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TALENs: a widely applicable technology for targeted genome editing
Open accessAbstract
Engineered nucleases enable the targeted alteration of nearly any gene in a wide range of cell types and organisms. The newly-developed transcription activator-like effector nucleases (TALENs) comprise a nonspecific DNA-cleaving nuclease fused to a DNA-binding domain that can be easily engineered so that TALENs can target essentially any sequence. The capability to quickly and efficiently alter genes using TALENs promises to have profound impacts on biological research and to yield potential therapeutic strategies for genetic diseases.
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“Each repeat binds to a single nucleotide, and the amino acids residues in the positions 12 and 13 of that repeat determine which nucleotide is bound [91].”
From CRISPR-Cas: Converting A Bacterial Defence Mechanism into A State-of-the-Art Genetic Manipulation Tool (2019) · cites this paper as [91]
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“The discovery that TALEs use a simple modular code for DNA recognition has provided an alternative platform for genome editing and gene disruption.”
From Newer Gene Editing Technologies toward HIV Gene Therapy (2013) · cites this paper as [66]
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“Alternatively, precise insertions have also been introduced into endogenous human genes using HDR with TALENs and a double-stranded homologous donor template plasmid 19, 20 .”
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“4 DNA binding by these TALEs is mediated by arrays of highly conserved 33–35 amino acid repeats flanked by additional TALE-derived domains at the amino-and carboxy-terminal ends of the array (Figure 1c).”
InfluentialČermák, T., Doyle, E., Christian, M. L., Wang, L., Zhang, Y., Schmidt, C. L., Baller, J. A., Somia, N. V., Bogdanove, A. J., & Voytas, D. F. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr218 · Cited by 2,034 · cited 6×
“To date, TALENs have been used to make knockout mutations in Arabidopsis 15 and to introduce resistance to infection by Xanthomonas bacteria in rice by disrupting the target sites of naturally occurring TALEs that contribute to pathogenicity 16 .”
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Vascular Endothelial Growth Factor
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FLASH assembly of TALENs for high-throughput genome editing
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“Although the high success rate and robust targeting range of dimeric TALENs has been recently established, 18 relatively less is known about these parameters for monomeric engineered TALE-based transcriptional activators or repressors.”
InfluentialGenetic engineering of human pluripotent cells using TALE nucleases
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High-efficiency TALEN-based gene editing produces disease-resistant rice
Li, T., Liu, B., Spalding, M. H., Weeks, D. P., & Yang, B. (2012) · Nature Biotechnology · doi:10.1038/nbt.2199 · Cited by 1,149 · cited 2×
“To date, TALENs have been used to make knockout mutations in Arabidopsis 15 and to introduce resistance to infection by Xanthomonas bacteria in rice by disrupting the target sites of naturally occurring TALEs that contribute to pathogenicity 16 .”
Hockemeyer, D. F., Soldner, F., Beard, C., Gao, Q., Mitalipova, M. M., DeKelver, R. C., Katibah, G. E., Amora, R., Boydston, E. A., Zeitler, B., et al. (2009) · Nature Biotechnology · doi:10.1038/nbt.1562 · Cited by 1,064
DNA Recognition by Cys2His2 Zinc Finger Proteins
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“83, 84 Engineered zinc fingers can be joined together into more extended arrays capable of recognizing longer DNA sequences.”
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“…38 , catfish 39 , sea urchin 40 , frog 41 , pig 42 , cattle 43 , cricket 8 , rabbit 44 , silkworm 45 , butterfly 46 , mouse 47, 48 , rat 49, 50 , soybean 51, 52 , thale cress 53, 54 , corn 55 , tobacco 56 , petunia 57 , hamster cells 58 , and human somatic 59, 60 and pluripotent stem cells 61–63 .”
Xanthomonas AvrBs3 Family-Type III Effectors: Discovery and Function
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In vivo genome editing using a high-efficiency TALEN system
Bedell, V. M., Wang, Y., Campbell, J. M., Poshusta, T. L., Starker, C. G., Krug, R. G., Tan, W. S., Penheiter, S. G., Ma, A. C. H., Leung, A. Y. H., et al. (2012) · Nature · doi:10.1038/nature11537 · Cited by 939 · cited 3×
“As with ZFNs, TALENs have enabled efficient introduction of targeted alterations in a number of model organisms that were previously difficult or impossible to manipulate genetically such as fruit fly 6 , roundworm 7 , zebrafish 9–11 , frog 12 , rat 13 , and pig 14 .”
Knockout Rats via Embryo Microinjection of Zinc-Finger Nucleases
Geurts, A. M., Cost, G. J., Freyvert, Y., Zeitler, B., Miller, J. C., Choi, V. M., Jenkins, S. S., Wood, A., Cui, X., Meng, X., et al. (2009) · Science · doi:10.1126/science.1172447 · Cited by 934 · cited 1×
“…trout 38 , catfish 39 , sea urchin 40 , frog 41 , pig 42 , cattle 43 , cricket 8 , rabbit 44 , silkworm 45 , butterfly 46 , mouse 47, 48 , rat 49, 50 , soybean 51, 52 , thale cress 53, 54 , corn 55 , tobacco 56 , petunia 57 , hamster cells 58 , and human somatic 59, 60 and pluripotent stem cells…”
Heritable targeted gene disruption in zebrafish using designed zinc-finger nucleases
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“87 Sangamo BioSciences, Inc. has developed a proprietary and highly effective platform for engineering zinc finger arrays 36 and customized proteins made by this method can be purchased from Sigma-Aldrich.”
