DNA-binding specificity is a major determinant of the activity and toxicity of zinc-finger nucleases

Molecular Therapy

Volumn 16, Issue 2, 2008, Pages 352-358

  Cornu, Tatjana I ^a   Thibodeau Beganny, Stacey ^b   Guhl, Eva ^a   Alwin, Stephen ^a   Eichtinger, Magdalena ^b,c   Joung, J K ^b,c   Cathomen, Toni ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEASE; ZINC FINGER PROTEIN;

ARTICLE; BINDING AFFINITY; BINDING SITE; CELL STRAIN HEK293; CONTROLLED STUDY; CYTOTOXICITY; DNA CLEAVAGE; HUMAN; HUMAN CELL; IN VITRO STUDY; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN ENGINEERING; PROTEIN FUNCTION;

EID: 38849103093     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/sj.mt.6300357     Document Type: Article

References (48)

1. Pabo, CO, Peisach, E and Grant, RA (2001). Design and selection of novel Cys2His2 zinc finger proteins. Annu Rev Biochem 70: 313-340.
2. Jamieson, AC, Miller, JC and Pabo, CO (2003). Drug discovery with engineered zinc-finger proteins. Nat Rev Drug Discov 2: 361-368.
3. Durai, S, Mani, M, Kandavelou, K, Wu, J, Porteus, MH and Chandrasegaran, S (2005). Zinc finger nucleases: Custom-designed molecular scissors for genome engineering of plant and mammalian cells. Nucleic Acids Res 33: 5978-5990.
4. Porteus, MH and Carroll, D (2005). Gene targeting using zinc finger nucleases. Nat Biotechnol 23: 967-973.
5. Paques, F and Duchateau, P (2007). Meganucleases and DNA double-strand break-induced recombination: Perspectives for gene therapy. Curr Gene Ther 7: 49-66.
6. Kim, YG, Cha, J and Chandrasegaran, S (1996). Hybrid restriction enzymes: Zinc finger fusions to Fok I cleavage domain. Proc Natl Acad Sci USA 93: 1156-1160.
7. Smith, J, Bibikova, M, Whitby, FG, Reddy, AR, 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.
8. Vasquez, KM, Marburger, K, Intody, Z and Wilson, JH (2001). Manipulating the mammalian genome by homologous recombination. Proc Natl Acad Sci USA 98: 8403-8410.
9. Choulika, A, Perrin, A, Dujon, B and Nicolas, JF (1995). Induction of homologous recombination in mammalian chromosomes by using the I-Scel system of Saccharomyces cerevisiae. Mol Cell Biol 15: 1968-1973.
10. Smih, F, Rouet, P, Romanienko, PJ and Jasin, M (1995). Double-strand breaks at the target locus stimulate gene targeting in embryonic stem cells. Nucleic Acids Res 23: 5012-5019.
11. Bibikova, M, Beumer, K, Trautman, JK and Carroll, D (2003). Enhancing gene targeting with designed zinc finger nucleases. Science 300 764.
12. Porteus, MH and Baltimore, D (2003). Chimeric nucleases stimulate gene targeting in human cells. Science 300: 763.
13. Alwin, S, Gere, MB, Guhl, E, Effertz, K, Barbas, CF 3rd, Segal, DJ et al. (2005). Custom zinc-finger nucleases for use in human cells. Mol Ther 12: 610-617.
14. Urnov, FD, Miller, JG, Lee, YL, Beausejour, CM, Rock JM, Augustus, S et al. (2005). Highly efficient endogenous human gene correction using designed zinc-finger nucleases. Nature 435: 646-651.
15. Wright, DA, Townsend, JA, Winfrey, RJ Jr., Irwin, PA, Rajagopal, J, Lonosky, PM et al. (2005). High-frequency homologous recombination in plants mediated by zinc-finger nucleases. Plant J 44: 693-705.
16. Beumer, K, Bhattacharyya, G, Bibikova, M, Trautman, JK and Carroll, D (2006). Efficient gene targeting in Drosophila with zinc-finger nucleases. Genetics 172: 2391-2403.
17. Porteus, MH (2006). Mammalian gene targeting with designed zinc finger nucleases. Mol Ther 13: 438-446.
18. Miller, JC, Holmes, MC, Wang, J, Guschin, DY, Lee, YL, Rupniewski, I et al. (2007). An improved zinc-finger nuclease architecture for highly specific genome editing. Nat Biotechnol 25: 778-785.
19. Szczepek, M, Brondani, V, Buchel, J, Serrano, L, Segal, DJ and Cathomen, T (2007). Structure-based redesign of the dimerization interface reduces the toxicity of zinc-finger nucleases. Nat Biotechnol 25: 786-793.
20. Pavletich, NP and Pabo, CO (1991). Zinc finger-DNA recognition: Crystal structure of a Zif268-DNA complex at 2.1 A. Science 252: 809-817.
21. Elrod-Erickson, M, Rould, MA, Nekludova, L and Pabo, CO (1996). Zif268 protein-DNA complex refined at 1.6 A: A Model system for understanding zinc finger-DNA interactions. Structure 4: 1171-1180.
22. Choo, Y and Klug, A (1994). Selection of DNA binding sites for zinc fingers using rationally randomized DNA reveals coded interactions. Proc Natl Acad Sci USA 91: 11168-11172.
