Browse > Article
http://dx.doi.org/10.14348/molcells.2017.0139

Engineering and Application of Zinc Finger Proteins and TALEs for Biomedical Research  

Kim, Moon-Soo (Department of Chemistry, Western Kentucky University)
Kini, Anu Ganesh (Department of Chemistry, Western Kentucky University)
Publication Information
Molecules and Cells / v.40, no.8, 2017 , pp. 533-541 More about this Journal
Abstract
Engineered DNA-binding domains provide a powerful technology for numerous biomedical studies due to their ability to recognize specific DNA sequences. Zinc fingers (ZF) are one of the most common DNA-binding domains and have been extensively studied for a variety of applications, such as gene regulation, genome engineering and diagnostics. Another novel DNA-binding domain known as a transcriptional activator-like effector (TALE) has been more recently discovered, which has a previously undescribed DNA-binding mode. Due to their modular architecture and flexibility, TALEs have been rapidly developed into artificial gene targeting reagents. Here, we describe the methods used to design these DNA-binding proteins and their key applications in biomedical research.
Keywords
biomedical application; sequence-specific DNA detection; transcriptional activator-like effector; zinc fingers;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Dreier, B., Fuller, R.P., Segal, D.J., Lund, C.V., Blancafort, P., Huber, A., Koksch, B., and Barbas, C.F., 3rd (2005). Development of zinc finger domains for recognition of the 5'-CNN-3' family DNA sequences and their use in the construction of artificial transcription factors. J. Biol. Chem. 280, 35588-35597.   DOI
2 Engler, C., Kandzia, R., and Marillonnet, S. (2008). A one pot, one step, precision cloning method with high throughput capability. PLoS One 3, e3647.   DOI
3 Feng, X., Bednarz, A.L., and Colloms, S.D. (2010). Precise targeted integration by a chimaeric transposase zinc-finger fusion protein. Nucleic Acids Res. 38, 1204-1216.   DOI
4 Gaj, T., Guo, J., Kato, Y., Sirk, S.J., and Barbas, C.F., 3rd (2012). Targeted gene knockout by direct delivery of zinc-finger nuclease proteins. Nat. Methods 9, 805-807.   DOI
5 Gaj, T., Gersbach, C.A., and Barbas, C.F., 3rd (2013a). ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol. 31, 397-405.   DOI
6 Gaj, T., Mercer, A.C., Sirk, S.J., Smith, H.L., and Barbas, C.F., 3rd (2013b). A comprehensive approach to zinc-finger recombinase customization enables genomic targeting in human cells. Nucleic Acids Res. 41, 3937-3946.   DOI
7 Gaj, T., Liu, J., Anderson, K.E., Sirk, S.J., and Barbas, C.F., 3rd (2014a). Protein delivery using Cys2-His2 zinc-finger domains. ACS Chem. Biol. 9, 1662-1667.   DOI
8 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.   DOI
9 Moore, M., Klug, A., and Choo, Y. (2001). Improved DNA binding specificity from polyzinc finger peptides by using strings of two-finger units. Proc. Natl. Acad. Sci. USA 98, 1437-1441.   DOI
10 Morbitzer, R., Elsaesser, J., Hausner, J., and Lahaye, T. (2011). Assembly of custom TALE-type DNA binding domains by modular cloning. Nucleic Acids Res. 39, 5790-5799.   DOI
11 Moscou, M.J., and Bogdanove, A.J. (2009). A simple cipher governs DNA recognition by TAL effectors. Science 326, 1501.   DOI
12 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.   DOI
13 Ooi, A.T., Stains, C.I., Ghosh, I., and Segal, D.J. (2006). Sequenceenabled reassembly of beta-lactamase (SEER-LAC): a sensitive method for the detection of double-stranded DNA. Biochemistry 45, 3620-3625.   DOI