Targeted Chromosomal Cleavage and Mutagenesis in Drosophila Using Zinc-Finger Nucleases
Bibikova, M., Golic, M., Golic, K. G., & Carroll, D. (2002) · Genetics · doi:10.1093/genetics/161.3.1169 · Cited by 860
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Enhancing Gene Targeting with Designed Zinc Finger Nucleases
Bibikova, M. V., Beumer, K. J., Trautman, J. K., & Carroll, D. (2003) · Science · doi:10.1126/science.1079512 · Cited by 824 · cited 1×
“ZFNs have been used to introduce NHEJ-or HDR-mediated gene alterations in fruit fly 33, 34 , roundworm 7, 35 , zebrafish 36, 37 , rainbow trout 38 , catfish 39 , sea urchin 40 , frog 41 , pig 42 , cattle 43 , cricket 8 , rabbit 44 , silkworm 45 , butterfly 46 , mouse 47, 48 , rat 49, 50 , soybean…”
High-frequency modification of plant genes using engineered zinc-finger nucleases
Townsend, J. A., Wright, D. A., Winfrey, R. J., Fu, F., Maeder, M. L., Joung, J. K., & Voytas, D. F. (2009) · Nature · doi:10.1038/nature07845 · Cited by 747 · cited 2×
“…38 , catfish 39 , sea urchin 40 , frog 41 , pig 42 , cattle 43 , cricket 8 , rabbit 44 , silkworm 45 , butterfly 46 , mouse 47, 48 , rat 49, 50 , soybean 51, 52 , thale cress 53, 54 , corn 55 , tobacco 56 , petunia 57 , hamster cells 58 , and human somatic 59, 60 and pluripotent stem cells 61–63 .”
Chimeric nucleases stimulate gene targeting in human cells
Porteus, M. H., & Baltimore, D. (2003) · Science · doi:10.1126/science.1078395 · Cited by 741 · cited 1×
“…38 , catfish 39 , sea urchin 40 , frog 41 , pig 42 , cattle 43 , cricket 8 , rabbit 44 , silkworm 45 , butterfly 46 , mouse 47, 48 , rat 49, 50 , soybean 51, 52 , thale cress 53, 54 , corn 55 , tobacco 56 , petunia 57 , hamster cells 58 , and human somatic 59, 60 and pluripotent stem cells 61–63 .”
Targeted gene inactivation in zebrafish using engineered zinc-finger nucleases
Meng, X., Noyes, M. B., Zhu, L. J., Lawson, N. D., & Wolfe, S. A. (2008) · Nature Biotechnology · doi:10.1038/nbt1398 · Cited by 741 · cited 2×
“Additional methods that explicitly account for context-dependent effects among zinc fingers in an array include: Oligomerized Pool Engineering ( OPEN ) 90 , Context-Dependent Assembly ( CoDA ) 52 , and a bacterial one-hybrid ( B1H ) selection-based system 37 .”
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Maeder, M. L., Thibodeau-Beganny, S., Osiak, A., Wright, D. A., Anthony, R. M., Eichtinger, M., Jiang, T., Foley, J. E., Winfrey, R. J., Townsend, J. A., et al. (2008) · Molecular Cell · doi:10.1016/j.molcel.2008.06.016 · Cited by 727
Design and Selection of Novel Cys2His2 Zinc Finger Proteins
Pabo, C. O., Peisach, E., & Grant, R. A. (2001) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.70.1.313 · Cited by 715 · cited 1×
“83, 84 Engineered zinc fingers can be joined together into more extended arrays capable of recognizing longer DNA sequences.”
A novel TALE nuclease scaffold enables high genome editing activity in combination with low toxicity
Mussolino, C., Morbitzer, R., Lütge, F., Dannemann, N., Lahaye, T., & Cathomen, T. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr597 · Cited by 714 · cited 2×
“24 The TALEN framework was then refined by showing that nuclease activities could be greatly enhanced by truncating the length of this carboxy-terminal TALE-derived sequence 19 , 68 .”
Efficient construction of sequence-specific TAL effectors for modulating mammalian transcription
Zhang, F., Cong, L., Lodato, S., Kosuri, S., Church, G. M., & Arlotta, P. (2011) · Nature Biotechnology · doi:10.1038/nbt.1775 · Cited by 712 · cited 1×
“…that TALE-based activators and repressors can be used to modulate expression of endogenous genes in plants and human cells, with changes in gene or protein expression in the range of two-to 30-fold, 15, 19, 29, 93–98 but the vast majority of these proteins show relatively modest levels of activity.”
Targeted Genome Editing Across Species Using ZFNs and TALENs
Wood, A. J., Lo, T., Zeitler, B., Pickle, C. S., Ralston, E. J., Lee, A. H., Amora, R., Miller, J. C., Leung, E., Meng, X., et al. (2011) · Science · doi:10.1126/science.1207773 · Cited by 682 · cited 2×
“As with ZFNs, TALENs have enabled efficient introduction of targeted alterations in a number of model organisms that were previously difficult or impossible to manipulate genetically such as fruit fly 6 , roundworm 7 , zebrafish 9–11 , frog 12 , rat 13 , and pig 14 .”
Heritable gene targeting in zebrafish using customized TALENs
Huang, P., Xiao, A., Zhou, M., Zhu, Z., Lin, S., & Zhang, B. (2011) · Nature Biotechnology · doi:10.1038/nbt.1939 · Cited by 658 · cited 2×
“10, 28 More recently, a repeat with hypervariable residues NH has been reported to be more specific than the NN repeat, but with only slightly lower activity.”
