Gene correction by homologous recombination with zinc finger nucleases in primary cells from a mouse model of a generic recessive genetic disease

Molecular Therapy

Volumn 18, Issue 6, 2010, Pages 1103-1110

  Connelly, Jon P ^a   Barker, Jenny C ^a   Pruett Miller, Shondra ^a   Porteus, Matthew H ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; ZINC FINGER PROTEIN; PRIMER DNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL DIFFERENTIATION; CELL LINEAGE; CELL STRAIN 3T3; CELL SURVIVAL; CELL TRANSPLANTATION; CELL TYPE; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; EX VIVO STUDY; FEMALE; FIBROBLAST; GENE EXPRESSION REGULATION; GENE FREQUENCY; GENE LOCUS; GENE MUTATION; GENE TARGETING; GENE THERAPY; GENETIC DISORDER; GENETIC TRANSFECTION; HOMOLOGOUS RECOMBINATION; MOUSE; NEWBORN; NONHUMAN; RECESSIVE INHERITANCE; TARGETED GENE REPAIR; TRANSGENIC MOUSE; ANIMAL; DISEASE MODEL; GENETIC DISEASES, INBORN; GENETIC RECOMBINATION; GENETICS; IMMUNOCOMPETENCE; METABOLISM; NUCLEOTIDE SEQUENCE; RECESSIVE GENE;

ANIMALS; BASE SEQUENCE; DISEASE MODELS, ANIMAL; DNA PRIMERS; EMBRYONIC STEM CELLS; GENE TARGETING; GENES, RECESSIVE; GENETIC DISEASES, INBORN; GREEN FLUORESCENT PROTEINS; IMMUNOCOMPETENCE; MICE; RECOMBINATION, GENETIC; TARGETED GENE REPAIR; ZINC FINGERS;

MURINAE; MUS MUSCULUS;

EID: 77953139680     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2010.57     Document Type: Article

References (50)

