Genome editing with engineered zinc finger nucleases (original) (raw)

• Carroll, D. Progress and prospects: zinc-finger nucleases as gene therapy agents. Gene Ther. 15, 1463–1468 (2008).
  CAS PubMed PubMed Central Google Scholar
• Bibikova, M., Golic, M., Golic, K. G. & Carroll, D. Targeted chromosomal cleavage and mutagenesis in Drosophila using zinc-finger nucleases. Genetics 161, 1169–1175 (2002).
  CAS PubMed PubMed Central Google Scholar
• Bibikova, M., Beumer, K., Trautman, J. K. & Carroll, D. Enhancing gene targeting with designed zinc finger nucleases. Science 300, 764 (2003). References 2 and 3 are early studies in the field of genome editing that applied ZFNs for the disruption and correction of endogenous genes in D. melanogaster.
  CAS PubMed Google Scholar
• Kim, Y. G., Cha, J. & Chandrasegaran, S. Hybrid restriction enzymes: zinc finger fusions to Fok I cleavage domain. Proc. Natl Acad. Sci. USA 93, 1156–1160 (1996).
  CAS PubMed PubMed Central Google Scholar
• Bibikova, M. et al. Stimulation of homologous recombination through targeted cleavage by chimeric nucleases. Mol. Cell Biol. 21, 289–297 (2001).
  CAS PubMed PubMed Central Google Scholar
• Miller, J., McLachlan, A. D. & Klug, A. Repetitive zinc-binding domains in the protein transcription factor IIIA from Xenopus oocytes. EMBO J. 4, 1609–1614 (1985). This paper describes the discovery of the Cys2-His2 zinc finger — the most common DNA recognition motif in metazoa.
  CAS PubMed PubMed Central Google Scholar
• Wolfe, S. A., Nekludova, L. & Pabo, C. O. DNA recognition by Cys2His2 zinc finger proteins. Annu. Rev. Biophys. Biomol. Struct. 29, 183–212 (2000).
  CAS PubMed Google Scholar
• Pavletich, N. P. & Pabo, C. O. Zinc finger-DNA recognition: crystal structure of a Zif268-DNA complex at 2.1 A. Science 252, 809–817 (1991). This study describes the first X-ray structure of a Cys2-His2 ZFP–DNA complex.
  CAS PubMed Google Scholar
• Segal, D. J. et al. Evaluation of a modular strategy for the construction of novel polydactyl zinc finger DNA-binding proteins. Biochemistry 42, 2137–2148 (2003).
  CAS PubMed Google Scholar
• Rebar, E. J. & Pabo, C. O. Zinc finger phage: affinity selection of fingers with new DNA-binding specificities. Science 263, 671–673 (1994).
  CAS PubMed Google Scholar
• Jamieson, A. C., Kim, S. H. & Wells, J. A. In vitro selection of zinc fingers with altered DNA-binding specificity. Biochemistry 33, 5689–5695 (1994).
  CAS PubMed Google Scholar
• Dreier, B., Beerli, R. R., Segal, D. J., Flippin, J. D. & Barbas, C. F. 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 (2001).
  Article CAS PubMed Google Scholar
• Dreier, B. et al. 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 (2005).
  Article CAS PubMed Google Scholar
• Segal, D. J., Dreier, B., Beerli, R. R. & Barbas, C. F. 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 (1999).
  CAS PubMed PubMed Central Google Scholar
• Choo, Y. & Klug, A. Toward a code for the interactions of zinc fingers with DNA: selection of randomized fingers displayed on phage. Proc. Natl Acad. Sci. USA 91, 11163–11167 (1994).
  CAS PubMed PubMed Central Google Scholar
• Bae, K. H. et al. Human zinc fingers as building blocks in the construction of artificial transcription factors. Nature Biotech. 21, 275–280 (2003).
  CAS Google Scholar
• Kim, H. J., Lee, H. J., Kim, H., Cho, S. W. & Kim, J. S. Targeted genome editing in human cells with zinc finger nucleases constructed via modular assembly. Genome Res. 19, 1279–1288 (2009).
  CAS PubMed PubMed Central Google Scholar
• Segal, D. J., Crotty, J. W., Bhakta, M. S., Barbas, C. F. & Horton, N. C. Structure of Aart, a designed six-finger zinc finger peptide, bound to DNA. J. Mol. Biol. 363, 405–421 (2006).
  CAS PubMed Google Scholar
• Wolfe, S. A., Grant, R. A., Elrod-Erickson, M. & Pabo, C. O. Beyond the 'recognition code' structures of two Cys2His2 zinc finger/TATA box complexes. Structure 9, 717–723 (2001).