Targeted gene correction of α1-antitrypsin deficiency in induced pluripotent stem cells
Yusa, K., Rashid, S. T., Strick‐Marchand, H., Varela, I., Liu, P.-Q., Paschon, D. E., Miranda, E., Ordóñez, A., Hannan, N. R. F., Rouhani, F. J., et al. (2011) · Nature · doi:10.1038/nature10424 · Cited by 647 · cited 1×
“…studies have shown that ZFN-induced HDR can be used to correct genetic mutations responsible for sickle cell anemia 72 or alpha1-antitypsin disease 73 or in the Parkinson’s disease-associated alpha-synuclein gene 74 in patient-specific induced pluripotent stem cells that have been reprogrammed…”
A transcription activator-like effector toolbox for genome engineering
Sanjana, N. E., Cong, L., Zhou, Y., Cunniff, M. M., Feng, G., & Zhang, F. (2012) · Nature Protocols · doi:10.1038/nprot.2011.431 · Cited by 643
Targeted gene disruption in somatic zebrafish cells using engineered TALENs
Sander, J. D., Cade, L., Khayter, C., Reyon, D., Peterson, R. T., Joung, J. K., & Yeh, J.-R. J. (2011) · Nature Biotechnology · doi:10.1038/nbt.1934 · Cited by 622 · cited 4×
“As with ZFNs, TALENs have enabled efficient introduction of targeted alterations in a number of model organisms that were previously difficult or impossible to manipulate genetically such as fruit fly 6 , roundworm 7 , zebrafish 9–11 , frog 12 , rat 13 , and pig 14 .”
InfluentialStructural Basis for Sequence-Specific Recognition of DNA by TAL Effectors
Deng, D., Yan, C., Pan, X., Mahfouz, M. M., Wang, J., Zhu, J., Shi, Y., & Yan, N. (2012) · Science · doi:10.1126/science.1215670 · Cited by 618 · cited 1×
“26, 27 Nearly all engineered TALE repeat arrays published to date use four domains with the hypervariable residues NN, NI, HD and NG, for the recognition of G, A, C, and T, respectively.”
The Crystal Structure of TAL Effector PthXo1 Bound to Its DNA Target
Mak, A. N.-S., Bradley, P. H., Cernadas, R. A., Bogdanove, A. J., & Stoddard, B. L. (2012) · Science · doi:10.1126/science.1216211 · Cited by 587 · cited 1×
“26, 27 Nearly all engineered TALE repeat arrays published to date use four domains with the hypervariable residues NN, NI, HD and NG, for the recognition of G, A, C, and T, respectively.”
TAL Effector-Nucleotide Targeter (TALE-NT) 2.0: tools for TAL effector design and target prediction
Doyle, E., Booher, N. J., Standage, D., Voytas, D. F., Brendel, V., VanDyk, J. K., & Bogdanove, A. J. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks608 · Cited by 587 · cited 1×
“In addition, it has been suggested that users should apply computationally derived design guidelines (originally proposed for dimeric TALENs 15 ) to monomeric TALE-based transcription factors 100 but no published experimental support yet exists for this recommendation.”
Knockout rats generated by embryo microinjection of TALENs
Tesson, L., Usal, C., Ménoret, S., Leung, E., Niles, B. J., Remy, S., Santiago, Y., Vincent, A. I., Meng, X., Zhang, L., et al. (2011) · Nature Biotechnology · doi:10.1038/nbt.1940 · Cited by 585 · cited 5×
“Although ZFNs and TALENs have not been directly compared, many studies have shown that TALENs and ZFNs have comparable efficiencies when targeted to the same gene 9, 13, 18, 20 .”
InfluentialEfficient TALEN-mediated gene knockout in livestock
Carlson, D. F., Tan, W. S., Lillico, S. G., Štveráková, D., Proudfoot, C., Christian, M. L., Voytas, D. F., Long, C. R., Whitelaw, B., & Fahrenkrug, S. C. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1211446109 · Cited by 580 · cited 6×
“Most of these studies used a single TALEN pair to generate NHEJ-induced knockout mutations but two of these reports also described the use of two TALEN pairs targeted to the same chromosome to generate deletions and/or inversions of large chromosomal segments 14, 17 .”
InfluentialYano, A., Guyomard, R. R., Nicol, B., Jouanno, E., Quillet, E., Klopp, C., Cabau, C., Bouchez, O., Fostier, A., & Guiguen, Y. (2012) · Current Biology · doi:10.1016/j.cub.2012.05.045 · Cited by 553
TAL nucleases (TALNs): hybrid proteins composed of TAL effectors and FokI DNA-cleavage domain
Li, T., Huang, S., Jiang, W. Z., Wright, D. A., Spalding, M. H., Weeks, D. P., & Yang, B. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq704 · Cited by 547 · cited 1×
“23–25 More recently, co-crystal structures of TALE DNA-binding domains bound to their cognate sites have shown that individual repeats comprise two-helix v-shaped bundles that stack to form a superhelix around the DNA and the hypervariable residues at positions 12 and 13 are positioned in the DNA…”
Selection-free zinc-finger-nuclease engineering by context-dependent assembly (CoDA)
Sander, J. D., Dahlborg, E. J., Goodwin, M. J., Cade, L., Zhang, F., Cifuentes, D., Curtin, S. J., Blackburn, J. S., Thibodeau-Beganny, S., Qi, Y., et al. (2010) · Nature Methods · doi:10.1038/nmeth.1542 · Cited by 518 · cited 3×
“…38 , catfish 39 , sea urchin 40 , frog 41 , pig 42 , cattle 43 , cricket 8 , rabbit 44 , silkworm 45 , butterfly 46 , mouse 47, 48 , rat 49, 50 , soybean 51, 52 , thale cress 53, 54 , corn 55 , tobacco 56 , petunia 57 , hamster cells 58 , and human somatic 59, 60 and pluripotent stem cells 61–63 .”