14 Ousterout, D.G., Perez-Pinera, P., Thakore, P.I., Kabadi, A.M., Brown, M.T., Qin, X., Fedrigo, O., Mouly, V., Tremblay, J.P., and Gersbach, C.A. (2013). Reading frame correction by targeted genome editing restores dystrophin expression in cells from Duchenne muscular dystrophy patients. Mol. Ther. 21, 1718-1726.   DOI
15 Owens, J.B., Urschitz, J., Stoytchev, I., Dang, N.C., Stoytcheva, Z., Belcaid, M., Maragathavally, K.J., Coates, C.J., Segal, D.J., and Moisyadi, S. (2012). Chimeric piggyBac transposases for genomic targeting in human cells. Nucleic Acids Res. 40, 6978-6991.   DOI
16 Gordley, R.M., Smith, J.D., Graslund, T., and Barbas, C.F., 3rd (2007). Evolution of programmable zinc finger-recombinases with activity in human cells. J. Mol. Biol. 367, 802-813.   DOI
17 Gaj, T., Sirk, S.J., Tingle, R.D., Mercer, A.C., Wallen, M.C., and Barbas, C.F., 3rd (2014b). Enhancing the specificity of recombinase-mediated genome engineering through dimer interface redesign. J. Am. Chem. Soc. 136, 5047-5056.   DOI
18 Gersbach, C.A., Gaj, T., and Barbas, C.F., 3rd (2014). Synthetic zinc finger proteins: the advent of targeted gene regulation and genome modification technologies. Acc. Chem. Res. 47, 2309-2318.   DOI
19 Ghosh, I., Stains, C.I., Ooi, A.T., and Segal, D.J. (2006). Direct detection of double-stranded DNA: Molecular methods and applications for DNA diagnostics. Mol. Biosyst. 2, 551-560.   DOI
20 Gordley, R.M., Gersbach, C.A., and Barbas, C.F., 3rd (2009). Synthesis of programmable integrases. Proc. Natl. Acad. Sci. USA 106, 5053-5058.   DOI
21 Graslund, T., Li, X., Magnenat, L., Popkov, M., and Barbas, C.F., 3rd (2005). Exploring strategies for the design of artificial transcription factors: targeting sites proximal to known regulatory regions for the induction of gamma-globin expression and the treatment of sickle cell disease. J. Biol. Chem. 280, 3707-3714.   DOI
22 Grindley, N.D., Whiteson, K.L., and Rice, P.A. (2006). Mechanisms of site-specific recombination. Annu. Rev. Biochem. 75, 567-605.   DOI
23 Hockemeyer, D., Wang, H., Kiani, S., Lai, C.S., Gao, Q., Cassady, J.P., Cost, G.J., Zhang, L., Santiago, Y., Miller, J.C., et al. (2011). Genetic engineering of human pluripotent cells using TALE nucleases. Nat. Biotechnol. 29, 731-734.   DOI
24 Owens, J.B., Mauro, D., Stoytchev, I., Bhakta, M.S., Kim, M.S., Segal, D.J., and Moisyadi, S. (2013). Transcription activator like effector (TALE)-directed piggyBac transposition in human cells. Nucleic Acids Res. 41, 9197-9207.   DOI
25 Reyon, D., Maeder, M.L., Khayter, C., Tsai, S.Q., Foley, J.E., Sander, J.D., and Joung, J.K. (2013). Engineering customized TALE nucleases (TALENs) and TALE transcription factors by fast ligation-based automatable solid-phase high-throughput (FLASH) assembly. Curr. Protoc. Mol. Biol. Chapter 12, Unit 12 16.
26 Perez, E.E., Wang, J., Miller, J.C., Jouvenot, Y., Kim, K.A., Liu, O., Wang, N., Lee, G., Bartsevich, V.V., Lee, Y.L., et al. (2008). Establishment of HIV-1 resistance in CD4+ T cells by genome editing using zinc-finger nucleases. Nat. Biotechnol. 26, 808-816.   DOI
27 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.   DOI
28 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.   DOI
29 Rogers, J.M., Barrera, L.A., Reyon, D., Sander, J.D., Kellis, M., Joung, J.K., and Bulyk, M.L. (2015). Context influences on TALE-DNA binding revealed by quantitative profiling. Nat. Commun. 6, 7440.   DOI
30 Sander, J.D., Cade, L., Khayter, C., Reyon, D., Peterson, R.T., Joung, J.K., and Yeh, J.R. (2011). Targeted gene disruption in somatic zebrafish cells using engineered TALENs. Nat. Biotechnol. 29, 697-698.   DOI
31 Sanjana, N.E., Cong, L., Zhou, Y., Cunniff, M.M., Feng, G., and Zhang, F. (2012). A transcription activator-like effector toolbox for genome engineering. Nat. Protoc. 7, 171-192.   DOI
