An unbiased genome-wide analysis of zinc-finger nuclease specificity

Nature Biotechnology

Volumn 29, Issue 9, 2011, Pages 816-823

  Gabriel, Richard ^a   Lombardo, Angelo ^b   Arens, Anne ^a   Miller, Jeffrey C ^c   Genovese, Pietro ^b   Kaeppel, Christine ^a   Nowrouzi, Ali ^a   Bartholomae, Cynthia C ^a   Wang, Jianbin ^c   Friedman, Geoffrey ^c   Holmes, Michael C ^c   Gregory, Philip D ^c   Glimm, Hanno ^a   Schmidt, Manfred ^a   Naldini, Luigi ^b   Von Kalle, Christof ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

^c SANGAMO BIOSCIENCES INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING SEQUENCE; BIOCHEMICAL EXPERIMENTS; BROAD APPLICATION; CLEAVAGE ACTIVITIES; CLEAVAGE SITES; DOUBLE-STRAND BREAKS; GENOMIC LOCUS; IN-SILICO; IN-VIVO; LENTIVIRAL VECTOR; LIVE CELL; NONHOMOLOGOUS END JOINING; NUCLEASE ACTIVITY; SPATIAL ARRANGEMENTS; TARGET SITES; TRANSIENT EVENTS; TRANSLATIONAL RESEARCH;

BINDING SITES; ZINC;

GENES;

CHEMOKINE RECEPTOR CCR5; DNA; GREEN FLUORESCENT PROTEIN; INTERLEUKIN 2 RECEPTOR GAMMA; LENTIVIRUS VECTOR; NUCLEASE; ZINC FINGER PROTEIN;

ADENO ASSOCIATED VIRUS; ARTICLE; DNA REPAIR; DNA STRAND BREAKAGE; ENZYME ACTIVITY; ENZYME SPECIFICITY; GENE LOCUS; GENOME; GENOME ANALYSIS; PRIORITY JOURNAL;

BINDING SITES; CELL LINE, TUMOR; CLUSTER ANALYSIS; DNA BREAKS, DOUBLE-STRANDED; ENDODEOXYRIBONUCLEASES; GENE TARGETING; GENETIC LOCI; GENETIC VECTORS; HIV INTEGRASE; HUMANS; LENTIVIRUS; PROTEIN BINDING; SEQUENCE ANALYSIS, DNA; SUBSTRATE SPECIFICITY; ZINC FINGERS;

EID: 80052766645     PISSN: 10870156     EISSN: 15461696     Source Type: Journal    
DOI: 10.1038/nbt.1948     Document Type: Article

References (45)