Gene Targeting of a Disease-Related Gene in Human Induced Pluripotent Stem and Embryonic Stem Cells
Zou, J., Maeder, M. L., Mali, P., Pruett‐Miller, S. M., Thibodeau-Beganny, S., Chou, B.-K., Chen, G., Ye, Z., Park, I., Daley, G. Q., et al. (2009) · Cell stem cell · doi:10.1016/j.stem.2009.05.023 · Cited by 513 · cited 1×
“…38 , catfish 39 , sea urchin 40 , frog 41 , pig 42 , cattle 43 , cricket 8 , rabbit 44 , silkworm 45 , butterfly 46 , mouse 47, 48 , rat 49, 50 , soybean 51, 52 , thale cress 53, 54 , corn 55 , tobacco 56 , petunia 57 , hamster cells 58 , and human somatic 59, 60 and pluripotent stem cells 61–63 .”
Engineering polydactyl zinc-finger transcription factors
Beerli, R. R., & Barbas, C. F. (2002) · Nature Biotechnology · doi:10.1038/nbt0202-135 · Cited by 498 · cited 1×
“Modular assembly of individual pre-selected zinc finger domains provides a simple and rapid method for creating customized arrays 88 but the success rate of this strategy has been reported to be low 89 .”
High-frequency genome editing using ssDNA oligonucleotides with zinc-finger nucleases
Chen, F., Pruett‐Miller, S. M., Huang, Y., Gjoka, M., Duda, K., Taunton, J., Collingwood, T. N., Frödin, M., & Davis, G. D. (2011) · Nature Methods · doi:10.1038/nmeth.1653 · Cited by 475 · cited 1×
“Recent work has also shown that oligonucleotides can be used with ZFNs to introduce precise alterations, small insertions, and large deletions 32 .”
Unexpected failure rates for modular assembly of engineered zinc fingers
Ramirez, C. L., Foley, J. E., Wright, D. A., Müller-Lerch, F., Rahman, S. H., Cornu, T. I., Winfrey, R. J., Sander, J. D., Fu, F., Townsend, J. A., et al. (2008) · Nature Methods · doi:10.1038/nmeth0508-374 · Cited by 426 · cited 1×
“Modular assembly of individual pre-selected zinc finger domains provides a simple and rapid method for creating customized arrays 88 but the success rate of this strategy has been reported to be low 89 .”
Targeted mutagenesis using zinc-finger nucleases in Arabidopsis
Lloyd, A., Plaisier, C. L., Carroll, D., & Drews, G. N. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0409339102 · Cited by 418 · cited 1×
“…38 , catfish 39 , sea urchin 40 , frog 41 , pig 42 , cattle 43 , cricket 8 , rabbit 44 , silkworm 45 , butterfly 46 , mouse 47, 48 , rat 49, 50 , soybean 51, 52 , thale cress 53, 54 , corn 55 , tobacco 56 , petunia 57 , hamster cells 58 , and human somatic 59, 60 and pluripotent stem cells 61–63 .”
Li, T., Huang, S., Zhao, X., Wright, D. A., Carpenter, S. L., Spalding, M. H., Weeks, D. P., & Yang, B. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr188 · Cited by 414 · cited 1×
“…technologies and methodologies previously developed for the use of ZFNs, several groups have used TALENs to modify endogenous genes in yeast 5 , fruit fly 6 , roundworm 7 , crickets 8 , zebrafish 9–11 , frog 12 , rat 13 , pig 14 , cow 14 , thale cress 15 , rice 16 , silkworm 17 , and human…”
Enhancing zinc-finger-nuclease activity with improved obligate heterodimeric architectures
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., & Holmes, M. C. (2011) · Nature Methods · doi:10.1038/nmeth.1539 · Cited by 402 · cited 2×
“In addition, although early studies used wild-type homodimeric FokI nuclease domains, more recent reports 10, 20, 75 have employed various obligate heterodimeric domains originally developed and used with ZFNs 76 (Box 1).”
High frequency targeted mutagenesis in Arabidopsis thaliana using zinc finger nucleases
Zhang, F., Maeder, M. L., Unger‐Wallace, E., Hoshaw, J. P., Reyon, D., Christian, M. L., Li, X., Pierick, C. J., Dobbs, D. L., Peterson, T., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0914991107 · Cited by 385 · cited 1×
“…38 , catfish 39 , sea urchin 40 , frog 41 , pig 42 , cattle 43 , cricket 8 , rabbit 44 , silkworm 45 , butterfly 46 , mouse 47, 48 , rat 49, 50 , soybean 51, 52 , thale cress 53, 54 , corn 55 , tobacco 56 , petunia 57 , hamster cells 58 , and human somatic 59, 60 and pluripotent stem cells 61–63 .”
Moehle, E. A., Rock, J. M., Lee, Y.-L., Jouvenot, Y., DeKelver, R. C., Gregory, P. D., Urnov, F. D., & Holmes, M. C. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0611478104 · Cited by 371 · cited 1×
“Alterantively, if a double-stranded DNA “donor template” is supplied, HDR of a nuclease-induced DSB can be used to introduce precise nucleotide substitutions or insertions of up to 7.6 kb at or near the site of the break 31 (Figure 2a).”
InfluentialEfficient generation of a biallelic knockout in pigs using zinc-finger nucleases
Hauschild‐Quintern, J., Petersen, B., Santiago, Y., Queisser, A. L., Carnwath, J. W., Lucas‐Hahn, A., Zhang, L., Meng, X., Gregory, P. D., Schwinzer, R., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1106422108 · Cited by 370
Targeted gene knockout in mammalian cells by using engineered zinc-finger nucleases
Santiago, Y., Chan, E. M., Liu, P., Orlando, S., Zhang, L., Urnov, F. D., Holmes, M. C., Guschin, D. Y., Waite, A. J., Miller, J. C., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0800940105 · Cited by 364 · cited 1×
“…38 , catfish 39 , sea urchin 40 , frog 41 , pig 42 , cattle 43 , cricket 8 , rabbit 44 , silkworm 45 , butterfly 46 , mouse 47, 48 , rat 49, 50 , soybean 51, 52 , thale cress 53, 54 , corn 55 , tobacco 56 , petunia 57 , hamster cells 58 , and human somatic 59, 60 and pluripotent stem cells 61–63 .”