32 Joung, J.K., Ramm, E.I., and Pabo, C.O. (2000). A bacterial twohybrid selection system for studying protein-DNA and protein-protein interactions. Proc. Natl. Acad. Sci. USA 97, 7382-7387.   DOI
33 Bae, K.H., Kwon, Y.D., Shin, H.C., Hwang, M.S., Ryu, E.H., Park, K.S., Yang, H.Y., Lee, D.K., Lee, Y., Park, J., et al. (2003). Human zinc fingers as building blocks in the construction of artificial transcription factors. Nat. Biotechnol. 21, 275-280.   DOI
34 Bailus, B.J., and Segal, D.J. (2014). The prospect of molecular therapy for Angelman syndrome and other monogenic neurologic disorders. BMC Neurosci. 15, 76.   DOI
35 Beerli, R.R., and Barbas, C.F., 3rd (2002). Engineering polydactyl zincfinger transcription factors. Nat. Biotechnol. 20, 135-141.   DOI
36 Jiang, F., and Doudna, J.A. (2015). The structural biology of CRISPRCas systems. Curr. Opin. Struct. Biol. 30, 100-111.   DOI
37 Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J.A., and Charpentier, E. (2012). A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337, 816-821.   DOI
38 Kim, M.S., Stybayeva, G., Lee, J.Y., Revzin, A., and Segal, D.J. (2011). A zinc finger protein array for the visual detection of specific DNA sequences for diagnostic applications. Nucleic Acids Res. 39, e29.   DOI
39 Kolb, A.F., Coates, C.J., Kaminski, J.M., Summers, J.B., Miller, A.D., and Segal, D.J. (2005). Site-directed genome modification: nucleic acid and protein modules for targeted integration and gene correction. Trends Biotechnol. 23, 399-406.   DOI
40 Li, H., Haurigot, V., Doyon, Y., Li, T., Wong, S.Y., Bhagwat, A.S., Malani, N., Anguela, X.M., Sharma, R., Ivanciu, L., et al. (2011a). In vivo genome editing restores haemostasis in a mouse model of haemophilia. Nature 475, 217-221.   DOI
41 Li, T., Huang, S., Zhao, X., Wright, D.A., Carpenter, S., Spalding, M.H., Weeks, D.P., and Yang, B. (2011b). Modularly assembled designer TAL effector nucleases for targeted gene knockout and gene replacement in eukaryotes. Nucleic Acids Res. 39, 6315-6325.   DOI
42 Holt, N., Wang, J., Kim, K., Friedman, G., Wang, X., Taupin, V., Crooks, G.M., Kohn, D.B., Gregory, P.D., Holmes, M.C., et al. (2010). Human hematopoietic stem/progenitor cells modified by zinc-finger nucleases targeted to CCR5 control HIV-1 in vivo. Nat. Biotechnol. 28, 839-847.   DOI
43 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., et al. (2011). In situ genetic correction of the sickle cell anemia mutation in human induced pluripotent stem cells using engineered zinc finger nucleases. Stem Cells 29, 1717-1726.   DOI
44 Segal, D.J., and Meckler, J.F. (2013). Genome engineering at the dawn of the golden age. Annu. Rev. Genomics Hum. Genet. 14, 135-158.   DOI
45 Segal, D.J., Dreier, B., Beerli, R.R., and Barbas, C.F., 3rd (1999). Toward controlling gene expression at will: selection and design of zinc finger domains recognizing each of the 5'-GNN-3' DNA target sequences. Proc. Natl. Acad. Sci. USA 96, 2758-2763.   DOI
46 Segal, D.J., Beerli, R.R., Blancafort, P., Dreier, B., Effertz, K., Huber, A., Koksch, B., Lund, C.V., Magnenat, L., Valente, D., et al. (2003). Evaluation of a modular strategy for the construction of novel polydactyl zinc finger DNA-binding proteins. Biochemistry 42, 2137-2148.   DOI
47 Segal, D.J., Goncalves, J., Eberhardy, S., Swan, C.H., Torbett, B.E., Li, X., and Barbas, C.F., 3rd (2004). Attenuation of HIV-1 replication in primary human cells with a designed zinc finger transcription factor. J. Biol. Chem. 279, 14509-14519.   DOI
48 Bhakta, M.S., and Segal, D.J. (2010). The generation of zinc finger proteins by modular assembly. Methods Mol. Biol. 649, 3-30.
