, B., Yamamoto, T. and Serikawa, T. (2013) Efficient gene targeting by TAL effector nucleases coinjected with exonucleases in zygotes. Sci. Rep. 3, 1253 CrossRef PubMed
88. Certo, M. T., Gwiazda, K. S., Kuhar, R., Sather, B., Curinga, G., Mandt, T., Brault, M., Lambert, A. R., Baxter, S. K., Jacoby, K. et al. (2012) Coupling endonucleases with DNA end-processing enzymes to drive gene disruption. Nat. Methods 9, 973-975 CrossRef PubMed
89. Boissel, S., Jarjour, J., Astrakhan, A., Adey, A., Gouble, A., Duchateau, P., Shendure, J., Stoddard, B. L., Certo, M. T., Baker, D. and Scharenberg, A. M. (2013) megaTALs: a rare-cleaving nuclease architecture for therapeutic genome engineering. Nucleic Acids Res. 2, 2591-2601
90. Hummel, A. W., Doyle, E. L. and Bogdanove, A. J. (2012) Addition of transcription activator-like effector binding sites to a pathogen strain-specific rice bacterial blight resistance gene makes it effective against additional strains and against bacterial leaf streak. New Phytol. 195, 883-893 CrossRef PubMed
91. Maeder, M. L., Linder, S. J., Reyon, D., Angstman, J. F., Fu, Y., Sander, J. D. and Joung, J. K. (2013) Robust, synergistic regulation of human gene expression using TALE activators. Nat. Methods 10, 243-245 CrossRef PubMed
92. Perez-Pinera, P., Ousterout, D. G., Brunger, J. M., Farin, A. M., Glass, K. A., Guilak, F., Crawford, G. E., Hartemink, A. J. and Gersbach, C. A. (2013) Synergistic and tunable human gene activation by combinations of synthetic transcription factors. Nat. Methods 10, 239-242 CrossRef PubMed
93. Scott, J. N., Kupinski, A. P., Kirkham, C. M., Tuma, R. and Boyes, J. (2014) TALE proteins bind to both active and inactive chromatin. Biochem. J. 458, 153-158 CrossRef PubMed
94. Zhu, W., Yang, B., Wills, N., Johnson, L. B. and White, F. F. (1999) The C terminus of AvrXa10 can be replaced by the transcriptional activation domain of VP16 from the herpes simplex virus. Plant Cell 11, 1665-1674 CrossRef PubMed
95. Cong, L., Zhou, R., Kuo, Y. C., Cunniff, M. and Zhang, F. (2012) Comprehensive interrogation of natural TALE DNA-binding modules and transcriptional repressor domains. Nat. Commun. 3, 968 CrossRef PubMed
96. Crocker, J. and Stern, D. L. (2013) TALE-mediated modulation of transcriptional enhancers in vivo. Nat. Methods 10, 762-767 CrossRef
97. Mahfouz, M. M., Li, L., Piatek, M., Fang, X., Mansour, H., Bangarusamy, D. K. and Zhu, J. K. (2012) Targeted transcriptional repression using a chimeric TALE-SRDX repressor protein. Plant Mol. Biol. 78, 311-321 CrossRef PubMed
98. Politz, M. C., Copeland, M. F. and Pfleger, B. F. (2013) Artificial repressors for controlling gene expression in bacteria. Chem. Commun. 49, 4325-4327 CrossRef