Cong, L., Zhou, R., Kuo, Y.-C., Cunniff, M. M., & Zhang, F. (2012) · Nature Communications · doi:10.1038/ncomms1962 · Cited by 346 · cited 2×
“…that TALE-based activators and repressors can be used to modulate expression of endogenous genes in plants and human cells, with changes in gene or protein expression in the range of two-to 30-fold, 15, 19, 29, 93–98 but the vast majority of these proteins show relatively modest levels of activity.”
Targeted Mutagenesis of Duplicated Genes in Soybean with Zinc-Finger Nucleases
Curtin, S. J., Zhang, F., Sander, J. D., Haun, W. J., Starker, C. G., Baltes, N. J., Reyon, D., Dahlborg, E. J., Goodwin, M. J., Coffman, A. P., et al. (2011) · PLANT PHYSIOLOGY · doi:10.1104/pp.111.172981 · Cited by 333 · cited 2×
“…38 , catfish 39 , sea urchin 40 , frog 41 , pig 42 , cattle 43 , cricket 8 , rabbit 44 , silkworm 45 , butterfly 46 , mouse 47, 48 , rat 49, 50 , soybean 51, 52 , thale cress 53, 54 , corn 55 , tobacco 56 , petunia 57 , hamster cells 58 , and human somatic 59, 60 and pluripotent stem cells 61–63 .”
A General Strategy for Selecting High-Affinity Zinc Finger Proteins for Diverse DNA Target Sites
Greisman, H. A., & Pabo, C. O. (1997) · Science · doi:10.1126/science.275.5300.657 · Cited by 331
Simsek, D., Brunet, E., Wong, S., Katyal, S., Gao, Y., McKinnon, P. J., Lou, J. F., Zhang, L., Li, J., Rebar, E. J., et al. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1002080 · Cited by 327 · cited 1×
“…deletions induced by introduction of two DSBs with subsequent deletion of intervening sequence of up to 15 Mbps in length 64 , translocations induced by two DSBs introduced on different chromosomes 65, 66 and inversions of chromosomal sequence between two DSBs induced on the same chromosome 67 .”
Targeted integration in rat and mouse embryos with zinc-finger nucleases
Cui, X., Ji, D., Fisher, D. A. C., Wu, Y., Briner, D. M., & Weinstein, E. J. (2010) · Nature Biotechnology · doi:10.1038/nbt.1731 · Cited by 315
Sebastiano, V., Maeder, M. L., Angstman, J. F., Haddad, B., Khayter, C., Yeo, D. T., Goodwin, M. J., Hawkins, J. S., Ramirez, C. L., Batista, L. F. Z., et al. (2011) · Stem Cells · doi:10.1002/stem.718 · Cited by 311 · cited 1×
“For example, recent studies have shown that ZFN-induced HDR can be used to correct genetic mutations responsible for sickle cell anemia 72 or alpha1-antitypsin disease 73 or in the Parkinson’s disease-associated alpha-synuclein gene 74 in patient-specific induced pluripotent stem cells that have…”
Targeted gene knockout by direct delivery of zinc-finger nuclease proteins
Gaj, T., Guo, J., Kato, Y., Sirk, S. J., & Barbas, C. F. (2012) · Nature Methods · doi:10.1038/nmeth.2030 · Cited by 306
TAL effector RVD specificities and efficiencies
Streubel, J., Blücher, C., Landgraf, A., & Boch, J. (2012) · Nature Biotechnology · doi:10.1038/nbt.2304 · Cited by 294 · cited 3×
“10, 28 More recently, a repeat with hypervariable residues NH has been reported to be more specific than the NN repeat, but with only slightly lower activity.”
Gene targeting by homologous recombination in mouse zygotes mediated by zinc-finger nucleases
Meyer, M., de Angelis, M. H., Wurst, W., & Kühn, R. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1009424107 · Cited by 286 · cited 1×
“…36, 37 , rainbow trout 38 , catfish 39 , sea urchin 40 , frog 41 , pig 42 , cattle 43 , cricket 8 , rabbit 44 , silkworm 45 , butterfly 46 , mouse 47, 48 , rat 49, 50 , soybean 51, 52 , thale cress 53, 54 , corn 55 , tobacco 56 , petunia 57 , hamster cells 58 , and human somatic 59, 60 and…”
Morbitzer, R., Römer, P., Boch, J., & Lahaye, T. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1013133107 · Cited by 283 · cited 1×
“23–25 More recently, co-crystal structures of TALE DNA-binding domains bound to their cognate sites have shown that individual repeats comprise two-helix v-shaped bundles that stack to form a superhelix around the DNA and the hypervariable residues at positions 12 and 13 are positioned in the DNA…”
Targeted Genome Modification in Mice Using Zinc-Finger Nucleases
Carbery, I. D., Ji, D., Harrington, A. N., Brown, V. E., Weinstein, E. J., Liaw, L., & Cui, X. (2010) · Genetics · doi:10.1534/genetics.110.117002 · Cited by 274 · cited 1×
“…37 , rainbow trout 38 , catfish 39 , sea urchin 40 , frog 41 , pig 42 , cattle 43 , cricket 8 , rabbit 44 , silkworm 45 , butterfly 46 , mouse 47, 48 , rat 49, 50 , soybean 51, 52 , thale cress 53, 54 , corn 55 , tobacco 56 , petunia 57 , hamster cells 58 , and human somatic 59, 60 and…”
Targeted chromosomal deletions in human cells using zinc finger nucleasesPreprint
Lee, H. J., Kim, E., & Kim, J. (2009) · Genome Research · doi:10.1101/gr.099747.109 · Cited by 259 · cited 1×
“These include large deletions induced by introduction of two DSBs with subsequent deletion of intervening sequence of up to 15 Mbps in length 64 , translocations induced by two DSBs introduced on different chromosomes 65, 66 and inversions of chromosomal sequence between two DSBs induced on the…”
Cade, L., Reyon, D., Hwang, W. Y., Tsai, S. Q., Patel, S., Khayter, C., Joung, J. K., Sander, J. D., Peterson, R. T., & Yeh, J.-R. J. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks518 · Cited by 249
Lei, Y., Guo, X., Liu, Y., Cao, Y., Deng, Y., Chen, X., Cheng, C. H. K., Dawid, I. B., Chen, Y., & Zhao, H. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1215421109 · Cited by 242 · cited 2×
“As with ZFNs, TALENs have enabled efficient introduction of targeted alterations in a number of model organisms that were previously difficult or impossible to manipulate genetically such as fruit fly 6 , roundworm 7 , zebrafish 9–11 , frog 12 , rat 13 , and pig 14 .”