1. Hacein-Bey-Abina, S, Le Deist, F, Carlier, F, Bouneaud, C, Hue, C, De Villartay, JP et al. (2002). Sustained correction of X-linked severe combined immunodefciency by ex vivo gene therapy. N Engl J Med 346: 1185-1193.
2. Aiuti, A, Cattaneo, F, Galimberti, S, Benninghoff, U, Cassani, B, Callegaro, L et al. (2009). Gene therapy for immunodefciency due to adenosine deaminase defciency. N Engl J Med 360: 447-458.
3. Bainbridge, JW, Smith, AJ, Barker, SS, Robbie, S, Henderson, R, Balaggan, K et al. (2008). Effect of gene therapy on visual function in Leber's congenital amaurosis. N Engl J Med 358: 2231-2239.
4. Maguire, AM, High, KA, Auricchio, A, Wright, JF, Pierce, EA, Testa, F et al. (2009). Age-dependent effects of RPE65 gene therapy for Leber's congenital amaurosis: a phase 1 dose-escalation trial. Lancet 374: 1597-1605.
5. Cartier, N, Hacein-Bey-Abina, S, Bartholomae, CC, Veres, G, Schmidt, M, Kutschera, I et al. (2009). Hematopoietic stem cell gene therapy with a lentiviral vector in X-linked adrenoleukodystrophy. Science 326: 818-823.
6. Hacein-Bey-Abina, S, Von Kalle, C, Schmidt, M, McCormack, MP, Wulffraat, N, Leboulch, P et al. (2003). LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1. Science 302: 415-419.
7. Lombardo, A, Genovese, P, Beausejour, CM, Colleoni, S, Lee, YL, Kim, KA et al. (2007). Gene editing in human stem cells using zinc fnger nucleases and integrase-defective lentiviral vector delivery. Nat Biotechnol 25: 1298-1306.
8. Porteus, MH and Carroll, D (2005). Gene targeting using zinc fnger nucleases. Nat Biotechnol 23: 967-973.
9. Doetschman, T, Gregg, RG, Maeda, N, Hooper, ML, Melton, DW, Thompson, S et al. (1987). Targetted correction of a mutant HPRT gene in mouse embryonic stem cells. Nature 330: 576-578.
10. Porteus, MH and Baltimore, D (2003). Chimeric nucleases stimulate gene targeting in human cells. Science 300: 763.
11. Donoho, G, Jasin, M and Berg, P (1998). Analysis of gene targeting and intrachromosomal homologous recombination stimulated by genomic double-strand breaks in mouse embryonic stem cells. Mol Cell Biol 18: 4070-4078.
12. Rouet, P, Smih, F and Jasin, M (1994). Introduction of double-strand breaks into the genome of mouse cells by expression of a rare-cutting endonuclease. Mol Cell Biol 14: 8096-8106.
13. Choulika, A, Perrin, A, Dujon, B and Nicolas, JF (1995). Induction of homologous recombination in mammalian chromosomes by using the I-SceI system of Saccharomyces cerevisiae. Mol Cell Biol 15: 1968-1973.
14. Brenneman, M, Gimble, FS and Wilson, JH (1996). Stimulation of intrachromosomal homologous recombination in human cells by electroporation with site-specifc endonucleases. Proc Natl Acad Sci USA 93: 3608-3612.
15. Arnould, S, Chames, P, Perez, C, Lacroix, E, Duclert, A, Epinat, JC et al. (2006). Engineering of large numbers of highly specifc homing endonucleases that induce recombination on novel DNA targets. J Mol Biol 355: 443-458.
16. Pâques, F and Duchateau, P (2007). Meganucleases and DNA double-strand break-induced recombination: perspectives for gene therapy. Curr Gene Ther 7: 49-66.
17. Ashworth, J, Havranek, JJ, Duarte, CM, Sussman, D, Monnat, RJ Jr, Stoddard, BL et al. (2006). Computational redesign of endonuclease DNA binding and cleavage specifcity. Nature 441: 656-659.
18. Durai, S, Mani, M, Kandavelou, K, Wu, J, Porteus, MH and Chandrasegaran, S (2005). Zinc fnger nucleases: custom-designed molecular scissors for genome engineering of plant and mammalian cells. Nucleic Acids Res 33: 5978-5990.
19. 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 fnger DNA-recognition domains. Nucleic Acids Res 28: 3361-3369.
20. Bitinaite, J, Wah, DA, Aggarwal, AK and Schildkraut, I (1998). FokI dimerization is required for DNA cleavage. Proc Natl Acad Sci USA 95: 10570-10575. (Pubitemid 28413108)
21. Cathomen, T and Joung, JK (2008). Zinc-fnger nucleases: the next generation emerges. Mol Ther 16: 1200-1207.
22. Bibikova, M, Beumer, K, Trautman, JK and Carroll, D (2003). Enhancing gene targeting with designed zinc fnger nucleases. Science 300: 764.
23. Carroll, D (2008). Progress and prospects: zinc-fnger nucleases as gene therapy agents. Gene Ther 15: 1463-1468.
24. Doyon, Y, McCammon, JM, Miller, JC, Faraji, F, Ngo, C, Katibah, GE et al. (2008). Heritable targeted gene disruption in zebrafsh using designed zinc-fnger nucleases. Nat Biotechnol 26: 702-708.
25. Geurts, AM, Cost, GJ, Freyvert, Y, Zeitler, B, Miller, JC, Choi, VM et al. (2009). Knockout rats via embryo microinjection of zinc-fnger nucleases. Science 325: 433.
26. Meng, X, Noyes, MB, Zhu, LJ, Lawson, ND and Wolfe, SA (2008). Targeted gene inactivation in zebrafsh using engineered zinc-fnger nucleases. Nat Biotechnol 26: 695-701.