  CAS PubMed Google Scholar
• Pavletich, N. P. & Pabo, C. O. Crystal structure of a five-finger GLI–DNA complex: new perspectives on zinc fingers. Science 261, 1701–1707 (1993).
  CAS PubMed Google Scholar
• Fairall, L., Schwabe, J. W., Chapman, L., Finch, J. T. & Rhodes, D. The crystal structure of a two zinc-finger peptide reveals an extension to the rules for zinc-finger/DNA recognition. Nature 366, 483–487 (1993).
  CAS PubMed Google Scholar
• Houbaviy, H. B., Usheva, A., Shenk, T. & Burley, S. K. Cocrystal structure of YY1 bound to the adeno-associated virus P5 initiator. Proc. Natl Acad. Sci. USA 93, 13577–13582 (1996).
  CAS PubMed PubMed Central Google Scholar
• Nolte, R. T., Conlin, R. M., Harrison, S. C. & Brown, R. S. Differing roles for zinc fingers in DNA recognition: structure of a six-finger transcription factor IIIA complex. Proc. Natl Acad. Sci. USA 95, 2938–2943 (1998).
  CAS PubMed PubMed Central Google Scholar
• Ramirez, C. L. et al. Unexpected failure rates for modular assembly of engineered zinc fingers. Nature Methods 5, 374–375 (2008).
  CAS PubMed PubMed Central Google Scholar
• Vanamee, E. S., Santagata, S. & Aggarwal, A. K. FokI requires two specific DNA sites for cleavage. J. Mol. Biol. 309, 69–78 (2001).
  CAS PubMed Google Scholar
• Miller, J. C. et al. An improved zinc-finger nuclease architecture for highly specific genome editing. Nature Biotech. 25, 778–785 (2007).
  CAS Google Scholar
• Szczepek, M. et al. Structure-based redesign of the dimerization interface reduces the toxicity of zinc-finger nucleases. Nature Biotech. 25, 786–793 (2007).
  CAS Google Scholar
• Shimizu, Y., Bhakta, M. S. & Segal, D. J. Restricted spacer tolerance of a zinc finger nuclease with a six amino acid linker. Bioorg. Med. Chem. Lett. 19, 3970–3972 (2009).
  CAS PubMed PubMed Central Google Scholar
• Handel, E. M., Alwin, S. & Cathomen, T. Expanding or restricting the target site repertoire of zinc-finger nucleases: the inter-domain linker as a major determinant of target site selectivity. Mol. Ther. 17, 104–111 (2009).
  PubMed Google Scholar
• Guo, J., Gaj, T. & Barbas, C. F. Directed evolution of an enhanced and highly efficient FokI cleavage domain for zinc finger nucleases. J. Mol. Biol. 400, 96–107 (2010).
  CAS PubMed PubMed Central Google Scholar
• Moynahan, M. E. & Jasin, M. Mitotic homologous recombination maintains genomic stability and suppresses tumorigenesis. Nature Rev. Mol. Cell Biol. 11, 196–207 (2010).
  CAS Google Scholar
• Lieber, M. R. The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu. Rev. Biochem. 79, 181–211 (2010).
  CAS PubMed PubMed Central Google Scholar
• Jackson, S. P. & Bartek, J. The DNA-damage response in human biology and disease. Nature 461, 1071–1078 (2009).
  CAS PubMed PubMed Central Google Scholar
• Beumer, K. J. et al. Efficient gene targeting in Drosophila by direct embryo injection with zinc-finger nucleases. Proc. Natl Acad. Sci. USA 105, 19821–19826 (2008).
  CAS PubMed PubMed Central Google Scholar
• Doyon, Y. et al. Heritable targeted gene disruption in zebrafish using designed zinc-finger nucleases. Nature Biotech. 26, 702–708 (2008).
  CAS Google Scholar
• Meng, X., Noyes, M. B., Zhu, L. J., Lawson, N. D. & Wolfe, S. A. Targeted gene inactivation in zebrafish using engineered zinc-finger nucleases. Nature Biotech. 26, 695–701 (2008).
  CAS Google Scholar
• Foley, J. E. et al. Rapid mutation of endogenous zebrafish genes using zinc finger nucleases made by Oligomerized Pool ENgineering (OPEN). PLoS ONE 4, e4348 (2009).
  PubMed PubMed Central Google Scholar
• Geurts, A. M. et al. Knockout rats via embryo microinjection of zinc-finger nucleases. Science 325, 433 (2009).