Liu, P., Rebar, E. J., Zhang, L., Liu, Q., Jamieson, A. C., Liang, Y., Qi, H., Li, P.-X., Chen, B., Mendel, M. C., et al. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m011172200 · Cited by 239 · cited 1×
“The epigenetic status (e.g.—chromatin or DNA methylation) of the target sites may influence the activities of TALE-based transcription factors, as has been noted previously for zinc finger-based activators 99 .”
Efficient and Specific Modifications of the Drosophila Genome by Means of an Easy TALEN Strategy
Liu, J., Li, C., Yu, Z., Huang, P., Wu, H., Wei, C., Zhu, N., Shen, Y., Chen, Y., Zhang, B., et al. (2012) · Journal of genetics and genomics/Journal of Genetics and Genomics · doi:10.1016/j.jgg.2012.04.003 · Cited by 209 · cited 1×
“As with ZFNs, TALENs have enabled efficient introduction of targeted alterations in a number of model organisms that were previously difficult or impossible to manipulate genetically such as fruit fly 6 , roundworm 7 , zebrafish 9–11 , frog 12 , rat 13 , and pig 14 .”
Surrogate reporters for enrichment of cells with nuclease-induced mutations
Kim, H., Um, E., Cho, S., Jung, C., Kim, J., & Kim, J. (2011) · Nature Methods · doi:10.1038/nmeth.1733 · Cited by 207
Chromosomal translocations induced at specified loci in human stem cells
Brunet, E., Simsek, D., Tomishima, M., DeKelver, R., Choi, V. M., Gregory, P., Urnov, F., Weinstock, D. M., & Jasin, M. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0902076106 · Cited by 200 · cited 1×
“…deletions induced by introduction of two DSBs with subsequent deletion of intervening sequence of up to 15 Mbps in length 64 , translocations induced by two DSBs introduced on different chromosomes 65, 66 and inversions of chromosomal sequence between two DSBs induced on the same chromosome 67 .”
Nontransgenic Genome Modification in Plant Cells
Marton, I., Zuker, A., Shklarman, E., Zeevi, V., Tovkach, A., Roffe, S., Ovadis, M. I., Tzfira, T., & Vainstein, A. (2010) · PLANT PHYSIOLOGY · doi:10.1104/pp.110.164806 · Cited by 191 · cited 1×
“…38 , catfish 39 , sea urchin 40 , frog 41 , pig 42 , cattle 43 , cricket 8 , rabbit 44 , silkworm 45 , butterfly 46 , mouse 47, 48 , rat 49, 50 , soybean 51, 52 , thale cress 53, 54 , corn 55 , tobacco 56 , petunia 57 , hamster cells 58 , and human somatic 59, 60 and pluripotent stem cells 61–63 .”
Bultmann, S., Morbitzer, R., Schmidt, C. S., Thanisch, K., Spada, F., Elsäesser, J., Lahaye, T., & Leonhardt, H. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks199 · Cited by 184 · cited 1×
“…that TALE-based activators and repressors can be used to modulate expression of endogenous genes in plants and human cells, with changes in gene or protein expression in the range of two-to 30-fold, 15, 19, 29, 93–98 but the vast majority of these proteins show relatively modest levels of activity.”
Morton, J. J., Davis, M. W., Jørgensen, E. M., & Carroll, D. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0605633103 · Cited by 181
Engineered zinc finger nickases induce homology-directed repair with reduced mutagenic effects
Ramirez, C. L., Certo, M. T., Mussolino, C., Goodwin, M. J., Cradick, T. J., McCaffrey, A. P., Cathomen, T., Scharenberg, A. M., & Joung, J. K. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks179 · Cited by 178
Wolfe, S. A., Greisman, H. A., Ramm, E. I., & Pabo, C. O. (1999) · Journal of Molecular Biology · doi:10.1006/jmbi.1998.2421 · Cited by 177 · cited 1×
“87 Sangamo BioSciences, Inc. has developed a proprietary and highly effective platform for engineering zinc finger arrays 36 and customized proteins made by this method can be purchased from Sigma-Aldrich.”