49 Beerli, R.R., Segal, D.J., Dreier, B., and Barbas, C.F., 3rd (1998). Toward controlling gene expression at will: specific regulation of the erbB-2/HER-2 promoter by using polydactyl zinc finger proteins constructed from modular building blocks. Proc. Natl. Acad. Sci. USA 95, 14628-14633.   DOI
50 Beerli, R.R., Dreier, B., and Barbas, C.F., 3rd (2000). Positive and negative regulation of endogenous genes by designed transcription factors. Proc. Natl. Acad. Sci. USA 97, 1495-1500.   DOI
51 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.   DOI
52 Camenisch, T.D., Brilliant, M.H., and Segal, D.J. (2008). Critical parameters for genome editing using zinc finger nucleases. Mini Rev. Med. Chem. 8, 669-676.   DOI
53 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.   DOI
54 Curtin, S.J., Zhang, F., Sander, J.D., Haun, W.J., Starker, C., Baltes, N.J., Reyon, D., Dahlborg, E.J., Goodwin, M.J., Coffman, A.P., et al. (2011). Targeted mutagenesis of duplicated genes in soybean with zinc-finger nucleases. Plant Physiol. 156, 466-473.   DOI
55 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.   DOI
56 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). Rapid "open-source" engineering of customized zinc-finger nucleases for highly efficient gene modification. Mol. Cell 31, 294-301.   DOI
57 Segal, D.J., Crotty, J.W., Bhakta, M.S., Barbas, C.F., 3rd, and Horton, N.C. (2006). Structure of Aart, a designed six-finger zinc finger peptide, bound to DNA. J. Mol. Biol. 363, 405-421.   DOI
58 Smith, M.C., and Thorpe, H.M. (2002). Diversity in the serine recombinases. Mol. Microbiol. 44, 299-307.   DOI
59 Soldner, F., Laganiere, J., Cheng, A.W., Hockemeyer, D., Gao, Q., Alagappan, R., Khurana, V., Golbe, L.I., Myers, R.H., Lindquist, S., et al. (2011). Generation of isogenic pluripotent stem cells differing exclusively at two early onset Parkinson point mutations. Cell 146, 318-331.   DOI
60 Li, L., Krymskaya, L., Wang, J., Henley, J., Rao, A., Cao, L.F., Tran, C.A., Torres-Coronado, M., Gardner, A., Gonzalez, N., et al. (2013). Genomic editing of the HIV-1 coreceptor CCR5 in adult hematopoietic stem and progenitor cells using zinc finger nucleases. Mol. Ther. 21, 1259-1269.   DOI
61 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.   DOI
62 Maeder, M.L., Thibodeau-Beganny, S., Sander, J.D., Voytas, D.F., and Joung, J.K. (2009). Oligomerized pool engineering (OPEN): an 'opensource' protocol for making customized zinc-finger arrays. Nat. Protoc. 4, 1471-1501.   DOI
63 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.   DOI
64 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.   DOI
65 Mak, A.N., Bradley, P., Bogdanove, A.J., and Stoddard, B.L. (2013). TAL effectors: function, structure, engineering and applications. Curr. Opin. Struct. Biol. 23, 93-99.   DOI
66 Mercer, A.C., Gaj, T., Fuller, R.P., and Barbas, C.F., 3rd (2012). Chimeric TALE recombinases with programmable DNA sequence specificity. Nucleic Acids Res. 40, 11163-11172.   DOI
67 Sun, N., Liang, J., Abil, Z., and Zhao, H. (2012). Optimized TAL effector nucleases (TALENs) for use in treatment of sickle cell disease. Mol. Biosyst. 8, 1255-1263.   DOI
68 Urnov, F.D., Rebar, E.J., Holmes, M.C., Zhang, H.S., and Gregory, P.D. (2010). Genome editing with engineered zinc finger nucleases. Nat. Rev. Genet. 11, 636-646.   DOI
69 Voigt, K., Gogol-Doring, A., Miskey, C., Chen, W., Cathomen, T., Izsvak, Z., and Ivics, Z. (2012). Retargeting sleeping beauty transposon insertions by engineered zinc finger DNA-binding domains. Mol. Ther. 20, 1852-1862.   DOI
70 Dreier, B., Segal, D.J., and Barbas, C.F., 3rd (2000). Insights into the molecular recognition of the 5'-GNN-3' family of DNA sequences by zinc finger domains. J. Mol. Biol. 303, 489-502.   DOI
71 Dreier, B., Beerli, R.R., Segal, D.J., Flippin, J.D., and Barbas, C.F., 3rd (2001). Development of zinc finger domains for recognition of the 5'-ANN-3' family of DNA sequences and their use in the construction of artificial transcription factors. J. Biol. Chem. 276, 29466-29478.   DOI
72 Zhang, F., Cong, L., Lodato, S., Kosuri, S., Church, G.M., and Arlotta, P. (2011). Efficient construction of sequence-specific TAL effectors for modulating mammalian transcription. Nat. Biotechnol. 29, 149-153.   DOI
73 Wilber, A., Tschulena, U., Hargrove, P.W., Kim, Y.S., Persons, D.A., Barbas, C.F., 3rd, and Nienhuis, A.W. (2010). A zinc-finger transcriptional activator designed to interact with the gamma-globin gene promoters enhances fetal hemoglobin production in primary human adult erythroblasts. Blood 115, 3033-3041.   DOI
74 Wu, H., Yang, W.P., and Barbas, C.F., 3rd (1995). Building zinc fingers by selection: toward a therapeutic application. Proc. Natl. Acad. Sci. USA 92, 344-348.   DOI
75 Yusa, K., Rashid, S.T., Strick-Marchand, H., Varela, I., Liu, P.Q., Paschon, D.E., Miranda, E., Ordonez, A., Hannan, N.R., Rouhani, F.J., et al. (2011). Targeted gene correction of alpha1-antitrypsin deficiency in induced pluripotent stem cells. Nature 478, 391-394.   DOI
76 Zou, J., Mali, P., Huang, X., Dowey, S.N., and Cheng, L. (2011). Sitespecific gene correction of a point mutation in human iPS cells derived from an adult patient with sickle cell disease. Blood 118, 4599-4608.   DOI