  CAS PubMed PubMed Central Google Scholar
• Mashimo, T. et al. Generation of knockout rats with X-linked severe combined immunodeficiency (X-SCID) using zinc-finger nucleases. PLoS ONE 5, e8870 (2010).
  PubMed PubMed Central Google Scholar
• Lloyd, A., Plaisier, C. L., Carroll, D. & Drews, G. N. Targeted mutagenesis using zinc-finger nucleases in Arabidopsis. Proc. Natl Acad. Sci. USA 102, 2232–2237 (2005).
  CAS PubMed PubMed Central Google Scholar
• Zhang, F. et al. High frequency targeted mutagenesis in Arabidopsis thaliana using zinc finger nucleases. Proc. Natl Acad. Sci. USA 107, 12023–12028 (2010).
  Google Scholar
• Osakabe, K., Osakabe, Y. & Toki, S. Site-directed mutagenesis in Arabidopsis using custom-designed zinc finger nucleases. Proc. Natl Acad. Sci. USA, 107, 12034–12039 (2010).
  CAS PubMed PubMed Central Google Scholar
• Thomas, K. R., Folger, K. R. & Capecchi, M. R. High frequency targeting of genes to specific sites in the mammalian genome. Cell 44, 419–428 (1986).
  CAS PubMed Google Scholar
• Kohli, M., Rago, C., Lengauer, C., Kinzler, K. W. & Vogelstein, B. Facile methods for generating human somatic cell gene knockouts using recombinant adeno-associated viruses. Nucleic Acids Res. 32, e3 (2004).
  PubMed PubMed Central Google Scholar
• Ruis, B. L., Fattah, K. R. & Hendrickson, E. A. The catalytic subunit of DNA-dependent protein kinase regulates proliferation, telomere length, and genomic stability in human somatic cells. Mol. Cell Biol. 28, 6182–6195 (2008).
  CAS PubMed PubMed Central Google Scholar
• Khan, I. F. et al. Engineering of human pluripotent stem cells by AAV-mediated gene targeting. Mol. Ther. 18, 1192–1199 (2010).
  CAS PubMed PubMed Central Google Scholar
• Doyon, Y., Vo, T., Choi, V. M., Gregory, P. D. & Holmes, M. C. A transient cold shock enhances zinc-finger nuclease-mediated gene disruption. Nature Methods 7, 459–460 (2010).
  CAS PubMed Google Scholar
• Santiago, Y. et al. Targeted gene knockout in mammalian cells using engineered zinc finger nucleases. Proc. Natl Acad. Sci. USA 105, 5809–5814 (2008).
  CAS PubMed PubMed Central Google Scholar
• Cost, G. J. et al. BAK and BAX deletion using zinc-finger nucleases yields apoptosis-resistant CHO cells. Biotechnol. Bioeng. 105, 330–340 (2009).
  Google Scholar
• Liu, P. Q. et al. Generation of a triple-gene knockout mammalian cell line using engineered zinc-finger nucleases. Biotechnol. Bioeng. 106, 97–105 (2010).
  CAS PubMed Google Scholar
• Lee, H. J., Kim, E. & Kim, J. S. Targeted chromosomal deletions in human cells using zinc finger nucleases. Genome Res. 20, 81–89 (2010).
  CAS PubMed PubMed Central Google Scholar
• Orlando, S. et al. Zinc-finger nuclease-driven targeted integration into mammalian genomes using donors with limited chromosomal homology. Nucleic Acids Res. 8 Jun 2010 (doi:10.1093/nar/gkq512).
  PubMed PubMed Central Google Scholar
• Petolino, J. F. et al. Zinc finger nuclease-mediated transgene deletion. Plant Mol. Biol. 73, 617–628 (2010).
  CAS PubMed Google Scholar
• Brunet, E. et al. Chromosomal translocations induced at specified loci in human stem cells. Proc. Natl Acad. Sci. USA 106, 10620–10625 (2009).
  CAS PubMed PubMed Central Google Scholar
• Brown, J. P., Wei, W. & Sedivy, J. M. Bypass of senescence after disruption of p21CIP1/WAF1 gene in normal diploid human fibroblasts. Science 277, 831–834 (1997).
  CAS PubMed Google Scholar
• Rouet, P., Smih, F. & Jasin, M. Introduction of double-strand breaks into the genome of mouse cells by expression of a rare-cutting endonuclease. Mol. Cell Biol. 14, 8096–8106 (1994). The conclusion drawn by this paper — that the DNA ends generated by a DSB in a mitotically dividing mammalian cell are recombinogenic — provided a starting point for the development of genome editing. See also reference 57.