Highly efficient modification of beta-lactoglobulin (BLG) gene via zinc-finger nucleases in cattle
Yu, S., Luo, J., Song, Z., Ding, F., Dai, Y., & Li, N. (2011) · Cell Research · doi:10.1038/cr.2011.153 · Cited by 173 · cited 1×
“…alterations in fruit fly 33, 34 , roundworm 7, 35 , zebrafish 36, 37 , rainbow trout 38 , catfish 39 , sea urchin 40 , frog 41 , pig 42 , cattle 43 , cricket 8 , rabbit 44 , silkworm 45 , butterfly 46 , mouse 47, 48 , rat 49, 50 , soybean 51, 52 , thale cress 53, 54 , corn 55 , tobacco 56 ,…”
Flisikowska, T., Thorey, I. S., Offner, S., Ros, F., Lifke, V., Zeitler, B., Rottmann, O., Vincent, A. I., Zhang, L., Jenkins, S. S., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0021045 · Cited by 171 · cited 1×
“…fly 33, 34 , roundworm 7, 35 , zebrafish 36, 37 , rainbow trout 38 , catfish 39 , sea urchin 40 , frog 41 , pig 42 , cattle 43 , cricket 8 , rabbit 44 , silkworm 45 , butterfly 46 , mouse 47, 48 , rat 49, 50 , soybean 51, 52 , thale cress 53, 54 , corn 55 , tobacco 56 , petunia 57 , hamster cells…”
Designing Transcription Factor Architectures for Drug Discovery
Blancafort, P., Segal, D. J., & Barbas, C. F. (2004) · Molecular Pharmacology · doi:10.1124/mol.104.002758 · Cited by 171 · cited 1×
“92”
Targeted chromosomal duplications and inversions in the human genome using zinc finger nucleasesPreprint
Lee, H. J., Kweon, J., Kim, E., Kim, S., & Kim, J. (2011) · Genome Research · doi:10.1101/gr.129635.111 · Cited by 169 · cited 1×
“…deletions induced by introduction of two DSBs with subsequent deletion of intervening sequence of up to 15 Mbps in length 64 , translocations induced by two DSBs introduced on different chromosomes 65, 66 and inversions of chromosomal sequence between two DSBs induced on the same chromosome 67 .”
Highly Efficient and Specific Genome Editing in Silkworm Using Custom TALENs
Ma, S., Zhang, S., Wang, F., Liu, Y., Liu, Y., Xu, H., Liu, C., Lin, Y., Zhao, P., & Xia, Q. (2012) · PLoS ONE · doi:10.1371/journal.pone.0045035 · Cited by 168 · cited 3×
“Most of these studies used a single TALEN pair to generate NHEJ-induced knockout mutations but two of these reports also described the use of two TALEN pairs targeted to the same chromosome to generate deletions and/or inversions of large chromosomal segments 14, 17 .”
Transcriptional Activators of Human Genes with Programmable DNA-Specificity
Geiβler, R., Scholze, H., Hahn, S., Streubel, J., Bonas, U., Behrens, S., & Boch, J. (2011) · PLoS ONE · doi:10.1371/journal.pone.0019509 · Cited by 164
Moore, F. E., Reyon, D., Sander, J. D., Martinez, S. A., Blackburn, J. S., Khayter, C., Ramirez, C. L., Joung, J. K., & Langenau, D. M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0037877 · Cited by 163 · cited 1×
“We note that as of the writing of this review, the most extensively tested and validated TALEN framework remains that described by Rebar and colleagues 7, 9, 13, 18–20, 75, 77 (Supplementary information S1).”
Targeted mutagenesis in the silkworm Bombyx mori using zinc finger nuclease mRNA injection
Takasu, Y., Kobayashi, I., Beumer, K. J., Uchino, K., Sezutsu, H., Sajwan, S., Carroll, D., Tamura, T., & Žurovec, M. (2010) · Insect Biochemistry and Molecular Biology · doi:10.1016/j.ibmb.2010.07.012 · Cited by 161 · cited 1×
“…roundworm 7, 35 , zebrafish 36, 37 , rainbow trout 38 , catfish 39 , sea urchin 40 , frog 41 , pig 42 , cattle 43 , cricket 8 , rabbit 44 , silkworm 45 , butterfly 46 , mouse 47, 48 , rat 49, 50 , soybean 51, 52 , thale cress 53, 54 , corn 55 , tobacco 56 , petunia 57 , hamster cells 58 , and…”
Engineering synthetic TAL effectors with orthogonal target sites
Garg, A., Lohmueller, J. J., Silver, P. A., & Armel, T. Z. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks404 · Cited by 155
Synergy between adjacent zinc fingers in sequence-specific DNA recognition
Isalan, M., Choo, Y., & Klug, A. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.11.5617 · Cited by 149
Chimeric TALE recombinases with programmable DNA sequence specificity
Mercer, A. C., Gaj, T., Fuller, R. P., & Barbas, C. F. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks875 · Cited by 144 · cited 1×
“TALE repeat arrays fused to a recombinase domain have recently been described 82 , raising the exciting possibility of enabling targetable site-specific recombination events.”
Watanabe, T., Ochiai, H., Sakuma, T., Horch, H. W., Hamaguchi, N., Nakamura, T., Bando, T., Ohuchi, H., Yamamoto, T., Noji, S., et al. (2012) · Nature Communications · doi:10.1038/ncomms2020 · Cited by 139 · cited 3×
“The residues at position 8 and position 12 within the same repeat make a contact with each other that may stabilize the structure of the domain while the residues at position 13 can make base-specific contacts with the DNA.”
Precision genome engineering with programmable DNA-nicking enzymesPreprint
Kim, E., Kim, S., Kim, D. H., Choi, B., Choi, I., & Kim, J. (2012) · Genome Research · doi:10.1101/gr.138792.112 · Cited by 138 · cited 1×
“For example, recent work 7879, 80 has demonstrated that ZFN-derived nickases that cleave only one strand, instead of both strands, of DNA can shift this balance, although the absolute rates of HDR-mediated repair can be lower than those induced by the ZFNs from which they are derived.”