1. Klug, A. The discovery of zinc fingers and their applications in gene regulation and genome manipulation. Annu. Rev. Biochem. 79, 13-231 (2010).
2. Urnov, F.D., Rebar, E.J., Holmes, M.C., Zhang, H.S. & Gregory, P.D. Genome editing with engineered zinc finger nucleases. Nat. Rev. enet. 11, 636-646 (2010).
3. Lombardo, A. et al. Gene editing in human stem cells using zinc finger nucleases and integrase-defective lentiviral vector delivery. at. Biotechnol. 25, 1298-1306 (2007). (Pubitemid 350076515)
4. Urnov, F.D. et al. Highly efficient endogenous human gene correction using designed zinc-finger nucleases. Nature 435, 646-651 2005). (Pubitemid 40825505)
5. Kim, Y.G., Cha, J. & Chandrasegaran, S. Hybrid restriction enzymes: zinc finger fusions to Fok I cleavage domain. Proc. Natl. Acad. Sci. SA 93, 1156-1160 (1996). (Pubitemid 26052857)
6. Mani, M., Smith, J., Kandavelou, K., Berg, J.M. & Chandrasegaran, S. Binding of two zinc finger nuclease monomers to two specific ites is required for effective double-strand DNA cleavage. Biochem. Biophys. Res. Commun. 334, 1191-1197 (2005). (Pubitemid 41074700)
7. Smith, J. et al. Requirements for double-strand cleavage by chimeric restriction enzymes with zinc finger DNA-recognition domains. Nucleic Acids Res. 28, 3361-3369 (2000). (Pubitemid 30662302)
8. Perez, E.E. et al. Establishment of HIV-1 resistance in CD4+ T cells by genome editing using zinc-finger nucleases. Nat. Biotechnol. 26, 08-816 (2008).
9. Liu, P.Q. et al. Generation of a triple-gene knockout mammalian cell line using engineered zinc-finger nucleases. Biotechnol. Bioeng. 06, 97-105 (2010).
10. Santiago, Y. et al. Targeted gene knockout in mammalian cells by using engineered zincfinger nucleases. Proc. Natl. Acad. Sci. USA 05, 5809-5814 (2008). (Pubitemid 351758454)
11. Bibikova, M., Golic, M., Golic, K.G. & Carroll, D. Targeted chromosomal cleavage and mutagenesis in Drosophila using zinc-finger ucleases. Genetics 161, 1169-1175 (2002). (Pubitemid 34831440)
12. Geurts, A.M. et al. Knockout rats via embryo microinjection of zinc-finger nucleases. Science 325, 433 (2009).
13. Hockemeyer, D. et al. Efficient targeting of expressed and silent genes in human ESCs and iPSCs using zinc-finger nucleases. Nat. iotechnol. 27, 851-857 (2009).
14. Moehle, E.A. et al. Targeted gene addition into a specified location in the human genome using designed zinc finger nucleases. Proc. atl. Acad. Sci. USA 104, 3055-3060 (2007). (Pubitemid 46364112)
15. Maeder, M.L. et al. Rapid "open-source" engineering of customized zinc-finger nucleases for highly efficient gene modification. Mol. ell 31, 294-301 (2008). (Pubitemid 352001401)
16. Bibikova, M., Beumer, K., Trautman, J.K. & Carroll, D. Enhancing gene targeting with designed zinc finger nucleases. Science 300, 764 2003). (Pubitemid 36532104)
17. DeKelver, R.C. et al. Functional genomics, proteomics, and regulatory DNA analysis in isogenic settings using zinc finger nuclease- riven transgenesis into a safe harbor locus in the human genome. Genome Res. 20, 1133-1142 (2010).
18. Doyon, J.B. et al. Rapid and efficient clathrin-mediated endocytosis revealed in genomeedited mammalian cells. Nat. Cell Biol. 13, 31-337 (2011).
19. Goldberg, A.D. et al. Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 140, 678-691 (2010).
20. Naldini, L. et al. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272, 263-267 (1996). (Pubitemid 26119138)
21. Vargas, J. Jr., Gusella, G.L., Najfeld, V., Klotman, M.E. & Cara, A. Novel integrasedefective lentiviral episomal vectors for gene ransfer. Hum. Gene Ther. 15, 361-372 (2004). (Pubitemid 38469778)
22. Li, L. et al. Role of the non-homologous DNA end joining pathway in the early steps of retroviral infection. EMBO J. 20, 3272-3281 2001). (Pubitemid 32612014)
23. Nightingale, S.J. et al. Transient gene expression by nonintegrating lentiviral vectors. Mol. Ther. 13, 1121-1132 (2006). (Pubitemid 43796157)
24. Gaur, M. & Leavitt, A.D. Mutations in the human immunodeficiency virus type 1 integrase D,D(35)E motif do not eliminate provirus formation. J. Virol. 72, 4678-4685 (1998). (Pubitemid 28215642)
25. Miller, D.G., Petek, L.M. & Russell, D.W. Adeno-associated virus vectors integrate at chromosome breakage sites. Nat. Genet. 36, 767-773 (2004). (Pubitemid 38886641)
26. Lin, Y. & Waldman, A.S. Promiscuous patching of broken chromosomes in mammalian cells with extrachromosomal DNA. Nucleic Acids Res. 29, 3975-3981 (2001). (Pubitemid 32962687)
27. Lin, Y. & Waldman, A.S. Capture of DNA sequences at double-strand breaks in mammalian chromosomes. Genetics 158, 1665-1674 (2001). (Pubitemid 32783147)
28. Petek, L.M., Russell, D.W. & Miller, D.G. Frequent endonuclease cleavage at off-target locations in vivo. Mol. Ther. 18, 983-986 (2010).
29. Deichmann, A. et al. Vector integration is nonrandom and clustered and influences the fate of lymphopoiesis in SCID-X1 gene therapy. J. Clin. Invest. 117, 2225-2232 (2007). (Pubitemid 47219567)
30. Schmidt, M. et al. High-resolution insertion-site analysis by linear amplificationmediated PCR (LAM-PCR). Nat. Methods 4, 1051-057 (2007). (Pubitemid 350201778)
31. Gabriel, R. et al. Comprehensive genomic access to vector integration in clinical gene therapy. Nat. Med. 15, 1431-1436 (2009).
32. Paruzynski, A. et al. Genome-wide high-throughput integrome analyses by nrLAM-PCR and next-generation sequencing. Nat. Protoc. , 1379-1395 (2010).
33. Schroeder, A.R. et al. HIV-1 integration in the human genome favors active genes and local hotspots. Cell 110, 521-529 (2002).
34. Mitchell, R.S. et al. Retroviral DNA integration: ASLV, HIV, and MLV show distinct target site preferences. PLoS Biol. 2, E234 (2004).
35. Matrai, J. et al. Hepatocyte-targeted expression by integrase-defective lentiviral vectors induces antigen-specific tolerance in mice ith low genotoxic risk. Hepatology 53, 1696-1707 (2011).
36. Miller, J.C. et al. An improved zinc-finger nuclease architecture for highly specific genome editing. Nat. Biotechnol. 25, 778-785 2007). (Pubitemid 47052191)
37. Honma, M. et al. Non-homologous end-joining for repairing I-SceI-induced DNA double strand breaks in human cells. DNA Repair Amst.) 6, 781-788 (2007). (Pubitemid 46670087)
38. Cornu, T.I. & Cathomen, T. Targeted genome modifications using integrase-deficient lentiviral vectors. Mol. Ther. 15, 2107-2113 2007). (Pubitemid 350148926)
39. Bibikova, M. et al. Stimulation of homologous recombination through targeted cleavage by chimeric nucleases. Mol. Cell. Biol. 21, 89-297 (2001).
40. Handel, E.M., Alwin, S. & Cathomen, T. Expanding or restricting the target site repertoire of zinc-finger nucleases: the inter-domain inker as a major determinant of target site selectivity. Mol. Ther. 17, 104-111 (2009).
41. Guschin, D.Y. et al. A rapid and general assay for monitoring endogenous gene modification. Methods Mol. Biol. 649, 247-256 2010).
42. Bitinaite, J., Wah, D.A., Aggarwal, A.K. & Schildkraut, I. FokI dimerization is required for DNA cleavage. Proc. Natl. Acad. Sci. USA 95, 0570-10575 (1998).
43. Vanamee, E.S., Santagata, S. & Aggarwal, A.K. FokI requires two specific DNA sites for cleavage. J. Mol. Biol. 309, 69-78 (2001). (Pubitemid 32553508)
44. Kent, W.J. BLAT-the BLAST-like alignment tool. Genome Res. 12, 656-664 (2002).
45. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. & Lipman, D.J. Basic local alignment search tool. J. Mol. Biol. 215, 403-410 (1990).