  CAS PubMed PubMed Central Google Scholar
• Puchta, H., Dujon, B. & Hohn, B. 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 (1993).
  CAS PubMed PubMed Central Google Scholar
• Porteus, M. H. & Baltimore, D. Chimeric nucleases stimulate gene targeting in human cells. Science 300, 763 (2003).
  PubMed Google Scholar
• Bozas, A., Beumer, K. J., Trautman, J. K. & Carroll, D. Genetic analysis of zinc-finger nuclease-induced gene targeting in Drosophila. Genetics 182, 641–651 (2009). This paper provides the first comprehensive study of the intranuclear requirements for resolving an endogenous DSB by NHEJ rather than HDR.
  CAS PubMed PubMed Central Google Scholar
• Beumer, K., Bhattacharyya, G., Bibikova, M., Trautman, J. K. & Carroll, D. Efficient gene targeting in Drosophila with zinc-finger nucleases. Genetics 172, 2391–2403 (2006).
  CAS PubMed PubMed Central Google Scholar
• Urnov, F. D. et al. Highly efficient endogenous human gene correction using designed zinc-finger nucleases. Nature 435, 646–651 (2005).
  CAS PubMed Google Scholar
• Maeder, M. L. et al. Rapid 'open-source' engineering of customized zinc-finger nucleases for highly efficient gene modification. Mol. Cell 31, 294–301 (2008).
  CAS PubMed PubMed Central Google Scholar
• Townsend, J. A. et al. High-frequency modification of plant genes using engineered zinc-finger nucleases. Nature 459, 442–445 (2009).
  CAS PubMed PubMed Central Google Scholar
• Formosa, T. & Alberts, B. M. DNA synthesis dependent on genetic recombination: characterization of a reaction catalyzed by purified bacteriophage T4 proteins. Cell 47, 793–806 (1986).
  CAS PubMed Google Scholar
• Nassif, N., Penney, J., Pal, S., Engels, W. R. & Gloor, G. B. Efficient copying of nonhomologous sequences from ectopic sites via P-element-induced gap repair. Mol. Cell Biol. 14, 1613–1625 (1994).
  CAS PubMed PubMed Central Google Scholar
• Moehle, E. A. et al. Targeted gene addition into a specified location in the human genome using designed zinc finger nucleases. Proc. Natl Acad. Sci. USA 104, 3055–3060 (2007).
  CAS PubMed PubMed Central Google Scholar
• Goldberg, A. D. et al. Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 140, 678–691 (2010).
  CAS PubMed PubMed Central Google Scholar
• Lombardo, A. et al. Gene editing in human stem cells using zinc finger nucleases and integrase-defective lentiviral vector delivery. Nature Biotech. 25, 1298–1306 (2007).
  CAS Google Scholar
• Benabdallah, B. F. et al. Targeted gene addition to human mesenchymal stromal cells as a cell-based plasma-soluble protein delivery platform. Cytotherapy 12, 394–399 (2010).
  CAS PubMed Google Scholar
• Zou, J. et al. Gene targeting of a disease-related gene in human induced pluripotent stem and embryonic stem cells. Stem Cell 5, 97–110 (2009).
  CAS Google Scholar
• Hockemeyer, D. et al. Efficient targeting of expressed and silent genes in human ESCs and iPSCs using zinc-finger nucleases. Nature Biotech. 27, 851–857 (2009).
  CAS Google Scholar
• DeKelver, R. C. et al. Functional genomics, proteomics, and regulatory DNA analysis in isogenic settings using zinc finger nuclease-driven transgenesis into a safe harbor locus in the human. Genome Res. 20, 1133–1142 (2010). A useful feature of ZFN-driven genome editing is the ability it provides to perform mammalian somatic cell genetics experiments in isogenic settings. This paper provides several examples of such isogenic engineering.
  CAS PubMed PubMed Central Google Scholar
• Hanin, M. & Paszkowski, J. Plant genome modification by homologous recombination. Curr. Opin. Plant Biol. 6, 157–162 (2003).
  CAS PubMed Google Scholar
• Cai, C. Q. et al. Targeted transgene integration in plant cells using designed zinc finger nucleases. Plant Mol. Biol. 69, 699–709 (2009).
  CAS PubMed Google Scholar
• Shukla, V. K. et al. Precise genome modification in the crop species Zea mays using zinc-finger nucleases. Nature 459, 437–441 (2009).
  CAS PubMed Google Scholar
• Perez, E. E. et al. Establishment of HIV-1 resistance in CD4+ T cells by genome editing using zinc-finger nucleases. Nature Biotech. 26, 808–816 (2008). This paper provides data underlying the first clinical trial on the genome editing of human cells. See also reference 81.