Young, J. J., Cherone, J. M., Doyon, Y., Ankoudinova, I., Faraji, F., Lee, A. H., Ngo, C., Guschin, D. Y., Paschon, D. E., Miller, J. C., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1102030108 · Cited by 134 · cited 1×
“…HDR-mediated gene alterations in fruit fly 33, 34 , roundworm 7, 35 , zebrafish 36, 37 , rainbow trout 38 , catfish 39 , sea urchin 40 , frog 41 , pig 42 , cattle 43 , cricket 8 , rabbit 44 , silkworm 45 , butterfly 46 , mouse 47, 48 , rat 49, 50 , soybean 51, 52 , thale cress 53, 54 , corn…”
Optimized TAL effector nucleases (TALENs) for use in treatment of sickle cell disease
Sun, N., Liang, J., Abil, Z., & Zhao, H. (2012) · Molecular BioSystems · doi:10.1039/c2mb05461b · Cited by 134
Targeted gene addition to a predetermined site in the human genome using a ZFN-based nicking enzymePreprint
Wang, J., Friedman, G., Doyon, Y., Wang, N. S., Li, C. J., Miller, J. C., Hua, K. L., Yan, J. J., Babiarz, J., Gregory, P. D., et al. (2012) · Genome Research · doi:10.1101/gr.122879.111 · Cited by 133
Baker, M. (2011) · Nature Methods · doi:10.1038/nmeth.1807 · Cited by 110
Efficient targeted mutagenesis in the monarch butterfly using zinc-finger nucleasesPreprint
Merlin, C., Beaver, L. E., Taylor, O. R., Wolfe, S. A., & Reppert, S. M. (2012) · Genome Research · doi:10.1101/gr.145599.112 · Cited by 107 · cited 1×
“…, zebrafish 36, 37 , rainbow trout 38 , catfish 39 , sea urchin 40 , frog 41 , pig 42 , cattle 43 , cricket 8 , rabbit 44 , silkworm 45 , butterfly 46 , mouse 47, 48 , rat 49, 50 , soybean 51, 52 , thale cress 53, 54 , corn 55 , tobacco 56 , petunia 57 , hamster cells 58 , and human somatic 59,…”
Human Umbilical Cord Blood Cells Restore Brain Damage Induced Changes in Rat Somatosensory Cortex
Geißler, M., Dinse, H. R., Neuhoff, S., Kreikemeier, K., & Meier, C. (2011) · PLoS ONE · doi:10.1371/journal.pone.0020194 · Cited by 103
Zinc-Finger Nuclease Based Genome Surgery: Its All About Specificity
Händel, E.-M., & Cathomen, T. (2011) · Current Gene Therapy · doi:10.2174/156652311794520120 · Cited by 99 · cited 1×
“A substantial body of literature demonstrates that normal cellular repair of ZFN-induced DSBs by non-homologous end-joining ( NHEJ ) or homology-directed repair ( HDR ) can be exploited to introduce targeted genome alterations in a wide range of organisms and cell types 2, 30 .”
Dong, Z., Ge, J., Li, K., Xu, Z., Liang, D., Li, J., Li, J., Jia, W., Li, Y., Dong, X., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0028897 · Cited by 85 · cited 1×
“…been used to introduce NHEJ-or HDR-mediated gene alterations in fruit fly 33, 34 , roundworm 7, 35 , zebrafish 36, 37 , rainbow trout 38 , catfish 39 , sea urchin 40 , frog 41 , pig 42 , cattle 43 , cricket 8 , rabbit 44 , silkworm 45 , butterfly 46 , mouse 47, 48 , rat 49, 50 , soybean 51, 52 ,…”
Targeted mutagenesis in the sea urchin embryo using zinc‐finger nucleases
Ochiai, H., Fujita, K., Suzuki, K., Nishikawa, M., Shibata, T., Sakamoto, N., & Yamamoto, T. (2010) · Genes to Cells · doi:10.1111/j.1365-2443.2010.01425.x · Cited by 84
An Integrated Chip for the High‐Throughput Synthesis of Transcription Activator‐like Effectors
Wang, Z., Li, J., Huang, H., Wang, G., Jiang, M., Yin, S., Sun, C., Zhang, H., Zhuang, F., & Xi, J. (2012) · Angewandte Chemie International Edition · doi:10.1002/anie.201203597 · Cited by 46
Transcription Activator-Like Effector Proteins Induce the Expression of the Frataxin Gene
Tremblay, J. P., Chapdelaine, P., Coulombe, Z., & Rousseau, J. (2012) · Human Gene Therapy · doi:10.1089/hum.2012.034 · Cited by 33
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Background
Metadata
- Authors
- Joung, J. K., & Sander, J. D.
- Affiliations
- Harvard University (US)
- Corresponding author
- Joung, J. Keith
- Venue
- Nature Reviews Molecular Cell Biology
- Published
- 2012-11-21
- Volume
- 14
- Issue
- 1
- Pages
- 49-55
- ISSN
- 1471-0072 (ISSN-L)
- 1471-0080
- PMC
- PMC3547402
- OpenAlex
- W2061184966
- Cited by
- 1,650
- References
- 103
- Citations by year
- 2026: 65 · 2025: 106 · 2024: 128 · 2023: 119 · 2022: 123 · 2021: 102 · 2020: 112 · 2019: 122 · 2018: 114 · 2017: 103 · 2016: 114 · 2015: 159 · 2014: 175 · 2013: 107
- FWCI
- 12.87
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Nature Reviews Molecular Cell Biology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Human Genome Research Institute (P50HG005550)
- National Cancer Institute (T32CA009216)
- National Institute of General Medical Sciences (DP1GM105378, R01GM088040)
- National Center for Chronic Disease Prevention and Health Promotion (DP1 GM105378)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › CRISPR and Genetic Engineering
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA regulation and disease
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Interference and Gene Delivery
- Keywords
- TALEN, targeted genome editing, engineered nucleases, genetic modification, genetic disease treatment
- MeSH terms
- Animals, Deoxyribonucleases, DNA, DNA-Binding Proteins, Humans, Protein Engineering, Transcriptional Activation, Genome, Protein Structure, Tertiary
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