23. Rebar, EJ and Pabo, CO (1994). Zinc finger phage: Affinity selection of fingers with new DNA-binding specificities. Science 263: 671-673.
24. Wu, H, Yang, WP and Barbas, CF 3rd (1995). Building zinc fingers by selection: Toward a therapeutic application. Proc Natl Acad Sci USA 92: 344-348.
25. Jamieson, AC, Wang, H and Kim, SH (1996). A zinc finger directory for high-affinity DNA recognition. Proc Natl Acad Sci USA 93: 12834-12839.
26. Segal, DJ, Dreier, B, Beerli, RR and Barbas, CF 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.
27. Dreier, B, Beerli, RR, Segal, DJ, Flippin, JD and Barbas, CF, 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.
28. Liu, Q, Xia, Z, Zhong, X and Case, CC (2002). Validated zinc finger protein designs for all 16 GNN DNA triplet targets. J Biol Chem 277: 3850-3856.
29. Blancafort P, Magnenat, L and Barbas, CF 3rd (2003). Scanning the human genome with combinatorial transcription factor libraries. Nat Biotechnol 21: 269-274.
30. Dreier, B, Fuller, RP, Segal, DJ, Lund, CV, Blancafort, P, Huber, A et al. (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.
31. Bitinaite, J, Wah, DA, Aggarwal, AK and Schildkraut, I (1998). Fold dimerization is required for DNA cleavage. Proc Natl Acad Sci USA 95: 10570-10575.
32. Bibikova, M, Carroll, D, Segal, DJ, Trautman, JK, Smith, J, Kim, YG etal. (2001). Stimulation of homologous recombination through targeted cleavage by chimeric nucleases. Mol Cell Biol 21: 289-297.
33. Hurt, JA, Thibodeau, SA, Hirsh, AS, Pabo, CO and Joung, JK (2003). Highly specific zinc finger proteins obtained by directed domain shuffling and cell-based selection. Prob Natl Acad Sci USA 100 12271-12276.
34. Joung, JK, Ramm, El and Pabo, CO (2000). A bacterial two-hybrid selection system for studying protein-DNA and protein-protein interactions. Proc Natl Acad Sci USA 97: 7382-7387.
35. Miller, DG, Petek, LM and Russell, DW (2003). Human gene targeting by adeno-associated virus vectors is enhanced by DNA double-strand breaks. Mol Cell Biol 23: 3550-3557.
36. Porteus, MH, Cathomen, T, Weitzman, MD and Baltimore, D (2003). Efficient gene targeting mediated by adeno-associated virus and DNA double-strand breaks. Mol Cell Biol 23: 3558-3565.
37. Rogakou, EP, Pilch, DR, Orr, AH, Ivanova, VS and Bonner, WM (1998). DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273: 5858-5868.
38. Wright, DA, Thibodeau-Beganny, S, Sander, JD, Winfrey, RJ, Hirsh, AS, Eichtinger, M et al. (2006). Standardized reagents and protocols for engineeiing zinc finger nucleases by modular assembly. Nat Protocols 1: 1637.
39. Segal, DJ, Beerli, RR, Blancafort, P, Dreier, B, Effertz, K, Huber, A et al. (2003). Evaluation of a modolar strategy for the construction of novel polydactyl zinc finger DNA-binding proteins. Biochemistry 42: 2137-2148.
40. Greisman, HA and Pabo, CO (1997). A general strategy for selecting high-affinity zinc finger proteins for diverse DNA target sites. Science 275: 657-661.
41. Isalan, M, Klug, A and Choo, Y (2001). A rapid, generally applicable method to engineer zinc fingers illustrated by targeting the HIV-1 promoter. Nat Biotechnol 19: 656-660.
42. Desjarlais, JR and Berg, JM (1993). Use of a zinc-finger consensus sequence framework and specificity rules to design specific DNA binding proteins. Proc Natl Acad Sci USA 90: 2256-2260.
43. Kim, CA and Berg, JM (1996). A 2.2 A resolution crystal structure of a designed zinc finger protein bound to DNA. Nat Struct Biol 3 940-945.
44. Isalan, M, Klug, A and Choo, Y (1998). Comprehensive DNA recognition through concerted interactions from adjacent zinc fingers. Biochemistry 37: 12026-12033.
45. Dreier, B, Segal, DJ and Barbas, CF 3rd (2000). Insights into the molecular recognition of the 5′-GNN-3′ family of DNA sequences by zinc finger domains. J Mot Biol 303: 489-502.
46. Cathomen, T, Stracker, TH, Gilbert, LB and Weitzman, MD (2001). A genetic screen identifies a cellular regulator of adeno-associated virus. Proc Natl Acad Sci USA 96: 14991-14996.
47. Cathomen, T, Collete, D and Weitzman, MD (2000). A chimeric protein containing the N terminus of the adeno-associated virus Rep protein recognizes its target site in an in vivo assay. J Virol 74: 2372-2382.
48. Thibodeau, SA, Fang, R and Joung, JK (2004). High-throughput β-galactosidase assay for bacterial cell-based reporter systems. Biotechniques 36: 410-415.