27. Morton, J, Davis, MW, Jorgensen, EM and Carroll, D (2006). Induction and repair of zinc-fnger nuclease-targeted double-strand breaks in Caenorhabditis elegans somatic cells. Proc Natl Acad Sci USA 103: 16370-16375.
28. Urnov, FD, Miller, JC, Lee, YL, Beausejour, CM, Rock, JM, Augustus, S et al. (2005). Highly effcient endogenous human gene correction using designed zinc-fnger nucleases. Nature 435: 646-651.
29. Shukla, VK, Doyon, Y, Miller, JC, DeKelver, RC, Moehle, EA, Worden, SE et al. (2009). Precise genome modifcation in the crop species Zea mays using zinc-fnger nucleases. Nature 459: 437-441.
30. Townsend, JA, Wright, DA, Winfrey, RJ, Fu, F, Maeder, ML, Joung, JK et al. (2009). High-frequency modifcation of plant genes using engineered zinc-fnger nucleases. Nature 459: 442-445.
31. Hockemeyer, D, Soldner, F, Beard, C, Gao, Q, Mitalipova, M, DeKelver, RC et al. (2009). Effcient targeting of expressed and silent genes in human ESCs and iPSCs using zinc-fnger nucleases. Nat Biotechnol 27: 851-857.
32. Zou, J, Maeder, ML, Mali, P, Pruett-Miller, SM, Thibodeau-Beganny, S, Chou, BK et al. (2009). Gene targeting of a disease-related gene in human induced pluripotent stem and embryonic stem cells. Cell Stem Cell 5: 97-110.
33. Perez, EE, Wang, J, Miller, JC, Jouvenot, Y, Kim, KA, Liu, O et al. (2008). Establishment of HIV-1 resistance in CD4+ T cells by genome editing using zinc-fnger nucleases. Nat Biotechnol 26: 808-816.
34. Zambrowicz, BP, Imamoto, A, Fiering, S, Herzenberg, LA, Kerr, WG and Soriano, P (1997). Disruption of overlapping transcripts in the ROSA beta geo 26 gene trap strain leads to widespread expression of beta-galactosidase in mouse embryos and hematopoietic cells. Proc Natl Acad Sci USA 94: 3789-3794.
35. Pruett-Miller, SM, Connelly, JP, Maeder, ML, Joung, JK and Porteus, MH (2008). Comparison of zinc fnger nucleases for use in gene targeting in mammalian cells. Mol Ther 16: 707-717.
36. Porteus, MH (2006). Mammalian gene targeting with designed zinc fnger nucleases. Mol Ther 13: 438-446.
37. Maeder, ML, Thibodeau-Beganny, S, Osiak, A, Wright, DA, Anthony, RM, Eichtinger, M et al. (2008). Rapid "open-source" engineering of customized zinc-fnger nucleases for highly effcient gene modifcation. Mol Cell 31: 294-301.
38. Potts, PR, Porteus, MH and Yu, H (2006). Human SMC5/6 complex promotes sister chromatid homologous recombination by recruiting the SMC1/3 cohesin complex to double-strand breaks. EMBO J 25: 3377-3388.
39. Todaro, GJ and Green, H (1963). Quantitative studies of the growth of mouse embryo cells in culture and their development into established lines. J Cell Biol 17: 299-313.
40. Qiu, X, Lu, D, Zhou, J, Wang, J, Yang, J, Meng, P et al. (1996). Implantation of autologous skin fbroblast genetically modifed to secrete clotting factor IX partially corrects the hemorrhagic tendencies in two hemophilia B patients. Chin Med J 109: 832-839.
41. Roth, DA, Tawa, NE Jr, O'Brien, JM, Treco, DA and Selden, RF; Factor VIII Transkaryotic Therapy Study Group (2001). Nonviral transfer of the gene encoding coagulation factor VIII in patients with severe hemophilia A. N Engl J Med 344: 1735-1742.
42. Palmer, TD, Thompson, AR and Miller, AD (1989). Production of human factor IX in animals by genetically modifed skin fbroblasts: potential therapy for hemophilia B. Blood 73: 438-445.
43. Miller, JC, Holmes, MC, Wang, J, Guschin, DY, Lee, YL, Rupniewski, I et al. (2007). An improved zinc-fnger nuclease architecture for highly specifc genome editing. Nat Biotechnol 25: 778-785.
44. Szczepek, M, Brondani, V, Büchel, J, Serrano, L, Segal, DJ and Cathomen, T (2007). Structure-based redesign of the dimerization interface reduces the toxicity of zinc-fnger nucleases. Nat Biotechnol 25: 786-793.
45. Bibikova, M, Golic, M, Golic, KG and Carroll, D (2002). Targeted chromosomal cleavage and mutagenesis in Drosophila using zinc-fnger nucleases. Genetics 161: 1169-1175.
46. Lloyd, A, Plaisier, CL, Carroll, D and Drews, GN (2005). Targeted mutagenesis using zinc-fnger nucleases in Arabidopsis. Proc Natl Acad Sci USA 102: 2232-2237.
47. Santiago, Y, Chan, E, Liu, PQ, Orlando, S, Zhang, L, Urnov, FD et al. (2008). Targeted gene knockout in mammalian cells by using engineered zinc-fnger nucleases. Proc Natl Acad Sci USA 105: 5809-5814.
48. Moehle, EA, Moehle, EA, Rock, JM, Rock, JM, Lee, YL, Lee, YL et al. (2007). Targeted gene addition into a specifed location in the human genome using designed zinc fnger nucleases. Proc Natl Acad Sci USA 104: 3055-3060.
49. Miller, DG, Wang, PR, Petek, LM, Hirata, RK, Sands, MS and Russell, DW (2006). Gene targeting in vivo by adeno-associated virus vectors. Nat Biotechnol 24: 1022-1026.
50. Hanna, J, Wernig, M, Markoulaki, S, Sun, CW, Meissner, A, Cassady, JP et al. (2007). Treatment of sickle cell anemia mouse model with iPS cells generated from autologous skin. Science 318: 1920-1923