  CAS Google Scholar
• Tuerk, C. & Gold, L. Systematic evolution of ligands by exponential enrichment: RNA ligands to bacteriophage T4 DNA polymerase. Science 249, 505–510 (1990).
  CAS PubMed Google Scholar
• Blackwell, T. K. & Weintraub, H. Differences and similarities in DNA-binding preferences of MyoD and E2A protein complexes revealed by binding site selection. Science 250, 1104–1110 (1990).
  CAS PubMed Google Scholar
• Phillips, C. M. et al. Identification of chromosome sequence motifs that mediate meiotic pairing and synapsis in, C. elegans. Nature Cell Biol. 11, 934–942 (2009).
  CAS PubMed Google Scholar
• Reik, A. et al. Zinc finger nucleases targeting the glucocorticoid receptor allow IL-13 zetakine transgenic CTLs to kill glioblastoma cells in vivo in the presence of immunosuppressing glucocorticoids. Mol. Ther. 16, S13–S14 (2008).
  Google Scholar
• Holt, N. et al. Human hematopoietic stem/progenitor cells modified by zinc-finger nuclease targeted to CCR5 control HIV-1 in vivo. Nature Biotech. 20 Jul 2010 (doi:10.1038/nbt.1663).
  CAS PubMed PubMed Central Google Scholar
• Bot., A. The landmark approval of Provenge, what it means to immunology and 'in this issue': the complex relation between vaccines and autoimmunity. Int. Rev. Immunol. 29, 235–238 (2010).
  CAS PubMed Google Scholar
• Hutter, G. et al. Long-term control of HIV by CCR5 Delta32/Delta32 stem-cell transplantation. N. Engl. J. Med. 360, 692–698 (2009).
  PubMed Google Scholar
• Hurt, J. A., Thibodeau, S. A., Hirsh, A. S., Pabo, C. O. & Joung, J. K. Highly specific zinc finger proteins obtained by directed domain shuffling and cell-based selection. Proc. Natl Acad. Sci. USA 100, 12271–12276 (2003).
  CAS PubMed PubMed Central Google Scholar
• Mandell, J. G. & Barbas, C. F. Zinc Finger Tools: custom DNA-binding domains for transcription factors and nucleases. Nucleic Acids Res. 34, W516–W523 (2006).
  CAS PubMed PubMed Central Google Scholar
• Sander, J. D., Zaback, P., Joung, J. K., Voytas, D. F. & Dobbs, D. An affinity-based scoring scheme for predicting DNA-binding activities of modularly assembled zinc-finger proteins. Nucleic Acids Res. 37, 506–515 (2009).
  CAS PubMed Google Scholar
• Moore, M., Klug, A. & Choo, Y. Improved DNA binding specificity from polyzinc finger peptides by using strings of two-finger units. Proc. Natl Acad. Sci. USA 98, 1437–1441 (2001).
  CAS PubMed PubMed Central Google Scholar
• Bartsevich, V. V. & Juliano, R. L. Regulation of the MDR1 gene by transcriptional repressors selected using peptide combinatorial libraries. Mol. Pharmacol. 58, 1–10 (2000).
  CAS PubMed Google Scholar
• Isalan, M., Klug, A. & Choo, Y. A rapid, generally applicable method to engineer zinc fingers illustrated by targeting the HIV-1 promoter. Nature Biotech. 19, 656–660 (2001).
  CAS Google Scholar
• Greisman, H. A. & Pabo, C. O. A general strategy for selecting high-affinity zinc finger proteins for diverse DNA target sites. Science 275, 657–661 (1997).
  CAS PubMed Google Scholar
• Rebar, E. J. & Miller, J. C. Design and applications of engineered zinc finger proteins. Biotech International 20–23 (April/May 2004).
• Malphettes, L. et al. Highly efficient deletion of FUT8 in CHO cell lines using zinc-finger nucleases yields cells that produce completely nonfucosylated antibodies. Biotechnol. Bioeng. 106, 774–783 (2010).
  CAS PubMed Google Scholar
• Siekmann, A. F., Standley, C., Fogarty, K. E., Wolfe, S. A. & Lawson, N. D. Chemokine signaling guides regional patterning of the first embryonic artery. Genes Dev. 23, 2272–2277 (2009).
  CAS PubMed PubMed Central Google Scholar
• Del Prete, G. Q. et al. Derivation and characterization of a simian immunodeficiency virus SIVmac239 variant with tropism for CXCR4. J. Virol. 83, 9911–9922 (2009).
  CAS PubMed PubMed Central Google Scholar